Three αSNAP and 10 ATP molecules are used in SNARE complex disassembly by N-ethylmaleimide-sensitive factor (NSF)

Journal of Biological Chemistry

Volumn 290, Issue 4, 2015, Pages 2175-2188

  Shah, Niket ^a   Colbert, Karen N ^a   Enos, Michael D ^a   Herschlag, Daniel ^a   Weis, William I ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINS;

ADAPTOR PROTEINS; ATP HYDROLYSIS; HELIX BUNDLE; HIGHLY STABLES; INTRACELLULAR MEMBRANES; SINGLE MOLECULE; SNARE PROTEINS;

MOLECULES;

ADAPTOR PROTEIN; ADENOSINE TRIPHOSPHATE; ALPHA SYNAPTOSOME ASSOCIATED PROTEIN; MEMBRANE PROTEIN; SNARE PROTEIN; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR; UNCLASSIFIED DRUG; NUCLEOTIDE; PROTEIN BINDING; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN;

ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; HYDROLYSIS; KINETICS; MOLECULAR BIOLOGY; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STEADY STATE; ANIMAL; ANISOTROPY; CELL MEMBRANE; CHEMISTRY; CRICETULUS; FLUORESCENCE MICROSCOPY; MEMBRANE FUSION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN ENGINEERING; PROTEIN TRANSPORT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANISOTROPY; BASE SEQUENCE; CELL MEMBRANE; CRICETULUS; ESCHERICHIA COLI; HYDROLYSIS; MEMBRANE FUSION; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN TRANSPORT; SNARE PROTEINS; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS;

EID: 84921676298     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.620849     Document Type: Article

References (33)

1. Brunger, A. T. (2005) Structure and function of SNARE and SNARE-interacting proteins. Q. Rev. Biophys. 38, 1-47
2. Söllner, T., Whiteheart, S. W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., and Rothman, J. E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324
3. Jahn, R., and Scheller, R. H. (2006) SNAREs: engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643
4. Gao, Y., Zorman, S., Gundersen, G., Xi, Z., Ma, L., Sirinakis, G., Rothman, J. E., and Zhang, Y. (2012) Single reconstituted neuronal SNARE complexes zipper in three distinct stages. Science 337, 1340-1343
5. Block, M. R., Glick, B. S., Wilcox, C. A., Wieland, F. T., and Rothman, J. E. (1988) Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc. Natl. Acad. Sci. U.S.A. 85, 7852-7856
6. Fleming, K. G., Hohl, T. M., Yu, R. C., Müller, S. A., Wolpensinger, B., Engel, A., Engelhardt, H., Brünger, A. T., Söllner, T. H., and Hanson, P. I. (1998) A revised model for the oligomeric state of the N-ethylmaleimide-sensitive fusion protein, NSF. J. Biol. Chem. 273, 15675-15681
7. Tagaya, M., Wilson, D. W., Brunner, M., Arango, N., and Rothman, J. E. (1993) Domain structure of an N-ethylmaleimide-sensitive fusion protein involved in vesicular transport. J. Biol. Chem. 268, 2662-2666
8. Whiteheart, S. W., Rossnagel, K., Buhrow, S. A., Brunner, M., Jaenicke, R., and Rothman, J. E. (1994) N-Ethylmaleimide-sensitive fusion protein: a trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J. Cell Biol. 126, 945-954
9. Matveeva, E., and Whiteheart, S. W. (1998) The effects of SNAP/SNARE complexes on the ATPase of NSF. FEBS Lett. 435, 211-214
10. White, S. R., and Lauring, B. (2007)AAA+ATPases: achieving diversity of fundtion with conserved machinery. Traffic 8, 1657-1667
11. Nagiec, E. E., Bernstein, A., and Whiteheart, S. W. (1995) Each domain of the N-ethylmaleimide-sensitive fusion protein contributes to its transport activity. J. Biol. Chem. 270, 29182-29188
12. Barnard, R. J. O., Morgan, A., and Burgoyne, R. D. (1997) Stimulation of NSF ATPase activity by α-SNAP is required for SNARE complex disassembly and exocytosis. J. Cell Biol. 139, 875-883
13. Morgan, A., Dimaline, R., and Burgoyne, R. D. (1994) The ATPase activity of N-ethylmaleimide-sensitive fusion protein (NSF) is regulated by soluble NSF attachment proteins. J. Biol. Chem. 269, 29347-29350
14. Steel, G. J., and Morgan, A. (1998) Selective stimulation of the D1 ATPase domain of N-ethylmaleimide-sensitive fusion protein (NSF) by soluble NSF attachment proteins. FEBS Lett. 423, 113-116
15. Vivona, S., Cipriano, D. J., O'Leary, S., Li, Y. H., Fenn, T. D., and Brunger, A. T. (2013) Disassembly of all SNARE complexes by N-ethylmaleimide-sensitive factor (NSF) is initiated by a conserved 1:1 interaction between α-soluble NSF attachment protein (SNAP) and SNARE complex. J. Biol. Chem. 288, 24984-24991
16. Rice, L. M., and Brunger, A. T. (1999) Crystal structure of the vesicular transport protein Sec17: implications for SNAP function in SNARE complex assembly. Mol. Cell 4, 85-95
17. Marz, K. E., Lauer, J. M., and Hanson, P. I. (2003) Defining the SNARE complex binding surface of α-SNAP: implications for SNARE complex disassembly. J. Biol. Chem. 278, 27000-27008
18. Hohl, T. M., Parlati, F., Wimmer, C., Rothman, J. E., Söllner, T. H., and Engelhardt, H. (1998) Arrangement of subunits in 20 S particles consisting of NSF, SNAPs, and SNARE complexes. Mol. Cell 2, 539-548
19. Wimmer, C., Hohl, T. M., Hughes, C. A., Müller, S. A., Söllner, T. H., Engel, A., and Rothman, J. E. (2001) Molecular mass, stoichiometry, and assembly of 20 S particles. J. Biol. Chem. 276, 29091-29097
20. Furst, J., Sutton, R. B., Chen, J., Brunger, A. T., and Grigorieff, N. (2003) Electron cryomicroscopy stucture of N-ethyl maleimide sensitive factor at 11 Å resolution. EMBO J. 22, 4365-4374
21. Chang, L. F., Chen, S., Liu, C. C., Pan, X., Jiang, J., Bai, X. C., Xie, X., Wang, H. W., and Sui, S. F. (2012) Structural characterization of full-length NSF and 20S particles. Nat. Struct. Mol. Biol. 19, 268-275
22. Matveeva, E. A., May, A. P., He, P., and Whiteheart, S. W. (2002) Uncoupling the ATPase activity of the N-ethylmaleimide sensitive factor (NSF) from 20S complex disassembly. Biochemistry 41, 530-536
23. Winter, U., Chen, X., and Fasshauer, D. (2009) A conserved membrane attachment site in α-SNAP facilitates N-ethylmaleimide-sensitive factor (NSF)-driven SNARE complex disassembly. J. Biol. Chem. 284, 31817-31826
24. Güthe, S., Kapinos, L., Möglich, A., Meier, S., Grzesiek, S., and Kiefhaber, T. (2004) Very fast folding and association of a trimerization domain from bacteriophage T4 fibritin. J. Mol. Biol. 337, 905-915
25. Papanikolopoulou, K., Forge, V., Goeltz, P., and Mitraki, A. (2004) Formation of highly stable chimeric trimers by fusion of an adenovirus fiber shaft fragment with the foldon domain of bacteriophage t4 fibritin. J. Biol. Chem. 279, 8991-8998
26. Rydzanicz, R., Zhao, X. S., and Johnson, P. E. (2005) Assembly PCR oligo maker: a tool for designing oligodeoxynucleotides for constructing long DNA molecules for RNA production. Nucleic Acids Res. 33, W521-W525
27. Stemmer, W. P., Crameri, A., Ha, K. D., Brennan, T. M., and Heyneker, H. L. (1995) Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides. Gene 164, 49-53
28. Fasshauer, D., Antonin, W., Margittai, M., Pabst, S., and Jahn, R. (1999) Mixed and non-cognate SNARE complexes. J. Biol. Chem. 274, 15440-15446
29. Lauer, J. M., Dalal, S., Marz, K. E., Nonet, M. L., and Hanson, P. I. (2006) SNARE complex zero layer residues are not critical for N-ethylmaleimide-sensitive factor-mediated disassembly. J. Biol. Chem. 281, 14823-14832
30. Buxbaum, E. (1999) Co-operating ATP sites in the multiple drug resistance transporter Mdr1. Eur. J. Biochem. 265, 54-63
31. Fasshauer, D., Eliason, W. K., Brünger, A. T., and Jahn, R. (1998) Identification of a minimal core of the synaptic SNARE complex sufficient for reversible assembly and disassembly. Biochemistry 37, 10354-10362
32. Cipriano, D. J., Jung, J., Vivona, S., Fenn, T. D., Brunger, A. T., and Bryant, Z. (2013) Processive ATP-driven substrate disassembly by the N-ethylma-leimide-sensitive facttor (NSF) molecular machine. J. Biol. Chem. 288, 23436-23445
33. Moeller, A., Zhao, C., Fried, M. G., Wilson-Kubalek, E. M., Carragher, B., and Whiteheart, S. W. (2012) Nucleotide-dependent conformational changes in the N-ethylmaleimide sensitive factor (NSF) and their potential role in SNARE complex disassembly. J. Struct. Biol. 177, 335-343