CAPS-1 and CAPS-2 Are Essential Synaptic Vesicle Priming Proteins

Cell

Volumn 131, Issue 4, 2007, Pages 796-808

  Jockusch, Wolf J ^a   Speidel, Dina ^a   Sigler, Albrecht ^b   Sørensen, Jakob B ^b   Varoqueaux, Frederique ^a   Rhee, Jeong Seop ^a   Brose, Nils ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

CELLBIO; MOLNEURO; PROTEINS

Indexed keywords

CAPS 1; CAPS 2; NEUROTRANSMITTER; PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL FUSION; CONTROLLED STUDY; EMBRYO; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

EID: 36049025863     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.11.002     Document Type: Article

References (48)

1. Andrews-Zwilling Y.S., Kawabe H., Reim K., Varoqueaux F., and Brose N. Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2. J. Biol. Chem. 281 (2006) 19720-19731
2. Ashery U., Betz A., Xu T., Brose N., and Rettig J. An efficient method for infection of adrenal chromaffin cells using the Semliki Forest virus gene expression system. Eur. J. Cell Biol. 78 (1999) 525-532
3. Augustin I., Rosenmund C., Sudhof T.C., and Brose N. Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400 (1999) 457-461
4. Basu J., Shen N., Dulubova I., Lu J., Guan R., Guryev O., Grishin N.V., Rosenmund C., and Rizo J. A minimal domain responsible for Munc13 activity. Nat. Struct. Mol. Biol. 12 (2005) 1017-1018
5. Beinfeld M.C., Blum A., Vishnuvardhan D., Fanous S., and Marchand J.E. Cholecystokinin levels in prohormone convertase 2 knock-out mouse brain regions reveal a complex phenotype of region-specific alterations. J. Biol. Chem. 280 (2005) 38410-38415
6. Bekkers J.M., and Stevens C.F. Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc. Natl. Acad. Sci. USA 88 (1991) 7834-7838
7. Betz A., Okamoto M., Benseler F., and Brose N. Direct interaction of the rat unc-13 homologue Munc13-1 with the N terminus of syntaxin. J. Biol. Chem. 272 (1997) 2520-2526
8. Betz A., Thakur P., Junge H.J., Ashery U., Rhee J.S., Scheuss V., Rosenmund C., Rettig J., and Brose N. Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30 (2001) 183-196
9. Cawley N.X., Zhou J., Hill J.M., Abebe D., Romboz S., Yanik T., Rodriguiz R.M., Wetsel W.C., and Loh Y.P. The carboxypeptidase E knockout mouse exhibits endocrinological and behavioral deficits. Endocrinology 145 (2004) 5807-5819
10. Charlie N.K., Schade M.A., Thomure A.M., and Miller K.G. Presynaptic UNC-31 (CAPS) is required to activate the G alpha(s) pathway of the Caenorhabditis elegans synaptic signaling network. Genetics 172 (2006) 943-961
11. Dimova K., Kawabe H., Betz A., Brose N., and Jahn O. Characterization of the Munc13-calmodulin interaction by photoaffinity labeling. Biochim. Biophys. Acta 1763 (2006) 1256-1265
12. Dulubova I., Lou X., Lu J., Huryeva I., Alam A., Schneggenburger R., Sudhof T.C., and Rizo J. A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity?. EMBO J. 24 (2005) 2839-2850
13. Furuta M., Yano H., Zhou A., Rouille Y., Holst J.J., Carroll R., Ravazzola M., Orci L., Furuta H., and Steiner D.F. Defective prohormone processing and altered pancreatic islet morphology in mice lacking active SPC2. Proc. Natl. Acad. Sci. USA 94 (1997) 6646-6651
14. Gracheva E.O., Burdina A.O., Holgado A.M., Berthelot-Grosjean M., Ackley B.D., Hadwiger G., Nonet M.L., Weimer R.M., and Richmond J.E. Tomosyn inhibits synaptic vesicle priming in Caenorhabditis elegans. PLoS Biol. 4 (2006) e261 10.1371/journal.pbio.0040261
15. Gracheva E.O., Burdina A.O., Touroutine D., Berthelot-Grosjean M., Parekh H., and Richmond J.E. Tomosyn negatively regulates CAPS-dependent peptide release at Caenorhabditis elegans synapses. J. Neurosci. 27 (2007) 10176-10184
16. Junge H.J., Rhee J.S., Jahn O., Varoqueaux F., Spiess J., Waxham M.N., Rosenmund C., and Brose N. Calmodulin and Munc13 form a Ca2+ sensor/effector complex that controls short-term synaptic plasticity. Cell 118 (2004) 389-401
17. Koch H., Hofmann K., and Brose N. Definition of Munc13-homology-domains and characterization of a novel ubiquitously expressed Munc13 isoform. Biochem. J. 349 (2000) 247-253
18. Mahapatra N.R., O'Connor D.T., Vaingankar S.M., Hikim A.P., Mahata M., Ray S., Staite E., Wu H., Gu Y., Dalton N., et al. Hypertension from targeted ablation of chromogranin A can be rescued by the human ortholog. J. Clin. Invest. 115 (2005) 1942-1952
19. Maycox P.R., Deckwerth T., Hell J.W., and Jahn R. Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J. Biol. Chem. 263 (1988) 15423-15428
20. McEwen J.M., Madison J.M., Dybbs M., and Kaplan J.M. Antagonistic regulation of synaptic vesicle priming by Tomosyn and UNC-13. Neuron 51 (2006) 303-315
21. Morgan A., and Burgoyne R.D. Common mechanisms for regulated exocytosis in the chromaffin cell and the synapse. Semin. Cell Dev. Biol. 8 (1997) 141-149
22. Otsu Y., and Murphy T.H. Optical postsynaptic measurement of vesicle release rates for hippocampal synapses undergoing asynchronous release during train stimulation. J. Neurosci. 24 (2004) 9076-9086
23. Palmer C.L., Cotton L., and Henley J.M. The molecular pharmacology and cell biology of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Pharmacol. Rev. 57 (2005) 253-277
24. Pan H., Che F.Y., Peng B., Steiner D.F., Pintar J.E., and Fricker L.D. The role of prohormone convertase-2 in hypothalamic neuropeptide processing: a quantitative neuropeptidomic study. J. Neurochem. 98 (2006) 1763-1777
25. Pyott S.J., and Rosenmund C. The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J. Physiol. 539 (2002) 523-535
26. Renden R., Berwin B., Davis W., Ann K., Chin C.T., Kreber R., Ganetzky B., Martin T.F., and Broadie K. Drosophila CAPS is an essential gene that regulates dense-core vesicle release and synaptic vesicle fusion. Neuron 31 (2001) 421-437
27. Rhee J.S., Betz A., Pyott S., Reim K., Varoqueaux F., Augustin I., Hesse D., Sudhof T.C., Takahashi M., Rosenmund C., and Brose N. Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108 (2002) 121-133
28. Richmond J.E., Weimer R.M., and Jorgensen E.M. An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming. Nature 412 (2001) 338-341
29. Rosenmund C., Clements J.D., and Westbrook G.L. Nonuniform probability of glutamate release at a hippocampal synapse. Science 262 (1993) 754-757
30. Rosenmund C., Sigler A., Augustin I., Reim K., Brose N., and Rhee J.S. Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33 (2002) 411-424
31. Rosenmund C., and Stevens C.F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16 (1996) 1197-1207
32. Rupnik M., Kreft M., Sikdar S.K., Grilc S., Romih R., Zupancic G., Martin T.F., and Zorec R. Rapid regulated dense-core vesicle exocytosis requires the CAPS protein. Proc. Natl. Acad. Sci. USA 97 (2000) 5627-5632
33. Sadakata T., Itakura M., Kozaki S., Sekine Y., Takahashi M., and Furuichi T. Differential distributions of the Ca2+ -dependent activator protein for secretion family proteins (CAPS2 and CAPS1) in the mouse brain. J. Comp. Neurol. 495 (2006) 735-753
34. Sadakata T., Kakegawa W., Mizoguchi A., Washida M., Katoh-Semba R., Shutoh F., Okamoto T., Nakashima H., Kimura K., Tanaka M., et al. Impaired cerebellar development and function in mice lacking CAPS2, a protein involved in neurotrophin release. J. Neurosci. 27 (2007) 2472-2482
35. Sadakata T., Mizoguchi A., Sato Y., Katoh-Semba R., Fukuda M., Mikoshiba K., and Furuichi T. The secretory granule-associated protein CAPS2 regulates neurotrophin release and cell survival. J. Neurosci. 24 (2004) 43-52
36. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Sudhof T.C., and Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294 (2001) 1117-1122
37. Speese S., Petrie M., Shuske K., Ailion M., Ann K., Iwasaki K., Jorgensen E.M., and Martin T.F. UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J. Neurosci. 27 (2007) 6150-6162
38. Speidel D., Bruederle C.E., Enk C., Voets T., Varoqueaux F., Reim K., Becherer U., Fornai F., Ruggieri S., Holighaus Y., et al. CAPS1 regulates catecholamine loading of large dense-core vesicles. Neuron 46 (2005) 75-88
39. Speidel D., Varoqueaux F., Enk C., Nojiri M., Grishanin R.N., Martin T.F., Hofmann K., Brose N., and Reim K. A family of Ca2+-dependent activator proteins for secretion: comparative analysis of structure, expression, localization, and function. J. Biol. Chem. 278 (2003) 52802-52809
40. Stevens C.F., and Tsujimoto T. Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc. Natl. Acad. Sci. USA 92 (1995) 846-849
41. Stevens D.R., Wu Z.X., Matti U., Junge H.J., Schirra C., Becherer U., Wojcik S.M., Brose N., and Rettig J. Identification of the minimal protein domain required for priming activity of Munc13-1. Curr. Biol. 15 (2005) 2243-2248
42. Takamori S., Holt M., Stenius K., Lemke E.A., Gronborg M., Riedel D., Urlaub H., Schenck S., Brugger B., Ringler P., et al. Molecular anatomy of a trafficking organelle. Cell 127 (2006) 831-846
43. Tandon A., Bannykh S., Kowalchyk J.A., Banerjee A., Martin T.F., and Balch W.E. Differential regulation of exocytosis by calcium and CAPS in semi-intact synaptosomes. Neuron 21 (1998) 147-154
44. Varoqueaux F., Sigler A., Rhee J.S., Brose N., Enk C., Reim K., and Rosenmund C. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl. Acad. Sci. USA 99 (2002) 9037-9042
45. Walent J.H., Porter B.W., and Martin T.F. A novel 145 kd brain cytosolic protein reconstitutes Ca(2+)-regulated secretion in permeable neuroendocrine cells. Cell 70 (1992) 765-775
46. Washbourne P., Thompson P.M., Carta M., Costa E.T., Mathews J.R., Lopez-Bendito G., Molnar Z., Becher M.W., Valenzuela C.F., Partridge L.D., and Wilson M.C. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 5 (2002) 19-26
47. Zhu X., Zhou A., Dey A., Norrbom C., Carroll R., Zhang C., Laurent V., Lindberg I., Ugleholdt R., Holst J.J., and Steiner D.F. Disruption of PC1/3 expression in mice causes dwarfism and multiple neuroendocrine peptide processing defects. Proc. Natl. Acad. Sci. USA 99 (2002) 10293-10298
48. Zucker R.S., and Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64 (2002) 355-405