Skip to main content

Microtubule Organization and Microtubule-Associated Proteins (MAPs)

  • Chapter
  • First Online:
Dendrites

Abstract

Dendrites have a unique microtubule organization. In vertebrates, dendritic microtubules are organized in antiparallel bundles, oriented with their plus ends either pointing away or toward the soma. The mixed microtubule arrays control intracellular trafficking and local signaling pathways, and are essential for dendrite development and function. The organization of microtubule arrays largely depends on the combined function of different microtubule regulatory factors or generally named microtubule-associated proteins (MAPs). Classical MAPs, also called structural MAPs, were identified more than 20 years ago based on their ability to bind to and copurify with microtubules. Most classical MAPs bind along the microtubule lattice and regulate microtubule polymerization, bundling, and stabilization. Recent evidences suggest that classical MAPs also guide motor protein transport, interact with the actin cytoskeleton, and act in various neuronal signaling networks. Here, we give an overview of microtubule organization in dendrites and the role of classical MAPs in dendrite development, dendritic spine formation, and synaptic plasticity.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
eBook
USD 129.00
Price excludes VAT (USA)
Softcover Book
USD 169.99
Price excludes VAT (USA)
Hardcover Book
USD 169.99
Price excludes VAT (USA)

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abdanipour A, Schluesener HJ, Tiraihi T, Noori-Zadeh A (2014) Systemic administration of valproic acid stimulates overexpression of microtubule-associated protein 2 in the spinal cord injury model to promote neurite outgrowth. Neurol Res 37(3):223–228. 1743132814Y0000000438

    Google Scholar 

  • Aguezzoul M, Andrieux A, Denarier E (2003) Overlap of promoter and coding sequences in the mouse STOP gene (Mtap6). Genomics 81:623–627

    Article  CAS  PubMed  Google Scholar 

  • Akhmanova A, Hoogenraad CC (2015) Microtubule minus-end-targeting proteins. Curr Biol 25:R162–R171

    Article  CAS  PubMed  Google Scholar 

  • Akhmanova A, Steinmetz MO (2008) Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 9:309–322

    Article  CAS  PubMed  Google Scholar 

  • Albala JS, Kress Y, Liu WK, Weidenheim K, Yen SH, Shafit-Zagardo B (1995) Human microtubule-associated protein-2c localizes to dendrites and axons in fetal spinal motor neurons. J Neurochem 64:2480–2490

    Article  CAS  PubMed  Google Scholar 

  • Al-Bassam J, Ozer RS, Safer D, Halpain S, Milligan RA (2002) MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. J Cell Biol 157:1187–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen E, Ding J, Wang W, Pramanik S, Chou J, Yau V, Yang Y (2005) Gigaxonin-controlled degradation of MAP1B light chain is critical to neuronal survival. Nature 438:224–228

    Article  CAS  PubMed  Google Scholar 

  • Andrieux A, Salin PA, Vernet M, Kujala P, Baratier J, Gory-Faure S, Bosc C, Pointu H, Proietto D, Schweitzer A et al (2002) The suppression of brain cold-stable microtubules in mice induces synaptic defects associated with neuroleptic-sensitive behavioral disorders. Genes Dev 16:2350–2364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrieux A, Salin P, Schweitzer A, Begou M, Pachoud B, Brun P, Gory-Faure S, Kujala P, Suaud-Chagny MF, Hofle G et al (2006) Microtubule stabilizer ameliorates synaptic function and behavior in a mouse model for schizophrenia. Biol Psychiatry 60:1224–1230

    Article  CAS  PubMed  Google Scholar 

  • Arrasate M, Perez M, Armas-Portela R, Avila J (1999) Polymerization of tau peptides into fibrillar structures. The effect of FTDP-17 mutations. FEBS Lett 446:199–202

    Article  CAS  PubMed  Google Scholar 

  • Asai DJ, Thompson WC, Wilson L, Dresden CF, Schulman H, Purich DL (1985) Microtubule-associated proteins (MAPs): a monoclonal antibody to MAP 1 decorates microtubules in vitro but stains stress fibers and not microtubules in vivo. Proc Natl Acad Sci U S A 82:1434–1438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avila J, Dominguez J, Diaz-Nido J (1994) Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int J Dev Biol 38:13–25

    CAS  PubMed  Google Scholar 

  • Avila J, Lucas JJ, Perez M, Hernandez F (2004) Role of tau protein in both physiological and pathological conditions. Physiol Rev 84:361–384

    Article  CAS  PubMed  Google Scholar 

  • Baas PW, Ahmad FJ (2013) Beyond taxol: microtubule-based treatment of disease and injury of the nervous system. Brain: J Neurol 136:2937–2951

    Article  Google Scholar 

  • Baas PW, Lin S (2011) Hooks and comets: the story of microtubule polarity orientation in the neuron. Dev Neurobiol 71:403–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baas PW, Deitch JS, Black MM, Banker GA (1988) Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc Natl Acad Sci U S A 85:8335–8339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baas PW, Slaughter T, Brown A, Black MM (1991) Microtubule dynamics in axons and dendrites. J Neurosci Res 30:134–153

    Article  CAS  PubMed  Google Scholar 

  • Baratier J, Peris L, Brocard J, Gory-Faure S, Dufour F, Bosc C, Fourest-Lieuvin A, Blanchoin L, Salin P, Job D et al (2006) Phosphorylation of microtubule-associated protein STOP by calmodulin kinase II. J Biol Chem 281:19561–19569

    Article  CAS  PubMed  Google Scholar 

  • Barlan K, Lu W, Gelfand VI (2013) The microtubule-binding protein ensconsin is an essential cofactor of kinesin-1. Curr Biol 23:317–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basbous J, Knani D, Bonneaud N, Giorgi D, Brondello JM, Rouquier S (2012) Induction of ASAP (MAP9) contributes to p53 stabilization in response to DNA damage. Cell Cycle 11:2380–2390

    Article  CAS  PubMed  Google Scholar 

  • Bash-Babula J, Toppmeyer D, Labassi M, Reidy J, Orlick M, Senzon R, Alli E, Kearney T, August D, Shih W et al (2002) A Phase I/pilot study of sequential doxorubicin/vinorelbine: effects on p53 and microtubule-associated protein 4. Clin Cancer Res 8:1057–1064

    CAS  PubMed  Google Scholar 

  • Baudier J, Mochly-Rosen D, Newton A, Lee SH, Koshland DE Jr, Cole RD (1987) Comparison of S100b protein with calmodulin: interactions with melittin and microtubule-associated tau proteins and inhibition of phosphorylation of tau proteins by protein kinase C. Biochemistry 26:2886–2893

    Article  CAS  PubMed  Google Scholar 

  • Beffert U, Dillon GM, Sullivan JM, Stuart CE, Gilbert JP, Kambouris JA, Ho A (2012) Microtubule plus-end tracking protein CLASP2 regulates neuronal polarity and synaptic function. J Neurosci 32:13906–13916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begou M, Volle J, Bertrand JB, Brun P, Job D, Schweitzer A, Saoud M, D’Amato T, Andrieux A, Suaud-Chagny MF (2008) The stop null mice model for schizophrenia displays [corrected] cognitive and social deficits partly alleviated by neuroleptics. Neuroscience 157:29–39

    Article  CAS  PubMed  Google Scholar 

  • Benoist M, Palenzuela R, Rozas C, Rojas P, Tortosa E, Morales B, Gonzalez-Billault C, Avila J, Esteban JA (2013) MAP1B-dependent Rac activation is required for AMPA receptor endocytosis during long-term depression. EMBO J 32:2287–2299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernhardt R, Matus A (1982) Initial phase of dendrite growth: evidence for the involvement of high molecular weight microtubule-associated proteins (HMWP) before the appearance of tubulin. J Cell Biol 92:589–593

    Article  CAS  PubMed  Google Scholar 

  • Bernhardt R, Huber G, Matus A (1985) Differences in the developmental patterns of three microtubule-associated proteins in the rat cerebellum. J Neurosci 5:977–991

    CAS  PubMed  Google Scholar 

  • Binder LI, Frankfurter A, Kim H, Caceres A, Payne MR, Rebhun LI (1984) Heterogeneity of microtubule-associated protein 2 during rat brain development. Proc Natl Acad Sci U S A 81:5613–5617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Binder LI, Frankfurter A, Rebhun LI (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101:1371–1378

    Article  CAS  PubMed  Google Scholar 

  • Bittner T, Fuhrmann M, Burgold S, Ochs SM, Hoffmann N, Mitteregger G, Kretzschmar H, LaFerla FM, Herms J (2010) Multiple events lead to dendritic spine loss in triple transgenic Alzheimer’s disease mice. PLoS One 5:e15477

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Black MM, Slaughter T, Fischer I (1994) Microtubule-associated protein 1b (MAP1b) is concentrated in the distal region of growing axons. J Neurosci 14:857–870

    CAS  PubMed  Google Scholar 

  • Black MM, Slaughter T, Moshiach S, Obrocka M, Fischer I (1996) Tau is enriched on dynamic microtubules in the distal region of growing axons. J Neurosci 16:3601–3619

    CAS  PubMed  Google Scholar 

  • Bloom GS, Vallee RB (1983) Association of microtubule-associated protein 2 (MAP 2) with microtubules and intermediate filaments in cultured brain cells. J Cell Biol 96:1523–1531

    Article  CAS  PubMed  Google Scholar 

  • Bloom GS, Luca FC, Vallee RB (1985) Microtubule-associated protein 1B: identification of a major component of the neuronal cytoskeleton. Proc Natl Acad Sci U S A 82:5404–5408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonnet C, Denarier E, Bosc C, Lazereg S, Denoulet P, Larcher JC (2002) Interaction of STOP with neuronal tubulin is independent of polyglutamylation. Biochem Biophys Res Commun 297:787–793

    Article  CAS  PubMed  Google Scholar 

  • Bornens M (2008) Organelle positioning and cell polarity. Nat Rev Mol Cell Biol 9:874–886

    Article  CAS  PubMed  Google Scholar 

  • Bosc C, Cronk JD, Pirollet F, Watterson DM, Haiech J, Job D, Margolis RL (1996) Cloning, expression, and properties of the microtubule-stabilizing protein STOP. Proc Natl Acad Sci U S A 93:2125–2130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosc C, Andrieux A, Job D (2003) STOP proteins. Biochemistry 42:12125–12132

    Article  CAS  PubMed  Google Scholar 

  • Bouquet C, Soares S, von Boxberg Y, Ravaille-Veron M, Propst F, Nothias F (2004) Microtubule-associated protein 1B controls directionality of growth cone migration and axonal branching in regeneration of adult dorsal root ganglia neurons. J Neurosci 24:7204–7213

    Article  CAS  PubMed  Google Scholar 

  • Bouvrais-Veret C, Weiss S, Andrieux A, Schweitzer A, McIntosh JM, Job D, Giros B, Martres MP (2007) Sustained increase of alpha7 nicotinic receptors and choline-induced improvement of learning deficit in STOP knock-out mice. Neuropharmacology 52:1691–1700

    Article  CAS  PubMed  Google Scholar 

  • Bouvrais-Veret C, Weiss S, Hanoun N, Andrieux A, Schweitzer A, Job D, Hamon M, Giros B, Martres MP (2008) Microtubule-associated STOP protein deletion triggers restricted changes in dopaminergic neurotransmission. J Neurochem 104:745–756

    CAS  PubMed  Google Scholar 

  • Brandt R, Leger J, Lee G (1995) Interaction of tau with the neural plasma membrane mediated by tau’s amino-terminal projection domain. J Cell Biol 131:1327–1340

    Article  CAS  PubMed  Google Scholar 

  • Bratman SV, Chang F (2008) Mechanisms for maintaining microtubule bundles. Trends Cell Biol 18:580–586

    Article  CAS  PubMed  Google Scholar 

  • Bre MH, Karsenti E (1990) Effects of brain microtubule-associated proteins on microtubule dynamics and the nucleating activity of centrosomes. Cell Motil Cytoskeleton 15:88–98

    Article  CAS  PubMed  Google Scholar 

  • Brenman JE, Topinka JR, Cooper EC, McGee AW, Rosen J, Milroy T, Ralston HJ, Bredt DS (1998) Localization of postsynaptic density-93 to dendritic microtubules and interaction with microtubule-associated protein 1A. J Neurosci 18:8805–8813

    CAS  PubMed  Google Scholar 

  • Brot S, Rogemond V, Perrot V, Chounlamountri N, Auger C, Honnorat J, Moradi-Ameli M (2010) CRMP5 interacts with tubulin to inhibit neurite outgrowth, thereby modulating the function of CRMP2. J Neurosci 30:10639–10654

    Article  CAS  PubMed  Google Scholar 

  • Brouhard GJ, Rice LM (2014) The contribution of alpha/beta-tubulin curvature to microtubule dynamics. J Cell Biol 207:323–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown V, Jin P, Ceman S, Darnell JC, O’Donnell WT, Tenenbaum SA, Jin X, Feng Y, Wilkinson KD, Keene JD et al (2001) Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107:477–487

    Article  CAS  PubMed  Google Scholar 

  • Brun P, Begou M, Andrieux A, Mouly-Badina L, Clerget M, Schweitzer A, Scarna H, Renaud B, Job D, Suaud-Chagny MF (2005) Dopaminergic transmission in STOP null mice. J Neurochem 94:63–73

    Article  CAS  PubMed  Google Scholar 

  • Bulinski JC, Borisy GG (1980) Widespread distribution of a 210,000 mol wt microtubule-associated protein in cells and tissues of primates. J Cell Biol 87:802–808

    Article  CAS  PubMed  Google Scholar 

  • Bulinski JC, Bossler A (1994) Purification and characterization of ensconsin, a novel microtubule stabilizing protein. J Cell Sci 107(Pt 10):2839–2849

    CAS  PubMed  Google Scholar 

  • Bulinski JC, McGraw TE, Gruber D, Nguyen HL, Sheetz MP (1997) Overexpression of MAP4 inhibits organelle motility and trafficking in vivo. J Cell Sci 110(Pt 24):3055–3064

    CAS  PubMed  Google Scholar 

  • Bulinski JC, Gruber D, Faire K, Prasad P, Chang W (1999) GFP chimeras of E-MAP-115 (ensconsin) domains mimic behavior of the endogenous protein in vitro and in vivo. Cell Struct Funct 24:313–320

    Article  CAS  PubMed  Google Scholar 

  • Bulinski JC, Odde DJ, Howell BJ, Salmon TD, Waterman-Storer CM (2001) Rapid dynamics of the microtubule binding of ensconsin in vivo. J Cell Sci 114:3885–3897

    CAS  PubMed  Google Scholar 

  • Burgin KE, Ludin B, Ferralli J, Matus A (1994) Bundling of microtubules in transfected cells does not involve an autonomous dimerization site on the MAP2 molecule. Mol Biol Cell 5:511–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burgoyne RD, Cumming R (1984) Ontogeny of microtubule-associated protein 2 in rat cerebellum: differential expression of the doublet polypeptides. Neuroscience 11:156–167

    Article  CAS  PubMed  Google Scholar 

  • Burton PR (1988) Dendrites of mitral cell neurons contain microtubules of opposite polarity. Brain Res 473:107–115

    Article  CAS  PubMed  Google Scholar 

  • Caceres A, Kosik KS (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343:461–463

    Article  CAS  PubMed  Google Scholar 

  • Caceres A, Payne MR, Binder LI, Steward O (1983) Immunocytochemical localization of actin and microtubule-associated protein MAP2 in dendritic spines. Proc Natl Acad Sci U S A 80:1738–1742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caceres A, Banker G, Steward O, Binder L, Payne M (1984) MAP2 is localized to the dendrites of hippocampal neurons which develop in culture. Brain Res 315:314–318

    Article  CAS  PubMed  Google Scholar 

  • Caceres A, Banker GA, Binder L (1986) Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J Neurosci 6:714–722

    CAS  PubMed  Google Scholar 

  • Caceres A, Potrebic S, Kosik KS (1991) The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J Neurosci 11:1515–1523

    CAS  PubMed  Google Scholar 

  • Caceres A, Mautino J, Kosik KS (1992) Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 9:607–618

    Article  CAS  PubMed  Google Scholar 

  • Calvert R, Anderton BH (1985) A microtubule-associated protein (MAP1) which is expressed at elevated levels during development of the rat cerebellum. EMBO J 4:1171–1176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Canas PM, Porciuncula LO, Cunha GM, Silva CG, Machado NJ, Oliveira JM, Oliveira CR, Cunha RA (2009) Adenosine A2A receptor blockade prevents synaptotoxicity and memory dysfunction caused by beta-amyloid peptides via p38 mitogen-activated protein kinase pathway. J Neurosci 29:14741–14751

    Article  CAS  PubMed  Google Scholar 

  • Capetillo-Zarate E, Staufenbiel M, Abramowski D, Haass C, Escher A, Stadelmann C, Yamaguchi H, Wiestler OD, Thal DR (2006) Selective vulnerability of different types of commissural neurons for amyloid beta-protein-induced neurodegeneration in APP23 mice correlates with dendritic tree morphology. Brain: J Neurol 129:2992–3005

    Article  Google Scholar 

  • Carlier MF, Simon C, Cassoly R, Pradel LA (1984) Interaction between microtubule-associated protein tau and spectrin. Biochimie 66:305–311

    Article  CAS  PubMed  Google Scholar 

  • Chan SL, Chua LL, Angeles DC, Tan EK (2014) MAP1B rescues LRRK2 mutant-mediated cytotoxicity. Mol Brain 7:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chang L, Jones Y, Ellisman MH, Goldstein LS, Karin M (2003) JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4:521–533

    Article  CAS  PubMed  Google Scholar 

  • Chapin SJ, Bulinski JC (1994) Cellular microtubules heterogeneous in their content of microtubule-associated protein 4 (MAP4). Cell Motil Cytoskeleton 27:133–149

    Article  CAS  PubMed  Google Scholar 

  • Chee F, Mudher A, Newman TA, Cuttle M, Lovestone S, Shepherd D (2006) Overexpression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions. Biochem Soc Trans 34:88–90

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Kanai Y, Cowan NJ, Hirokawa N (1992) Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360:674–677

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Rolls MM, Hancock WO (2014) An EB1-kinesin complex is sufficient to steer microtubule growth in vitro. Curr Biol 24:316–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng A, Krueger BK, Bambrick LL (1999) MAP5 expression in proliferating neuroblasts. Brain Res Dev Brain Res 113:107–113

    Article  CAS  PubMed  Google Scholar 

  • Cheng G, Iijima Y, Ishibashi Y, Kuppuswamy D, Cooper G (2002) Inhibition of G protein-coupled receptor trafficking in neuroblastoma cells by MAP 4 decoration of microtubules. Am J Physiol Heart Circ Physiol 283:H2379–H2388

    Article  CAS  PubMed  Google Scholar 

  • Cheng G, Qiao F, Gallien TN, Kuppuswamy D, Cooper G (2005) Inhibition of beta-adrenergic receptor trafficking in adult cardiocytes by MAP4 decoration of microtubules. Am J Physiol Heart Circ Physiol 288:H1193–H1202

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Desai J, Miranda CJ, Duncan JS, Qiu W, Nugent AA, Kolpak AL, Wu CC, Drokhlyansky E, Delisle MM et al (2014) Human CFEOM1 mutations attenuate KIF21A autoinhibition and cause oculomotor axon stalling. Neuron 82:334–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chevalier-Larsen E, Holzbaur EL (2006) Axonal transport and neurodegenerative disease. Biochim Biophys Acta 1762:1094–1108

    Article  CAS  PubMed  Google Scholar 

  • Chin SS, Goldman JE (1996) Glial inclusions in CNS degenerative diseases. J Neuropathol Exp Neurol 55:499–508

    Article  CAS  PubMed  Google Scholar 

  • Choi MC, Raviv U, Miller HP, Gaylord MR, Kiris E, Ventimiglia D, Needleman DJ, Kim MW, Wilson L, Feinstein SC et al (2009) Human microtubule-associated-protein tau regulates the number of protofilaments in microtubules: a synchrotron x-ray scattering study. Biophys J 97:519–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung WJ, Kindler S, Seidenbecher C, Garner CC (1996) MAP2a, an alternatively spliced variant of microtubule-associated protein 2. J Neurochem 66:1273–1281

    Article  CAS  PubMed  Google Scholar 

  • Clemmensen C, Aznar S, Knudsen GM, Klein AB (2012) The microtubule-associated protein 1A (MAP1A) is an early molecular target of soluble Abeta-peptide. Cell Mol Neurobiol 32:561–566

    Article  CAS  PubMed  Google Scholar 

  • Cleveland DW, Hwo SY, Kirschner MW (1977a) Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J Mol Biol 116:227–247

    Article  CAS  PubMed  Google Scholar 

  • Cleveland DW, Hwo SY, Kirschner MW (1977b) Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J Mol Biol 116:207–225

    Article  CAS  PubMed  Google Scholar 

  • Code RJ, Olmsted JB (1992) Mouse microtubule-associated protein 4 (MAP4) transcript diversity generated by alternative polyadenylation. Gene 122:367–370

    Article  CAS  PubMed  Google Scholar 

  • Collins MO, Yu L, Coba MP, Husi H, Campuzano I, Blackstock WP, Choudhary JS, Grant SG (2005) Proteomic analysis of in vivo phosphorylated synaptic proteins. J Biol Chem 280:5972–5982

    Article  CAS  PubMed  Google Scholar 

  • Conde C, Caceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319–332

    Article  CAS  PubMed  Google Scholar 

  • Cunningham CC, Leclerc N, Flanagan LA, Lu M, Janmey PA, Kosik KS (1997) Microtubule-associated protein 2c reorganizes both microtubules and microfilaments into distinct cytological structures in an actin-binding protein-280-deficient melanoma cell line. J Cell Biol 136:845–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daoust A, Bohic S, Saoudi Y, Debacker C, Gory-Faure S, Andrieux A, Barbier EL, Deloulme JC (2014) Neuronal transport defects of the MAP6 KO mouse – a model of schizophrenia – and alleviation by Epothilone D treatment, as observed using MEMRI. Neuroimage 96:133–142

    Article  CAS  PubMed  Google Scholar 

  • Davare MA, Dong F, Rubin CS, Hell JW (1999) The A-kinase anchor protein MAP2B and cAMP-dependent protein kinase are associated with class C L-type calcium channels in neurons. J Biol Chem 274:30280–30287

    Article  CAS  PubMed  Google Scholar 

  • Davidkova G, Carroll RC (2007) Characterization of the role of microtubule-associated protein 1B in metabotropic glutamate receptor-mediated endocytosis of AMPA receptors in hippocampus. J Neurosci 27:13273–13278

    Article  CAS  PubMed  Google Scholar 

  • Dawson HN, Ferreira A, Eyster MV, Ghoshal N, Binder LI, Vitek MP (2001) Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 114:1179–1187

    CAS  PubMed  Google Scholar 

  • Dehmelt L, Halpain S (2005) The MAP2/Tau family of microtubule-associated proteins. Genome Biol 6:204

    Article  PubMed  Google Scholar 

  • Dehmelt L, Smart FM, Ozer RS, Halpain S (2003) The role of microtubule-associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation. J Neurosci 23:9479–9490

    CAS  PubMed  Google Scholar 

  • Del Rio JA, Gonzalez-Billault C, Urena JM, Jimenez EM, Barallobre MJ, Pascual M, Pujadas L, Simo S, La Torre A, Wandosell F et al (2004) MAP1B is required for netrin 1 signaling in neuronal migration and axonal guidance. Curr Biol 14:840–850

    Article  PubMed  CAS  Google Scholar 

  • Delotterie D, Ruiz G, Brocard J, Schweitzer A, Roucard C, Roche Y, Suaud-Chagny MF, Bressand K, Andrieux A (2010) Chronic administration of atypical antipsychotics improves behavioral and synaptic defects of STOP null mice. Psychopharmacology (Berl) 208:131–141

    Article  CAS  Google Scholar 

  • Denarier E, Aguezzoul M, Jolly C, Vourc’h C, Roure A, Andrieux A, Bosc C, Job D (1998a) Genomic structure and chromosomal mapping of the mouse STOP gene (Mtap6). Biochem Biophys Res Commun 243:791–796

    Article  CAS  PubMed  Google Scholar 

  • Denarier E, Fourest-Lieuvin A, Bosc C, Pirollet F, Chapel A, Margolis RL, Job D (1998b) Nonneuronal isoforms of STOP protein are responsible for microtubule cold stability in mammalian fibroblasts. Proc Natl Acad Sci U S A 95:6055–6060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desai A, Mitchison TJ (1997) Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 13:83–117

    Article  CAS  PubMed  Google Scholar 

  • Dhamodharan R, Wadsworth P (1995) Modulation of microtubule dynamic instability in vivo by brain microtubule associated proteins. J Cell Sci 108(Pt 4):1679–1689

    CAS  PubMed  Google Scholar 

  • Diaz-Nido J, Serrano L, Mendez E, Avila J (1988) A casein kinase II-related activity is involved in phosphorylation of microtubule-associated protein MAP-1B during neuroblastoma cell differentiation. J Cell Biol 106:2057–2065

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Nido J, Serrano L, Hernandez MA, Avila J (1990) Phosphorylation of microtubule proteins in rat brain at different developmental stages: comparison with that found in neuronal cultures. J Neurochem 54:211–222

    Article  CAS  PubMed  Google Scholar 

  • Ding J, Liu JJ, Kowal AS, Nardine T, Bhattacharya P, Lee A, Yang Y (2002) Microtubule-associated protein 1B: a neuronal binding partner for gigaxonin. J Cell Biol 158:427–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding J, Allen E, Wang W, Valle A, Wu C, Nardine T, Cui B, Yi J, Taylor A, Jeon NL et al (2006a) Gene targeting of GAN in mouse causes a toxic accumulation of microtubule-associated protein 8 and impaired retrograde axonal transport. Hum Mol Genet 15:1451–1463

    Article  CAS  PubMed  Google Scholar 

  • Ding J, Valle A, Allen E, Wang W, Nardine T, Zhang Y, Peng L, Yang Y (2006b) Microtubule-associated protein 8 contains two microtubule binding sites. Biochem Biophys Res Commun 339:172–179

    Article  CAS  PubMed  Google Scholar 

  • DiTella MC, Feiguin F, Carri N, Kosik KS, Caceres A (1996) MAP-1B/TAU functional redundancy during laminin-enhanced axonal growth. J Cell Sci 109(Pt 2):467–477

    CAS  PubMed  Google Scholar 

  • Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319:1086–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doll T, Meichsner M, Riederer BM, Honegger P, Matus A (1993) An isoform of microtubule-associated protein 2 (MAP2) containing four repeats of the tubulin-binding motif. J Cell Sci 106(Pt 2):633–639

    CAS  PubMed  Google Scholar 

  • Dombeck DA, Kasischke KA, Vishwasrao HD, Ingelsson M, Hyman BT, Webb WW (2003) Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy. Proc Natl Acad Sci U S A 100:7081–7086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doodhi H, Katrukha EA, Kapitein LC, Akhmanova A (2014) Mechanical and geometrical constraints control kinesin-based microtubule guidance. Curr Biol 24:322–328

    Article  CAS  PubMed  Google Scholar 

  • Dou F, Netzer WJ, Tanemura K, Li F, Hartl FU, Takashima A, Gouras GK, Greengard P, Xu H (2003) Chaperones increase association of tau protein with microtubules. Proc Natl Acad Sci U S A 100:721–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drechsel DN, Hyman AA, Cobb MH, Kirschner MW (1992) Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3:1141–1154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drubin DG, Kirschner MW (1986) Tau protein function in living cells. J Cell Biol 103:2739–2746

    Article  CAS  PubMed  Google Scholar 

  • Dubey M, Chaudhury P, Kabiru H, Shea TB (2008) Tau inhibits anterograde axonal transport and perturbs stability in growing axonal neurites in part by displacing kinesin cargo: neurofilaments attenuate tau-mediated neurite instability. Cell Motil Cytoskeleton 65:89–99

    Article  CAS  PubMed  Google Scholar 

  • Dunn S, Morrison EE, Liverpool TB, Molina-Paris C, Cross RA, Alonso MC, Peckham M (2008) Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells. J Cell Sci 121:1085–1095

    Article  CAS  PubMed  Google Scholar 

  • Dziewczapolski G, Glogowski CM, Masliah E, Heinemann SF (2009) Deletion of the alpha 7 nicotinic acetylcholine receptor gene improves cognitive deficits and synaptic pathology in a mouse model of Alzheimer’s disease. J Neurosci 29:8805–8815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer’s disease. J Cell Biol 143:777–794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebneth A, Drewes G, Mandelkow EM, Mandelkow E (1999) Phosphorylation of MAP2c and MAP4 by MARK kinases leads to the destabilization of microtubules in cells. Cell Motil Cytoskeleton 44:209–224

    Article  CAS  PubMed  Google Scholar 

  • Edelmann W, Zervas M, Costello P, Roback L, Fischer I, Hammarback JA, Cowan N, Davies P, Wainer B, Kucherlapati R (1996) Neuronal abnormalities in microtubule-associated protein 1B mutant mice. Proc Natl Acad Sci U S A 93:1270–1275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, Andreyeva N, Gleeson P, Galjart N, Maia AR, McLeod IX et al (2007) Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 12:917–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eot-Houllier G, Venoux M, Vidal-Eychenie S, Hoang MT, Giorgi D, Rouquier S (2010) Plk1 regulates both ASAP localization and its role in spindle pole integrity. J Biol Chem 285:29556–29568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erck C, Peris L, Andrieux A, Meissirel C, Gruber AD, Vernet M, Schweitzer A, Saoudi Y, Pointu H, Bosc C et al (2005) A vital role of tubulin-tyrosine-ligase for neuronal organization. Proc Natl Acad Sci U S A 102:7853–7858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson M, Samuelsson H, Samuelsson EB, Liu L, McKeehan WL, Benedikz E, Sundstrom E (2007) The NMDAR subunit NR3A interacts with microtubule-associated protein 1S in the brain. Biochem Biophys Res Commun 361:127–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fabre-Jonca N, Allaman JM, Radlgruber G, Meda P, Kiss JZ, French LE, Masson D (1998) The distribution of murine 115-kDa epithelial microtubule-associated protein (E-MAP-115) during embryogenesis and in adult organs suggests a role in epithelial polarization and differentiation. Differ Res Biol Divers 63:169–180

    Article  CAS  Google Scholar 

  • Faire K, Waterman-Storer CM, Gruber D, Masson D, Salmon ED, Bulinski JC (1999) E-MAP-115 (ensconsin) associates dynamically with microtubules in vivo and is not a physiological modulator of microtubule dynamics. J Cell Sci 112(Pt 23):4243–4255

    CAS  PubMed  Google Scholar 

  • Faller EM, Brown DL (2009) Modulation of microtubule dynamics by the microtubule-associated protein 1a. J Neurosci Res 87:1080–1089

    Article  CAS  PubMed  Google Scholar 

  • Fanara P, Husted KH, Selle K, Wong PY, Banerjee J, Brandt R, Hellerstein MK (2010) Changes in microtubule turnover accompany synaptic plasticity and memory formation in response to contextual fear conditioning in mice. Neuroscience 168:167–178

    Article  CAS  PubMed  Google Scholar 

  • Farah CA, Liazoghli D, Perreault S, Desjardins M, Guimont A, Anton A, Lauzon M, Kreibich G, Paiement J, Leclerc N (2005) Interaction of microtubule-associated protein-2 and p63: a new link between microtubules and rough endoplasmic reticulum membranes in neurons. J Biol Chem 280:9439–9449

    Article  CAS  PubMed  Google Scholar 

  • Felgner H, Frank R, Biernat J, Mandelkow EM, Mandelkow E, Ludin B, Matus A, Schliwa M (1997) Domains of neuronal microtubule-associated proteins and flexural rigidity of microtubules. J Cell Biol 138:1067–1075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fellous A, Francon J, Lennon AM, Nunez J (1977) Microtubule assembly in vitro. Purification of assembly-promoting factors. Eur J Biochem/FEBS 78:167–174

    Article  CAS  Google Scholar 

  • Ferhat L, Represa A, Ferhat W, Ben-Ari Y, Khrestchatisky M (1998) MAP2d mRNA is expressed in identified neuronal populations in the developing and adult rat brain and its subcellular distribution differs from that of MAP2b in hippocampal neurones. Eur J Neurosci 10:161–171

    Article  CAS  PubMed  Google Scholar 

  • Fifkova E, Morales M (1992) Actin matrix of dendritic spines, synaptic plasticity, and long-term potentiation. Int Rev Cytol 139:267–307

    Article  CAS  PubMed  Google Scholar 

  • Fischer I, Romano-Clarke G (1990) Changes in microtubule-associated protein MAP1B phosphorylation during rat brain development. J Neurochem 55:328–333

    Article  CAS  PubMed  Google Scholar 

  • Fontenille L, Rouquier S, Lutfalla G, Giorgi D (2014) Microtubule-associated protein 9 (Map9/Asap) is required for the early steps of zebrafish development. Cell Cycle 13:1101–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fournet V, Jany M, Fabre V, Chali F, Orsal D, Schweitzer A, Andrieux A, Messanvi F, Giros B, Hamon M et al (2010) The deletion of the microtubule-associated STOP protein affects the serotonergic mouse brain network. J Neurochem 115:1579–1594

    Article  CAS  PubMed  Google Scholar 

  • Fournet V, de Lavilleon G, Schweitzer A, Giros B, Andrieux A, Martres MP (2012a) Both chronic treatments by epothilone D and fluoxetine increase the short-term memory and differentially alter the mood status of STOP/MAP6 KO mice. J Neurochem 123:982–996

    Article  CAS  PubMed  Google Scholar 

  • Fournet V, Schweitzer A, Chevarin C, Deloulme JC, Hamon M, Giros B, Andrieux A, Martres MP (2012b) The deletion of STOP/MAP6 protein in mice triggers highly altered mood and impaired cognitive performances. J Neurochem 121:99–114

    Article  CAS  PubMed  Google Scholar 

  • Fradley RL, O’Meara GF, Newman RJ, Andrieux A, Job D, Reynolds DS (2005) STOP knockout and NMDA NR1 hypomorphic mice exhibit deficits in sensorimotor gating. Behav Brain Res 163:257–264

    Article  CAS  PubMed  Google Scholar 

  • Frandemiche ML, De Seranno S, Rush T, Borel E, Elie A, Arnal I, Lante F, Buisson A (2014) Activity-dependent tau protein translocation to excitatory synapse is disrupted by exposure to amyloid-beta oligomers. J Neurosci 34:6084–6097

    Article  PubMed  CAS  Google Scholar 

  • Fuhrmann-Stroissnigg H, Noiges R, Descovich L, Fischer I, Albrecht DE, Nothias F, Froehner SC, Propst F (2012) The light chains of microtubule-associated proteins MAP1A and MAP1B interact with alpha1-syntrophin in the central and peripheral nervous system. PLoS One 7:e49722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujio K, Sato M, Uemura T, Sato T, Sato-Harada R, Harada A (2007) 14-3-3 proteins and protein phosphatases are not reduced in tau-deficient mice. Neuroreport 18:1049–1052

    Article  CAS  PubMed  Google Scholar 

  • Fukata Y, Itoh TJ, Kimura T, Menager C, Nishimura T, Shiromizu T, Watanabe H, Inagaki N, Iwamatsu A, Hotani H et al (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 4:583–591

    CAS  PubMed  Google Scholar 

  • Galiano MR, Bosc C, Schweitzer A, Andrieux A, Job D, Hallak ME (2004) Astrocytes and oligodendrocytes express different STOP protein isoforms. J Neurosci Res 78:329–337

    Article  CAS  PubMed  Google Scholar 

  • Garcia Rocha M, Avila J (1995) Characterization of microtubule-associated protein phosphoisoforms present in isolated growth cones. Brain Res Dev Brain Res 89:47–55

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Perez J, Avila J, Diaz-Nido J (1998) Implication of cyclin-dependent kinases and glycogen synthase kinase 3 in the phosphorylation of microtubule-associated protein 1B in developing neuronal cells. J Neurosci Res 52:445–452

    Article  CAS  PubMed  Google Scholar 

  • Garner CC, Tucker RP, Matus A (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336:674–677

    Article  CAS  PubMed  Google Scholar 

  • Garner CC, Matus A, Anderton B, Calvert R (1989) Microtubule-associated proteins MAP5 and MAP1x: closely related components of the neuronal cytoskeleton with different cytoplasmic distributions in the developing brain. Brain Res Mol Brain Res 5:85–92

    Article  CAS  PubMed  Google Scholar 

  • Gerdes JM, Katsanis N (2005) Small molecule intervention in microtubule-associated human disease. Hum Mol Genet 14(suppl 2):291–300

    Google Scholar 

  • Gevorkian G, Gonzalez-Noriega A, Acero G, Ordonez J, Michalak C, Munguia ME, Govezensky T, Cribbs DH, Manoutcharian K (2008) Amyloid-beta peptide binds to microtubule-associated protein 1B (MAP1B). Neurochem Int 52:1030–1036

    Article  CAS  PubMed  Google Scholar 

  • Goedert M, Crowther RA, Garner CC (1991) Molecular characterization of microtubule-associated proteins tau and MAP2. Trends Neurosci 14:193–199

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez SL, Lopez-Costa JJ, Labombarda F, Gonzalez Deniselle MC, Guennoun R, Schumacher M, De Nicola AF (2009) Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in rats with acute spinal cord injury. Cell Mol Neurobiol 29:27–39

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Billault C, Demandt E, Wandosell F, Torres M, Bonaldo P, Stoykova A, Chowdhury K, Gruss P, Avila J, Sanchez MP (2000) Perinatal lethality of microtubule-associated protein 1B-deficient mice expressing alternative isoforms of the protein at low levels. Mol Cell Neurosci 16:408–421

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Billault C, Avila J, Caceres A (2001) Evidence for the role of MAP1B in axon formation. Mol Biol Cell 12:2087–2098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Billault C, Engelke M, Jimenez-Mateos EM, Wandosell F, Caceres A, Avila J (2002a) Participation of structural microtubule-associated proteins (MAPs) in the development of neuronal polarity. J Neurosci Res 67:713–719

    Google Scholar 

  • Gonzalez-Billault C, Owen R, Gordon-Weeks PR, Avila J (2002b) Microtubule-associated protein 1B is involved in the initial stages of axonogenesis in peripheral nervous system cultured neurons. Brain Res 943:56–67

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Billault C, Del Rio JA, Urena JM, Jimenez-Mateos EM, Barallobre MJ, Pascual M, Pujadas L, Simo S, Torre AL, Gavin R et al (2005) A role of MAP1B in reelin-dependent neuronal migration. Cereb Cortex 15:1134–1145

    Article  PubMed  Google Scholar 

  • Good PF, Alapat D, Hsu A, Chu C, Perl D, Wen X, Burstein DE, Kohtz DS (2004) A role for semaphorin 3A signaling in the degeneration of hippocampal neurons during Alzheimer’s disease. J Neurochem 91:716–736

    Article  CAS  PubMed  Google Scholar 

  • Goode BL, Denis PE, Panda D, Radeke MJ, Miller HP, Wilson L, Feinstein SC (1997) Functional interactions between the proline-rich and repeat regions of tau enhance microtubule binding and assembly. Mol Biol Cell 8:353–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon-Weeks PR, Fischer I (2000) MAP1B expression and microtubule stability in growing and regenerating axons. Microsc Res Tech 48:63–74

    Article  CAS  PubMed  Google Scholar 

  • Griffith LM, Pollard TD (1982) The interaction of actin filaments with microtubules and microtubule-associated proteins. J Biol Chem 257:9143–9151

    CAS  PubMed  Google Scholar 

  • Grossman GH, Beight CD, Ebke LA, Pauer GJ, Hagstrom SA (2014) Interaction of tubby-like protein-1 (Tulp1) and microtubule-associated protein (MAP) 1A and MAP1B in the mouse retina. Adv Exp Med Biol 801:511–518

    Article  PubMed  Google Scholar 

  • Grueber WB, Sagasti A (2010) Self-avoidance and tiling: mechanisms of dendrite and axon spacing. Cold Spring Harb Perspect Biol 2:a001750

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gu J, Zheng JQ (2009) Microtubules in dendritic spine development and plasticity. Open Neurosci J 3:128–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillaud L, Bosc C, Fourest-Lieuvin A, Denarier E, Pirollet F, Lafanechere L, Job D (1998) STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J Cell Biol 142:167–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta M, Yarwood SJ (2005) MAP1A light chain 2 interacts with exchange protein activated by cyclic AMP 1 (EPAC1) to enhance Rap1 GTPase activity and cell adhesion. J Biol Chem 280:8109–8116

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Tsai LH, Wynshaw-Boris A (2002) Life is a journey: a genetic look at neocortical development. Nat Rev Genet 3:342–355

    Article  CAS  PubMed  Google Scholar 

  • Hait WN, Yang JM (2006) The individualization of cancer therapy: the unexpected role of p53. Trans Am Clin Climatol Assoc 117:85–101; discussion 101

    PubMed  PubMed Central  Google Scholar 

  • Halpain S, Dehmelt L (2006) The MAP1 family of microtubule-associated proteins. Genome Biol 7:224

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hammond JW, Cai D, Verhey KJ (2008) Tubulin modifications and their cellular functions. Curr Opin Cell Biol 20:71–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammond JW, Huang CF, Kaech S, Jacobson C, Banker G, Verhey KJ (2010) Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons. Mol Biol Cell 21:572–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harada A, Oguchi K, Okabe S, Kuno J, Terada S, Ohshima T, Sato-Yoshitake R, Takei Y, Noda T, Hirokawa N (1994) Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369:488–491

    Article  CAS  PubMed  Google Scholar 

  • Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N (2002) MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 158:541–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartel R, Matus A (1997) Cytoskeletal maturation in cultured hippocampal slices. Neuroscience 78:1–5

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa M, Arai T, Ihara Y (1990) Immunochemical evidence that fragments of phosphorylated MAP5 (MAP1B) are bound to neurofibrillary tangles in Alzheimer’s disease. Neuron 4:909–918

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K, Ishikawa R, Ye LH, He XL, Takata K, Kohama K, Shirao T (1996) Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex. J Neurosci 16:7161–7170

    CAS  PubMed  Google Scholar 

  • Heins S, Song YH, Wille H, Mandelkow E, Mandelkow EM (1991) Effect of MAP2, MAP2c, and tau on kinesin-dependent microtubule motility. J Cell Sci Suppl 14:121–124

    Article  CAS  PubMed  Google Scholar 

  • Hirokawa N, Funakoshi T, Sato-Harada R, Kanai Y (1996) Selective stabilization of tau in axons and microtubule-associated protein 2C in cell bodies and dendrites contributes to polarized localization of cytoskeletal proteins in mature neurons. J Cell Biol 132:667–679

    Article  CAS  PubMed  Google Scholar 

  • Hirokawa N, Niwa S, Tanaka Y (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68:610–638

    Article  CAS  PubMed  Google Scholar 

  • Holmfeldt P, Brattsand G, Gullberg M (2002) MAP4 counteracts microtubule catastrophe promotion but not tubulin-sequestering activity in intact cells. Curr Biol 12:1034–1039

    Article  CAS  PubMed  Google Scholar 

  • Holmfeldt P, Brattsand G, Gullberg M (2003) Interphase and monoastral-mitotic phenotypes of overexpressed MAP4 are modulated by free tubulin concentrations. J Cell Sci 116:3701–3711

    Article  CAS  PubMed  Google Scholar 

  • Hoogenraad CC, Bradke F (2009) Control of neuronal polarity and plasticity – a renaissance for microtubules? Trends Cell Biol 19:669–676

    Article  CAS  PubMed  Google Scholar 

  • Hoover BR, Reed MN, Su J, Penrod RD, Kotilinek LA, Grant MK, Pitstick R, Carlson GA, Lanier LM, Yuan LL et al (2010) Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 68:1067–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horton AC, Racz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48:757–771

    Article  CAS  PubMed  Google Scholar 

  • Hoshi M, Ohta K, Gotoh Y, Mori A, Murofushi H, Sakai H, Nishida E (1992) Mitogen-activated-protein-kinase-catalyzed phosphorylation of microtubule-associated proteins, microtubule-associated protein 2 and microtubule-associated protein 4, induces an alteration in their function. Eur J Biochem/FEBS 203:43–52

    Article  CAS  Google Scholar 

  • Howard J, Hyman AA (2003) Dynamics and mechanics of the microtubule plus end. Nature 422:753–758

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Viesselmann C, Nam S, Merriam E, Dent EW (2008) Activity-dependent dynamic microtubule invasion of dendritic spines. J Neurosci 28:13094–13105

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Furuya A, Furuichi T (2007) Very-KIND, a KIND domain containing RasGEF, controls dendrite growth by linking Ras small GTPases and MAP2. J Cell Biol 179:539–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huber G, Alaimo-Beuret D, Matus A (1985) MAP3: characterization of a novel microtubule-associated protein. J Cell Biol 100:496–507

    Article  CAS  PubMed  Google Scholar 

  • Huber G, Pehling G, Matus A (1986) The novel microtubule-associated protein MAP3 contributes to the in vitro assembly of brain microtubules. J Biol Chem 261:2270–2273

    CAS  PubMed  Google Scholar 

  • Hwang SC, Jhon DY, Bae YS, Kim JH, Rhee SG (1996) Activation of phospholipase C-gamma by the concerted action of tau proteins and arachidonic acid. J Biol Chem 271:18342–18349

    Article  CAS  PubMed  Google Scholar 

  • Ikeda A, Zheng QY, Zuberi AR, Johnson KR, Naggert JK, Nishina PM (2002) Microtubule-associated protein 1A is a modifier of tubby hearing (moth1). Nat Genet 30:401–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikegami S, Harada A, Hirokawa N (2000) Muscle weakness, hyperactivity, and impairment in fear conditioning in tau-deficient mice. Neurosci Lett 279:129–132

    Article  CAS  PubMed  Google Scholar 

  • Illenberger S, Drewes G, Trinczek B, Biernat J, Meyer HE, Olmsted JB, Mandelkow EM, Mandelkow E (1996) Phosphorylation of microtubule-associated proteins MAP2 and MAP4 by the protein kinase p110mark. Phosphorylation sites and regulation of microtubule dynamics. J Biol Chem 271:10834–10843

    Article  CAS  PubMed  Google Scholar 

  • Iriuchijima N, Sato-Harada R, Takano M, Fujio K, Sato T, Goto F, Harada A (2005) Reduced expression of kinase-associated phosphatase in cortical dendrites of MAP2-deficient mice. Biochem Biophys Res Commun 338:1216–1221

    Article  CAS  PubMed  Google Scholar 

  • Itoh TJ, Hisanaga S, Hosoi T, Kishimoto T, Hotani H (1997) Phosphorylation states of microtubule-associated protein 2 (MAP2) determine the regulatory role of MAP2 in microtubule dynamics. Biochemistry 36:12574–12582

    Article  CAS  PubMed  Google Scholar 

  • Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wolfing H, Chieng BC, Christie MJ, Napier IA et al (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer’s disease mouse models. Cell 142:387–397

    Article  CAS  PubMed  Google Scholar 

  • Jaglin XH, Chelly J (2009) Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects. Trends Genet 25:555–566

    Article  CAS  PubMed  Google Scholar 

  • Jaglin XH, Poirier K, Saillour Y, Buhler E, Tian G, Bahi-Buisson N, Fallet-Bianco C, Phan-Dinh-Tuy F, Kong XP, Bomont P et al (2009) Mutations in the beta-tubulin gene TUBB2B result in asymmetrical polymicrogyria. Nat Genet 41:746–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jalava NS, Lopez-Picon FR, Kukko-Lukjanov TK, Holopainen IE (2007) Changes in microtubule-associated protein-2 (MAP2) expression during development and after status epilepticus in the immature rat hippocampus. Int J Dev Neurosci 25:121–131

    Article  CAS  PubMed  Google Scholar 

  • Janke C, Bulinski JC (2011) Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat Rev Mol Cell Biol 12:773–786

    Article  CAS  PubMed  Google Scholar 

  • Janke C, Kneussel M (2010) Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci 33:362–372

    Article  CAS  PubMed  Google Scholar 

  • Jaworski J, Kapitein LC, Gouveia SM, Dortland BR, Wulf PS, Grigoriev I, Camera P, Spangler SA, Di Stefano P, Demmers J et al (2009) Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61:85–100

    Article  CAS  PubMed  Google Scholar 

  • Jensen PH, Hager H, Nielsen MS, Hojrup P, Gliemann J, Jakes R (1999) alpha-synuclein binds to Tau and stimulates the protein kinase A-catalyzed tau phosphorylation of serine residues 262 and 356. J Biol Chem 274:25481–25489

    Article  CAS  PubMed  Google Scholar 

  • Jensen PH, Islam K, Kenney J, Nielsen MS, Power J, Gai WP (2000) Microtubule-associated protein 1B is a component of cortical Lewy bodies and binds alpha-synuclein filaments. J Biol Chem 275:21500–21507

    Article  CAS  PubMed  Google Scholar 

  • Jiang K, Akhmanova A (2011) Microtubule tip-interacting proteins: a view from both ends. Curr Opin Cell Biol 23:94–101

    Article  CAS  PubMed  Google Scholar 

  • Jinushi-Nakao S, Arvind R, Amikura R, Kinameri E, Liu AW, Moore AW (2007) Knot/Collier and cut control different aspects of dendrite cytoskeleton and synergize to define final arbor shape. Neuron 56:963–978

    Article  CAS  PubMed  Google Scholar 

  • Job D, Fischer EH, Margolis RL (1981) Rapid disassembly of cold-stable microtubules by calmodulin. Proc Natl Acad Sci U S A 78:4679–4682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Job D, Rauch CT, Fischer EH, Margolis RL (1983) Regulation of microtubule cold stability by calmodulin-dependent and -independent phosphorylation. Proc Natl Acad Sci U S A 80:3894–3898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson KA, Porter ME, Shimizu T (1984) Mechanism of force production for microtubule-dependent movements. J Cell Biol 99:132s–136s

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kage E, Hayashi Y, Takeuchi H, Hirotsu T, Kunitomo H, Inoue T, Arai H, Iino Y, Kubo T (2005) MBR-1, a novel helix-turn-helix transcription factor, is required for pruning excessive neurites in Caenorhabditis elegans. Curr Biol 15:1554–1559

    Article  CAS  PubMed  Google Scholar 

  • Kahn OI, Sharma V, Gonzalez-Billault C, Baas PW (2015) Effects of kinesin-5 inhibition on dendritic architecture and microtubule organization. Mol Biol Cell 26:66–77

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kajitani K, Thorne M, Samson M, Robertson GS (2010) Nitric oxide synthase mediates the ability of darbepoetin alpha to improve the cognitive performance of STOP null mice. Neuropsychopharmacology 35:1718–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalcheva N, Rockwood JM, Kress Y, Steiner A, Shafit-Zagardo B (1998) Molecular and functional characteristics of MAP-2a: ability of MAP-2a versus MAP-2b to induce stable microtubules in COS cells. Cell Motil Cytoskeleton 40:272–285

    Article  CAS  PubMed  Google Scholar 

  • Kanai Y, Hirokawa N (1995) Sorting mechanisms of tau and MAP2 in neurons: suppressed axonal transit of MAP2 and locally regulated microtubule binding. Neuron 14:421–432

    Article  CAS  PubMed  Google Scholar 

  • Kanai Y, Takemura R, Oshima T, Mori H, Ihara Y, Yanagisawa M, Masaki T, Hirokawa N (1989) Expression of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA. J Cell Biol 109:1173–1184

    Article  CAS  PubMed  Google Scholar 

  • Kanai Y, Chen J, Hirokawa N (1992) Microtubule bundling by tau proteins in vivo: analysis of functional domains. EMBO J 11:3953–3961

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kapitein LC, Hoogenraad CC (2011) Which way to go? Cytoskeletal organization and polarized transport in neurons. Mol Cell Neurosci 46:9–20

    Article  CAS  PubMed  Google Scholar 

  • Kapitein LC, Schlager MA, Kuijpers M, Wulf PS, van Spronsen M, MacKintosh FC, Hoogenraad CC (2010) Mixed microtubules steer dynein-driven cargo transport into dendrites. Curr Biol 20:290–299

    Article  CAS  PubMed  Google Scholar 

  • Kapitein LC, Yau KW, Gouveia SM, van der Zwan WA, Wulf PS, Keijzer N, Demmers J, Jaworski J, Akhmanova A, Hoogenraad CC (2011) NMDA receptor activation suppresses microtubule growth and spine entry. J Neurosci 31:8194–8209

    Article  CAS  PubMed  Google Scholar 

  • Karagoz GE, Duarte AM, Akoury E, Ippel H, Biernat J, Moran Luengo T, Radli M, Didenko T, Nordhues BA, Veprintsev DB et al (2014) Hsp90-Tau complex reveals molecular basis for specificity in chaperone action. Cell 156:963–974

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kardon JR, Vale RD (2009) Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 10:854–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karki S, Holzbaur EL (1999) Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr Opin Cell Biol 11:45–53

    Article  CAS  PubMed  Google Scholar 

  • Kawachi A, Ichihara K, Hisanaga S, Iida J, Toyota H, Hotani H, Itoh TJ (2003) Different protofilament-dependence of the microtubule binding between MAP2 and MAP4. Biochem Biophys Res Commun 305:72–78

    Article  CAS  PubMed  Google Scholar 

  • Kawakami S, Muramoto K, Ichikawa M, Kuroda Y (2003) Localization of microtubule-associated protein (MAP) 1B in the postsynaptic densities of the rat cerebral cortex. Cell Mol Neurobiol 23:887–894

    Article  CAS  PubMed  Google Scholar 

  • Kawauchi T, Chihama K, Nishimura YV, Nabeshima Y, Hoshino M (2005) MAP1B phosphorylation is differentially regulated by Cdk5/p35, Cdk5/p25, and JNK. Biochem Biophys Res Commun 331:50–55

    Article  CAS  PubMed  Google Scholar 

  • Keays DA, Tian G, Poirier K, Huang GJ, Siebold C, Cleak J, Oliver PL, Fray M, Harvey RJ, Molnar Z et al (2007) Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 128:45–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kempf M, Clement A, Faissner A, Lee G, Brandt R (1996) Tau binds to the distal axon early in development of polarity in a microtubule- and microfilament-dependent manner. J Neurosci 16:5583–5592

    CAS  PubMed  Google Scholar 

  • Khuchua Z, Wozniak DF, Bardgett ME, Yue Z, McDonald M, Boero J, Hartman RE, Sims H, Strauss AW (2003) Deletion of the N-terminus of murine map2 by gene targeting disrupts hippocampal ca1 neuron architecture and alters contextual memory. Neuroscience 119:101–111

    Article  CAS  PubMed  Google Scholar 

  • Kleele T, Marinkovi CP, Williams PR, Stern S, Weigand EE, Engerer P, Naumann R, Hartmann J, Karl RM, Bradke F et al (2014) An assay to image neuronal microtubule dynamics in mice. Nat Commun 5:4827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein C, Kramer EM, Cardine AM, Schraven B, Brandt R, Trotter J (2002) Process outgrowth of oligodendrocytes is promoted by interaction of fyn kinase with the cytoskeletal protein tau. J Neurosci 22:698–707

    CAS  PubMed  Google Scholar 

  • Kobayashi N, Heid HW, Sakai T, Kriz W, Huber G, Mundel P (2000) Molecular characterization reveals identity of microtubule-associated proteins MAP3 and MAP4. Biochem Biophys Res Commun 268:306–309

    Article  CAS  PubMed  Google Scholar 

  • Koleske AJ (2013) Molecular mechanisms of dendrite stability. Nat Rev Neurosci 14:536–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kollins KM, Bell RL, Butts M, Withers GS (2009) Dendrites differ from axons in patterns of microtubule stability and polymerization during development. Neural Dev 4:26

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Komada M, McLean DJ, Griswold MD, Russell LD, Soriano P (2000) E-MAP-115, encoding a microtubule-associated protein, is a retinoic acid-inducible gene required for spermatogenesis. Genes Dev 14:1332–1342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Konishi Y, Setou M (2009) Tubulin tyrosination navigates the kinesin-1 motor domain to axons. Nat Neurosci 12:559–567

    Article  CAS  PubMed  Google Scholar 

  • Kosik KS, Finch EA (1987) MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: an immunocytochemical study of cultured rat cerebrum. J Neurosci 7:3142–3153

    CAS  PubMed  Google Scholar 

  • Kotani S, Nishida E, Kumagai H, Sakai H (1985) Calmodulin inhibits interaction of actin with MAP2 and Tau, two major microtubule-associated proteins. J Biol Chem 260:10779–10783

    CAS  PubMed  Google Scholar 

  • Kowalski RJ, Williams RC Jr (1993) Microtubule-associated protein 2 alters the dynamic properties of microtubule assembly and disassembly. J Biol Chem 268:9847–9855

    CAS  PubMed  Google Scholar 

  • Kremer A, Maurin H, Demedts D, Devijver H, Borghgraef P, Van Leuven F (2011) Early improved and late defective cognition is reflected by dendritic spines in Tau.P301L mice. J Neurosci 31:18036–18047

    Article  CAS  PubMed  Google Scholar 

  • Kuijpers M, Hoogenraad CC (2011) Centrosomes, microtubules and neuronal development. Mol Cell Neurosci 48:349–358

    Article  CAS  PubMed  Google Scholar 

  • Kumarapeli AR, Wang X (2004) Genetic modification of the heart: chaperones and the cytoskeleton. J Mol Cell Cardiol 37:1097–1109

    CAS  PubMed  Google Scholar 

  • Kurz JC, Williams RC Jr (1995) Microtubule-associated proteins and the flexibility of microtubules. Biochemistry 34:13374–13380

    Article  CAS  PubMed  Google Scholar 

  • Kwan AC, Dombeck DA, Webb WW (2008) Polarized microtubule arrays in apical dendrites and axons. Proc Natl Acad Sci U S A 105:11370–11375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacroix B, van Dijk J, Gold ND, Guizetti J, Aldrian-Herrada G, Rogowski K, Gerlich DW, Janke C (2010) Tubulin polyglutamylation stimulates spastin-mediated microtubule severing. J Cell Biol 189:945–954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lajoie-Mazenc I, Tovar D, Penary M, Lortal B, Allart S, Favard C, Brihoum M, Pradines A, Favre G (2008) MAP1A light chain-2 interacts with GTP-RhoB to control epidermal growth factor (EGF)-dependent EGF receptor signaling. J Biol Chem 283:4155–4164

    Article  CAS  PubMed  Google Scholar 

  • Langnaese K, Seidenbecher C, Wex H, Seidel B, Hartung K, Appeltauer U, Garner A, Voss B, Mueller B, Garner CC et al (1996) Protein components of a rat brain synaptic junctional protein preparation. Brain Res Mol Brain Res 42:118–122

    Article  CAS  PubMed  Google Scholar 

  • Lansbergen G, Akhmanova A (2006) Microtubule plus end: a hub of cellular activities. Traffic 7:499–507

    Article  CAS  PubMed  Google Scholar 

  • Lebeau G, Miller LC, Tartas M, McAdam R, Laplante I, Badeaux F, DesGroseillers L, Sossin WS, Lacaille JC (2011) Staufen 2 regulates mGluR long-term depression and Map1b mRNA distribution in hippocampal neurons. Learn Mem 18:314–326

    Article  CAS  PubMed  Google Scholar 

  • Lee G, Newman ST, Gard DL, Band H, Panchamoorthy G (1998) Tau interacts with src-family non-receptor tyrosine kinases. J Cell Sci 111(Pt 21):3167–3177

    CAS  PubMed  Google Scholar 

  • Lee HH, Jan LY, Jan YN (2009) Drosophila IKK-related kinase Ik2 and Katanin p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc Natl Acad Sci U S A 106:6363–6368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leenders AG, Lin L, Huang LD, Gerwin C, Lu PH, Sheng ZH (2008) The role of MAP1A light chain 2 in synaptic surface retention of Cav2.2 channels in hippocampal neurons. J Neurosci 28:11333–11346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei P, Ayton S, Finkelstein DI, Spoerri L, Ciccotosto GD, Wright DK, Wong BX, Adlard PA, Cherny RA, Lam LQ et al (2012) Tau deficiency induces parkinsonism with dementia by impairing APP-mediated iron export. Nat Med 18:291–295

    Article  CAS  PubMed  Google Scholar 

  • Lev DL, White EL (1997) Organization of pyramidal cell apical dendrites and composition of dendritic clusters in the mouse: emphasis on primary motor cortex. Eur J Neurosci 9:280–290

    Article  CAS  PubMed  Google Scholar 

  • Liao G, Gundersen GG (1998) Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J Biol Chem 273:9797–9803

    Article  CAS  PubMed  Google Scholar 

  • Liao H, Li Y, Brautigan DL, Gundersen GG (1998) Protein phosphatase 1 is targeted to microtubules by the microtubule-associated protein Tau. J Biol Chem 273:21901–21908

    Article  CAS  PubMed  Google Scholar 

  • Lim RW, Halpain S (2000) Regulated association of microtubule-associated protein 2 (MAP2) with Src and Grb2: evidence for MAP2 as a scaffolding protein. J Biol Chem 275:20578–20587

    Article  CAS  PubMed  Google Scholar 

  • Lin S, Liu M, Mozgova OI, Yu W, Baas PW (2012) Mitotic motors coregulate microtubule patterns in axons and dendrites. J Neurosci 32:14033–14049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lipka J, Kuijpers M, Jaworski J, Hoogenraad CC (2013) Mutations in cytoplasmic dynein and its regulators cause malformations of cortical development and neurodegenerative diseases. Biochem Soc Trans 41:1605–1612

    Article  CAS  PubMed  Google Scholar 

  • Liu CW, Lee G, Jay DG (1999) Tau is required for neurite outgrowth and growth cone motility of chick sensory neurons. Cell Motil Cytoskeleton 43:232–242

    Article  CAS  PubMed  Google Scholar 

  • Loeb DM, Tsao H, Cobb MH, Greene LA (1992) NGF and other growth factors induce an association between ERK1 and the NGF receptor, gp140prototrk. Neuron 9:1053–1065

    Article  CAS  PubMed  Google Scholar 

  • Lopez LA, Sheetz MP (1993) Steric inhibition of cytoplasmic dynein and kinesin motility by MAP2. Cell Motil Cytoskeleton 24:1–16

    Article  CAS  PubMed  Google Scholar 

  • Lopez LA, Sheetz MP (1995) A microtubule-associated protein (MAP2) kinase restores microtubule motility in embryonic brain. J Biol Chem 270:12511–12517

    Article  CAS  PubMed  Google Scholar 

  • Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP (1999) The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 399:784–788

    Article  CAS  PubMed  Google Scholar 

  • Lu R, Wang H, Liang Z, Ku L, O’Donnell WT, Li W, Warren ST, Feng Y (2004) The fragile X protein controls microtubule-associated protein 1B translation and microtubule stability in brain neuron development. Proc Natl Acad Sci U S A 101:15201–15206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luders J, Stearns T (2007) Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 8:161–167

    Article  PubMed  CAS  Google Scholar 

  • Luo L, O’Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127–156

    Article  CAS  PubMed  Google Scholar 

  • Ma QL, Zuo X, Yang F, Ubeda OJ, Gant DJ, Alaverdyan M, Kiosea NC, Nazari S, Chen PP, Nothias F et al (2014) Loss of MAP function leads to hippocampal synapse loss and deficits in the Morris Water Maze with aging. J Neurosci 34:7124–7136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maas C, Belgardt D, Lee HK, Heisler FF, Lappe-Siefke C, Magiera MM, van Dijk J, Hausrat TJ, Janke C, Kneussel M (2009) Synaptic activation modifies microtubules underlying transport of postsynaptic cargo. Proc Natl Acad Sci U S A 106:8731–8736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maccioni RB, Cambiazo V (1995) Role of microtubule-associated proteins in the control of microtubule assembly. Physiol Rev 75:835–864

    CAS  PubMed  Google Scholar 

  • Mandell JW, Banker GA (1996) A spatial gradient of tau protein phosphorylation in nascent axons. J Neurosci 16:5727–5740

    CAS  PubMed  Google Scholar 

  • Maniar TA, Kaplan M, Wang GJ, Shen K, Wei L, Shaw JE, Koushika SP, Bargmann CI (2011) UNC-33 (CRMP) and ankyrin organize microtubules and localize kinesin to polarize axon-dendrite sorting. Nat Neurosci 15:48–56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mansfield SG, Diaz-Nido J, Gordon-Weeks PR, Avila J (1991) The distribution and phosphorylation of the microtubule-associated protein MAP 1B in growth cones. J Neurocytol 20:1007–1022

    Article  CAS  PubMed  Google Scholar 

  • Manzini MC, Walsh CA (2011) What disorders of cortical development tell us about the cortex: one plus one does not always make two. Curr Opin Genet Dev 21:333–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masson D, Kreis TE (1993) Identification and molecular characterization of E-MAP-115, a novel microtubule-associated protein predominantly expressed in epithelial cells. J Cell Biol 123:357–371

    Article  CAS  PubMed  Google Scholar 

  • Matsushima K, Aosaki M, Tokuraku K, Hasan MR, Nakagawa H, Kotani S (2005) Identification of a neural cell specific variant of microtubule-associated protein 4. Cell Struct Funct 29:111–124

    Article  CAS  PubMed  Google Scholar 

  • Mattie FJ, Stackpole MM, Stone MC, Clippard JR, Rudnick DA, Qiu Y, Tao J, Allender DL, Parmar M, Rolls MM (2010) Directed microtubule growth, +TIPs, and kinesin-2 are required for uniform microtubule polarity in dendrites. Curr Biol 20:2169–2177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matus A (1988) Microtubule-associated proteins: their potential role in determining neuronal morphology. Annu Rev Neurosci 11:29–44

    Article  CAS  PubMed  Google Scholar 

  • Matus A, Huber G, Bernhardt R (1983) Neuronal microdifferentiation. Cold Spring Harb Symp Quant Biol 48(Pt 2):775–782

    Article  CAS  PubMed  Google Scholar 

  • McNally FJ (2013) Mechanisms of spindle positioning. J Cell Biol 200:131–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McNally KP, Buster D, McNally FJ (2002) Katanin-mediated microtubule severing can be regulated by multiple mechanisms. Cell Motil Cytoskeleton 53:337–349

    Article  CAS  PubMed  Google Scholar 

  • Meichsner M, Doll T, Reddy D, Weisshaar B, Matus A (1993) The low molecular weight form of microtubule-associated protein 2 is transported into both axons and dendrites. Neuroscience 54:873–880

    Article  CAS  PubMed  Google Scholar 

  • Meixner A, Haverkamp S, Wassle H, Fuhrer S, Thalhammer J, Kropf N, Bittner RE, Lassmann H, Wiche G, Propst F (2000) MAP1B is required for axon guidance and is involved in the development of the central and peripheral nervous system. J Cell Biol 151:1169–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merenlender-Wagner A, Pikman R, Giladi E, Andrieux A, Gozes I (2010) NAP (davunetide) enhances cognitive behavior in the STOP heterozygous mouse – a microtubule-deficient model of schizophrenia. Peptides 31:1368–1373

    Article  CAS  PubMed  Google Scholar 

  • Merino-Serrais P, Benavides-Piccione R, Blazquez-Llorca L, Kastanauskaite A, Rabano A, Avila J, DeFelipe J (2013) The influence of phospho-tau on dendritic spines of cortical pyramidal neurons in patients with Alzheimer’s disease. Brain: J Neurol 136:1913–1928

    Article  Google Scholar 

  • Metzger T, Gache V, Xu M, Cadot B, Folker ES, Richardson BE, Gomes ER, Baylies MK (2012) MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function. Nature 484:120–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Migheli A, Butler M, Brown K, Shelanski ML (1988) Light and electron microscope localization of the microtubule-associated tau protein in rat brain. J Neurosci 8:1846–1851

    CAS  PubMed  Google Scholar 

  • Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312:237–242

    Article  CAS  PubMed  Google Scholar 

  • Mocanu MM, Nissen A, Eckermann K, Khlistunova I, Biernat J, Drexler D, Petrova O, Schonig K, Bujard H, Mandelkow E et al (2008) The potential for beta-structure in the repeat domain of tau protein determines aggregation, synaptic decay, neuronal loss, and coassembly with endogenous Tau in inducible mouse models of tauopathy. J Neurosci 28:737–748

    Article  CAS  PubMed  Google Scholar 

  • Moolman DL, Vitolo OV, Vonsattel JP, Shelanski ML (2004) Dendrite and dendritic spine alterations in Alzheimer models. J Neurocytol 33:377–387

    Article  CAS  PubMed  Google Scholar 

  • Mori A, Aizawa H, Saido TC, Kawasaki H, Mizuno K, Murofushi H, Suzuki K, Sakai H (1991) Site-specific phosphorylation by protein kinase C inhibits assembly-promoting activity of microtubule-associated protein 4. Biochemistry 30:9341–9346

    Article  CAS  PubMed  Google Scholar 

  • Morris JA, Kandpal G, Ma L, Austin CP (2003) DISC1 (Disrupted-In-Schizophrenia 1) is a centrosome-associated protein that interacts with MAP1A, MIPT3, ATF4/5 and NUDEL: regulation and loss of interaction with mutation. Hum Mol Genet 12:1591–1608

    Article  CAS  PubMed  Google Scholar 

  • Murakami N, Bolton DC, Kida E, Xie W, Hwang YW (2012) Phosphorylation by Dyrk1A of clathrin coated vesicle-associated proteins: identification of the substrate proteins and the effects of phosphorylation. PLoS One 7:e34845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen HL, Chari S, Gruber D, Lue CM, Chapin SJ, Bulinski JC (1997) Overexpression of full- or partial-length MAP4 stabilizes microtubules and alters cell growth. J Cell Sci 110(Pt 2):281–294

    CAS  PubMed  Google Scholar 

  • Nguyen HL, Gruber D, Bulinski JC (1999) Microtubule-associated protein 4 (MAP4) regulates assembly, protomer-polymer partitioning and synthesis of tubulin in cultured cells. J Cell Sci 112(Pt 12):1813–1824

    CAS  PubMed  Google Scholar 

  • Nunez J (1988) Immature and mature variants of MAP2 and tau proteins and neuronal plasticity. Trends Neurosci 11:477–479

    Article  CAS  PubMed  Google Scholar 

  • Obar RA, Dingus J, Bayley H, Vallee RB (1989) The RII subunit of cAMP-dependent protein kinase binds to a common amino-terminal domain in microtubule-associated proteins 2A, 2B, and 2C. Neuron 3:639–645

    Article  CAS  PubMed  Google Scholar 

  • Ochoa CD, Stevens T, Balczon R (2011) Cold exposure reveals two populations of microtubules in pulmonary endothelia. Am J Physiol Lung Cell Mol Physiol 300:L132–L138

    Article  CAS  PubMed  Google Scholar 

  • Ohkawa N, Fujitani K, Tokunaga E, Furuya S, Inokuchi K (2007) The microtubule destabilizer stathmin mediates the development of dendritic arbors in neuronal cells. J Cell Sci 120:1447–1456

    Article  CAS  PubMed  Google Scholar 

  • Okabe S, Hirokawa N (1989) Rapid turnover of microtubule-associated protein MAP2 in the axon revealed by microinjection of biotinylated MAP2 into cultured neurons. Proc Natl Acad Sci U S A 86:4127–4131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olmsted JB (1986) Microtubule-associated proteins. Annu Rev Cell Biol 2:421–457

    Article  CAS  PubMed  Google Scholar 

  • Olson KR, McIntosh JR, Olmsted JB (1995) Analysis of MAP 4 function in living cells using green fluorescent protein (GFP) chimeras. J Cell Biol 130:639–650

    Article  CAS  PubMed  Google Scholar 

  • Opal P, Garcia JJ, Propst F, Matilla A, Orr HT, Zoghbi HY (2003) Mapmodulin/leucine-rich acidic nuclear protein binds the light chain of microtubule-associated protein 1B and modulates neuritogenesis. J Biol Chem 278:34691–34699

    Article  CAS  PubMed  Google Scholar 

  • Orban-Nemeth Z, Simader H, Badurek S, Trancikova A, Propst F (2005) Microtubule-associated protein 1S, a short and ubiquitously expressed member of the microtubule-associated protein 1 family. J Biol Chem 280:2257–2265

    Article  CAS  PubMed  Google Scholar 

  • Ori-McKenney KM, Jan LY, Jan YN (2012) Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76:921–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paglini G, Pigino G, Kunda P, Morfini G, Maccioni R, Quiroga S, Ferreira A, Caceres A (1998) Evidence for the participation of the neuron-specific CDK5 activator P35 during laminin-enhanced axonal growth. J Neurosci 18:9858–9869

    CAS  PubMed  Google Scholar 

  • Papasozomenos SC, Binder LI (1986) Microtubule-associated protein 2 (MAP2) is present in astrocytes of the optic nerve but absent from astrocytes of the optic tract. J Neurosci 6:1748–1756

    CAS  PubMed  Google Scholar 

  • Papasozomenos SC, Binder LI, Bender PK, Payne MR (1985) Microtubule-associated protein 2 within axons of spinal motor neurons: associations with microtubules and neurofilaments in normal and beta, beta’-iminodipropionitrile-treated axons. J Cell Biol 100:74–85

    Article  CAS  PubMed  Google Scholar 

  • Park SM, Liu G, Kubal A, Fury M, Cao L, Marx SO (2004) Direct interaction between BKCa potassium channel and microtubule-associated protein 1A. FEBS Lett 570:143–148

    Article  CAS  PubMed  Google Scholar 

  • Parysek LM, Asnes CF, Olmsted JB (1984) MAP 4: occurrence in mouse tissues. J Cell Biol 99:1309–1315

    Article  CAS  PubMed  Google Scholar 

  • Paschal BM, Vallee RB (1987) Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330:181–183

    Article  CAS  PubMed  Google Scholar 

  • Paschal BM, Shpetner HS, Vallee RB (1987) MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J Cell Biol 105:1273–1282

    Article  CAS  PubMed  Google Scholar 

  • Peck A, Sargin ME, LaPointe NE, Rose K, Manjunath BS, Feinstein SC, Wilson L (2011) Tau isoform-specific modulation of kinesin-driven microtubule gliding rates and trajectories as determined with tau-stabilized microtubules. Cytoskeleton (Hoboken) 68:44–55

    Article  CAS  Google Scholar 

  • Pedrotti B, Islam K (1995) Purification of microtubule associated protein MAP1B from bovine brain: MAP1B binds to microtubules but not to microfilaments. Cell Motil Cytoskeleton 30:301–309

    Article  CAS  PubMed  Google Scholar 

  • Pedrotti B, Colombo R, Islam K (1994a) Interactions of microtubule-associated protein MAP2 with unpolymerized and polymerized tubulin and actin using a 96-well microtiter plate solid-phase immunoassay. Biochemistry 33:8798–8806

    Article  CAS  PubMed  Google Scholar 

  • Pedrotti B, Colombo R, Islam K (1994b) Microtubule associated protein MAP1A is an actin-binding and crosslinking protein. Cell Motil Cytoskeleton 29:110–116

    Article  CAS  PubMed  Google Scholar 

  • Pedrotti B, Ulloa L, Avila J, Islam K (1996) Characterization of microtubule-associated protein MAP1B: phosphorylation state, light chains, and binding to microtubules. Biochemistry 35:3016–3023

    Article  CAS  PubMed  Google Scholar 

  • Peng J, Kim MJ, Cheng D, Duong DM, Gygi SP, Sheng M (2004) Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J Biol Chem 279:21003–21011

    Article  CAS  PubMed  Google Scholar 

  • Perez M, Santa-Maria I, Gomez de Barreda E, Zhu X, Cuadros R, Cabrero JR, Sanchez-Madrid F, Dawson HN, Vitek MP, Perry G et al (2009) Tau – an inhibitor of deacetylase HDAC6 function. J Neurochem 109:1756–1766

    Article  CAS  PubMed  Google Scholar 

  • Pigino G, Paglini G, Ulloa L, Avila J, Caceres A (1997) Analysis of the expression, distribution and function of cyclin dependent kinase 5 (cdk5) in developing cerebellar macroneurons. J Cell Sci 110(Pt 2):257–270

    CAS  PubMed  Google Scholar 

  • Poplawski GH, Tranziska AK, Leshchyns’ka I, Meier ID, Streichert T, Sytnyk V, Schachner M (2012) L1CAM increases MAP2 expression via the MAPK pathway to promote neurite outgrowth. Mol Cell Neurosci 50:169–178

    Article  CAS  PubMed  Google Scholar 

  • Poulain FE, Sobel A (2010) The microtubule network and neuronal morphogenesis: dynamic and coordinated orchestration through multiple players. Mol Cell Neurosci 43:15–32

    Article  CAS  PubMed  Google Scholar 

  • Poulain FE, Chauvin S, Wehrle R, Desclaux M, Mallet J, Vodjdani G, Dusart I, Sobel A (2008) SCLIP is crucial for the formation and development of the Purkinje cell dendritic arbor. J Neurosci 28:7387–7398

    Article  CAS  PubMed  Google Scholar 

  • Powell KJ, Hori SE, Leslie R, Andrieux A, Schellinck H, Thorne M, Robertson GS (2007) Cognitive impairments in the STOP null mouse model of schizophrenia. Behav Neurosci 121:826–835

    Article  PubMed  Google Scholar 

  • Praefcke GJ, Ford MG, Schmid EM, Olesen LE, Gallop JL, Peak-Chew SY, Vallis Y, Babu MM, Mills IG, McMahon HT (2004) Evolving nature of the AP2 alpha-appendage hub during clathrin-coated vesicle endocytosis. EMBO J 23:4371–4383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Przyborski SA, Cambray-Deakin MA (1995) Developmental regulation of MAP2 variants during neuronal differentiation in vitro. Brain Res Dev Brain Res 89:187–201

    Article  CAS  PubMed  Google Scholar 

  • Ray M, Ruan J, Zhang W (2008) Variations in the transcriptome of Alzheimer’s disease reveal molecular networks involved in cardiovascular diseases. Genome Biol 9:R148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16:2166–2172

    Article  CAS  PubMed  Google Scholar 

  • Reese ML, Dakoji S, Bredt DS, Dotsch V (2007) The guanylate kinase domain of the MAGUK PSD-95 binds dynamically to a conserved motif in MAP1a. Nat Struct Mol Biol 14:155–163

    Article  CAS  PubMed  Google Scholar 

  • Rehbein M, Kindler S, Horke S, Richter D (2000) Two trans-acting rat-brain proteins, MARTA1 and MARTA2, interact specifically with the dendritic targeting element in MAP2 mRNAs. Brain Res Mol Brain Res 79:192–201

    Article  CAS  PubMed  Google Scholar 

  • Riederer B, Matus A (1985) Differential expression of distinct microtubule-associated proteins during brain development. Proc Natl Acad Sci U S A 82:6006–6009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riederer B, Cohen R, Matus A (1986) MAP5: a novel brain microtubule-associated protein under strong developmental regulation. J Neurocytol 15:763–775

    Article  CAS  PubMed  Google Scholar 

  • Rocher AB, Crimins JL, Amatrudo JM, Kinson MS, Todd-Brown MA, Lewis J, Luebke JI (2010) Structural and functional changes in tau mutant mice neurons are not linked to the presence of NFTs. Exp Neurol 223:385–393

    Article  CAS  PubMed  Google Scholar 

  • Roll-Mecak A, McNally FJ (2010) Microtubule-severing enzymes. Curr Opin Cell Biol 22:96–103

    Article  CAS  PubMed  Google Scholar 

  • Rolls MM (2011) Neuronal polarity in Drosophila: sorting out axons and dendrites. Dev Neurobiol 71:419–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosoklija G, Keilp JG, Toomayan G, Mancevski B, Haroutunian V, Liu D, Malespina D, Hays AP, Sadiq S, Latov N et al (2005) Altered subicular MAP2 immunoreactivity in schizophrenia. Prilozi 26:13–34

    PubMed  Google Scholar 

  • Rubino HM, Dammerman M, Shafit-Zagardo B, Erlichman J (1989) Localization and characterization of the binding site for the regulatory subunit of type II cAMP-dependent protein kinase on MAP2. Neuron 3:631–638

    Article  CAS  PubMed  Google Scholar 

  • Ryan XP, Alldritt J, Svenningsson P, Allen PB, Wu GY, Nairn AC, Greengard P (2005) The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47:85–100

    Article  CAS  PubMed  Google Scholar 

  • Saffin JM, Venoux M, Prigent C, Espeut J, Poulat F, Giorgi D, Abrieu A, Rouquier S (2005) ASAP, a human microtubule-associated protein required for bipolar spindle assembly and cytokinesis. Proc Natl Acad Sci U S A 102:11302–11307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salinas S, Carazo-Salas RE, Proukakis C, Schiavo G, Warner TT (2007) Spastin and microtubules: functions in health and disease. J Neurosci Res 85:2778–2782

    Article  CAS  PubMed  Google Scholar 

  • Samora CP, Mogessie B, Conway L, Ross JL, Straube A, McAinsh AD (2011) MAP4 and CLASP1 operate as a safety mechanism to maintain a stable spindle position in mitosis. Nat Cell Biol 13:1040–1050

    Article  CAS  PubMed  Google Scholar 

  • Samsonov A, Yu JZ, Rasenick M, Popov SV (2004) Tau interaction with microtubules in vivo. J Cell Sci 117:6129–6141

    Article  CAS  PubMed  Google Scholar 

  • Sanchez C, Diaz-Nido J, Avila J (2000) Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol 61:133–168

    Article  CAS  PubMed  Google Scholar 

  • Satoh D, Sato D, Tsuyama T, Saito M, Ohkura H, Rolls MM, Ishikawa F, Uemura T (2008) Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat Cell Biol 10:1164–1171

    Article  CAS  PubMed  Google Scholar 

  • Scales TM, Lin S, Kraus M, Goold RG, Gordon-Weeks PR (2009) Nonprimed and DYRK1A-primed GSK3 beta-phosphorylation sites on MAP1B regulate microtubule dynamics in growing axons. J Cell Sci 122:2424–2435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheetz AJ, Dubin MW (1994) Cytochemical polarity in lateral geniculate interneurons. Brain Res 639:181–192

    Article  CAS  PubMed  Google Scholar 

  • Schoenfeld TA, Obar RA (1994) Diverse distribution and function of fibrous microtubule-associated proteins in the nervous system. Int Rev Cytol 151:67–137

    Article  CAS  PubMed  Google Scholar 

  • Schoenfeld TA, McKerracher L, Obar R, Vallee RB (1989) MAP 1A and MAP 1B are structurally related microtubule associated proteins with distinct developmental patterns in the CNS. J Neurosci 9:1712–1730

    CAS  PubMed  Google Scholar 

  • Scholz T, Mandelkow E (2014) Transport and diffusion of Tau protein in neurons. Cell Mol Life Sci 71:3139–3150

    Article  CAS  PubMed  Google Scholar 

  • Schwenk BM, Lang CM, Hogl S, Tahirovic S, Orozco D, Rentzsch K, Lichtenthaler SF, Hoogenraad CC, Capell A, Haass C et al (2014) The FTLD risk factor TMEM106B and MAP6 control dendritic trafficking of lysosomes. EMBO J 33:450–467

    CAS  PubMed  Google Scholar 

  • Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E (2002) Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 21:4896–4905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selden SC, Pollard TD (1983) Phosphorylation of microtubule-associated proteins regulates their interaction with actin filaments. J Biol Chem 258:7064–7071

    CAS  PubMed  Google Scholar 

  • Semenova I, Ikeda K, Resaul K, Kraikivski P, Aguiar M, Gygi S, Zaliapin I, Cowan A, Rodionov V (2014) Regulation of microtubule-based transport by MAP4. Mol Biol Cell 25:3119–3132

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shafit-Zagardo B, Kalcheva N (1998) Making sense of the multiple MAP-2 transcripts and their role in the neuron. Mol Neurobiol 16:149–162

    Article  CAS  PubMed  Google Scholar 

  • Sharma N, Kress Y, Shafit-Zagardo B (1994) Antisense MAP-2 oligonucleotides induce changes in microtubule assembly and neuritic elongation in pre-existing neurites of rat cortical neurons. Cell Motil Cytoskeleton 27:234–247

    Article  CAS  PubMed  Google Scholar 

  • Sharp DJ, Ross JL (2012) Microtubule-severing enzymes at the cutting edge. J Cell Sci 125:2561–2569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin E, Kashiwagi Y, Kuriu T, Iwasaki H, Tanaka T, Koizumi H, Gleeson JG, Okabe S (2013) Doublecortin-like kinase enhances dendritic remodelling and negatively regulates synapse maturation. Nat Commun 4:1440

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shirao T, Gonzalez-Billault C (2013) Actin filaments and microtubules in dendritic spines. J Neurochem 126:155–164

    Article  CAS  PubMed  Google Scholar 

  • Siegrist SE, Doe CQ (2007) Microtubule-induced cortical cell polarity. Genes Dev 21:483–496

    Article  CAS  PubMed  Google Scholar 

  • Sirajuddin M, Rice LM, Vale RD (2014) Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat Cell Biol 16:335–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slaughter T, Black MM (2003) STOP (stable-tubule-only-polypeptide) is preferentially associated with the stable domain of axonal microtubules. J Neurocytol 32:399–413

    Article  CAS  PubMed  Google Scholar 

  • Sobue K, Agarwal-Mawal A, Li W, Sun W, Miura Y, Paudel HK (2000) Interaction of neuronal Cdc2-like protein kinase with microtubule-associated protein tau. J Biol Chem 275:16673–16680

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Kirkpatrick LL, Schilling AB, Helseth DL, Chabot N, Keillor JW, Johnson GV, Brady ST (2013) Transglutaminase and polyamination of tubulin: posttranslational modification for stabilizing axonal microtubules. Neuron 78:109–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, Kuret J, White CL 3rd, Mumby MC, Bloom GS (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J Biol Chem 274:25490–25498

    Article  CAS  PubMed  Google Scholar 

  • Sontag JM, Nunbhakdi-Craig V, White CL 3rd, Halpain S, Sontag E (2012) The protein phosphatase PP2A/Balpha binds to the microtubule-associated proteins Tau and MAP2 at a motif also recognized by the kinase Fyn: implications for tauopathies. J Biol Chem 287:14984–14993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sparacino J, Farias MG, Lamberti PW (2014) Effect of the microtubule-associated protein tau on dynamics of single-headed motor proteins KIF1A. Phys Rev E Stat Nonlin Soft Matter Phys 89:022714

    Article  CAS  PubMed  Google Scholar 

  • Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156:1051–1063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stepanova T, Slemmer J, Hoogenraad CC, Lansbergen G, Dortland B, De Zeeuw CI, Grosveld F, van Cappellen G, Akhmanova A, Galjart N (2003) Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J Neurosci 23:2655–2664

    CAS  PubMed  Google Scholar 

  • Stewart A, Tsubouchi A, Rolls MM, Tracey WD, Sherwood NT (2012) Katanin p60-like1 promotes microtubule growth and terminal dendrite stability in the larval class IV sensory neurons of Drosophila. J Neurosci 32:11631–11642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stiess M, Maghelli N, Kapitein LC, Gomis-Ruth S, Wilsch-Brauninger M, Hoogenraad CC, Tolic-Norrelykke IM, Bradke F (2010) Axon extension occurs independently of centrosomal microtubule nucleation. Science 327:704–707

    Article  CAS  PubMed  Google Scholar 

  • Stone MC, Roegiers F, Rolls MM (2008) Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol Biol Cell 19:4122–4129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strittmatter WJ, Saunders AM, Goedert M, Weisgraber KH, Dong LM, Jakes R, Huang DY, Pericak-Vance M, Schmechel D, Roses AD (1994) Isoform-specific interactions of apolipoprotein E with microtubule-associated protein tau: implications for Alzheimer disease. Proc Natl Acad Sci U S A 91:11183–11186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su KY, Chien WL, Fu WM, Yu IS, Huang HP, Huang PH, Lin SR, Shih JY, Lin YL, Hsueh YP et al (2007) Mice deficient in collapsin response mediator protein-1 exhibit impaired long-term potentiation and impaired spatial learning and memory. J Neurosci 27:2513–2524

    Article  CAS  PubMed  Google Scholar 

  • Sudo H, Baas PW (2010) Acetylation of microtubules influences their sensitivity to severing by katanin in neurons and fibroblasts. J Neurosci 30:7215–7226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sung HH, Telley IA, Papadaki P, Ephrussi A, Surrey T, Rorth P (2008) Drosophila ensconsin promotes productive recruitment of Kinesin-1 to microtubules. Dev Cell 15:866–876

    Article  CAS  PubMed  Google Scholar 

  • Swiech L, Blazejczyk M, Urbanska M, Pietruszka P, Dortland BR, Malik AR, Wulf PS, Hoogenraad CC, Jaworski J (2011) CLIP-170 and IQGAP1 cooperatively regulate dendrite morphology. J Neurosci 31:4555–4568

    Article  CAS  PubMed  Google Scholar 

  • Szebenyi G, Bollati F, Bisbal M, Sheridan S, Faas L, Wray R, Haferkamp S, Nguyen S, Caceres A, Brady ST (2005) Activity-driven dendritic remodeling requires microtubule-associated protein 1A. Curr Biol 15:1820–1826

    Article  CAS  PubMed  Google Scholar 

  • Takahashi RH, Capetillo-Zarate E, Lin MT, Milner TA, Gouras GK (2013) Accumulation of intraneuronal beta-amyloid 42 peptides is associated with early changes in microtubule-associated protein 2 in neurites and synapses. PLoS One 8:e51965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takashima A, Murayama M, Murayama O, Kohno T, Honda T, Yasutake K, Nihonmatsu N, Mercken M, Yamaguchi H, Sugihara S et al (1998) Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc Natl Acad Sci U S A 95:9637–9641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takei Y, Kikkawa YS, Atapour N, Hensch TK, Hirokawa N (2015) Defects in synaptic plasticity, reduced NMDA-receptor transport, and instability of postsynaptic density proteins in mice lacking Microtubule-Associated Protein 1A. J Neurosci 35:15539–15554

    Article  CAS  PubMed  Google Scholar 

  • Takei Y, Kondo S, Harada A, Inomata S, Noda T, Hirokawa N (1997) Delayed development of nervous system in mice homozygous for disrupted microtubule-associated protein 1B (MAP1B) gene. J Cell Biol 137:1615–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takei Y, Teng J, Harada A, Hirokawa N (2000) Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J Cell Biol 150:989–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takemura R, Okabe S, Umeyama T, Kanai Y, Cowan NJ, Hirokawa N (1992) Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau. J Cell Sci 103(Pt 4):953–964

    CAS  PubMed  Google Scholar 

  • Teng J, Takei Y, Harada A, Nakata T, Chen J, Hirokawa N (2001) Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J Cell Biol 155:65–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terry-Lorenzo RT, Roadcap DW, Otsuka T, Blanpied TA, Zamorano PL, Garner CC, Shenolikar S, Ehlers MD (2005) Neurabin/protein phosphatase-1 complex regulates dendritic spine morphogenesis and maturation. Mol Biol Cell 16:2349–2362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terwel D, Dewachter I, Van Leuven F (2002) Axonal transport, tau protein, and neurodegeneration in Alzheimer’s disease. Neuromolecular Med 2:151–165

    Article  CAS  PubMed  Google Scholar 

  • Theurkauf WE, Vallee RB (1982) Molecular characterization of the cAMP-dependent protein kinase bound to microtubule-associated protein 2. J Biol Chem 257:3284–3290

    CAS  PubMed  Google Scholar 

  • Tischfield MA, Engle EC (2010) Distinct alpha- and beta-tubulin isotypes are required for the positioning, differentiation and survival of neurons: new support for the ‘multi-tubulin’ hypothesis. Biosci Rep 30:319–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tischfield MA, Baris HN, Wu C, Rudolph G, Van Maldergem L, He W, Chan WM, Andrews C, Demer JL, Robertson RL et al (2010) Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance. Cell 140:74–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tischfield MA, Cederquist GY, Gupta ML Jr, Engle EC (2011) Phenotypic spectrum of the tubulin-related disorders and functional implications of disease-causing mutations. Curr Opin Genet Dev 21:286–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tokuraku K, Noguchi TQ, Nishie M, Matsushima K, Kotani S (2007) An isoform of microtubule-associated protein 4 inhibits kinesin-driven microtubule gliding. J Biochem 141:585–591

    Article  CAS  PubMed  Google Scholar 

  • Tokuraku K, Okuyama S, Matsushima K, Ikezu T, Kotani S (2010) Distinct neuronal localization of microtubule-associated protein 4 in the mammalian brain. Neurosci Lett 484:143–147

    Article  CAS  PubMed  Google Scholar 

  • Tortosa E, Montenegro-Venegas C, Benoist M, Hartel S, Gonzalez-Billault C, Esteban JA, Avila J (2011) Microtubule-associated protein 1B (MAP1B) is required for dendritic spine development and synaptic maturation. J Biol Chem 286:40638–40648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tortosa E, Galjart N, Avila J, Sayas CL (2013) MAP1B regulates microtubule dynamics by sequestering EB1/3 in the cytosol of developing neuronal cells. EMBO J 32:1293–1306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trinczek B, Ebneth A, Mandelkow EM, Mandelkow E (1999) Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J Cell Sci 112(Pt 14):2355–2367

    CAS  PubMed  Google Scholar 

  • Tucker RP, Matus AI (1988) Microtubule-associated proteins characteristic of embryonic brain are found in the adult mammalian retina. Dev Biol 130:423–434

    Article  CAS  PubMed  Google Scholar 

  • Tucker RP, Binder LI, Matus AI (1988a) Differential localization of the high- and low-molecular weight variants of MAP2 in the developing retina. Brain Res 466:313–318

    Article  CAS  PubMed  Google Scholar 

  • Tucker RP, Binder LI, Matus AI (1988b) Neuronal microtubule-associated proteins in the embryonic avian spinal cord. J Comp Neurol 271:44–55

    Article  CAS  PubMed  Google Scholar 

  • Tucker RP, Garner CC, Matus A (1989) In situ localization of microtubule-associated protein mRNA in the developing and adult rat brain. Neuron 2:1245–1256

    Article  CAS  PubMed  Google Scholar 

  • Tucker KL, Meyer M, Barde YA (2001) Neurotrophins are required for nerve growth during development. Nat Neurosci 4:29–37

    Article  CAS  PubMed  Google Scholar 

  • Tymanskyj SR, Scales TM, Gordon-Weeks PR (2012) MAP1B enhances microtubule assembly rates and axon extension rates in developing neurons. Mol Cell Neurosci 49:110–119

    Article  CAS  PubMed  Google Scholar 

  • Ulloa L, Diaz-Nido J, Avila J (1993) Depletion of casein kinase II by antisense oligonucleotide prevents neuritogenesis in neuroblastoma cells. EMBO J 12:1633–1640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ulloa L, Ibarrola N, Avila J, Diez-Guerra FJ (1994a) Microtubule-associated protein 1B (MAP1B) is present in glial cells phosphorylated different than in neurones. Glia 10:266–275

    Article  CAS  PubMed  Google Scholar 

  • Ulloa L, Montejo de Garcini E, Gomez-Ramos P, Moran MA, Avila J (1994b) Microtubule-associated protein MAP1B showing a fetal phosphorylation pattern is present in sites of neurofibrillary degeneration in brains of Alzheimer’s disease patients. Brain Res Mol Brain Res 26:113–122

    Article  CAS  PubMed  Google Scholar 

  • Utreras E, Jimenez-Mateos EM, Contreras-Vallejos E, Tortosa E, Perez M, Rojas S, Saragoni L, Maccioni RB, Avila J, Gonzalez-Billault C (2008) Microtubule-associated protein 1B interaction with tubulin tyrosine ligase contributes to the control of microtubule tyrosination. Dev Neurosci 30:200–210

    Article  CAS  PubMed  Google Scholar 

  • Vaillant AR, Zanassi P, Walsh GS, Aumont A, Alonso A, Miller FD (2002) Signaling mechanisms underlying reversible, activity-dependent dendrite formation. Neuron 34:985–998

    Article  CAS  PubMed  Google Scholar 

  • Vale RD, Schnapp BJ, Reese TS, Sheetz MP (1985) Organelle, bead, and microtubule translocations promoted by soluble factors from the squid giant axon. Cell 40:559–569

    Article  CAS  PubMed  Google Scholar 

  • Vallee RB, Wall JS, Paschal BM, Shpetner HS (1988) Microtubule-associated protein 1C from brain is a two-headed cytosolic dynein. Nature 332:561–563

    Article  CAS  PubMed  Google Scholar 

  • Vallee RB, Williams JC, Varma D, Barnhart LE (2004) Dynein: an ancient motor protein involved in multiple modes of transport. J Neurobiol 58:189–200

    Article  CAS  PubMed  Google Scholar 

  • Vallee RB, Seale GE, Tsai JW (2009) Emerging roles for myosin II and cytoplasmic dynein in migrating neurons and growth cones. Trends Cell Biol 19:347–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandecandelaere A, Pedrotti B, Utton MA, Calvert RA, Bayley PM (1996) Differences in the regulation of microtubule dynamics by microtubule-associated proteins MAP1B and MAP2. Cell Motil Cytoskeleton 35:134–146

    Article  CAS  PubMed  Google Scholar 

  • Velazquez-Bernardino P, Garcia-Sierra F, Hernandez-Hernandez O, Bermudez de Leon M, Gourdon G, Gomes-Pereira M, Cisneros B (2012) Myotonic dystrophy type 1-associated CTG repeats disturb the expression and subcellular distribution of microtubule-associated proteins MAP1A, MAP2, and MAP6/STOP in PC12 cells. Mol Biol Rep 39:415–424

    Article  CAS  PubMed  Google Scholar 

  • Venoux M, Basbous J, Berthenet C, Prigent C, Fernandez A, Lamb NJ, Rouquier S (2008) ASAP is a novel substrate of the oncogenic mitotic kinase Aurora-A: phosphorylation on Ser625 is essential to spindle formation and mitosis. Hum Mol Genet 17:215–224

    Article  CAS  PubMed  Google Scholar 

  • Verhey KJ, Gaertig J (2007) The tubulin code. Cell Cycle 6:2152–2160

    Article  CAS  PubMed  Google Scholar 

  • Vershinin M, Carter BC, Razafsky DS, King SJ, Gross SP (2007) Multiple-motor based transport and its regulation by Tau. Proc Natl Acad Sci U S A 104:87–92

    Article  CAS  PubMed  Google Scholar 

  • Viereck C, Tucker RP, Matus A (1989) The adult rat olfactory system expresses microtubule-associated proteins found in the developing brain. J Neurosci 9:3547–3557

    CAS  PubMed  Google Scholar 

  • Villarroel-Campos D, Gonzalez-Billault C (2014) The MAP1B case: an old MAP that is new again. Dev Neurobiol 74:953–971

    Article  CAS  PubMed  Google Scholar 

  • von Massow A, Mandelkow EM, Mandelkow E (1989) Interaction between kinesin, microtubules, and microtubule-associated protein 2. Cell Motil Cytoskeleton 14:562–571

    Article  Google Scholar 

  • Voss AK, Thomas T, Gruss P (1998) Compensation for a gene trap mutation in the murine microtubule-associated protein 4 locus by alternative polyadenylation and alternative splicing. Dev Dyn 212:258–266

    Article  CAS  PubMed  Google Scholar 

  • Vouyiouklis DA, Brophy PJ (1995) Microtubule-associated proteins in developing oligodendrocytes: transient expression of a MAP2c isoform in oligodendrocyte precursors. J Neurosci Res 42:803–817

    Article  CAS  PubMed  Google Scholar 

  • Walczak CE, Gayek S, Ohi R (2013) Microtubule-depolymerizing kinesins. Annu Rev Cell Dev Biol 29:417–441

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Lundin VF, Millan I, Zeng A, Chen X, Yang J, Allen E, Chen N, Bach G, Hsu A et al (2012) Nemitin, a novel Map8/Map1s interacting protein with Wd40 repeats. PLoS One 7:e33094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW (1975) A protein factor essential for microtubule assembly. Proc Natl Acad Sci U S A 72:1858–1862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West RR, Tenbarge KM, Olmsted JB (1991) A model for microtubule-associated protein 4 structure. Domains defined by comparisons of human, mouse, and bovine sequences. J Biol Chem 266:21886–21896

    CAS  PubMed  Google Scholar 

  • Wiche G, Oberkanins C, Himmler A (1991) Molecular structure and function of microtubule-associated proteins. Int Rev Cytol 124:217–273

    Article  CAS  PubMed  Google Scholar 

  • Witte H, Neukirchen D, Bradke F (2008) Microtubule stabilization specifies initial neuronal polarization. J Cell Biol 180:619–632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolff S, Xiao Z, Wittau M, Sussner N, Stoter M, Knippschild U (2005) Interaction of casein kinase 1 delta (CK1 delta) with the light chain LC2 of microtubule associated protein 1A (MAP1A). Biochim Biophys Acta 1745:196–206

    Article  CAS  PubMed  Google Scholar 

  • Wu CC, Chawla F, Games D, Rydel RE, Freedman S, Schenk D, Young WG, Morrison JH, Bloom FE (2004) Selective vulnerability of dentate granule cells prior to amyloid deposition in PDAPP mice: digital morphometric analyses. Proc Natl Acad Sci U S A 101:7141–7146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao H, Wang H, Zhang X, Tu Z, Bulinski C, Khrapunovich-Baine M, Hogue Angeletti R, Horwitz SB (2012) Structural evidence for cooperative microtubule stabilization by Taxol and the endogenous dynamics regulator MAP4. ACS Chem Biol 7:744–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie R, Nguyen S, McKeehan K, Wang F, McKeehan WL, Liu L (2011) Microtubule-associated protein 1S (MAP1S) bridges autophagic components with microtubules and mitochondria to affect autophagosomal biogenesis and degradation. J Biol Chem 286:10367–10377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav S, Linstedt AD (2011) Golgi positioning. Cold Spring Harbor Perspect Biol 3:a005322

    Google Scholar 

  • Yamashita N, Morita A, Uchida Y, Nakamura F, Usui H, Ohshima T, Taniguchi M, Honnorat J, Thomasset N, Takei K et al (2007) Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. J Neurosci 27:12546–12554

    Article  CAS  PubMed  Google Scholar 

  • Yamashita N, Mosinger B, Roy A, Miyazaki M, Ugajin K, Nakamura F, Sasaki Y, Yamaguchi K, Kolattukudy P, Goshima Y (2011) CRMP5 (collapsin response mediator protein 5) regulates dendritic development and synaptic plasticity in the cerebellar Purkinje cells. J Neurosci 31:1773–1779

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi PS, Flynn GC, Marsh RL, Purich DL (1993) Reduction in microtubule dynamics in vitro by brain microtubule-associated proteins and by a microtubule-associated protein-2 second repeated sequence analogue. J Neurochem 60:817–826

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Sun XB, Wang HQ, Zhao H, Zhao XY, Xu YX, Guo JC, Zhu CQ (2010) Chronic restraint stress alters the expression and distribution of phosphorylated tau and MAP2 in cortex and hippocampus of rat brain. Brain Res 1347:132–141

    Article  CAS  PubMed  Google Scholar 

  • Yan XX, Cai Y, Zhang XM, Luo XG, Cai H, Rose GM, Patrylo PR (2012) BACE1 elevation is associated with aberrant limbic axonal sprouting in epileptic CD1 mice. Exp Neurol 235:228–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan J, Chao DL, Toba S, Koyasako K, Yasunaga T, Hirotsune S, Shen K (2013) Kinesin-1 regulates dendrite microtubule polarity in Caenorhabditis elegans. eLife 2:e00133

    Article  PubMed Central  PubMed  Google Scholar 

  • Yang HJ, Li YF, Zhang HT, Zhang FQ, Zhao N, Gong ZH, Luo ZP (2003) Up-regulation of microtubule-associated protein 4 and drebrin A mRNA expression by antidepressants in rat hippocampus following chronic stress. Neurosci Lett 351:206–208

    Article  CAS  PubMed  Google Scholar 

  • Yau KW, Schatzle P, Tortosa E, Pages S, Holtmaat A, Kapitein LC, Hoogenraad CC (2016) Dendrites in vitro and in vivo contain microtubules of opposite polarity and axon formation correlates with uniform plus-end-out microtubule orientation. J Neurosci 36:1071–1085

    Article  PubMed  PubMed Central  Google Scholar 

  • Yau KW, van Beuningen SF, Cunha-Ferreira I, Cloin BM, van Battum EY, Will L, Schatzle P, Tas RP, van Krugten J, Katrukha EA et al (2014) Microtubule minus-end binding protein CAMSAP2 controls axon specification and dendrite development. Neuron 82:1058–1073

    Article  CAS  PubMed  Google Scholar 

  • Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130:717–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye B, Kim JH, Yang L, McLachlan I, Younger S, Jan LY, Jan YN (2011) Differential regulation of dendritic and axonal development by the novel Kruppel-like factor Dar1. J Neurosci 31:3309–3319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu W, Qiang L, Solowska JM, Karabay A, Korulu S, Baas PW (2008) The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol Biol Cell 19:1485–1498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zalfa F, Giorgi M, Primerano B, Moro A, Di Penta A, Reis S, Oostra B, Bagni C (2003) The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112:317–327

    Article  CAS  PubMed  Google Scholar 

  • Zamora-Leon SP, Lee G, Davies P, Shafit-Zagardo B (2001) Binding of Fyn to MAP-2c through an SH3 binding domain. Regulation of the interaction by ERK2. J Biol Chem 276:39950–39958

    Article  CAS  PubMed  Google Scholar 

  • Zempel H, Mandelkow E (2014) Lost after translation: missorting of Tau protein and consequences for Alzheimer disease. Trends Neurosci 37:721–732

    Article  CAS  PubMed  Google Scholar 

  • Zempel H, Luedtke J, Kumar Y, Biernat J, Dawson H, Mandelkow E, Mandelkow EM (2013) Amyloid-beta oligomers induce synaptic damage via Tau-dependent microtubule severing by TTLL6 and spastin. EMBO J 32:2920–2937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Dong XP (2012) Dysfunction of microtubule-associated proteins of MAP2/tau family in Prion disease. Prion 6:334–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, Younger SH, Zimmerman S, Jan LY, Jan YN (2008) Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat Cell Biol 10:1172–1180

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Phebe Wulf for critically reading the manuscript. This work was supported by the Netherlands Organization for Scientific Research (NOW-ALW-VIDI, LCK; NWO-ALW-VICI, CCH); the Foundation for Fundamental Research on Matter (FOM, LCK, and CCH), which is part of the NWO; the Netherlands Organization for Health Research and Development (ZonMW-TOP, CCH); the European Research Council (ERC) (ERC-starting, LCK; ERC-consolidator, CCH); the Spanish Education Ministry (ET); and an FP7 EU Marie Curie postdoctoral fellowship (ET).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Casper C. Hoogenraad .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Japan

About this chapter

Cite this chapter

Tortosa, E., Kapitein, L.C., Hoogenraad, C.C. (2016). Microtubule Organization and Microtubule-Associated Proteins (MAPs). In: Emoto, K., Wong, R., Huang, E., Hoogenraad, C. (eds) Dendrites. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56050-0_3

Download citation

Publish with us

Policies and ethics