Contact-induced clustering of syntaxin and munc18 docks secretory granules at the exocytosis site

Nature Communications

Volumn 5, Issue , 2014, Pages

  Gandasi, Nikhil R ^a   Barg, Sebastian ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; MUNC13 PROTEIN; MUNC18 PROTEIN; NEUROPEPTIDE Y; PROTEIN; RAB3 PROTEIN; SNAP25 PROTEIN; SYNTAXIN; UNCLASSIFIED DRUG; STX1A PROTEIN, RAT; STXBP1 PROTEIN, RAT; STXBP2 PROTEIN, RAT; SYNTAXIN 1;

GENE EXPRESSION; PLASMA; PROTEIN; SECRETION;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXOCYTOSIS; MOLECULAR DOCKING; NONHUMAN; PROTEIN DOMAIN; QUANTITATIVE ANALYSIS; RAT; SECRETORY GRANULE; SECRETORY VESICLE; ANIMAL; CELL MEMBRANE; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL MEMBRANE; EXOCYTOSIS; INSULIN; MUNC18 PROTEINS; RATS; SECRETORY VESICLES; SYNTAXIN 1;

EID: 84901050663     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4914     Document Type: Article

References (70)

1. Klenchin, V. A. & Martin, T. F. Priming in exocytosis: attaining fusion-competence after vesicle docking. Biochimie 82, 399-407 (2000). (Pubitemid 30391896)
2. Barg, S. et al. Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron 33, 287-299 (2002). (Pubitemid 34127760)
3. Parsons, T. D., Coorssen, J. R., Horstmann, H. & Almers, W. Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 15, 1085-1096 (1995).
4. Hugo, S. et al. Deciphering dead-end docking of large dense core vesicles in bovine chromaffin cells. J. Neurosci. 33, 17123-17137 (2013).
5. Olofsson, C. et al. Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic B-cells. Pflugers Archiv. Eur. J. Physiol. 444, 43-51 (2002). (Pubitemid 34499244)
6. Michael, D. J., Xiong, W., Geng, X., Drain, P. & Chow, R. H. Human insulin vesicle dynamics during pulsatile secretion. Diabetes 56, 1277-1288 (2007). (Pubitemid 46715608)
7. Barg, S. et al. Fast exocytosis with few Ca(2) channels in insulin-secreting mouse pancreatic B cells. Biophys. J. 81, 3308-3323 (2001). (Pubitemid 33111478)
8. Rorsman, P. et al. The cell physiology of biphasic insulin secretion. News. Physiol. Sci. 15, 72-77 (2000).
9. Porksen, N. The in vivo regulation of pulsatile insulin secretion. Diabetologia 45, 3-20 (2002). (Pubitemid 34118538)
10. Toonen, R. F. et al. Dissecting docking and tethering of secretory vesicles at the target membrane. EMBO J. 25, 3725-3737 (2006). (Pubitemid 44300259)
11. Nofal, S., Becherer, U., Hof, D., Matti, U. & Rettig, J. Primed vesicles can be distinguished from docked vesicles by analyzing their mobility. J. Neurosci. 27, 1386-1395 (2007).
12. Ohara-Imaizumi, M. et al. Imaging analysis reveals mechanistic differences between first-and second-phase insulin exocytosis. J. Cell Biol. 177, 695-705 (2007). (Pubitemid 46799840)
13. de Wit, H., Cornelisse, L. N., Toonen, R. F. & Verhage, M. Docking of secretory vesicles is syntaxin dependent. PLoS ONE 1, e126 (2006).
14. Hammarlund, M., Palfreyman, M. T., Watanabe, S., Olsen, S. & Jorgensen, E. M. Open syntaxin docks synaptic vesicles. PLoS Biol. 5, e198 (2007).
15. Voets, T. et al. Munc18-1 promotes large dense-core vesicle docking. Neuron 31, 581-591 (2001). (Pubitemid 32835113)
16. de Wit, H. et al. Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138, 935-946 (2009).
17. Weimer, R. M. et al. Defects in synaptic vesicle docking in unc-18 mutants. Nat. Neurosci. 6, 1023-1030 (2003). (Pubitemid 37186193)
18. Han, G. A. et al. Munc18-1 domain-1 controls vesicle docking and secretion by interacting with syntaxin-1 and chaperoning it to the plasma membrane. Mol. Biol. Cell 22, 4134-4149 (2011).
19. Wu, Y. et al. All three components of the neuronal SNARE complex contribute to secretory vesicle docking. J. Cell Biol. 198, 323-330 (2012).
20. Reist, N. E. et al. Morphologically docked synaptic vesicles are reduced in synaptotagmin mutants of Drosophila. J. Neurosci. 18, 7662-7673 (1998). (Pubitemid 28441008)
21. Kasai, K. et al. Rab27a mediates the tight docking of insulin granules onto the plasma membrane during glucose stimulation. J. Clin. Invest. 115, 388-396 (2005). (Pubitemid 40385480)
22. Tsuboi, T. & Fukuda, M. Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells. J. Cell Sci. 119, 2196-2203 (2006). (Pubitemid 43960309)
23. Coppola, T. et al. Pancreatic beta-cell protein granuphilin binds Rab3 and Munc-18 and controls exocytosis. Mol. Biol. Cell 13, 1906-1915 (2002). (Pubitemid 34651481)
24. Lang, T., Margittai, M., Holzler, H. & Jahn, R. SNAREs in native plasma membranes are active and readily form core complexes with endogenous and exogenous SNAREs. J. Cell Biol. 158, 751-760 (2002). (Pubitemid 34920113)
25. Arac, D. et al. Close membrane-membrane proximity induced by Ca(2)-dependent multivalent binding of synaptotagmin-1 to phospholipids. Nat. Struct. Mol. Biol. 13, 209-217 (2006). (Pubitemid 43348506)
26. Honigmann, A. et al. Phosphatidylinositol 4, 5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nat. Struct. Mol. Biol. 20, 679-686 (2013).
27. Khuong, T. M. et al. Synaptic PI(3, 4, 5)P3 is required for Syntaxin1A clustering and neurotransmitter release. Neuron 77, 1097-1108 (2013).
28. Bar-On, D. et al. Super-resolution imaging reveals the internal architecture of nano-sized syntaxin clusters. J. Biol. Chem. 287, 27158-27167 (2012).
29. Sieber, J. J. et al. Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317, 1072-1076 (2007). (Pubitemid 47330189)
30. Knowles, M. et al. Single secretory granules of live cells recruit syntaxin-1 and synaptosomal associated protein 25 (SNAP-25) in large copy numbers. Proc. Natl Acad. Sci. USA 107, 20810-20815 (2010).
31. Lang, T. et al. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20, 2202-2213 (2001). (Pubitemid 32410590)
32. Pertsinidis, A. et al. Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ. Proc. Natl Acad. Sci. USA 110, E2812-E2820 (2013).
33. Aoyagi, K. et al. The activation of exocytotic sites by the formation of phosphatidylinositol 4, 5-bisphosphate microdomains at syntaxin clusters. J. Biol. Chem. 280, 17346-17352 (2005). (Pubitemid 41389204)
34. van den Bogaart, G. et al. Membrane protein sequestering by ionic protein-lipid interactions. Nature 479, 552-555 (2011).
35. Zilly, F. E., Sorensen, J. B., Jahn, R. & Lang, T. Munc18-bound syntaxin readily forms SNARE complexes with synaptobrevin in native plasma membranes. PLoS Biol. 4, e330 (2006).
36. Barg, S., Knowles, M., Chen, X., Midorikawa, M. & Almers, W. Syntaxin clusters assemble reversibly at sites of secretory granules in live cells. Proc. Natl Acad. Sci. USA 107, 20804-20809 (2010).
37. Dulubova, I. et al. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 18, 4372-4382 (1999). (Pubitemid 29391247)
38. Richmond, J. E., Davis, W. S. & Jorgensen, E. M. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 2, 959-964 (1999). (Pubitemid 30599557)
39. 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). (Pubitemid 27058545)
40. 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. 18, 542-549 (2011).
41. Gromada, J. et al. CaM kinase II-dependent mobilization of secretory granules underlies acetylcholine-induced stimulation of exocytosis in mouse pancreatic B-cells. J. Physiol. 518(Pt 3): 745-759 (1999). (Pubitemid 29387244)
42. Ashery, U. et al. Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. EMBO J. 19, 3586-3596 (2000). (Pubitemid 30462117)
43. Sieber, J. J., Willig, K. I., Heintzmann, R., Hell, S. W. & Lang, T. The SNARE motif is essential for the formation of syntaxin clusters in the plasma membrane. Biophys. J. 90, 2843-2851 (2006).
44. Zhou, P. et al. Syntaxin-1 N-peptide and Habc-domain perform distinct essential functions in synaptic vesicle fusion. EMBO J. 32, 159-171 (2013).
45. Rickman, C. et al. t-SNARE protein conformations patterned by the lipid microenvironment. J. Biol. Chem. 285, 13535-13541 (2010).
46. Smith, M. B. et al. Interactive, computer-assisted tracking of speckle trajectories in fluorescence microscopy: application to actin polymerization and membrane fusion. Biophys. J. 101, 1794-1804 (2011).
47. Sbalzarini, I. F. & Koumoutsakos, P. Feature point tracking and trajectory analysis for video imaging in cell biology. J. Struct. Biol. 151, 182-195 (2005). (Pubitemid 41074826)
48. Schutz, D., Zilly, F., Lang, T., Jahn, R. & Bruns, D. A dual function for Munc-18 in exocytosis of PC12 cells. Eur. J. Neurosci. 21, 2419-2432 (2005). (Pubitemid 40813924)
49. Fernandez-Busnadiego, R. et al. Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. J. Cell Biol. 188, 145-156 (2010).
50. Hodel, A., Schafer, T., Gerosa, D. & Burger, M. M. In chromaffin cells, the mammalian Sec1p homologue is a syntaxin 1A-binding protein associated with chromaffin granules. J. Biol. Chem. 269, 8623-8626 (1994).
51. Kee, Y. & Scheller, R. H. Localization of synaptotagmin-binding domains on syntaxin. J. Neurosci. 16, 1975-1981 (1996). (Pubitemid 26144010)
52. Zhong, P. et al. An alpha-helical minimal binding domain within the H3 domain of syntaxin is required for SNAP-25 binding. Biochemistry 36, 4317-4326 (1997). (Pubitemid 27171606)
53. Shi, L., Kummel, D., Coleman, J., Melia, T. J. & Giraudo, C. G. Dual roles of Munc18-1 rely on distinct binding modes of the central cavity with Stx1A and SNARE complex. Mol. Biol. Cell 22, 4150-4160 (2011).
54. Kabachinski, G., Yamaga, M., Kielar-Grevstad, D. M., Bruinsma, S. & Martin, T. F. CAPS and Munc13 utilize distinct PIP2-linked mechanisms to promote vesicle exocytosis. Mol. Biol. Cell 25, 508-521 (2014).
55. Betz, A. et al. Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30, 183-196 (2001). (Pubitemid 32441686)
56. Coppola, T. et al. Direct interaction of the Rab3 effector RIM with Ca2 channels, SNAP-25, and synaptotagmin. J. Biol. Chem. 276, 32756-32762 (2001).
57. Zhu, D. et al. Syntaxin-3 regulates newcomer insulin granule exocytosis and compound fusion in pancreatic beta cells. Diabetologia 56, 359-369 (2013).
58. Kasai, K., Fujita, T., Gomi, H. & Izumi, T. Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 9, 1191-1203 (2008). (Pubitemid 351916892)
59. Gembal, M., Detimary, P., Gilon, P., Gao, Z. Y. & Henquin, J. C. Mechanisms by which glucose can control insulin release independently from its action on adenosine triphosphate-sensitive K channels in mouse B cells. J. Clin. Invest. 91, 871-880 (1993). (Pubitemid 23095261)
60. Lorenz, M. A., El Azzouny, M. A., Kennedy, R. T. & Burant, C. F. Metabolome response to glucose in the beta-cell line INS-1 832/13. J. Biol. Chem. 288, 10923-10935 (2013).
61. Straub, S. G., Shanmugam, G. & Sharp, G. W. Stimulation of insulin release by glucose is associated with an increase in the number of docked granules in the beta-cells of rat pancreatic islets. Diabetes 53, 3179-3183 (2004). (Pubitemid 39564493)
62. Ostenson, C. G., Gaisano, H., Sheu, L., Tibell, A. & Bartfai, T. Impaired gene and protein expression of exocytotic soluble N-ethylmaleimide attachment protein receptor complex proteins in pancreatic islets of type 2 diabetic patients. Diabetes 55, 435-440 (2006). (Pubitemid 43343274)
63. Hohmeier, H. E. et al. Isolation of INS-1-derived cell lines with robust ATP-sensitive K channel-dependent and-independent glucose-stimulated insulin secretion. Diabetes 49, 424-430 (2000). (Pubitemid 30131788)
64. Stevens, D. R. et al. Identification of the minimal protein domain required for priming activity of Munc13-1. Curr. Biol. 15, 2243-2248 (2005). (Pubitemid 41790618)
65. Handley, M. T., Haynes, L. P. & Burgoyne, R. D. Differential dynamics of Rab3A and Rab27A on secretory granules. J. Cell Sci. 120, 973-984 (2007). (Pubitemid 46638512)
66. An, S. J. & Almers, W. Tracking SNARE complex formation in live endocrine cells. Science 306, 1042-1046 (2004). (Pubitemid 39482909)
67. Prekeris, R., Yang, B., Oorschot, V., Klumperman, J. & Scheller, R. H. Differential roles of syntaxin 7 and syntaxin 8 in endosomal trafficking. Mol. Biol. Cell 10, 3891-3908 (1999). (Pubitemid 29534033)
68. Yang, L. et al. Secretory vesicles are preferentially targeted to areas of low molecular SNARE density. PLoS ONE 7, e49514 (2012).
69. Taraska, J. W., 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. USA 100, 2070-2075 (2003). (Pubitemid 36254575)
70. Henriques, R. et al. QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ. Nat. Methods 7, 339-340.