UNC-13 is required for synaptic vesicle fusion in C. elegans (original) (raw)

References

  1. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).
    CAS PubMed PubMed Central Google Scholar
  2. Rose, A. M. & Baillie, D. L. Genetic organization of the region around UNC-15 (I), a gene affecting paramyosin in Caenorhabditis elegans . Genetics 96, 639– 648 (1980).
    CAS PubMed PubMed Central Google Scholar
  3. Hosono, R., Sassa, T. & Kuno, S. Spontaneous mutations of trichlorfon resistance in the nematode, Caenorhabditis elegans. Zoological Sci. 6, 697– 708 (1989).
    CAS Google Scholar
  4. Nguyen, M., Alfonso, A., Johnson, C. D. & Rand, J. B. Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 140, 527–535 (1995).
    CAS PubMed PubMed Central Google Scholar
  5. Maruyama, I. N. & Brenner, S. A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 88, 5729– 5733 (1991).
    Article CAS Google Scholar
  6. Rizo, J. & Sudhof, T. C. C2-domains, structure and function of a universal Ca2+-binding domain. J. Biol. Chem. 273, 15879–15882 ( 1998).
    Article CAS Google Scholar
  7. Newton, A. C. Regulation of protein kinase C. Curr. Opin. Cell Biol. 9, 161–167 (1997).
    Article CAS Google Scholar
  8. Brose, N., Hofmann, K., Hata, Y. & Sudhof, T. C. Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J. Biol. Chem. 270, 25273– 25280 (1995).
    Article CAS Google Scholar
  9. Augustin, I., Betz, A., Herrmann, C., Jo, T. & Brose, N. Differential expression of two novel Munc13 proteins in rat brain. Biochem. J. 337, 363–371 (1999).
    Article CAS Google Scholar
  10. Xu, X. Z. et al. Retinal targets for calmodulin include proteins implicated in synaptic transmission. J. Biol. Chem. 273, 31297–31307 (1998).
    Article CAS Google Scholar
  11. Aravamudan, B., Fergestad, T., Davis, W. S. & Broadie, K. Drosophila UNC-13 is essential for synaptic transmission. Nat. Neurosci. 2, 965–971 ( 1999).
    Article CAS Google Scholar
  12. Betz, A. et al. Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21, 123 –136 (1998).
    Article CAS Google Scholar
  13. Ahmed, S. et al. The Caenorhabditis elegans unc-13 gene product is a phospholipid- dependent high-affinity phorbol ester receptor. Biochem. J. 287, 995–999 (1992).
    Article CAS Google Scholar
  14. Kazanietz, M. G., Lewin, N. E., Bruns, J. D. & Blumberg, P. M. Characterization of the cysteine-rich region of the Caenorhabditis elegans protein Unc-13 as a high affinity phorbol ester receptor. Analysis of ligand-binding interactions, lipid cofactor requirements, and inhibitor sensitivity. J. Biol. Chem. 270, 10777– 10783 (1995).
    Article CAS Google Scholar
  15. Nurrish, S., Segalat, L. & Kaplan, J. M. Serotonin inhibition of synaptic transmission: Gα o decreases the abundance of UNC-13 at release sites. Neuron 24, 231–242, ( 1999).
    Article CAS Google Scholar
  16. McIntire, S. L., Reimer, R. J., Schuske, K., Edwards, R. H. & Jorgensen, E. M. Identification and characterization of the vesicular GABA transporter. Nature 389, 870–876 (1997).
    Article CAS Google Scholar
  17. Jorgensen, E. M. et al. Defective recycling of synaptic vesicles in synaptotagmin mutants of Caenorhabditis elegans. Nature 378 , 196–199 (1995).
    Article CAS Google Scholar
  18. Jin, Y., Jorgensen, E., Hartwieg, E. & Horvitz, H. R. The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J. Neurosci. 19, 539–548 (1999).
    Article CAS Google Scholar
  19. Richmond, J. E. & Jorgensen, E. M. One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat. Neurosci. 2, 791– 797 (1999).
    Article CAS Google Scholar
  20. Li, J. & Schwarz, T. L. Genetic evidence for an equilibrium between docked and undocked vesicles. Phil. Trans. R. Soc. Lond. B Biol. Sci. 354, 299–306 (1999).
    Article CAS Google Scholar
  21. Niles, W. D. & Smith, D. O. Effects of hypertonic solutions on quantal transmitter release at the crayfish neuromuscular junction. J. Physiol. (Lond.) 329, 185–202 (1982).
    Article CAS Google Scholar
  22. Stevens, C. F. & 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, 846–849 (1995).
    Article CAS Google Scholar
  23. Rosenmund, C. & Stevens, C. F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16 , 1197–1207 (1996).
    Article CAS Google Scholar
  24. Augustin, I., Rosenmund, C., Sudhof, T. C. & Brose, N. Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400, 457–461 (1999).
    Article CAS Google Scholar
  25. Hata, Y., Slaughter, C. A. & Sudhof, T. C. Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366, 347–351 (1993).
    Article CAS Google Scholar
  26. Ogawa, H., Harada, S., Sassa, T., Yamamoto, H. & Hosono, R. Functional properties of the unc-64 gene encoding a Caenorhabditis elegans syntaxin. J. Biol. Chem. 273, 2192–2198 (1998).
    Article CAS Google Scholar
  27. Pevsner, J. et al. Specificity and regulation of a synaptic vesicle docking complex. Neuron 13, 353–361 (1994).
    Article CAS Google Scholar
  28. Schulze, K. L. et al. rop, a Drosophila homolog of yeast Sec1 and vertebrate n-Sec1/Munc-18 proteins, is a negative regulator of neurotransmitter release in vivo. Neuron 13, 1099– 1108 (1994).
    Article CAS Google Scholar
  29. Wu, M. N. et al. Syntaxin 1A interacts with multiple exocytic proteins to regulate neurotransmitter release in vivo. Neuron 23, 593–605 (1999).
    Article CAS Google Scholar
  30. Betz, A., Okamoto, M., Benseler, F. & Brose, N. Direct interaction of the rat unc-13 homologue Munc13-1 with the N terminus of syntaxin. J. Biol. Chem. 272, 2520–2526 (1997).
    Article CAS Google Scholar
  31. Sassa, T. et al. Regulation of the UNC-18-Caenorhabditis elegans syntaxin complex by UNC- 13. J. Neurosci. 19, 4772 –4777 (1999).
    Article CAS Google Scholar
  32. Sollner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. & Rothman, J. E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409–418 (1993).
    Article CAS Google Scholar
  33. Bamber, B. A., Beg, A. A., Twyman, R. E. & Jorgensen, E. M. The Caenorhabditis elegans unc-49 locus encodes multiple subunits of a heteromultimeric GABA receptor. J. Neurosci. 19, 5348–5359 (1999).
    Article CAS Google Scholar

Download references