Involvement of Rab3A in vesicle priming during exocytosis: Interaction with Munc13-1 and Munc18-1

Traffic

Volumn 12, Issue 10, 2011, Pages 1356-1370

  Huang, Chien Chang ^a   Yang, De Ming ^a,b   Lin, Chung Chih ^a,c   Kao, Lung Sen ^a,c  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^c University System of Taiwan   (Taiwan)

Author keywords

Exocytosis; Munc13 1; Munc18 1; Priming; Rab3A; RIM

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL PROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; PROTEIN MUNC13 1; PROTEIN MUNC18 1; RAB PROTEIN; SYNTAXIN 1A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM VESICLE; EXOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECRETION; RAT;

ANIMALS; EXOCYTOSIS; MICROSCOPY, CONFOCAL; MUNC18 PROTEINS; NERVE TISSUE PROTEINS; PC12 CELLS; PHOTOBLEACHING; PROTEIN BINDING; PROTEIN TRANSPORT; RAB3A GTP-BINDING PROTEIN; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SECRETORY VESICLES; TRANSFECTION;

EID: 80052636800     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01237.x     Document Type: Article

References (43)

1. Macara IG. Role of the Rab3A GTPase in regulated secretion from neuroendocrine cells. Trends Endocrinol Metab 1994;5:267-271.
2. Geppert M, Südhof TC. RAB3 and synaptotagmin: the yin and yang of synaptic membrane fusion. Annu Rev Neurosci 1998;21:75-95.
3. Leenders AG, Lopes da Silva FH, Ghijsen WE, Verhage M. Rab3a is involved in transport of synaptic vesicles to the active zone in mouse brain nerve terminals. Mol Biol Cell 2001;12:3095-3102.
4. Lin CC, Huang CC, Lin KH, Cheng KH, Yang DM, Tsai YS, Ong RY, Huang YN, Kao LS. Visualization of Rab3A dissociation during exocytosis: a study by total internal reflection microscopy. J Cell Physiol 2007;211:316-326.
5. Dulubova I, Lou X, Lu J, Huryeva I, Alam A, Schneggenburger R, Südhof TC, Rizo J. A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity? EMBO J 2005;24:2839-2850.
6. Wang X, Thiagarajan R, Wang Q, Tewolde T, Rich MM, Engisch KL. Regulation of quantal shape by Rab3A: evidence for a fusion pore-dependent mechanism. J Physiol 2008;586:3949-3962.
7. Geppert M, Bolshakov VY, Siegelbaum SA, Takei K, De Camilli P, Hammer RE, Südhof TC. The role of Rab3A in neurotransmitter release. Nature 1994;369:493-497.
8. Ashery U, Varoqueaux F, Voets T, Betz A, Thakur P, Koch H, Neher E, Brose N, Rettig J. Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. EMBO J 2000;19:3586-3596.
9. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Südhof TC, Takahashi M, Rosenmund C, Brose N. β-phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 2002;108:121-133.
10. Virmani T, Ertunc M, Sara Y, Mozhayeva M, Kavalali ET. Phorbol esters target the activity-dependent recycling pool and spare spontaneous vesicle recycling. J Neurosci 2005;25:10922-10929.
11. Betz A, Ashery U, Rickmann M, Augustin I, Neher E, Südhof TC, Rettig J, Brose N. Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 1998;21:123-136.
12. Wierda KD, Toonen RF, de Wit H, Brussaard AB, Verhage M. Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity. Neuron 2007;54:275-290.
13. Barclay JW, Craig TJ, Fisher RJ, Ciufo LF, Evans GJ, Morgan A, Burgoyne RD. Phosphorylation of Munc18 by protein kinase C regulates the kinetics of exocytosis. J Biol Chem 2003;278:10538-10545.
14. Wang Y, Okamoto M, Schmitz F, Hofmann K, Südhof TC. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 1997;388:593-598.
15. Betz A, Thakur P, Junge HJ, Ashery U, Rhee JS, Scheuss V, Rosenmund C, Rettig J, Brose N. Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 2001;30:183-196.
16. Schoch S, Castillo PE, Jo T, Mukherjee K, Geppert M, Wang Y, Schmitz F, Malenka RC, Südhof TC. RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 2002;415:321-326.
17. Verhage M, Maia AS, Plomp JJ, Brussaard AB, Heeroma JH, Vermeer H, Toonen RF, Hammer RE, van den Berg TK, Missler M, Geuze HJ, Südhof TC. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000;287:864-869.
18. Voets T, Toonen RF, Brian EC, de Wit H, Moser T, Rettig J, Südhof TC, Neher E, Verhage M. Munc18-1 promotes large dense-core vesicle docking. Neuron 2001;31:581-591.
19. Yang B, Steegmaier M, Gonzalez LC Jr, Scheller RH. nSec1 binds a closed conformation of syntaxin1A. J Cell Biol 2000;148:247-252.
20. Medine CN, Rickman C, Chamberlain LH, Duncan RR. Munc18-1 prevents the formation of ectopic SNARE complexes in living cells. J Cell Sci 2007;120:4407-4415.
21. Gladycheva SE, Ho CS, Lee YY, Stuenkel EL. Regulation of syntaxin1A-munc18 complex for SNARE pairing in HEK293 cells. J Physiol 2004;558:857-871.
22. Fujita Y, Sasaki T, Fukui K, Kotani H, Kimura T, Hata Y, Südhof TC, Scheller RH, Takai Y. Phosphorylation of Munc-18/n-Sec1/rbSec1 by protein kinase C: its implication in regulating the interaction of Munc-18/n-Sec1/rbSec1 with syntaxin. J Biol Chem 1996;271:7265-7268.
23. Graham ME, Handley MT, Barclay JW, Ciufo LF, Barrow SL, Morgan A, Burgoyne RD. 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.
24. van Weering JR, Toonen RF, Verhage M. The role of Rab3a in secretory vesicle docking requires association/dissociation of guanidine phosphates and Munc18-1. PLoS One 2007;2:e616.
25. Zenisek D, Steyer JA, Almers W. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 2000;406:849-854.
26. Barg S, Olofsson CS, Schriever-Abeln J, Wendt A, Gebre-Medhin S, Renstrom E, Rorsman P. Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron 2002;33:287-299.
27. Taraska JW, Perrais D, Ohara-Imaizumi M, Nagamatsu S, Almers W. Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci U S A 2003;100:2070-2075.
28. Perrais D, Kleppe IC, Taraska JW, Almers W. Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J Physiol 2004;560:413-428.
29. Gulyás-Kovács A, de Wit H, Milosevic I, Kochubey O, Toonen R, Klingauf J, Verhage M, Sørensen JB. Munc18-1: sequential interactions with the fusion machinery stimulate vesicle docking and priming. J Neurosci 2007;27:8676-8686.
30. Deák F, Xu Y, Chang WP, Dulubova I, Khvotchev M, Liu X, Südhof TC, Rizo J. Munc18-1 binding to the neuronal SNARE complex controls synaptic vesicle priming. J Cell Biol 2009;184:751-764.
31. Fisher RJ, Pevsner J, Burgoyne RD. Control of fusion pore dynamics during exocytosis by Munc18. Science 2001;291:875-878.
32. Diao J, Su Z, Lu X, Yoon TY, Shin YK, Ha T. Single-vesicle fusion assay reveals Munc18-1 binding to the SNARE core is sufficient for stimulating membrane fusion. ACS Chem Neurosci 2010;1:168-174.
33. Südhof TC. The synaptic vesicle cycle. Annu Rev Neurosci 2004;27:509-547.
34. Schonn JS, van Weering RT, Mohrmann R, Schlüter OM, Südhof TC, de Wit H, Verhage M, Sørensen JB. Rab3 proteins involved in vesicle biogenesis and priming in embryonic mouse chromaffin cells. Traffic 2010;11:1415-1428.
35. Lu J, Machius M, Dulubova I, Dai H, Südhof TC, Tomchick DR, Rizo J. Structural basis for a Munc13-1 homodimer to Munc13-1/RIM heterodimer switch. PLoS Biol 2006;4:e192.
36. Basu J, Shen N, Dulubova I, Lu J, Guan R, Guryev O, Grishin NV, Rosenmund C, Rizo J. A minimal domain responsible for Munc13 activity. Nat Struct Mol Biol 2005;12:1017-1018.
37. Stevens DR, Wu ZX, Matti U, Junge HJ, Schirra C, Becherer U, Wojcik SM, Brose N, Rettig J. Identification of the minimal protein domain required for priming activity of Munc13-1. Curr Biol 2005;15:2243-2248.
38. Dulubova I, Khvotchev M, Liu S, Huryeva I, Südhof TC, Rizo J. Munc18-1 binds directly to the neuronal SNARE complex. Proc Natl Acad Sci U S A 2007;104:2697-2702.
39. Südhof TC, Rothman JE. Membrane fusion: grappling with SNARE and SM proteins. Science 2009;323:474-477.
40. Guan R, Dai H, Rizo J. Binding of the Munc13-1 MUN domain to membrane-anchored SNARE complexes. Biochemistry 2008;47: 1471-1481.
41. Yang DM, Huang CC, Lin HY, Tsai DP, Kao LS, Chi CW, Lin CC. Tracking of secretory vesicles of PC12 cells by total internal reflection fluorescence microscopy. J Microsc 2003;209:223-227.
42. Tsuboi T, Fukuda M. Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells. J Cell Sci 2006;119:2196-2203.
43. Liu J, Ernst SA, Gladycheva SE, Lee YY, Lentz SI, Ho CS, Li Q, Stuenkel EL. Fluorescence resonance energy transfer reports properties of syntaxin1A interaction with Munc18-1 in vivo. J Biol Chem 2004;279:55924-55936.