Abstract
Synaptic tagging and capture (STC) hypothesis has been receiving increasing attention because it reflects the heterosynaptic association of information processing during memory formation in the brain. Indeed, electrophysiological and behavioral studies suggest that STC is a better cellular model for memory formation than the conventional homosynaptic experiment. In STC, a short-lasting potentiation in one pathway becomes persistent when it is paired with a long-lasting potentiation in the other independent pathway. It has been proposed that the setting of a synapse-specific tag and the capture of nonsynapse-specific diffusible gene products by the tag determines the fate of each pathway. However, the mechanism of STC is still elusive and three major questions should be answered: 1. What is the tag and how does it modulate synapse-specific plasticity? 2. How does the tag capture gene products? 3. What are the gene products and how are they produced? Although several molecules and processes have been suggested to answer these questions, they only provide partial explanations about the phenomenon. Here, this chapter will discuss how PKA modulates synapse-specific neuronal activity by coordinating signaling molecules and processes through PKA anchoring proteins, and how anchored PKA is involved in the generation and capture of plasticity-related gene products. We will also introduce new findings on PKA-dependent presynaptic mechanisms and in vivo signatures of STC. Having PKA as a key molecule, the goal of this chapter is to provide a unified model of STC that addresses the key questions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aakalu G, Smith WB, Nguyen N et al (2001) Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30:489–502
Abel T, Nguyen PV, Barad M et al (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615–626
Alberini CM, Kandel ER (2015) The regulation of transcription in memory consolidation. Cold Spring Harb Perspect Biol 7:a021741. https://doi.org/10.1101/cshperspect.a021741
Auer RN, Jensen ML, Whishaw IQ (1989) Neurobehavioral deficit due to ischemic brain damage limited to half of the CA1 sector of the hippocampus. J Neurosci 9:1641–1647
Baillie GS, Sood A, McPhee I et al (2003) beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci USA 100:940–945. https://doi.org/10.1073/pnas.262787199
Ballarini F, Moncada D, Martinez MC et al (2009) Behavioral tagging is a general mechanism of long-term memory formation. Proc Natl Acad Sci USA 106:14599–14604
Baltaci SB, Mogulkoc R, Baltaci AK (2019) Molecular mechanisms of early and late LTP. Neurochem Res 44:281–296. https://doi.org/10.1007/s11064-018-2695-4
Banke TG, Bowie D, Lee H et al (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20:89–102
Barad M, Bourtchouladze R, Winder DG et al (1998) Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci USA 95:15020–15025
Barco A, Alarcon JM, Kandel ER (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689–703
Barco A, Patterson SL, Patterson S et al (2005) Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 48:123–137
Barco A, Lopez de Armentia M, Alarcon JM (2008) Synapse-specific stabilization of plasticity processes: the synaptic tagging and capture hypothesis revisited 10 years later. Neurosci Biobehav Rev 32:831–851. https://doi.org/10.1016/j.neubiorev.2008.01.002
Barondes SH, Jarvik ME (1964) The influence of Actinomycin-D on brain RNA synthesis and on memory. J Neurochem 11:187–195
Benarroch EE (2013) HCN channels: function and clinical implications. Neurology 80:304–310
Bernabeu R, Bevilaqua L, Ardenghi P et al (1997) Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc Natl Acad Sci USA 94:7041–7046
Bliss TV, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232:357–374
Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356
Blitzer RD, Connor JH, Brown GP et al (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280:1940–1942
Bolshakov VY, Golan H, Kandel ER, Siegelbaum SA (1997) Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron 19(3):635–651. https://doi.org/10.1016/s0896-6273(00)80377-3. PMID: 9331354.
Brandon NJ, Jovanovic JN, Colledge M et al (2003) A-kinase anchoring protein 79/150 facilitates the phosphorylation of GABA(A) receptors by cAMP-dependent protein kinase via selective interaction with receptor beta subunits. Mol Cell Neurosci 22:87–97
Bregman DB, Bhattacharyya N, Rubin CS (1989) High affinity binding protein for the regulatory subunit of cAMP-dependent protein kinase II-B. Cloning, characterization, and expression of cDNAs for rat brain P150. J Biol Chem 264:4648–4656
Carr DW, Stofko-Hahn RE, Fraser ID et al (1992) Localization of the cAMP-dependent protein kinase to the postsynaptic densities by A-kinase anchoring proteins. Characterization of AKAP 79. J Biol Chem 267:16816–16823
Casadio A, Martin KC, Giustetto M et al (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99:221–237
Chavez-Noriega LE, Stevens CF (1994) Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J Neurosci 14(1):310–317. https://doi.org/10.1523/JNEUROSCI.14-01-00310.1994. PMID: 7506766; PMCID: PMC6576865
Chen LY, Rex CS, Casale MS et al (2007) Changes in synaptic morphology accompany actin signaling during LTP. J Neurosci 27:5363–5372
Coghlan VM, Perrino BA, Howard M et al (1995) Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science 267:108–111
Colledge M, Scott JD (1999) AKAPs: from structure to function. Trends Cell Biol 9:216–221
Colledge M, Dean RA, Scott GK et al (2000) Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron 27:107–119
Connor SA, Wang YT, Nguyen PV (2011) Activation of {beta}-adrenergic receptors facilitates heterosynaptic translation-dependent long-term potentiation. J Physiol 589:4321–4340
Daaka Y, Luttrell LM, Lefkowitz RJ (1997) Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature 390:88–91
de Carvalho MJ, Benetti F, Izquierdo I (2013) Behavioral tagging of extinction learning. Proc Natl Acad Sci USA 110:1071–1076. https://doi.org/10.1073/pnas.1220875110
Esteban JA, Shi S-H, Wilson C et al (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136–143. https://doi.org/10.1038/nn997
Feliciello A, Giuliano P, Porcellini A et al (1996) The v-Ki-Ras oncogene alters cAMP nuclear signaling by regulating the location and the expression of cAMP-dependent protein kinase IIbeta. J Biol Chem 271:25350–25359
Feliciello A, Li Y, Avvedimento EV et al (1997) A-kinase anchor protein 75 increases the rate and magnitude of cAMP signaling to the nucleus. Curr Biol 7:1011–1014
Fraser ID, Cong M, Kim J et al (2000) Assembly of an A kinase-anchoring protein-beta(2)-adrenergic receptor complex facilitates receptor phosphorylation and signaling. Curr Biol 10:409–412
Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533–536. https://doi.org/10.1038/385533a0
Frey U, Morris RG (1998) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37:545–552
Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57–65
Frey U, Matthies H, Reymann KG (1991) The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci Lett 129:111–114
Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661–1664
Frey U, Frey S, Schollmeier F, Krug M (1996) Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J Physiol 490(Pt 3):703–711
Gao T, Yatani A, Dell’Acqua ML et al (1997) cAMP-dependent regulation of cardiac L-type Ca2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron 19:185–196
Garner CC, Tucker RP, Matus A (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336:674–677. https://doi.org/10.1038/336674a0
Gelinas JN, Nguyen PV (2005) Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J Neurosci 25:3294–3303
Gelinas JN, Tenorio G, Lemon N et al (2008) Beta-adrenergic receptor activation during distinct patterns of stimulation critically modulates the PKA-dependence of LTP in the mouse hippocampus. Learn Mem 15:281–289
Gelman IH, Lee K, Tombler E et al (1998) Control of cytoskeletal architecture by the src-suppressed C kinase substrate, SSeCKS. Cell Motil Cytoskeleton 41:1–17. https://doi.org/10.1002/(SICI)1097-0169(1998)41:1<1::AID-CM1>3.0.CO;2-J
Gerits N, Kostenko S, Shiryaev A et al (2008) Relations between the mitogen-activated protein kinase and the cAMP-dependent protein kinase pathways: comradeship and hostility. Cell Signal 20:1592–1607
Gomez LL, Alam S, Smith KE et al (2002) Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin. J Neurosci 22:7027–7044
Greengard P, Jen J, Nairn AC, Stevens CF (1991) Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science 253:1135–1138. https://doi.org/10.1126/science.1716001
Gu J, Lee CW, Fan Y et al (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci 13:1208–1215
Harada A, Teng J, Takei Y et al (2002) MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 158:541–549. https://doi.org/10.1083/jcb.200110134
Hasegawa Y, Mukai H, Asashima M et al (2014) Acute modulation of synaptic plasticity of pyramidal neurons by activin in adult hippocampus. Front Neural Circuits 8:56. https://doi.org/10.3389/fncir.2014.00056
Havekes R, Canton DA, Park AJ et al (2012) Gravin orchestrates protein kinase A and β2-adrenergic receptor signaling critical for synaptic plasticity and memory. J Neurosci 32:18137–18149. https://doi.org/10.1523/JNEUROSCI.3612-12.2012
Hoshi N, Zhang J-S, Omaki M et al (2003) AKAP150 signaling complex promotes suppression of the M-current by muscarinic agonists. Nat Neurosci 6:564–571
Hou Y-Y, Lu B, Li M et al (2009) Involvement of actin rearrangements within the amygdala and the dorsal hippocampus in aversive memories of drug withdrawal in acute morphine-dependent rats. J Neurosci 29:12244–12254
Huang YY, Kandel ER (1994) Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1:74–82. https://doi.org/10.1101/lm.1.1.74
Huang T, McDonough CB, Abel T (2006) Compartmentalized PKA signaling events are required for synaptic tagging and capture during hippocampal late-phase long-term potentiation. Eur J Cell Biol 85:635–642. https://doi.org/10.1016/j.ejcb.2006.02.005
Impey S, Mark M, Villacres EC et al (1996) Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973–982
Impey S, Obrietan K, Wong ST et al (1998a) Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869–883
Impey S, Smith DM, Obrietan K et al (1998b) Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1:595–601
Ji Y, Pang PT, Feng L, Lu B (2005) Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat Neurosci 8:164–172. https://doi.org/10.1038/nn1381
Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402–1406
Kang H, Jia LZ, Suh KY et al (1996) Determinants of BDNF-induced hippocampal synaptic plasticity: role of the Trk B receptor and the kinetics of neurotrophin delivery. Learn Mem 3:188–196
Kelleher RJ, Govindarajan A, Jung H-Y et al (2004a) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467–479
Kelleher RJ, Govindarajan A, Tonegawa S (2004b) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44:59–73
Khuchua Z, Wozniak DF, Bardgett ME et al (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
Kim M, Park AJAJAJ, Havekes R et al (2011) Colocalization of protein kinase A with adenylyl cyclase enhances protein kinase A activity during induction of long-lasting long-term-potentiation. PLoS Comput Biol 7:e1002084. https://doi.org/10.1371/journal.pcbi.1002084
Kramár EA, Lin B, Rex CS et al (2006) Integrin-driven actin polymerization consolidates long-term potentiation. Proc Natl Acad Sci USA 103:5579–5584
Krichevsky AM, Kosik KS (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32:683–696
Krucker T, Siggins GR, Halpain S (2000) Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci USA 97:6856–6861
Kuczewski N, Porcher C, Gaiarsa J-L (2010) Activity-dependent dendritic secretion of brain-derived neurotrophic factor modulates synaptic plasticity. Eur J Neurosci 32:1239–1244
Lamprecht R, LeDoux J (2004) Structural plasticity and memory. Nat Rev Neurosci 5:45–54
Laurent A-C, Breckler M, Berthouze M, Lezoualc’h F (2012) Role of Epac in brain and heart. Biochem Soc Trans 40:51–57
Liao L, Pilotte J, Xu T et al (2007) BDNF induces widespread changes in synaptic protein content and up-regulates components of the translation machinery: an analysis using high-throughput proteomics. J Proteome Res 6:1059–1071
Lin X, Gelman IH (2002) Calmodulin and cyclin D anchoring sites on the Src-suppressed C kinase substrate, SSeCKS. Biochem Biophys Res Commun 290:1368–1375
Lin X, Tombler E, Nelson PJ et al (1996) A novel src- and ras-suppressed protein kinase C substrate associated with cytoskeletal architecture. J Biol Chem 271:28430–28438
Lin B, Kramár EA, Bi X et al (2005) Theta stimulation polymerizes actin in dendritic spines of hippocampus. J Neurosci 25:2062–2069
Lisman J (2003) Actin’s actions in LTP-induced synapse growth. Neuron 38:361–362
Lu Y, Ji Y, Ganesan S et al (2011) TrkB as a potential synaptic and behavioral tag. J Neurosci 31:11762–11771
Malinow R, Mainen ZF, Hayashi Y (2000) LTP mechanisms: from silence to four-lane traffic. Curr Opin Neurobiol 10:352–357
Martin KC, Kosik KS (2002) Synaptic tagging – who’s it? Nat Rev Neurosci 3:813–820
Martin KC, Casadio A, Zhu H et al (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927–938
Matsushita M, Tomizawa K, Moriwaki A et al (2001) A high-efficiency protein transduction system demonstrating the role of PKA in long-lasting long-term potentiation. J Neurosci 21:6000–6007
Matthies H, Reymann KG (1993) Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation. Neuroreport 4:712–714
Mayford M, Baranes D, Podsypanina K, Kandel ER (1996) The 3′-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc Natl Acad Sci USA 93:13250–13255
Mayford M, Siegelbaum S, Kandel ER (2012) Synapses and memory storage. Cold Spring Harb Perspect Biol 4:a005751
Meiri N, Rosenblum K (1998) Lateral ventricle injection of the protein synthesis inhibitor anisomycin impairs long-term memory in a spatial memory task. Brain Res 789:48–55
Messaoudi E, Ying S-W, Kanhema T et al (2002) Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J Neurosci 22:7453–7461
Michel JJC, Scott JD (2002) AKAP mediated signal transduction. Annu Rev Pharmacol Toxicol 42:235–257
Moncada D, Viola H (2007) Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J Neurosci 27:7476–7481
Moncada D, Ballarini F, Martinez MC et al (2011) Identification of transmitter systems and learning tag molecules involved in behavioral tagging during memory formation. Proc Natl Acad Sci USA 108:12931–12936. https://doi.org/10.1073/pnas.1104495108
Morris RGMG, Anderson E, Lynch GSS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774–776. https://doi.org/10.1038/319774a0
Nadella KS, Saji M, Jacob NK et al (2009) Regulation of actin function by protein kinase A-mediated phosphorylation of Limk1. EMBO Rep 10:599–605
Nauert JB, Klauck TM, Langeberg LK, Scott JD (1997) Gravin, an autoantigen recognized by serum from myasthenia gravis patients, is a kinase scaffold protein. Curr Biol 7:52–62
Navakkode S, Sajikumar S, Frey JU (2004) The type IV-specific phosphodiesterase inhibitor rolipram and its effect on hippocampal long-term potentiation and synaptic tagging. J Neurosci 24:7740–7744
Nayak A, Zastrow DJ, Lickteig R et al (1998) Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394:680–683. https://doi.org/10.1038/29305
Nguyen PV, Kandel ER (1997) Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 4:230–243. https://doi.org/10.1101/lm.4.2.230
Nguyen PV, Woo NH (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 71:401–437
Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104–1107
Nie T, McDonough CB, Huang T et al (2007) Genetic disruption of protein kinase A anchoring reveals a role for compartmentalized kinase signaling in theta-burst long-term potentiation and spatial memory. J Neurosci 27:10278–10288. https://doi.org/10.1523/JNEUROSCI.1602-07.2007
Ostroff LE, Fiala JC, Allwardt B, Harris KM (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35:535–545
Otmakhov N, Khibnik L, Otmakhova N et al (2004) Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J Neurophysiol 91:1955–1962
Ouyang Y, Rosenstein A, Kreiman G et al (1999) Tetanic stimulation leads to increased accumulation of Ca(2+)/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J Neurosci 19:7823–7833
Park AJ, Havekes R, Choi JH et al (2014) A presynaptic role for PKA in synaptic tagging and memory. Neurobiol Learn Mem 114:101–112. https://doi.org/10.1016/j.nlm.2014.05.005. PMID: 24882624; PMCID: PMC4143446
Park AJ, Havekes R, Fu X et al (2017) Learning induces the translin/trax RNase complex to express activin receptors for persistent memory. elife 6. https://doi.org/10.7554/eLife.27872
Park AJ, Shetty MS, Baraban JM, Abel T (2020) Selective role of the translin/trax RNase complex in hippocampal synaptic plasticity. Mol Brain 13:145. https://doi.org/10.1186/s13041-020-00691-5
Park AJ, Harris AZ, Martyniuk KM et al (2021) Reset of hippocampal-prefrontal circuitry facilitates learning. Nature 591:615–619. https://doi.org/10.1038/s41586-021-03272-1
Patterson SL, Pittenger C, Morozov A et al (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123–140
Pittenger C, Kandel E (1998) A genetic switch for long-term memory. C R Acad Sci III 321:91–96
Ramachandran B, Frey JU (2009) Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J Neurosci 29:12167–12173
Redondo RL, Morris RGM (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12:17–30
Redondo RL, Okuno H, Spooner PA et al (2010) Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30:4981–4989
Rex CS, Lin C-Y, Kramár EA et al (2007) Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci 27:3017–3029
Richter-Levin G, Akirav I (2003) Emotional tagging of memory formation--in the search for neural mechanisms. Brain Res Brain Res Rev 43:247–256
Roberson ED, English JD, Adams JP et al (1999) The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19:4337–4348
Rosenmund C, Carr DW, Bergeson SE et al (1994) Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons. Nature 368:853–856
Sajikumar S, Frey JU (2004) Resetting of “synaptic tags” is time- and activity-dependent in rat hippocampal CA1 in vitro. Neuroscience 129:503–507
Sajikumar S, Li Q, Abraham WC, Xiao ZC (2009) Priming of short-term potentiation and synaptic tagging/capture mechanisms by ryanodine receptor activation in rat hippocampal CA1. Learn Mem 16:178–186. https://doi.org/10.1101/lm.1255909
Sánchez C, Díaz-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
Santos AR, Comprido D, Duarte CB (2010) Regulation of local translation at the synapse by BDNF. Prog Neurobiol 92:505–516
Schuman EM (1997) Synapse specificity and long-term information storage. Neuron 18:339–342
Selbach O, Brown RE, Haas HL (1998) Long-term increase of hippocampal excitability by histamine and cyclic AMP. Neuropharmacology 36:1539–1548
Shen K, Meyer T (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284:162–166
Sheng M, Lee SH (2001) AMPA receptor trafficking and the control of synaptic transmission. Cell 105:825–828
Shih M, Lin F, Scott JD et al (1999) Dynamic complexes of beta2-adrenergic receptors with protein kinases and phosphatases and the role of gravin. J Biol Chem 274:1588–1595. https://doi.org/10.1074/jbc.274.3.1588
Shoji-Kasai Y, Ageta H, Hasegawa Y et al (2007) Activin increases the number of synaptic contacts and the length of dendritic spine necks by modulating spinal actin dynamics. J Cell Sci 120:3830–3837. https://doi.org/10.1242/jcs.012450
Skeberdis VA, Chevaleyre V, Lau CG et al (2006) Protein kinase A regulates calcium permeability of NMDA receptors. Nat Neurosci 9:501–510
Slack JR, Walsh C (1995) Effects of a cAMP analogue simulate the distinct components of long-term potentiation in CA1 region of rat hippocampus. Neurosci Lett 201:25–28
Snyder EM, Colledge M, Crozier R a., et al (2005) Role for A kinase-anchoring proteins (AKAPS) in glutamate receptor trafficking and long term synaptic depression. J Biol Chem 280:16962–16968. https://doi.org/10.1074/jbc.M409693200
Steward O, Halpain S (1999) Lamina-specific synaptic activation causes domain-specific alterations in dendritic immunostaining for MAP2 and CAM kinase II. J Neurosci 19:7834–7845
Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299–325
Streb JW, Kitchen CM, Gelman IH, Miano JM (2004) Multiple promoters direct expression of three AKAP12 isoforms with distinct subcellular and tissue distribution profiles. J Biol Chem 279:56014–56023. https://doi.org/10.1074/jbc.M408828200
Tao X, Finkbeiner S, Arnold DB et al (1998) Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709–726
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
Tongiorgi E, Righi M, Cattaneo A (1997) Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17:9492–9505
Tsien JZ, Huerta PT, Tonegawa S (1996) The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87:1327–1338
Vecsey CG, Baillie GS, Jaganath D et al (2009) Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461:1122–1125. https://doi.org/10.1038/nature08488
Vecsey CG, Huang T, Abel T (2018) Sleep deprivation impairs synaptic tagging in mouse hippocampal slices. Neurobiol Learn Mem 154:136–140. https://doi.org/10.1016/j.nlm.2018.03.016
Wang DO, Martin KC, Zukin RS (2010a) Spatially restricting gene expression by local translation at synapses. Trends Neurosci 33:173–182
Wang S-H, Redondo RL, Morris RGM (2010b) Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci USA 107:19537–19542
Willoughby D, Wong W, Schaack J et al (2006) An anchored PKA and PDE4 complex regulates subplasmalemmal cAMP dynamics. EMBO J 25:2051–2061
Woo NH, Abel T, Nguyen PV (2002) Genetic and pharmacological demonstration of a role for cyclic AMP-dependent protein kinase-mediated suppression of protein phosphatases in gating the expression of late LTP. Eur J Neurosci 16:1871–1876. https://doi.org/10.1046/j.1460-9568.2002.02260.x
Wu XQ, Petrusz P, Hecht NB (1999) Testis-brain RNA-binding protein (Translin) is primarily expressed in neurons of the mouse brain. Brain Res 819:174–178
Yao Y, Kelly MT, Sajikumar S et al (2008) PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J Neurosci 28:7820–7827
Yoshii A, Constantine-Paton M (2007) BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat Neurosci 10:702–711
Young JZ, Nguyen PV (2005) Homosynaptic and heterosynaptic inhibition of synaptic tagging and capture of long-term potentiation by previous synaptic activity. J Neurosci 25:7221–7231
Young JZ, Isiegas C, Abel T, Nguyen PV (2006) Metaplasticity of the late-phase of long-term potentiation: a critical role for protein kinase A in synaptic tagging. Eur J Neurosci 23:1784–1794. https://doi.org/10.1111/j.1460-9568.2006.04707.x
Zakharenko SS, Patterson SL, Dragatsis I, Zeitlin SO, Siegelbaum SA, Kandel ER, Morozov A (2003) Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39(6):975–990. https://doi.org/10.1016/s0896-6273(03)00543-9. PMID: 12971897.
Zhong H, Sia G-M, Sato TR et al (2009) Subcellular dynamics of type II PKA in neurons. Neuron 62:363–374
Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950–2967
Acknowledgments
We thank Ted Huang for the scheme in Fig. 6.1. This work was supported by the New Faculty Startup Fund from Seoul National University, Creative-Pioneering Researchers Program through Seoul National University, POSCO Science Fellowship of POSCO TJ Park Foundation, the National Research Foundation of Korea [RS-2023-00211417].
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Park, A.J. (2024). PKA Anchoring and Synaptic Tagging and Capture. In: Sajikumar, S., Abel, T. (eds) Synaptic Tagging and Capture. Springer, Cham. https://doi.org/10.1007/978-3-031-54864-2_6
Download citation
DOI: https://doi.org/10.1007/978-3-031-54864-2_6
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-54863-5
Online ISBN: 978-3-031-54864-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)