Neurotransmitter release mechanisms studied in Caenorhabditis elegans

Cell Calcium

Volumn 52, Issue 3-4, 2012, Pages 289-295

  Barclay, Jeff W ^a   Morgan, Alan ^a   Burgoyne, Robert D ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

C. elegans; Exocytosis; Munc18; Presynaptic; SNARE; Vesicle fusion

Indexed keywords

ALPHA LIPRIN; ALPHA SYNAPTOSOMAL ASSOCIATED PROTEIN; CHAPERONE; COMPLEXIN; HEAT SHOCK COGNATE PROTEIN 70; MEMBRANE PROTEIN; MUNC18 PROTEIN; PROTEIN ELKS; PROTEIN MUNC13; PROTEIN MUNC18 1; PROTEIN RIM; RAB PROTEIN; SNARE PROTEIN; SYNAPSIN; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN; SYNTAXIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; ELECTRON MICROSCOPY; EXOCYTOSIS; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; GENETIC MODEL; MEMBRANE FUSION; MOLECULAR DYNAMICS; MORPHOLOGICAL TRAIT; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

CAENORHABDITIS ELEGANS;

EID: 84865797945     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2012.03.005     Document Type: Article

References (85)

1. Jahn R., Lang T., Südhof T.C. Membrane fusion. Cell 2003, 112:519-533.
2. Burgoyne R.D., Morgan A. Secretory granule exocytosis. Physiol. Rev. 2003, 83:581-632.
3. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
4. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. Biol. 1986, 314:1-340.
5. Mahoney T.R., Luo S., Nonet M.L. Analysis of synaptic transmission in Caenorhabditis elegans using an aldicarb-sensitivity assay. Nat. Protoc. 2006, 1:1772-1777.
6. Nguyen M., Alfonso A., Johnson C.D., Rand J.B. Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 1995, 140:527-535.
7. Miller K.G., Alfonso A., Nguyen M., Crowell J.A., Johnson C.D., Rand J.B. A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:12593-12598.
8. Lockery S.R., Goodman M.B. Tight-seal whole-cell patch clamping of Caenorhabditis elegans neurons. Methods Enzymol. 1998, 293:201-217.
9. Richmond J.E., Jorgensen E.M. One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat. Neurosci. 1999, 2:791-797.
10. Zhou K.M., Dong Y.M., Ge Q., Zhu D., Zhou W., Lin X.G., Liang T., Wu Z.X., Xu T. PKA activation bypasses the requirement for UNC-31 in the docking of dense core vesicles from C. elegans neurons. Neuron 2007, 56:657-669.
11. Sieburth D., Madison J.M., Kaplan J.M. PKC-1 regulates secretion of neuropeptides. Nat. Neurosci. 2007, 10:49-57.
12. Speese S., Petrie M., Schuske K., Ailion M., Ann K., Iwasaki K., Jorgensen E.M., Martin T.F. UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J. Neurosci. 2007, 27:6150-6162.
13. Weimer R.M. Preservation of C. elegans tissue via high-pressure freezing and freeze-substitution for ultrastructural analysis and immunocytochemistry. Methods Mol. Biol. 2006, 351:203-221.
14. Sudhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
15. Saifee O., Wei L., Nonet M.L. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol. Biol. Cell 1998, 9:1235-1252.
16. Nonet M.L., Saifee O., Zzhao H., Rand J.B., Wei L. Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J. Neurosci. 1998, 18:70-80.
17. Sieburth D., Ch'ng Q., Dybbs M., Tavazoie M., Kennedy S., Wang D., Dupuy D., Rual J.F., Hill D.E., Vidal M., Ruvkun G., Kaplan J.M. Systematic analysis of genes required for synapse structure and function. Nature 2005, 436:510-517.
18. de Wit H., Walter A.M., Milosevic I., Gulyas-Kovacs A., Riedel D., Sorensen J.B., Verhage M. Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 2009, 138:935-946.
19. Hammarlund M., Palfreyman M.T., Watanabe S., Olsen S., Jorgensen E.M. Open syntaxin docks synaptic vesicles. PLoS Biol. 2007, 5:e198.
20. Dulubova I., Sugita S., Hill S., Hosaka M., Fernandez I., Sudhof T.C., Rizo J. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 1999, 18:4372-4382.
21. Hammarlund M., Watanabe S., Schuske K., Jorgensen E.M. CAPS and syntaxin dock dense core vesicles to the plasma membrane in neurons. J. Cell Biol. 2008, 180:483-491.
22. Burgoyne R.D., Barclay J.W., Ciufo L.F., Graham M.E., Handley M.T., Morgan A. The functions of Munc18-1 in regulated exocytosis. Ann. N. Y. Acad. Sci. 2009, 1152:76-86.
23. Weimer R.M., Richmond J.E., Davis W.S., Hadwinger G., Nonet M.L., Jorgensen E.M. Defects in synaptic vesicle docking in unc-18 mutants. Nat. Neurosci. 2003, 6:1023-1030.
24. Gengyo-Ando K., Kitayama H., Mukaida M., Ikawa Y. A murine neural specific homolog corrects cholinergic defects in Caenorhabditis elegans unc-18 mutants. J. Neurosci. 1996, 16:6695-6702.
25. Sassa T., Harada S.-i., Ogawa H., Rand J.B., Maruyama I.N., Hosono R. Regulation of the UNC-18-Caenorhabditis elegans syntaxin complex by UNC-13. J. Neurosci. 1999, 19:4772-4777.
26. McEwen J.M., Kaplan J.M. UNC-18 promotes both the anterograde trafficking and synaptic function of syntaxin. Mol. Biol. Cell 2008, 19:3836-3846.
27. Burgoyne R.D., Morgan A. Membrane trafficking: three steps to fusion. Curr. Biol. 2007, 17:R255-R258.
28. Johnson J.R., Ferdek P., Lian L.Y., Barclay J.W., Burgoyne R.D., Morgan A. Binding of UNC-18 to the N-terminus of syntaxin is essential for neurotransmission in Caenorhabditis elegans. Biochem. J. 2009, 418:73-80.
29. Graham M.E., Edwards M.R., Holden-Dye L., Morgan A., Burgoyne R.D., Barclay J.W. UNC-18 modulates ethanol sensitivity in Caenorhabditis elegans. Mol. Biol. Cell 2009, 20:43-55.
30. Han L., Jiang T., Han G.A., Malintan N.T., Xie L., Wang L., Tse F.W., Gaisano H.Y., Collins B.M., Meunier F.A., Sugita S. Rescue of Munc18-1 and -2 double knockdown reveals the essential functions of interaction between Munc18 and closed syntaxin in PC12 cells. Mol. Biol. Cell 2009, 20:4962-4975.
31. Voets T., Toonen R., Brian E.C., de Wit H., Moser T., Rettig J., Sudhof T.C., Neher E., Verhage M. Munc-18 promotes large dense-core vesicle docking. Neuron 2001, 31:581-591.
32. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., Geuze H.J., Sudhof T.C. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000, 287:864-869.
33. Gracheva E.O., Maryon E.B., Berthelot-Grosjean M., Richmond J.E. Differential regulation of synaptic vesicle tethering and docking by UNC-18 and TOM-1. Front. Synaptic Neurosci. 2010, 2:141.
34. Hatsuzawa K., Lang T., Fasshauer D., Bruns D., Jahn R. The R-SNARE motif of tomosyn forms SNARE core complexes with syntaxin 1 and SNAP-25 and down-regulates exocytosis. J. Biol. Chem. 2003.
35. Dybbs M., Ngai J., Kaplan J.M. Using microarrays to facilitate positional cloning: identification of tomosyn as an inhibitor of neurosecretion. PLoS Genet. 2005, 1:6-16.
36. Gracheva E.O., Burdina A.O., Holgado A.M., Berthelot-Grosjean M., Ackley B.D., Hadwiger G., Nonet M.L., Weimer R.M., Richmond J.E. Tomosyn inhibits synaptic vesicle priming in Caenorhabditis elegans. PLoS Biol. 2006, 4:e261.
37. McEwen J.M., Madison J.M., Dybbs M., Kaplan J.M. Antagonistic regulation of synaptic vesicle priming by Tomosyn and UNC-13. Neuron 2006, 51:303-315.
38. Gracheva E.O., Burdina A.O., Touroutine D., Berthelot-Grosjean M., Parekh H., Richmond J.E. Tomosyn negatively regulates both synaptic transmitter and neuropeptide release at the C. elegans neuromuscular junction. J. Physiol. 2007, 585:705-709.
39. Fisher R.J., Pevsner J., Burgoyne R.D. Control of fusion pore dynamics during exocytosis by Munc18. Science 2001, 291:875-878.
40. Barclay J.W. Munc-18-1 regulates the initial release rate of exocytosis. Biophys. J. 2008, 94:1084-1093.
41. Shen J., Tareste D.C., Paumet F., Rothman J.E., Melia T.J. Selective activation of cognate SNAREpins by Sec1/Munc18 (SM) proteins. Cell 2007, 128:1-13.
42. Jorgacevski J., Potokar M., Grilc S., Kreft M., Liu W., Barclay J.W., Buckers J., Medda R., Hell S.W., Parpura V., Burgoyne R.D., Zorec R. Munc18-1 tuning of vesicle merger and fusion pore properties. J. Neurosci. 2011, 31:9055-9066.
43. Deak F., Xu Y., Chang W.P., Dulubova I., Khvotchev M., Liu X., Sudhof T.C., Rizo J. Munc18-1 binding to the neuronal SNARE complex controls synaptic vesicle priming. J. Cell Biol. 2009, 184:751-764.
44. Rathore S.S., Bend E.G., Yu H., Hammarlund M., Jorgensen E.M., Shen J. Syntaxin N-terminal peptide motif is an initiation factor for the assembly of the SNARE-Sec1/Munc18 membrane fusion complex. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:22399-22406.
45. Ma C., Li W., Xu Y., Rizo J. Munc13 mediates the transition from the closed syntaxin-Munc18 complex to the SNARE complex. Nat. Struct. Mol. Biol. 2011, 18:542-549.
46. Li W., Ma C., Guan R., Xu Y., Tomchick D.R., Rizo J. The crystal structure of a Munc13 C-terminal module exhibits a remarkable similarity to vesicle tethering factors. Structure 2011, 19:1443-1455.
47. Ciufo L.F., Barclay J.W., Burgoyne R.D., Morgan A. Munc18-1 regulates early and late stages of exocytosis via syntaxin-independent protein interactions. Mol. Biol. Cell 2005, 16:470-482.
48. Graham M.E., Prescott G.R., Johnson J.R., Jones M., Walmesley A., Haynes L.P., Morgan A., Burgoyne R.D., Barclay J.W. Structure-function study of mammalian Munc18-1 and C. elegans UNC-18 implicates domain 3b in the regulation of exocytosis. PLoS One 2011, 6:e17999.
49. Graham M.E., Handley M.T., Barclay J.W., Ciufo L.F., Barrow S.L., Morgan A., Burgoyne R.D. A gain of function mutant of Munc18-1 stimulates secretory granule recruitment and exocytosis and reveals a direct interaction of Munc18-1 with Rab3. Biochem. J. 2008, 409:407-416.
50. Melia T.J. Putting the clamps on membrane fusion: how complexin sets the stage for calcium-mediated exocytosis. FEBS Lett. 2007, 581:2131-2139.
51. Hobson R.J., Liu Q., Watanabe S., Jorgensen E.M. Complexin maintains vesicles in the primed state in C. elegans. Curr. Biol. 2011.
52. 2+-dependent neurotransmitter release. Cell 2001, 104:71-81.
53. Martin J.A., Hu Z., Fenz K.M., Fernandez J., Dittman J.S. Complexin has opposite effects on two modes of synaptic vesicle fusion. Curr. Biol. 2011.
54. Augustin I., Rosenmund C., Sudhof T.C., Brose N. Munc 13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 1999, 400:457-461.
55. Richmond J.E., Davis W.S., Jorgensen E.M. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 1999, 2:959-964.
56. Weimer R.M., Gracheva E.O., Meyrignac O., Miller K.G., Richmond J.E., Bessereau J.-L. Unc-13 and Unc-10/Rim localize synaptic vesicles to specific membrane domains. J. Neurosci. 2006, 26:8040-8047.
57. Madison J.M., Nurrish S., Kaplan J.M. UNC-13 interaction with syntaxin is required for synaptic transmission. Curr. Biol. 2005, 15:2236-2242.
58. Richmond J.E., Weimer R.M., Jorgensen E.M. An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming. Nature 2001, 412:338-341.
59. Nurrish S., Segalat L., Kaplan J.M. Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 1999, 24:231-242.
60. Lackner M.R., Nurrish S.J., Kaplan J.M. Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 1999, 24:335-346.
61. 2+-triggered exocytosis. Curr. Opin. Cell Biol. 2010, 22:496-505.
62. Nonet M.L., Grundahl K., Meyer B.J., Rand J.B. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 1993, 73:1291-1305.
63. 2+ sensor required for asynchronous neurotransmitter release. Cell 2011, 147:666-677.
64. 2+ sensor for spontaneous neurotransmitter release. Science 2010, 327:1614-1618.
65. 2+ signalling. Nat. Rev. Neurosci. 2007, 8:182-193.
66. Fukuda M. Regulation of secretory vesicle traffic by Rab small GTPases. Cell Mol. Life Sci. 2008, 65:2801-2813.
67. Mahoney T.R., Liu Q., Itoh T., Luo S., Hadwiger G., Vincent R., Wang Z.W., Fukuda M., Nonet M.L. Regulation of synaptic transmission by RAB-3 and RAB-27 in Caenorhabditis elegans. Mol. Biol. Cell 2006, 17:2617-2625.
68. Nonet M.L., Staunton J.E., Kilgard M.P., Fergestad T., Hartwieg E., Horvitz H.R., Jorgensen E.M., Meyer B.J. Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 1997, 17:8061-8073.
69. Gracheva E.O., Hadwiger G., Nonet M.L., Richmond J.E. Direct interactions between C. elegans RAB-3 and Rim provide a mechanism to target vesicles to the presynaptic density. Neurosci. Lett. 2008, 444:137-142.
70. Staunton J., Ganetzky B., Nonet M.L. Rabphilin potentiates soluble N-ethylmaleimide sensitive factor attachment protein receptor function independently of rab3. J. Neurosci. 2001, 21:9255-9264.
71. Giovedi S., Vaccaro P., Valtorta F., Darchen F., Greengard P., Cesareni G., Benfenati F. Synapsin is a novel Rab3 effector protein on small synaptic vesicles. I. Identification and characterization of the synapsin I-Rab3 interactions in vitro and in intact nerve terminals. J. Biol. Chem. 2004, 279:43760-43768.
72. Patel M.R., Lehrman E.K., Poon V.Y., Crump J.G., Zhen M., Bargmann C.I., Shen K. Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat. Neurosci. 2006, 9:1488-1498.
73. Sigrist S.J., Schmitz D. Structural and functional plasticity of the cytoplasmic active zone. Curr. Opin. Neurobiol. 2011, 21:144-150.
74. Koushika S.P., Richmond J.E., Hadwiger G., Weimer R.M., Jorgensen E.M., Nonet M.L. A post docking role for active zone protein Rim. Nat. Neurosci. 2001, 4:997-1005.
75. Deken S.L., Vincent R., Hadwiger G., Liu Q., Wang Z.W., Nonet M.L. Redundant localization mechanisms of RIM and ELKS in Caenorhabditis elegans. J. Neurosci. 2005, 25:5975-5983.
76. Dai Y., Taru H., Deken S.L., Grill B., Ackley B., Nonet M.L., Jin Y. SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 2006, 9:1479-1487.
77. Stigloher C., Zhan H., Zhen M., Richmond J., Bessereau J.L. The presynaptic dense projection of the Caenorhabditis elegans cholinergic neuromuscular junction localizes synaptic vesicles at the active zone through SYD-2/liprin and UNC-10/RIM-dependent interactions. J. Neurosci. 2011, 31:4388-4396.
78. Evans G.J.O., Morgan A., Burgoyne R.D. Tying everything together: the multiple roles of cysteine string protein (CSP) in regulated exocytosis. Traffic 2003, 4:653-659.
79. Chandra S., Gallardo G., Fernandez-Chacon R., Schluter O.M., Sudhof T.C. Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 2005, 123:383-396.
80. Johnson J.R., Jenn R.C., Barclay J.W., Burgoyne R.D., Morgan A. Caenorhabditis elegans: a useful tool to decipher neurodegenerative pathways. Biochem. Soc. Trans. 2010, 38:559-563.
81. Barclay J.W., Graham M.E., Edwards M.R., Johnson J.R., Morgan A., Burgoyne R.D. Presynaptic targets for acute ethanol sensitivity. Biochem. Soc. Trans. 2010, 38:172-176.
82. Kapfhamer D., Bettinger J.C., Davies A.G., Eastman C.L., Smail E.A., Heberlein U., McIntire S.L. Loss of RAB-3/A in C. elegans and the mouse affects behavioral response to ethanol. Genes Brain Behav. 2008, 7:669-676.
83. van Swinderen B., Saifee O., Shebester L., Roberson R., Nonet M.L., Crowder C.M. A neomorphic syntaxin mutation blocks volatile-anesthetic action in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:2479-2484.
84. Metz L.B., Dasgupta N., Liu C., Hunt S.J., Crowder C.M. An evolutionarily conserved presynaptic protein is required for isoflurane sensitivity in Caenorhabditis elegans. Anesthesiology 2007, 107:971-982.
85. Wagner O.I., Esposito A., Kohler B., Chen C.W., Shen C.P., Wu G.H., Butkevich E., Mandalapu S., Wenzel D., Wouters F.S., Klopfenstein D.R. Synaptic scaffolding protein SYD-2 clusters and activates kinesin-3 UNC-104 in C. elegans. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19605-19610.