. 2024 Jan 3;112(1):93-112.e10.

doi: 10.1016/j.neuron.2023.11.008. Epub 2023 Dec 13.

Astrocyte growth is driven by the Tre1/S1pr1 phospholipid-binding G protein-coupled receptor

Affiliations

¹ Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA. Electronic address: chenjk@unc.edu.
² Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA.
³ Departments of Otolaryngology and Neuroscience and Physiology, Neuroscience Institute, New York University Grossman School of Medicine, New York, NY 10016, USA.
⁴ Neuroscience Institute, NYU Medical Center, New York, NY 10016, USA.
⁵ Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA. Electronic address: monk@ohsu.edu.
⁶ Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA. Electronic address: freemmar@ohsu.edu.

PMID: 38096817
PMCID: PMC11073822
DOI: 10.1016/j.neuron.2023.11.008

Astrocyte growth is driven by the Tre1/S1pr1 phospholipid-binding G protein-coupled receptor

Jiakun Chen et al. Neuron. 2024.

. 2024 Jan 3;112(1):93-112.e10.

doi: 10.1016/j.neuron.2023.11.008. Epub 2023 Dec 13.

Authors

Affiliations

¹ Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA. Electronic address: chenjk@unc.edu.
² Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA.
³ Departments of Otolaryngology and Neuroscience and Physiology, Neuroscience Institute, New York University Grossman School of Medicine, New York, NY 10016, USA.
⁴ Neuroscience Institute, NYU Medical Center, New York, NY 10016, USA.
⁵ Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA. Electronic address: monk@ohsu.edu.
⁶ Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA. Electronic address: freemmar@ohsu.edu.

PMID: 38096817
PMCID: PMC11073822
DOI: 10.1016/j.neuron.2023.11.008

Abstract

Astrocytes play crucial roles in regulating neural circuit function by forming a dense network of synapse-associated membrane specializations, but signaling pathways regulating astrocyte morphogenesis remain poorly defined. Here, we show the Drosophila lipid-binding G protein-coupled receptor (GPCR) Tre1 is required for astrocytes to establish their intricate morphology in vivo. The lipid phosphate phosphatases Wunen/Wunen2 also regulate astrocyte morphology and, via Tre1, mediate astrocyte-astrocyte competition for growth-promoting lipids. Loss of s1pr1, the functional analog of Tre1 in zebrafish, disrupts astrocyte process elaboration, and live imaging and pharmacology demonstrate that S1pr1 balances proper astrocyte process extension/retraction dynamics during growth. Loss of Tre1 in flies or S1pr1 in zebrafish results in defects in simple assays of motor behavior. Tre1 and S1pr1 are thus potent evolutionarily conserved regulators of the elaboration of astrocyte morphological complexity and, ultimately, astrocyte control of behavior.

Keywords: Drosophila; S1pr1; Tre1 GPCR; astrocyte; lipid phosphate phosphatase; morphogenesis; zebrafish.

PubMed Disclaimer

Conflict of interest statement

Declaration of interests The authors declare no competing interests.

Figures

**Figure 1.. *Drosophila* Tre1 regulates astrocyte fine process infiltration autonomously in astrocytes**
(A) Astrocytes labeled with membrane marker α-Gat antibody (green) and synaptic neuropil with α-Brp (blue) in the adult *Drosophila* brain antennal lobe (AL) in control (N=5) and *Tre1*^attP mutants (N=8). Insets show enlarged views to highlight the astrocyte membrane infiltration differences observed in control and *Tre1*^attP mutants. N, number of animals. Scale bars, 20 µm and 5 µm (insets). (B) *alrm-Gal4 UAS-mCD8-GFP*-labeled astrocytes (green) and the neuropil (blue) in control (N=5) and *Tre1*^attP mutant (N=4) protocerebrum. Dashed lines mark the mushroom body. (C) Quantification of Gat-labeled (green) astrocyte membrane coverage area percentage in the AL as shown in (A). Data points represent an independent region-of-interest (ROI) in each AL. N, number of animals. ****, p<0.0001; unpaired t test. Error bars, mean values ± S.D. (D) Quantification of GFP-labeled (green) astrocyte membrane coverage area percentage in the MB as shown in (B). Data points represent an independent region-of-interest (ROI) in each AL. N, number of animals. ****, p<0.0001; unpaired t test. Error bars, mean values ± S.D. (E) Images of single-cell astrocytes labeled with membrane marker myrGFP (green) using the FLP-out system and the representative IMARIS 3D-rendering surface (grey) in control and *Tre1*^attP mutants. Scale bar, 20 µm. (F) Quantification of individual astrocyte volumes in control (N=17) and *Tre1*^attP mutants (N=15), related to (E). Data points represent single astrocytes. N, number of animals. ****, p<0.0001; unpaired t test. Error bars, mean values ± S.D. (G) *Tre1*^Gal4-expressing mCD8-mCherry cell membrane (magenta) with astrocyte-specific *GMR25H07-LexA 13xLexAop2-mCD8-GFP*-labeled astrocyte membrane (green) in the ALs (N=7), and the synaptic neuropil is labeled by α-Brp (blue). N, number of animals. Scale bar, 20 µm. (H) Images of AL astrocyte membrane surface labeled with *alrm-Gal4 UAS-mCD8-GFP* (green) and neuropil by α-Brp (blue) in control (N=9), *Tre1*^KK102307 *RNAi* (N=10), and *Tre1*^HMS00599 *RNAi* (N=10). N, number of animals. Scale bar, 20 µm. (I) Images of FLP-out approach generated mosaic astrocyte clones labeled by mCD8-mCherry (magenta) in control or *Tre1*^KK102307 *RNAi* in adjacent to neighboring WT mCD8-GFP-expressing astrocytes (green). Dashed lines mark the boundaries of mCD8-mCherry-labeled astrocytes at a single-Z plane. Representative of several experimental repeats. Scale bar, 20 µm. (J) Images of single-cell astrocytes labeled with mCD8-mCherry (magenta) and the representative IMARIS 3D-rendering surface (grey) in control and *Tre1*^KK102307 *RNAi*. Scale bar, 20 µm. (K) Quantification of individual astrocyte volumes in control (N=16) and *Tre1*^KK102307 *RNAi* (N=22), related to (J). Data points represent single astrocytes. N, number of animals. ****, p<0.0001; unpaired t test. Error bars, mean values ± S.D. (L) Images of single-cell astrocytes labeled with mCD8-mCherry (magenta) and the representative IMARIS 3D-rendering surface (grey) in control and *Tre1*^HMS00599 *RNAi*. Scale bar, 20 µm. (M) Quantification of individual astrocyte volumes in control (N=7) and *Tre1*^HMS00599 *RNAi* (N=10), related to (L). Data points represent single astrocytes. N, number of animals. ****, p<0.0001; unpaired t test. Error bars, mean values ± S.D. See also Figure S1, S2.

**Figure 2.. Tre1 controls astrocyte morphology via the NPIIY motif but not the NRY motif**
(A) Schematics of Tre1 GPCR with the conserved NRY and NPIIY motifs and the *UAS*-driven transgenic constructs. (B) Images of AL astrocytes labeled by *alrm-Gal4 UAS-mCD8-GFP* (green) and the neuropil by α-Brp (blue) in WT control (N=6) and in the *Tre1*^attP mutant backgrounds either alone (N=11) or that co-express *UAS-Tre1* (N=8), *UAS-Tre1*^NAY (N=8), *UAS-Tre1*^AAIIY (N=11), *UAS-Tre1*^NAY,AAIIY (N=10). Insets show enlarged views to highlight the astrocyte membrane infiltration differences observed in different experimental conditions. N, number of animals. Scale bars, 20 µm and 5 µm (insets). (C) Images of astrocytes labeled by mCD8-GFP (green) with FLP-out clones expressing mCD8-mCherry (magenta) in the contexts of WT control or *Tre1*^attP mutants that also express various forms of *Tre1* transgenic constructs. Dashed lines mark the boundaries of mCD8-mCherry-labeled astrocytes at a single-Z plane. Representative of several experimental repeats. Scale bar, 20 µm. (D) Images of single-cell astrocytes labeled with mCD8-mCherry (magenta) and the representative IMARIS 3D-rendering surface (grey) in WT control and in the *Tre1*^attP mutant backgrounds that express various *Tre1* transgenic constructs. Scale bar, 20 µm. (E) Quantification of individual astrocyte volumes in the corresponding experimental conditions as shown in (D). N, number of animals. WT control, N=8; *Tre1*^attP, N=11; *Tre1*^attP + *Tre1*, N=16; *Tre1*^attP + *Tre1*^NAY, N=16; *Tre1*^attP + *Tre1*^AAIIY, N=20; *Tre1*^attP + *Tre1*^NAY,AAIIY, N=16. Data points represent single astrocytes. N, number of animals. ns, not significant; **, p<0.01; ****, p<0.0001; one-way ANOVA with multiple comparisons. Error bars, mean values ± S.D. See also Figure S3.

**Figure 3.. Tre1 balances Rac1 activity to govern proper astrocyte growth**
(A) Images of astrocytes labeled by mCD8-GFP (green) with FLP-out clones expressing mCD8-mCherry (magenta) in the WT backgrounds that also express *UAS-Rac1.N17* or *UAS-Rac1.W*, and Brp labels the neuropil (blue). Dashed lines mark the boundaries of mCD8-mCherry-labeled astrocytes at a single-Z plane. Representative of several experimental repeats. Scale bar, 20 µm. (B) Images of single-cell astrocytes labeled with mCD8-mCherry (magenta) and the representative IMARIS 3D-rendering surface (grey) in WT backgrounds that express *Rac1.N17* or *Rac1.W*. Scale bar, 20 µm. (C) Quantification of individual astrocyte volumes in (B). Data points represent each single astrocyte. N, number of animals. WT control, N=12; *Rac1.N17*, N=11; *Rac1.W*, N=12. ****, p<0.0001; one-way ANOVA with multiple comparisons. Error bars, mean values ± S.D. (D) Images of AL astrocyte membrane labeled with *alrm-Gal4 UAS-mCD8-GFP* (green) and neuropil with α-Brp (blue) in WT control (N=8), and in the *Tre1*^attP mutant backgrounds that either alone (N=8) or co-express *UAS-Rac1.N17* (N=7), *UAS-Rac1.W* (N=8). N, number of animals. Scale bar, 20 µm. (E) Images of astrocytes labeled by mCD8-GFP (green) with FLP-out clones expressing mCD8-mCherry (magenta) in the contexts of WT control or *Tre1*^attP mutants that also express *UAS-Rac1.N17* or *UAS-Rac1.W*. Dashed lines mark the boundaries of mCD8-mCherry-labeled astrocytes at a single-Z plane. Representative of several experimental repeats. Scale bar, 20 µm. (F) Images of single-cell astrocytes labeled with mCD8-mCherry (magenta) and the representative IMARIS 3D-rendering surface (grey) in WT control and in the *Tre1*^attP mutant backgrounds that express *Rac1.N17* or *Rac1.W*. Scale bar, 20 µm. (G) Quantification of individual astrocyte volumes in (F). Data points represent single astrocytes. N, number of animals. WT control, N=12; *Tre1*^attP, N=12; *Tre1*^attP + *Rac1.N17*, N=15; *Tre1*^attP + *Rac1.W*, N=13. ****, p<0.0001; one-way ANOVA with multiple comparisons. Error bars, mean values ± S.D. See also Figure S4.

**Figure 4.. Tre1 regulates the actin cytoskeleton during astrocyte morphogenesis**
(A) Images of single-cell astrocytes labeled with actin marker Lifeact-GFP.W (green) and the representative IMARIS 3D-rendering filament structures (grey) in WT control and in the *Tre1*^attP mutant backgrounds either alone or that co-express *Tre1* and *Tre1*^NAY,AAIIY constructs. Scale bar, 20 µm. (B-E) Quantification of single-cell astrocyte actin cytoskeletal branch level (B), branch points (C), total length (D), and distribution of mean diameter (E) in WT control (N=8), *Tre1*^attP (N=10), *Tre1*^attP + *Tre1* (N=12), and *Tre1*^attP + *Tre1*^NAY,AAIIY (N=10), related to (A). N, number of animals. Data points represent single astrocytes. ns, not significant; *, p<0.05; **, p<0.01; ****, p<0.0001; one-way ANOVA with multiple comparisons. Error bars, mean values ± S.D. (F) Images of single-cell astrocytes labeled with Lifeact-GFP.W (green) and the representative IMARIS 3D-rendering filament structures (grey) in WT control and in the *Tre1*^attP mutant backgrounds that express *Rac1.N17* or *Rac1.W*. Scale bar, 20 µm. (G-J) Quantification of single-cell astrocyte cytoskeletal branch level (G), branch points (H), total length (I), and distribution of mean diameter (J) in WT control (N=12), *Tre1*^attP (N=16), *Tre1*^attP + *Rac1.N17* (N=19), and *Tre1*^attP + *Rac1.W* (N=14), related to (F). N, number of animals. Data points represent single astrocytes. ns, not significant; *, p<0.05; ***, p<0.001; ****, p<0.0001; one-way ANOVA with Multiple comparisons. Error bars, mean values ± S.D. See also Figure S5, S6, and Video S1.

**Figure 5.. S1pr1 regulates astrocyte morphogenesis in zebrafish**
(A) Images of spinal cord astrocyte membrane labeled with myrGFP (green) and nuclei labeled with H2AmCherry (magenta) in 6 dpf *Tg(slc1a3b:myrGFP-P2A-H2AmCherry)* transgenic control (N=15, dorsal view; N=3 lateral view) and *s1pr1*^vo88/vo88 mutants (N=17, dorsal view; N=5, lateral view). N, number of animals. Scale bar, 20 µm. (B) Images of sparsely labeled individual astrocytes by *slc1a3b:myrGFP-P2A-H2Amcherry* DNA constructs and the representative IMARIS 3D-rendering surface (grey) at 6 dpf in the spinal cord of control and *s1pr1*^vo88/vo88 mutant zebrafish. Scale bar, 20 µm. (C) Quantification of individual astrocyte volumes in control (N=18) and *s1pr1*^vo88/vo88 mutants (N=23) at 6 dpf, related to (B). N, number of animals. Data points represent single astrocytes. ****, p<0.0001; unpaired t test. Error bars, mean values ± S.D. (D) Images of 6 dpf *Tg(slc1a3b:myrGFP-P2A-H2AmCherry)* larval brain in control (N=5) and *s1pr1*^vo88/vo88 mutants (N=6). Dashed lines mark astrocyte processes densely infiltrated neuropil in the forebrain, midbrain, and hindbrain. N, number of animals. Scale bar, 50 µm. (E) Time-lapse still images of astrocyte process dynamics labeled with myrGFP (green) in control and *s1pr1*^vo88/vo88 mutants at 3 dpf. Dashed boxes mark the regions shown to the right. Scale bar, 20 µm. (F) Quantification of astrocyte individual process extension and retraction displacement speed in control (N=10) and *s1pr1*^vo88/vo88 mutants (N=8) at 3 dpf. N, number of animals. Data points represent single astrocyte processes tracked. *, p<0.05; ***, p<0.001; unpaired t test. Error bars, mean values ± S.D. (G and I) Images of 6 dpf *Tg(slc1a3b:myrGFP-P2A-H2AmCherry)* transgenic larval spinal cord astrocytes after treatment with DMSO, 1 µM FTY720, or 1 µM Ex26 at 2–4 dpf (G) or 4–6 dpf (I). Dashed boxes represent 4 independent 10 µm x 10 µm areas in the astrocyte process-enriched regions were used to quantify the GFP coverage area percentage. Scale bar, 20 µm. (H) Quantification of relative GFP coverage area percentage at 6 dpf in the astrocyte process-enriched regions in DMSO (N=12), FTY720 (N=12), and Ex26 (N=12) after 2–4 dpf treatment. N, number of animals. Data points represent average GFP coverage area percentage of the 4 independent areas in a single fish. ****, p<0.0001; one-way ANOVA with multiple comparisons. (J) Quantification of relative GFP coverage area percentage at 6 dpf in the astrocyte process-enriched regions in DMSO (N=10), FTY720 (N=12), and Ex26 (N=11) after 4–6 dpf treatment. N, number of animals. Data points represent average GFP coverage area percentage of the 4 independent areas in a single fish. ****, p<0.0001; one-way ANOVA with multiple comparisons. See also Figure S7 and Video S2.

**Figure 6.. Loss of *Tre1*/*s1pr1* leads to behavioral deficits in *Drosophila* and zebrafish**
(A) Quantification of climbing activity in w¹¹¹⁸ control (N=10), *Tre1*^attP mutants (N=8), and astrocyte-specific *Tre1*^HMS00599 RNAi flies (N=11, *alrm-Gal4 UAS-Tre1*^HMS00599) at 30 dpe. N, number of groups, each group contains 10–20 flies. ns, not significant; *, p<0.05; ***, p<0.001; one-way ANOVA with Multiple comparisons. Error bars, mean values ± S.D. (B) Quantification of climbing activity in control (N=14, *alrm-Gal4 UAS-FLP*) and astrocyte-specific *Tre1* FLP-out mutants (N=9, *alrm-Gal4 UAS-FLP Tre1*^FRT-Gal4) at 30 dpe. N, number of groups, each group contains 10–20 flies. ****, p<0.0001; unpaired t test. Error bars, mean values ± S.D. (C) Quantification of climbing activity in w¹¹¹⁸ *alrm-Gal4* (N=28), w¹¹¹⁸ *alrm-Gal4 UAS-Rac1.N17* (N=17), *Tre1*^attP *alrm-Gal4* (N=21), and *Tre1*^attP *alrm-Gal4 UAS-Rac1.N17* (N=8) at 3 dpe. N, number of groups, each group contains 10–20 flies. ns, not significant; *, p<0.05; ****, p<0.0001; one-way ANOVA with Multiple comparisons. Error bars, mean values ± S.D. (D) Example traces of a freely swimming zebrafish. Shaded area indicates a swim bout with postural angle shown at the top and speed over time shown in the lower traces. (E) Quantification of bouts detected per experimental repeat for WT (N=24), *s1pr1*^vo89/+ (N=36), and *s1pr1*^vo89/vo89 fish (N=48). N, number of animals. ***, p<0.001; Kruskal-Wallis test. (F-H) Average posture (F), speed (G), and angular velocity (H) during bout of WT, *s1pr1*^vo89/+, and *s1pr1*^vo89/vo89 fish. Dashed line indicates peak speed. (I-K) Quantification of average posture at peak speed (I), average bout duration (J), and average total rotation (K) WT, *s1pr1*^vo89/+, and *s1pr1*^vo89/vo89 fish. **, p<0.01; ***, p<0.001; Kruskal-Wallis test. See also Figure S8.

**Figure 7.. The *Drosophila* LPPs Wun/Wun2 control astrocyte infiltration**
(A) Confocal single section images of ventral nerve cords of third instar larvae (L3) in coronal sections (upper panels) or cross-sectional 3D projections of 100 µm along the anterior-posterior axis (lower panels). Astrocyte membranes are labeled by α-Gat antibody (magenta) and nuclei labeled by α-Pros antibody (green). Scale bars, 30 µm. (B) Quantification of normalized astrocyte infiltration volume of control (w¹¹¹⁸, N= 7); and *Df(2R)w45-19g* / *wun49 wun2*^Ex34; *alrm*-Gal4/+ animals expressing UAS-*wun2*^H326K (N= 10), UAS-*wun2* (N= 9), UAS-*wun* (N= 9), UAS-*mLPP3* (N= 7) related to (A). N denotes the number of animals, and individual data points represent the astrocyte volume averaged over 10 sampling volumes per larva each sized 200*100*20 pixels located in a mid-dorsal neuropil region along the a-p axis. Error bars: mean values ±SD. One-way ANOVA with multiple comparisons. ns, not significant; *, p<0.05; **, p<0.01; ***, p<0.001; ****, p<0.0001. (C) Cross-sectional 3D projections of MARCM astrocyte clones labeled with mCD8-mCherry (magenta) and all astrocyte membrane labeled with α-Gat antibody (green) in the L3 VNC. Cell bodies of the MARCM astrocyte clones are indicated with grey spheres for clarity. Scale bar, 15 µm. (D) Quantification of astrocyte volumes of MARCM clones for control (N= 14); *wun*⁴⁹,*wun2*^EX34 (N= 12); *wun*⁴⁹,*wun2*^EX34 + UAS-*wun2* (N= 8); and *wun*⁴⁹,*wun2*^EX34 + UAS-*wun* (N= 7) related to (C). N denotes the number of animals and individual data points represent single clones. Kruskal-Wallis test with Dunn’s multiple comparisons test. Error bars: mean values ± 95% CI. ns, not significant; *, p<0.05; **, p<0.01; ***, p<0.001; ****, p<0.0001. (E) Images of L3 VNC with astrocyte membranes labeled with α-Gat (magenta) and astrocyte nuclei labeled with α-Pros (blue) in the *Df(2R)w45-19g* /*wun*⁴⁹,*wun2*^EX34 *; RN2-FLP tub<<Gal4* UAS-CD8-GFP FLP-out background expressing different *wunen* or *mLPP3* transgene in the mCD8-GFP-labeled neuronal clones (green). Dashed lines mark the boundaries of mCD8-GFP-labeled neurons at a single-Z plane. Scale bar: 20 µm. (F) Quantification of relative α-Gat mean fluorescence intensity in the dashed line areas normalized to neighboring regions of the same size lacking a neuronal clone related to (E). UAS-*wun2*^H326K (N= 5); UAS-*wun2* (N= 7); UAS-*wun* (N=8); UAS- *mLPP3* (N= 8); Kruskal-Wallis test with Dunn’s multiple comparisons test. Error bars: mean values ± 95% CI. *, p<0.05; ****, p<0.0001. See also Figure S9.

Figure 8.. Wunen activity is suppressed by the loss of *Tre1*
(A) 3D projections of confocal images of astrocyte FLP-out clones labeled with myr::tdTomato (magenta) using *alrm*>QF>Gal4 *ftz*-FLP with all astrocytes labeled by α-Gat (green) in the L3 VNC. Clones also express UAS-*wun2*^H326K or UAS-*wun2* in either the *Df(2R)w45-19g/*/*wun*⁴⁹,*wun2*^EX34 mutant background or the *Tre1*^attP; *Df(2R)w45-19g/*/*wun*⁴⁹*,wun2*^EX34 triple mutant background. The right and bottom panels show 3D renderings of segmented astrocyte clones, and cell bodies of cells in the clone are highlighted with grey spheres for clarity. Bottom panels show a lateral view of the VNC. Arrowheads point out ectopic projections into the cortex of astrocytes adjacent to the astrocyte clones expressing UAS-*wun2*. Scale bars, 30 µm. (B and C) Quantification of the cell volume of individual astrocytes (B) and the length of a minimal bounding box (BB) enclosing astrocyte clones (C) in UAS-*wun2*-expressing astrocytes (related to (A): *Df(2R)w45-19g*/*wun*⁴⁹,*wun2*^EX34 + UAS-*wun2*^H326K (N= 9); *Df(2R-w45-19g*/*wun*⁴⁹,*wun2*^EX34 + UAS-*wun2* (N= 7); and *Tre1*^attP/Y; *Df(2R)w45-19g*/*wun*⁴⁹*,wun2*^EX34 + UAS-*wun2* (N= 7). N denotes the number of animals and individual data points represents single clones. Error bars: mean values ± 95% CI. Kruskal-Wallis test with Dunn’s multiple comparisons test. ns, not significant; ****, p<0.0001. (D) Cross-sectional 3D projections of confocal images representing 100 µm along the anterior-posterior axis of the VNC (upper panels). Astrocyte membranes are labeled by α-Gat antibody (magenta). Scale bars, 20 µm. Lower panels show a schematic representation of the expression domain in either astrocytes alone or astrocytes and cortex glia. (E) Quantification of the number of ectopic astrocyte processes projecting from the neuropil visible in 100 µm cross-sectional 3D projections related to (D). Genotypes are indicated in the legend table. Data points represent the number of larvae tested (N=7–11). Error bars: mean values ± SD; One-way ANOVA with multiple comparisons. ****, p<0.0001. See also Figures S10 and S11.

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Astrocyte growth is driven by the Tre1/S1pr1 phospholipid-binding G protein-coupled receptor

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Astrocyte growth is driven by the Tre1/S1pr1 phospholipid-binding G protein-coupled receptor

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