A presynaptic role for the cytomatrix protein GIT in synaptic vesicle recycling

Cell Reports

Volumn 7, Issue 5, 2014, Pages 1417-1425

  Podufall, Jasmin ^a,b   Tian, Rui ^b,d   Knoche, Elena ^c   Puchkov, Dmytro ^a,b   Walter, Alexander M ^a,b,c   Rosa, Stefanie ^a,b   Quentin, Christine ^b   Vukoja, Anela ^a,b   Jung, Nadja ^b   Lampe, Andre ^a,b   Wichmann, Carolin ^b   Böhme, Mathias ^b   Depner, Harald ^b   Zhang, Yong Q ^d   Schmoranzer, Jan ^a,b   Sigrist, Stephan J ^b,c   Haucke, Volker ^a,b,c  

^a LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; G PROTEIN COUPLED RECEPTOR KINASE 2; G PROTEIN COUPLED RECEPTOR KINASE 2 INTERACTING PROTEIN 1; STONIN 2; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; BINDING PROTEIN; CYTOMATRIX PROTEIN; G PROTEIN COUPLED RECEPTOR KINASE 2 INTERACTING PROTEIN; MEMBRANE PROTEIN; STONED B PROTEIN; SYNAPTOTAGMIN;

ACTIVE ZONE; ARTICLE; CONFOCAL MICROSCOPY; CONNECTOME; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENDOCYTOSIS; GENE; GIT1 GENE; GIT2 GENE; HIPPOCAMPUS; HUMAN; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SYNAPSE VESICLE; ANIMAL CELL; ATTENTION DEFICIT DISORDER; ORTHOLOGY; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

EID: 84902305310     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.04.051     Document Type: Article

References (37)

1. Bahri S.M., Choy J.M., Manser E., Lim L., Yang X. The Drosophila homologue of Arf-GAP GIT1, dGIT, is required for proper muscle morphogenesis and guidance during embryogenesis. Dev. Biol. 2009, 325:15-23.
2. Bruckner J.J., Gratz S.J., Slind J.K., Geske R.R., Cummings A.M., Galindo S.E., Donohue L.K., O'Connor-Giles K.M. Fife, a Drosophila Piccolo-RIM homolog, promotes active zone organization and neurotransmitter release. J.Neurosci. 2012, 32:17048-17058.
3. Claing A., Perry S.J., Achiriloaie M., Walker J.K., Albanesi J.P., Lefkowitz R.J., Premont R.T. Multiple endocytic pathways of G protein-coupled receptors delineated by GIT1 sensitivity. Proc. Natl. Acad. Sci. USA 2000, 97:1119-1124.
4. Dani A., Huang B., Bergan J., Dulac C., Zhuang X. Superresolution imaging of chemical synapses in the brain. Neuron 2010, 68:843-856.
5. Diril M.K., Wienisch M., Jung N., Klingauf J., Haucke V. Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev. Cell 2006, 10:233-244.
6. Dittman J., Ryan T.A. Molecular circuitry of endocytosis at nerve terminals. Annu. Rev. Cell Dev. Biol. 2009, 25:133-160.
7. Fergestad T., Broadie K. Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis. J.Neurosci. 2001, 21:1218-1227.
8. Fouquet W., Owald D., Wichmann C., Mertel S., Depner H., Dyba M., Hallermann S., Kittel R.J., Eimer S., Sigrist S.J. Maturation of active zone assembly by Drosophila Bruchpilot. J.Cell Biol. 2009, 186:129-145.
9. Göttfert F., Wurm C.A., Mueller V., Berning S., Cordes V.C., Honigmann A., Hell S.W. Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20nm resolution. Biophys. J. 2013, 105:L01-L03.
10. Granseth B., Odermatt B., Royle S.J., Lagnado L. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 2006, 51:773-786.
11. Gundelfinger E.D., Fejtova A. Molecular organization and plasticity of the cytomatrix at the active zone. Curr. Opin. Neurobiol. 2012, 22:423-430.
12. Haucke V., Neher E., Sigrist S.J. Protein scaffolds in the coupling of synaptic exocytosis and endocytosis. Nat. Rev. Neurosci. 2011, 12:127-138.
13. Heerssen H., Fetter R.D., Davis G.W. Clathrin dependence ofsynaptic-vesicle formation at the Drosophila neuromuscular junction. Curr. Biol. 2008, 18:401-409.
14. Hosoi N., Holt M., Sakaba T. Calcium dependence of exo- and endocytotic coupling at a glutamatergic synapse. Neuron 2009, 63:216-229.
15. Hua Y., Sinha R., Thiel C.S., Schmidt R., Hüve J., Martens H., Hell S.W., Egner A., Klingauf J. A readily retrievable pool of synaptic vesicles. Nat. Neurosci. 2011, 14:833-839.
16. Kaeser P.S., Deng L., Wang Y., Dulubova I., Liu X., Rizo J., Südhof T.C. RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 2011, 144:282-295.
17. Kim S., Ko J., Shin H., Lee J.R., Lim C., Han J.H., Altrock W.D., Garner C.C., Gundelfinger E.D., Premont R.T., et al. The GIT family of proteins forms multimers and associates with the presynaptic cytomatrix protein Piccolo. J.Biol. Chem. 2003, 278:6291-6300.
18. Kittel R.J., Wichmann C., Rasse T.M., Fouquet W., Schmidt M., Schmid A., Wagh D.A., Pawlu C., Kellner R.R., Willig K.I., et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 2006, 312:1051-1054.
19. Kononenko N.L., Diril M.K., Puchkov D., Kintscher M., Koo S.J., Pfuhl G., Winter Y., Wienisch M., Klingauf J., Breustedt J., et al. Compromised fidelity of endocytic synaptic vesicle protein sorting in the absence of stonin 2. Proc. Natl. Acad. Sci. USA 2013, 110:E526-E535.
20. Koo S.J., Markovic S., Puchkov D., Mahrenholz C.C., Beceren-Braun F., Maritzen T., Dernedde J., Volkmer R., Oschkinat H., Haucke V. SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proc. Natl. Acad. Sci. USA 2011, 108:13540-13545.
21. Lampe A., Haucke V., Sigrist S.J., Heilemann M., Schmoranzer J. Multi-colour direct STORM with red emitting carbocyanines. Biol. Cell 2012, 104:229-237.
22. Liu K.S., Siebert M., Mertel S., Knoche E., Wegener S., Wichmann C., Matkovic T., Muhammad K., Depner H., Mettke C., et al. RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science 2011, 334:1565-1569.
23. Menon P., Deane R., Sagare A., Lane S.M., Zarcone T.J., O'Dell M.R., Yan C., Zlokovic B.V., Berk B.C. Impaired spine formation and learning in GPCR kinase 2 interacting protein-1 (GIT1) knockout mice. Brain Res. 2010, 1317:218-226.
24. Miesenböck G., De Angelis D.A., Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998, 394:192-195.
25. Miśkiewicz K., Jose L.E., Bento-Abreu A., Fislage M., Taes I., Kasprowicz J., Swerts J., Sigrist S., Versées W., Robberecht W., Verstreken P. ELP3 controls active zone morphology by acetylating the ELKS family member Bruchpilot. Neuron 2011, 72:776-788.
26. Mullen G.P., Grundahl K.M., Gu M., Watanabe S., Hobson R.J., Crowell J.A., McManus J.R., Mathews E.A., Jorgensen E.M., Rand J.B. UNC-41/stonin functions with AP2 to recycle synaptic vesicles in Caenorhabditis elegans. PLoS ONE 2012, 7:e40095.
27. Owald D., Fouquet W., Schmidt M., Wichmann C., Mertel S., Depner H., Christiansen F., Zube C., Quentin C., Körner J., et al. A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J.Cell Biol. 2010, 188:565-579.
28. Phillips G.R., Huang J.K., Wang Y., Tanaka H., Shapiro L., Zhang W., Shan W.S., Arndt K., Frank M., Gordon R.E., et al. The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 2001, 32:63-77.
29. Sakaba T., Kononenko N.L., Bacetic J., Pechstein A., Schmoranzer J., Yao L., Barth H., Shupliakov O., Kobler O., Aktories K., Haucke V. Fast neurotransmitter release regulated by the endocytic scaffold intersectin. Proc. Natl. Acad. Sci. USA 2013, 110:8266-8271.
30. Schikorski T. Readily releasable vesicles recycle at the active zone ofhippocampal synapses. Proc. Natl. Acad. Sci. USA 2014, 111:5415-5420.
31. Segura I., Essmann C.L., Weinges S., Acker-Palmer A. Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat. Neurosci. 2007, 10:301-310.
32. Stimson D.T., Estes P.S., Rao S., Krishnan K.S., Kelly L.E., Ramaswami M. Drosophila stoned proteins regulate the rate and fidelity of synaptic vesicle internalization. J.Neurosci. 2001, 21:3034-3044.
33. Verstreken P., Ohyama T., Bellen H.J. FM 1-43 labeling of synaptic vesicle pools at the Drosophila neuromuscular junction. Methods Mol. Biol. 2008, 440:349-369.
34. Watanabe S., Rost B.R., Camacho-Pérez M., Davis M.W., Söhl-Kielczynski B., Rosenmund C., Jorgensen E.M. Ultrafast endocytosis at mouse hippocampal synapses. Nature 2013, 504:242-247.
35. Won H., Mah W., Kim E., Kim J.W., Hahm E.K., Kim M.H., Cho S., Kim J., Jang H., Cho S.C., et al. GIT1 is associated with ADHD in humans and ADHD-like behaviors in mice. Nat. Med. 2011, 17:566-572.
36. Xu J., Luo F., Zhang Z., Xue L., Wu X.S., Chiang H.C., Shin W., Wu L.G. SNARE proteins synaptobrevin, SNAP-25, and syntaxin are involved in rapid and slow endocytosis at synapses. Cell Rep 2013, 3:1414-1421.
37. Zhang H., Webb D.J., Asmussen H., Niu S., Horwitz A.F. A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J.Neurosci. 2005, 25:3379-3388.