Domain 3a of Munc18-1 plays a crucial role at the priming stage of exocytosis

Journal of Cell Science

Volumn 126, Issue 11, 2013, Pages 2361-2371

  Han, Gayoung Anna ^a,b   Bin, Na Ryum ^a,b   Kang, Soo Young Ann ^a   Han, Liping ^a,b   Sugita, Shuzo ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Exocytosis; Munc18; Secretory vesicles; Snare; Syntaxin

Indexed keywords

MUNC18 PROTEIN; MUTANT PROTEIN; SNARE PROTEIN; SYNTAXIN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; EXOCYTOSIS; GENE EXPRESSION; GENE INSERTION; GENE SILENCING; MOLECULAR DOCKING; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; STOICHIOMETRY;

EXOCYTOSIS; MUNC18; SECRETORY VESICLES; SNARE; SYNTAXIN;

ANIMALS; EXOCYTOSIS; MEMBRANE FUSION; MUNC18 PROTEINS; PC12 CELLS; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; QA-SNARE PROTEINS; RATS; SNARE PROTEINS;

EID: 84880012224     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.126862     Document Type: Article

References (41)

1. Arunachalam, L., Han, L., Tassew, N. G., He, Y., Wang, L., Xie, L., Fujita, Y., Kwan, E., Davletov, B., Monnier, P. P. et al. (2008). Munc18-1 is critical for plasma membrane localization of syntaxin1 but not of SNAP-25 in PC12 cells. Mol. Biol. Cell 19, 722-734.
2. Barnstable, C. J., Hofstein, R. and Akagawa, K. (1985). A marker of early amacrine cell development in rat retina. Brain Res. 352, 286-290.
3. Boyd, A., Ciufo, L. F., Barclay, J. W., Graham, M. E., Haynes, L. P., Doherty, M. K., Riesen, M., Burgoyne, R. D. and Morgan, A. (2008). A random mutagenesis approach to isolate dominant-negative yeast sec1 mutants reveals a functional role for domain 3a in yeast and mammalian Sec1/Munc18 proteins. Genetics 180, 165-178.
4. de Wit, H., Walter, A. M., Milosevic, I., Gulyás-Kovács, A., Riedel, D., Sørensen, J. B. and Verhage, M. (2009). Synaptotagmin-1 docks secretory vesicles to syntaxin- 1/SNAP-25 acceptor complexes. Cell 138, 935-946.
5. Deák, F., Xu, Y., Chang, W. P., Dulubova, I., Khvotchev, M., Liu, X., Südhof, T. C. and Rizo, J. (2009). Munc18-1 binding to the neuronal SNARE complex controls synaptic vesicle priming. J. Cell Biol. 184, 751-764.
6. Dulubova, I., Khvotchev, M., Liu, S., Huryeva, I., Südhof, T. C. and Rizo, J. (2007). Munc18-1 binds directly to the neuronal SNARE complex. Proc. Natl. Acad. Sci. USA 104, 2697-2702.
7. Gerber, S. H., Rah, J. C., Min, S. W., Liu, X., de Wit, H., Dulubova, I., Meyer, A. C., Rizo, J., Arancillo, M., Hammer, R. E. et al. (2008). Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science 321, 1507-1510.
8. Guan, K. L. and Dixon, J. E. (1991). Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192, 262-267.
9. Gulyás-Kovács, A., de Wit, H., Milosevic, I., Kochubey, O., Toonen, R., Klingauf, J., Verhage, M. and Sørensen, J. B. (2007). Munc18-1: sequential interactions with the fusion machinery stimulate vesicle docking and priming. J. Neurosci. 27, 8676-8686.
10. 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. et al. (2009). 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 20, 4962-4975.
11. Han, G. A., Malintan, N. T., Collins, B. M., Meunier, F. A. and Sugita, S. (2010). Munc18-1 as a key regulator of neurosecretion. J. Neurochem. 115, 1-10.
12. Han, G. A., Malintan, N. T., Saw, N. M., Li, L., Han, L., Meunier, F. A., Collins, B. M. and Sugita, S. (2011). 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.
13. Harrison, S. D., Broadie, K., van de Goor, J. Rubin G. M. (1994). Mutations in the Drosophila Rop gene suggest a function in general secretion and synaptic transmission. Neuron 13, 555-566.
14. Hosono, R., Hekimi, S., Kamiya, Y., Sassa, T., Murakami, S., Nishiwaki, K., Miwa, J., Taketo, A. and Kodaira, K. I. (1992). The unc-18 gene encodes a novel protein affecting the kinetics of acetylcholine metabolism in the nematode Caenorhabditis elegans. J. Neurochem. 58, 1517-1525.
15. Hu, S. H., Latham, C. F., Gee, C. L., James, D. E. and Martin, J. L. (2007). Structure of the Munc18c/Syntaxin4 N-peptide complex defines universal features of the Npeptide binding mode of Sec1/Munc18 proteins. Proc. Natl. Acad. Sci. USA 104, 8773-8778.
16. Hu, S. H., Christie, M. P., Saez, N. J., Latham, C. F., Jarrott, R., Lua, L. H., Collins, B. M. and Martin, J. L. (2010). Possible roles for Munc18-1 domain 3a and Syntaxin1 N-peptide and C-terminal anchor in SNARE complex formation. Proc. Natl. Acad. Sci. USA 108, 1040-1045.
17. Johnson, J. R., Ferdek, P., Lian, L. Y., Barclay, J. W., Burgoyne, R. D. and Morgan, A. (2009). Binding of UNC-18 to the N-terminus of syntaxin is essential for neurotransmission in Caenorhabditis elegans. Biochem. J. 418, 73-80.
18. Kauppi, M., Wohlfahrt, G. and Olkkonen, V. M. (2002). Analysis of the Munc18bsyntaxin binding interface. Use of a mutant Munc18b to dissect the functions of syntaxins 2 and 3. J. Biol. Chem. 277, 43973-43979.
19. Khvotchev, M., Dulubova, I., Sun, J., Dai, H., Rizo, J. and Südhof, T. C. (2007). Dual modes of Munc18-1/SNARE interactions are coupled by functionally critical binding to syntaxin-1 N terminus. J. Neurosci. 27, 12147-12155.
20. Martin, S., Tomatis, V. M., Papadopulos, A., Christie, M. P., Malintan, N. T., Gormal, R. S., Sugita, S., Martin, J. L., Collins, B. M. and Meunier, F. A. (2013). The Munc18-1 domain 3a loop is essential for neuroexocytosis but not for syntaxin- 1A transport to the plasma membrane. J. Cell Sci. 126, 2353-2360.
21. Malintan, N. T., Nguyen, T. H., Han, L., Latham, C. F., Osborne, S. L., Wen, P. J., Lim, S. J., Sugita, S., Collins, B. M. and Meunier, F. A. (2009). Abrogating Munc18-1-SNARE complex interaction has limited impact on exocytosis in PC12 cells. J. Biol. Chem. 284, 21637-21646.
22. McEwen, J. M. and Kaplan, J. M. (2008). UNC-18 promotes both the anterograde trafficking and synaptic function of syntaxin. Mol. Biol. Cell 19, 3836-3846.
23. Medine, C. N., Rickman, C., Chamberlain, L. H. and Duncan, R. R. (2007). Munc18- 1 prevents the formation of ectopic SNARE complexes in living cells. J. Cell Sci. 120, 4407-4415.
24. Meijer, M., Burkhardt, P., de Wit, H., Toonen, R. F., Fasshauer, D. and Verhage, M. (2012). Munc18-1 mutations that strongly impair SNARE-complex binding ort normal synaptic transmission. EMBO J. 31, 2156-2168.
25. Misura, K. M., Scheller, R. H. and Weis, W. I. (2000). Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature 404, 355-362.
26. Okamoto, M. and Südhof, T. C. (1997). Mints, Munc18-interacting proteins in synaptic vesicle exocytosis. J. Biol. Chem. 272, 31459-31464.
27. Rickman, C., Medine, C. N., Bergmann, A. and Duncan, R. R. (2007). Functionally and spatially distinct modes of munc18-syntaxin 1 interaction. J. Biol. Chem. 282, 12097-12103.
28. Rodkey, T. L., Liu, S., Barry, M. and McNew, J. A. (2008). Munc18a scaffolds SNARE assembly to promote membrane fusion. Mol. Biol. Cell 19, 5422-5434.
29. Rowe, J., Corradi, N., Malosio, M. L., Taverna, E., Halban, P., Meldolesi, J. and Rosa, P. (1999). Blockade of membrane transport and disassembly of the Golgi complex by expression of syntaxin 1A in neurosecretion-incompetent cells: prevention by rbSEC1. J. Cell Sci. 112, 1865-1877.
30. Rowe, J., Calegari, F., Taverna, E., Longhi, R. and Rosa, P. (2001). Syntaxin 1A is delivered to the apical and basolateral domains of epithelial cells: the role of munc-18 proteins. J. Cell Sci. 114, 3323-3332.
31. Schiestl, R. H. and Gietz, R. D. (1989). High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16, 339-346.
32. Shen, J., Tareste, D. C., Paumet, F., Rothman, J. E. and Melia, T. J. (2007). Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128, 183-195.
33. Südhof, T. C. and Rothman, J. E. (2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477.
34. Tareste, D., Shen, J., Melia, T. J. and Rothman, J. E. (2008). SNAREpin/Munc18 promotes adhesion and fusion of large vesicles to giant membranes. Proc. Natl. Acad. Sci. USA 105, 2380-2385.
35. Toonen, R. F., Kochubey, O., de Wit, H., Gulyas-Kovacs, A., Konijnenburg, B., Sørensen, J. B., Klingauf, J. and Verhage, M. (2006). Dissecting docking and tethering of secretory vesicles at the target membrane. EMBO J. 25, 3725-3737.
36. 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. et al. (2000). Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864-869.
37. Voets, T., Toonen, R. F., Brian, E. C., de Wit, H., Moser, T., Rettig, J., Südhof, T. C., Neher, E. and Verhage, M. (2001). Munc18-1 promotes large dense-core vesicle docking. Neuron 31, 581-591.
38. Vojtek, A. B., Hollenberg, S. M. and Cooper, J. A. (1993). Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74, 205-214.
39. Voss, S. and Skerra, A. (1997). Mutagenesis of a flexible loop in streptavidin leads to higher affinity for the Strep-tag II peptide and improved performance in recombinant protein purification. Protein Eng. 10, 975-982.
40. Xu, Y., Su, L. and Rizo, J. (2010). Binding of Munc18-1 to synaptobrevin and to the SNARE four-helix bundle. Biochemistry 49, 1568-1576.
41. Zhou, P., Pang, Z. P., Yang, X., Zhang, Y., Rosenmund, C., Bacaj, T. and Südhof, T. C. (2012). Syntaxin-1 N-peptide and Habc-domain perform distinct essential functions in synaptic vesicle fusion. EMBO J. 32, 159-171.