aex-3 encodes a novel regulator of presynaptic activity in C. elegans

Neuron

Volumn 18, Issue 4, 1997, Pages 613-622

  Iwasaki, Kouichi ^a   Staunton, Jane ^b,c   Saifee, Owais ^b   Nonet, Michael ^b   Thomas, James H ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; RAB PROTEIN;

ARTICLE; BEHAVIOR; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; MUTATION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

EID: 0030989110     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80302-5     Document Type: Article

References (59)

1. Alfonso, A., Grundahl, K., Duerr, J.S., Man, H.P., and Rand, J.B. (1993). The Caenorhabditis elegans unc- 17 gene: a putative vesicular acetylcholine transporter. Science 261, 617-619.
2. Alfonso, A., Grundahl, K., McManus, J.R., and Rand, J.B. (1994). Cloning and characterization of the choline acetyltransferase structural gene (cha-1) from C. elegans. J. Neurosci. 4, 2290-2300.
3. Andres, D.A., Seabra, M.C., Brown, M.S., Armstrong, S.A., Smeland, T.E., Cremers, F.P., and Goldstein, J.L. (1993). cDNA cloning of component Aof Rab geranylgeranyl transferase and demonstration of its role as a Rab escort protein. Cell 7, 1091-1099.
4. Avery, L. (1993). The genetics of feeding in Caenorhabditis elegans. Genetics 133, 897-917.
5. Avery, L., Raizen, D., and Lockery, S. (1995). Electrophysiological methods. In Methods in Cell Biology, Caenorhabditis elegans: Modern Biological Analysis of an Organism, H.F. Epstein and D.C. Shakes, eds. (San Diego, California: Academic Press, Inc.), pp. 251-269.
6. Bargmann, C.I., and Horvitz, H.R. (1991). Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 251, 1243-1246.
7. Barstead, R.J., Kleiman, L., and Waterston, R.H. (1991). Cloning, sequencing, and mapping of an alpha-actinin gene from the nematode Caenorhabditis elegans. Cell Motil. Cytoskeleton 20, 69-78.
8. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
9. Brondyk, W.H., McKiernan, C.J., Fortner, K.A., Stabila, P., Holz, R.W., and Macara, I.G. (1995). Interaction cloning of Rabin3, a novel protein that associates with the Ras-like GTPase Rab3A. Mol. Cell. Biol. 15, 1137-1143.
10. Brose, N., Hofmann, K., Hata, Y., and Südhof, T.C. (1993). Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J. Biol. Chem. 270, 25273-25280.
11. Burton, J.L., Burns, M.E., Gatti, E., Augustine, G.J., and DeCamilli, P. (1994). Specific interactions of Mss4 with members of the Rab GTPase subfamily. EMBO J. 13, 5547-5558.
12. deHoop, M.J., Huber, L.A., Stenmark, H., Williamson, E., Zerial, M., Parton, R.G., and Dotti, C.G. (1994). The involvement of the small GTP-binding protein Rab5a in neuronal endocytosis. Neuron 13, 11-22.
13. Ferro-Novick, S., and Novick, P. (1993). The role of GTP-binding proteins in transport along the exocytic pathway. Annu. Rev. Cell Biol. 9, 575-599.
14. Fischer von Mollard, G., Südhof, T.C., and Jahn, R. (1991). Asmall GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 349, 79-91.
15. Fischer von Mollard, G., Stahl, B., Walch-Solimena, C., Takei, K., Daniels, L., Khoklatchev, A., DeCamilli, P., Südhof, T.C., Jahn, R. (1994a). Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur. J. Cell Biol. 65, 319-326.
16. Fischer von Mollard, G., Khoklatchev, A., Stahl, B., Südhof, T.C., and Jahn, R. (1994b). Rab3C is a synaptic vesicle protein that dissociates from synaptic vesicles after stimulation of exocytosis.J. Biol. Chem. 269, 10971-10974.
17. Fleming, J.T., Tornoe, C., Riina, H.A., Coadwell, J., Lewis, J.A., and Sattelle, D.B. (1993). Acetylcholine receptor molecules of the nematode Caenorhabditis elegans. Comp. Mol. Neurobiol. 63, 65-80.
18. Gengyo-Ando, K., Kamiya, Y., Yamakawa, A., Kodaira, K., Nishiwaki, K., Miwa, J., Hori, I., and Hosono, R. (1993). The C. elegans unc-18 gene encodes a protein expressed in motor neurons. Neuron 11, 703-711.
19. Geppert, M., Bolshakov, V.Y., Siegelbaum, S.A., Takei, K., DeCamilli, P., Hammer, R.E., and Südhof, T.C. (1994a). The role of Rab3A in neurotransmitter release. Nature 369, 493-497.
20. Hall, D.H., and Hedgecock, E.M. (1991). Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65, 837-847.
21. Hata, Y., Slaughter, C.A., and Südhof, T.C. (1993). Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366, 347-351.
22. Hodgkin, J. (1983). Male phenotypes and mating efficiency in C. elegans. Genetics 103, 43-64.
23. Horvitz, H.R., Brenner, S., Hodgkin, J., and Herman, R.K. (1979). A uniform genetic nomenclature for the nematode Caenorhabditis elegans. Mol. Gen. Genet. 175, 129-133.
24. Huang, L.-S., Tzou, P., and Sternberg, P.W. (1994). The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development. Mol. Biol. Cell 5, 395-411.
25. Johannes, L., Lledo, P.M., Roa, M., Vincent, J.D., Henry, J.P., and Darchen, F. (1994). The GTPase Rab3a negatively controls calcium-dependent exocytosis in neuroendocrine cells. EMBO J. 13, 2029-2037.
26. Johnston, P.A., Archer, BT., III, Robinson, K., Mignery, G.A., Jahn, R., and Südhof, T.C. (1991). rab3A attachment to the synaptic vesicle membrane mediated by a conserved polyisoprenylated carboxyterminal sequence. Neuron 7, 101-109.
27. Kyte, J., and Doolittle, R.F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
28. Lewis, J.A., Wu, C.H., Berg, H., and Levine, J.H. (1980). The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 95, 905-928.
29. Lichy, J.H., Modi, W.S., Seuanez, H.N., and Howley, P.M. (1992). Identification of a human chromosome 11 gene which is differentially regulated in tumorigenic and nontumorigenic somatic cell hybrids of HeLa cells. Cell Growth Differ. 3, 541-548.
30. Liu, D.W., and Thomas, J.H. (1994). Regulation of a periodic motor program in C. elegans. J. Neurosci. 14, 1953-1962.
31. Livingstone, D. (1991). Studies onthe unc-37 gene of Caenorhabditis elegans. Ph.D. dissertation. University of Cambridge.
32. Maruyama, I.N., and Brenner, S.A. (1991). A phorbol ester/diacylglycerol-binding protein encoded by the unc-73 gene of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 88, 5729-5733.
33. McIntire, S.L., Jorgensen, E., and Horvitz, H.R. (1993). Genes required for GABA function in Caenorhabditis elegans. Nature 364, 334-337.
34. Mello, C.C., Kramer, J.M., Stinchcomb, D., and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
35. Miller, K.G., Alfonso, A., Nguyen, M., Crowell, J.A., Johnson, C.D., and Rand, J.B. (1996). A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc. Natl. Acad. Sci. USA 93, 12593-12598.
36. Nguyen, M., Alfonso, A., Johnson, C.D., and Rand, J.B. (1995). Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 140, 527-535.
37. Nonet, M.L., Grundahl, K., Meyer, B.J., and Rand, J.B. (1993).Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73, 1291-1305.
38. Oberhauser, A.F., Monck, J.R., Balch, W.E., and Fernandez, J.M. (1992). Exocytotic fusion is activated by Rab3a peptides. Nature 360, 270-273.
39. Okada, Y., Yamazaki, H., Sekine-Aizawa, Y., and Hirokawa, N. (1995). The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81, 769-780.
40. Olszewski, S., Deeney, J.T., Schuppin, G.T., Williams, K.P., Corkey, B.E., and Rhodes, C.J. (1994). Rab3A effector domain peptides induce insulin exocytosis via a specific interaction with a cytosolic protein doublet. J. Biol. Chem. 269, 27987-27991.
41. Raizen, D.M., and Avery, L. (1994). Electrical activity and behavior in the pharynx of Caenorhabditis elegans. Neuron 12, 483-495.
42. Raizen, D.M., Lee, R.Y.N., and Avery, L. (1995). Interacting genes required for pharyngeal excitation by motor neuron MC in Caenorhabditis elegans. Genetics 141, 1365-1382.
43. Salminen, A., Novick, P.J. (1987). A ras-like protein is required for a post-Golgi event in secretion. Cell 49, 527-538.
44. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning, A Laboratory Manual. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
45. Sasaki, T., Kikuchi, A., Araki, S., Hata, Y., Isomura, M., Kuroda, S., and Takai, Y. (1990). Purification and characterization from bovine brain cytosol of a protein that inhibits the dissociation of GDP from and the subsequent binding of GTP to smg p25A, a ras p21-like GTP-binding protein. J. Biol. Chem. 265, 2333-2337.
46. Schackwitz, W., Inoue,T., and Thomas, J.H. (1996). Sensory neurons function in parallel to regulate development in C. elegans. Neuron 17, 719-728.
47. Seabra, M.C., Brown, M.S., Slaughter, C.A., Sudhof, T.C., and Goldstein, J.L. (1992). Purification of component A of Rab geranyl-geranyl transferase: possible identity with the choroideremia gene product. Cell 70, 1049-1057.
48. Segev, N., Mulholland, J., Botstein, D. (1988). Theyeast GTP-binding YPT1 protein and a mammalian counterpart are associated with the secretion machinery. Cell 52, 915-924.
49. Shirataki, H., Kaibuchi, K., Sakoda, T., Kishida, S., Yamaguchi, T., Wada, K., Miyazaki, M., and Takai, Y. (1993). Rabphilin-3A, a putative target protein for smg p25A/rab3A p25 small GTP-binding protein related to synaptotagmin. Mol. Cell. Biol. 13, 2061-2068.
50. Stahl, B., von Mollard, G.F., Walch-Solimena, C., and Jahn, R. (1994). GTP cleavage by the small GTP-binding protein Rab3A is associated with exocytosis of synaptic vesicles induced by alpha-latrotoxin. J. Biol. Chem. 269, 24770-24776.
51. Südhof, T.C. (1995). The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
52. Sulston, J., and Hodgkin, J. (1988). Methods Appendix in The Nematode Caenorhabditis elegans. W. Wood, ed. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory).
53. Thomas, J.H. (1990). Genetic analysis of defecation in Caenorhabditis elegans. Genetics 124, 855-872.
54. Thomas, J.H. (1993). Chemosensory regulation of development in C. elegans. Bioessays 15, 791-797.
55. Vowels, J.J., and Thomas, J.H. (1992). Genetic analysis of chemo-sensory control of dauer formation in Caenorhabditis elegans. Genetics 130, 105-123.
56. Walent, J.H., Porter, B.W., and Martin, T.F. (1992). A novel 145 kd brain cytosolic protein reconstitutes Ca(2+)-regulated secretion in permeable neuroendocrine cells. Cell 70, 765-775.
57. White, J.G., Southgate, E., Thomson, J.N., and Brenner, S. (1976). The structure of the ventral nerve cord of Caenorhabditis. Philos. Trans. R. Soc. Lond. [Biol.] 275B, 327-348.
58. Wilson, R., Ainscough, R., Anderson, K., Baynes, C., Berks, M., Burton, J., Connell, M., Bonfield, J., Copsey, T., and Cooper, J. (1994). 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368, 32-38.
59. Yu, H., Chen, J.K., Feng, S., Dalgarno, D.C., Brauer, A.W., and Schreiber, S.L. (1994). Structural basis for the binding of prolinerich peptides to SH3 domains. Cell 76, 933-945.