Network motif comparison rationalizes Sec1/Munc18-SNARE regulation mechanism in exocytosis

BMC Systems Biology

Volumn 6, Issue , 2012, Pages

  Xia, Tian ^a   Tong, Jiansong ^b   Rathore, Shailendra S ^c   Gu, Xun ^b   Dickerson, Julie A ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUNC18 PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SEC1 PROTEIN, S CEREVISIAE; SNARE PROTEIN; SYNTAXIN;

ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE; COMPARATIVE STUDY; CYTOLOGY; EXOCYTOSIS; METABOLISM; NERVE CELL; SACCHAROMYCES CEREVISIAE; SYNAPSE;

CELL MEMBRANE; EXOCYTOSIS; MODELS, BIOLOGICAL; MUNC18 PROTEINS; NEURONS; QA-SNARE PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SNARE PROTEINS; SYNAPSES;

EID: 84858258772     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-6-19     Document Type: Article

References (56)

1. Hartwell LH, Hopfield JJ, Leibler S, Murray AW. From molecular to modular cell biology. Nature 1999, 402:C47-C52. 10.1038/35011540, 10591225.
2. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U. Network motifs: simple building blocks of complex networks. Science 2002, 298:824-827. 10.1126/science.298.5594.824, 12399590.
3. Barabasi AL, Oltvai ZN. Network biology: understanding the cell's functional organization. Nat Rev Genet 2004, 5:101-113. 10.1038/nrg1272, 14735121.
4. Song C, Havlin S, Makse HA. Self-similarity of complex networks. Nature 2005, 433:392-395. 10.1038/nature03248, 15674285.
5. Han JD, Bertin N, Hao T, Goldberg DS, Berriz GF, Zhang LV, Dupuy D, Walhout AJ, Cusick ME, Roth FP, Vidal M. Evidence for dynamically organized modularity in the yeast protein-protein interaction network. Nature 2004, 430:88-93. 10.1038/nature02555, 15190252.
6. Wuchty S, Oltvai ZN, Barabasi AL. Evolutionary conservation of motif constituents in the yeast protein interaction network. Nat Genet 2003, 35:176-179. 10.1038/ng1242, 12973352.
7. Song C, Havlin S, Makse HA. Origins of fractality in the growth of complex networks. Nat Phys 2006, 2:275-281.
8. Tyson JJ, Novak B. Functional motifs in biochemical reaction networks. Annu Rev Phys Chem 2010, 61:219-240. 10.1146/annurev.physchem.012809.103457, 20055671.
9. Sharan R, Ideker T. Modeling cellular machinery through biological network comparison. Nat Biotechnol 2006, 24:427-433. 10.1038/nbt1196, 16601728.
10. Barabasi AL, Albert R. Emergence of scaling in random networks. Science 1999, 286:509-512. 10.1126/science.286.5439.509, 10521342.
11. Jones S, Thornton JM. Principles of protein-protein interactions. Proc Natl Acad Sci USA 1996, 93:13-20. 10.1073/pnas.93.1.13, 40170, 8552589.
12. Sollner T, Bennett MK, Whiteheart SW, Scheller RH, Rothman JE. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 1993, 75:409-418. 10.1016/0092-8674(93)90376-2, 8221884.
13. Jahn R, Lang T, Sudhof TC. Membrane fusion. Cell 2003, 112:519-533. 10.1016/S0092-8674(03)00112-0, 12600315.
14. Sudhof TC, Rothman JE. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477. 10.1126/science.1161748, 19164740.
15. Rizo J, Sudhof TC. Snares and Munc18 in synaptic vesicle fusion. Nat Rev Neurosci 2002, 3:641-653.
16. Toonen RF, Verhage M. Munc18-1 in secretion: lonely Munc joins SNARE team and takes control. Trends Neurosci 2007, 30:564-572. 10.1016/j.tins.2007.08.008, 17956762.
17. Schutz D, Zilly F, Lang T, Jahn R, Bruns D. A dual function for Munc-18 in exocytosis of PC12 cells. Eur J Neurosci 2005, 21:2419-2432. 10.1111/j.1460-9568.2005.04095.x, 15932600.
18. Wu MN, Littleton JT, Bhat MA, Prokop A, Bellen HJ. ROP, the Drosophila Sec1 homolog, interacts with syntaxin and regulates neurotransmitter release in a dosage-dependent manner. EMBO J 1998, 17:127-139. 10.1093/emboj/17.1.127, 1170364, 9427747.
19. Gerber SH, Rah JC, Min SW, Liu X, de Wit H, Dulubova I, Meyer AC, Rizo J, Arancillo M, Hammer RE, et al. Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science 2008, 321:1507-1510. 10.1126/science.1163174, 3235364, 18703708.
20. Toonen RF, Verhage M. Vesicle trafficking: pleasure and pain from SM genes. Trends Cell Biol 2003, 13:177-186. 10.1016/S0962-8924(03)00031-X, 12667755.
21. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13:2498-2504. 10.1101/gr.1239303, 403769, 14597658.
22. Burgoyne RD, Morgan A. Membrane trafficking: three steps to fusion. Curr Biol 2007, 17:R255-R258. 10.1016/j.cub.2007.02.006, 17407758.
23. Dacks JB, Field MC. Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J Cell Sci 2007, 120:2977-2985. 10.1242/jcs.013250, 17715154.
24. Khvotchev M, Dulubova I, Sun J, Dai H, Rizo J, Sudhof TC. Dual modes of Munc18-1/SNARE interactions are coupled by functionally critical binding to syntaxin-1 N terminus. J Neurosci 2007, 27:12147-12155. 10.1523/JNEUROSCI.3655-07.2007, 17989281.
25. Shen J, Rathore SS, Khandan L, Rothman JE. SNARE bundle and syntaxin N-peptide constitute a minimal complement for Munc18-1 activation of membrane fusion. J Cell Biol 2010, 190:55-63. 10.1083/jcb.201003148, 2911676, 20603329.
26. Shen J, Tareste DC, Paumet F, Rothman JE, Melia TJ. Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 2007, 128:183-195. 10.1016/j.cell.2006.12.016, 17218264.
27. Xu Y, Su L, Rizo J. Binding of Munc18-1 to synaptobrevin and to the SNARE four-helix bundle. Biochemistry 2010, 49:1568-1576. 10.1021/bi9021878, 2834481, 20102228.
28. Togneri J, Cheng YS, Munson M, Hughson FM, Carr CM. Specific SNARE complex binding mode of the Sec1/Munc-18 protein, Sec1p. Proc Natl Acad Sci USA 2006, 103:17730-17735. 10.1073/pnas.0605448103, 1693815, 17090679.
29. Scott BL, Van Komen JS, Irshad H, Liu S, Wilson KA, McNew JA. Sec1p directly stimulates SNARE-mediated membrane fusion in vitro. J Cell Biol 2004, 167:75-85. 10.1083/jcb.200405018, 2172507, 15466482.
30. Graham ME, Sudlow AW, Burgoyne RD. Evidence against an acute inhibitory role of nSec-1 (munc-18) in late steps of regulated exocytosis in chromaffin and PC12 cells. J Neurochem 1997, 69:2369-2377.
31. Voets T, Toonen RF, Brian EC, de Wit H, Moser T, Rettig J, Sudhof TC, Neher E, Verhage M. Munc18-1 promotes large dense-core vesicle docking. Neuron 2001, 31:581-591. 10.1016/S0896-6273(01)00391-9, 11545717.
32. Thurmond DC, Ceresa BP, Okada S, Elmendorf JS, Coker K, Pessin JE. Regulation of insulin-stimulated GLUT4 translocation by Munc18c in 3T3L1 adipocytes. J Biol Chem 1998, 273:33876-33883. 10.1074/jbc.273.50.33876, 9837979.
33. Fisher RJ, Pevsner J, Burgoyne RD. Control of fusion pore dynamics during exocytosis by Munc18. Science 2001, 291:875-878. 10.1126/science.291.5505.875, 11157167.
34. Sudhof TC. The synaptic vesicle cycle. Annu Rev Neurosci 2004, 27:509-547. 10.1146/annurev.neuro.26.041002.131412, 15217342.
35. Ma W, Trusina A, El-Samad H, Lim WA, Tang C. Defining network topologies that can achieve biochemical adaptation. Cell 2009, 138:760-773. 10.1016/j.cell.2009.06.013, 3068210, 19703401.
36. 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. 10.1038/nsmb.2047, 3087822, 21499244.
37. Fujita Y, Shirataki H, Sakisaka T, Asakura T, Ohya T, Kotani H, Yokoyama S, Nishioka H, Matsuura Y, Mizoguchi A, et al. Tomosyn: a syntaxin-1-binding protein that forms a novel complex in the neurotransmitter release process. Neuron 1998, 20:905-915. 10.1016/S0896-6273(00)80472-9, 9620695.
38. Furgason ML, MacDonald C, Shanks SG, Ryder SP, Bryant NJ, Munson M. The N-terminal peptide of the syntaxin Tlg2p modulates binding of its closed conformation to Vps45p. Proc Natl Acad Sci USA 2009, 106:14303-14308. 10.1073/pnas.0902976106, 2732825, 19667197.
39. Kweon DH, Kim CS, Shin YK. Regulation of neuronal SNARE assembly by the membrane. Nat Struct Biol 2003, 10:440-447. 10.1038/nsb928, 12740606.
40. Lu X, Zhang F, McNew JA, Shin YK. Membrane fusion induced by neuronal SNAREs transits through hemifusion. J Biol Chem 2005, 280:30538-30541. 10.1074/jbc.M506862200, 15980065.
41. Parlati F, Weber T, McNew JA, Westermann B, Sollner TH, Rothman JE. Rapid and efficient fusion of phospholipid vesicles by the alpha-helical core of a SNARE complex in the absence of an N-terminal regulatory domain. Proc Natl Acad Sci USA 1999, 96:12565-12570. 10.1073/pnas.96.22.12565, 22992, 10535962.
42. Scott BL, Van Komen JS, Liu S, Weber T, Melia TJ, McNew JA. Liposome fusion assay to monitor intracellular membrane fusion machines. Methods Enzymol 2003, 372:274-300.
43. Mezer A, Nachliel E, Gutman M, Ashery U. A new platform to study the molecular mechanisms of exocytosis. J Neurosci 2004, 24:8838-8846. 10.1523/JNEUROSCI.2815-04.2004, 15470150.
44. Lang T, Bruns D, Wenzel D, Riedel D, Holroyd P, Thiele C, Jahn R. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J 2001, 20:2202-2213. 10.1093/emboj/20.9.2202, 125434, 11331586.
45. Rickman C, Meunier FA, Binz TD, Davletov B. High affinity interaction of syntaxin and SNAP-25 on the plasma membrane is abolished by botulinum toxin E. J Biol Chem 2004, 279:644-651.
46. Weninger K, Bowen ME, Brunger AT. Single-molecule studies of SNARE complex assembly reveal parallel and antiparallel configurations. Proc Natl Acad Sci USA 2003, 14800-14805.
47. Pevsner J, Hsu SC, Braun JE, Calakos N, Ting AE, Bennett MK, Scheller RH. Specificity and regulation of a synaptic vesicle docking complex. Neuron 1994, 13:353-361. 10.1016/0896-6273(94)90352-2, 8060616.
48. Burkhardt P, Hattendorf DA, Weis WI, Fasshauer D. Munc18a controls SNARE assembly through its interaction with the syntaxin N-peptide. EMBO J 2008, 27:923-933. 10.1038/emboj.2008.37, 2323264, 18337752.
49. Hua Y, Scheller RH. Three SNARE complexes cooperate to mediate membrane fusion. Proc Natl Acad Sci USA 2001, 98:8065-8070. 10.1073/pnas.131214798, 35468, 11427709.
50. Schmidt H, Jirstrand M. Systems Biology Toolbox for MATLAB: a computational platform for research in systems biology. Bioinformatics 2006, 22(4):514-515. 10.1093/bioinformatics/bti799, 16317076.
51. Hoops S, et al. COPASI--a COmplex PAthway SImulator. Bioinformatics 2006, 22(24):3067-3074. 10.1093/bioinformatics/btl485, 17032683.
52. Nicholson KL, et al. Regulation of SNARE complex assembly by an N-terminal domain of the t-SNARE Sso1p. Nat Struct Biol 1998, 5(9):793-802. 10.1038/1834, 9731774.
53. Pobbati AV, Stein A, Fasshauer D. N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 2006, 313(5787):673-676. 10.1126/science.1129486, 16888141.
54. Margittai M, et al. Single-molecule fluorescence resonance energy transfer reveals a dynamic equilibrium between closed and open conformations of syntaxin 1. Proc Natl Acad Sci USA 2003, 100(26):15516-15521. 10.1073/pnas.2331232100, 307599, 14668446.
55. Fasshauer D, Margittai M. A transient N-terminal interaction of SNAP-25 and syntaxin nucleates SNARE assembly. J Biol Chem 2004, 279(9):7613-7621.
56. Tareste D, et al. SNAREpin/Munc18 promotes adhesion and fusion of large vesicles to giant membranes. Proc Natl Acad Sci USA 2008, 105(7):2380-2385. 10.1073/pnas.0712125105, 2268145, 18268324.