Structure and dynamics of γ-SNAP: Insight into flexibility of proteins from the SNAP family

Proteins: Structure, Function and Genetics

Volumn 70, Issue 1, 2008, Pages 93-104

  Bitto, Eduard ^a   Bingman, Craig A ^a   Kondrashov, Dmitry A ^a   McCoy, Jason G ^a   Bannen, Ryan M ^a   Wesenberg, Gary E ^a   Phillips Jr , George N ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Membrane trafficking; Normal mode analysis; SNARE recycling; X ray structure

Indexed keywords

CARRIER PROTEIN; PROTEIN SEC17; SNARE PROTEIN; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN GAMMA; UNCLASSIFIED DRUG;

ACCURACY; ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN MOTIF; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURE ANALYSIS; X RAY ANALYSIS;

ANIMALS; CATTLE; ELECTROCHEMISTRY; ELECTRODES; MICROSCOPY, ATOMIC FORCE; PROTEIN CONFORMATION; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS;

DANIO RERIO; EUKARYOTA;

EID: 37349082442     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21468     Document Type: Article

References (68)

1. Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell 2004;116:153-166.
2. Rothman JE. Mechanisms of intracellular protein transport. Nature 1994;372:55-63.
3. Aridor M, Traub LM. Cargo selection in vesicular transport: the making and breaking of a coat. Traffic 2002;3:537-546.
4. Kirchhausen T. Three ways to make a vesicle. Nat Rev Mol Cell Biol 2000;1:187-198.
5. Pfeffer SR. Transport-vesicle targeting: tethers before SNAREs. Nat Cell Biol 1999;1:E17-22.
6. Sztul E, Lupashin V. Role of tethering factors in secretory membrane traffic. Am J Physiol Cell Physiol 2006;290:C11-26.
7. Brunger AT. Structure and function of SNARE and SNARE-interacting proteins. Q Rev Biophys 2005;38:1-47.
8. Duman JG, Forte JG. What is the role of SNARE proteins in membrane fusion? Am J Physiol Cell Physiol 2003;285:C237-249.
9. Hong W. SNAREs and traffic. Biochim Biophys Acta 2005;1744:493-517.
10. Jahn R, Scheller RH. SNAREs - engines for membrane fusion. Nat Rev Mol Cell Biol 2006;7:631-643.
11. Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci USA 2006;103:11821-11827.
12. Sollner T, Bennett MK, Whiteheart SW, Serieller 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.
13. Antonin W, Fasshauer D, Becker S, Jahn R, Schneider TR. Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat Struct Biol 2002;9:107-111.
14. Sutton RB, Fasshauer D, Jahn R, Brunger AT. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 1998;395:347-353.
15. Clary DO, Griff IC, Rothman JE. SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell 1990;61:709-721.
16. Wilson DW, Wilcox CA, Flynn GC, Chen E, Kuang WJ, Henzel WJ, Block MR, Ullrich A, Rothman JE. A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast. Nature 1989;339:355-359.
17. Furst J, Sutton RB, Chen J, Brunger AT, Grigorieff N. Electron cryomicroscopy structure of N-ethyl maleimide sensitive factor at 11 A resolution. EMBO J 2003;22:4365-4374.
18. Hohl TM, Parlati F, Wimmer C, Rothman JE, Sollner TH, Engelhardt H. Arrangement of subunits in 20 S particles consisting of NSF, SNAPs, and SNARE complexes. Mol Cell 1998;2:539-548.
19. Wilson DW, Whiteheart SW, Wiedmann M, Brunner M, Rothman JE. A multisubunit particle implicated in membrane fusion. J Cell Biol 1992;117:531-538.
20. Fleming KG, Hohl TM, Yu RC, Muller SA, Wolpensinger B, Engel A, Engelhardt H, Brunger AT, Sollner TH, Hanson PI. A revised model for the oligomeric state of the N-ethylmaleimide-sensitive fusion protein, NSF. J Biol Chem 1998;273:15675-15681.
21. Wimmer C, Hohl TM, Hughes CA, Muller SA, Sollner TH, Engel A, Rothman JE. Molecular mass, stoichiometry, and assembly of 20 S particles. J Biol Chem 2001;276:29091-29097.
22. Clary DO, Rothman JE. Purification of three related peripheral membrane proteins needed for vesicular transport. J Biol Chem 1990;265:10109-10117.
23. Whiteheart SW, Griff IC, Brunner M, Clary DO, Mayer T, Buhrow SA, Rothman JE. SNAP family of NSF attachment proteins includes a brain-specific isoform. Nature 1993;362:353-355.
24. Weidenhaupt M, Bruckert F, Louwagie M, Garin J, Satre M. Functional and molecular identification of novel members of the ubiquitous membrane fusion proteins α- and γ-SNAP (soluble N-ethylmaleimide-sensitive factor-attachment proteins) families in Dictyostelium discoideum. Eur J Biochem 2000;267:2062-2070.
25. Stenbeck G. Soluble NSF-attachment proteins. Int J Biochem Cell Biol 1998;30:573-577.
26. Rice LM, Brunger AT. Crystal structure of the vesicular transport protein Sec17: implications for SNAP function in SNARE complex disassembly. Mol Cell 1999;4:85-95.
27. Whiteheart SW, Brunner M, Wilson DW, Wiedmann M, Rothman JE. Soluble N-ethylmaleimide-sensitive fusion attachment proteins (SNAPs) bind to a multi-SNAP receptor complex in golgi membranes. J Biol Chem 1992;267:12239- 12243.
28. Tani K, Shibata M, Kawase K, Kawashima H, Hatsuzawa K, Nagahama M, Tagaya M. Mapping of functional domains of γ-SNAP. J Biol Chem 2003;278:13531-13538.
29. Chen D, Xu W, He P, Medrano EE, Whiteheart SW. Gaf-1, a γ-SNAP-binding protein associated with the mitochondria. J Biol Chem 2001;276:13127-13135.
30. Kawase K, Shibata M, Kawashima H, Hatsuzawa K, Nagahama M, Tagaya M, Tani K. Gaf-1b is an alternative splice variant of Gaf-1/Rip11. Biochem Biophys Res Commun 2003;303:1042-1046.
31. Prekeris R, Klumperman J, Scheller RH. A Rab11/Rip11 protein complex regulates apical membrane trafficking via recycling endosomes. Mol Cell 2000;6:1437-1448.
32. Howlin B, Butler SA, Moss DS, Harris GW, Driessen HPC. Tlsanl - Tls parameter-analysis program for segmented anisotropic refinement of macromolecular structures. J Appl Crystallogr 1993;26:622-624.
33. Holm L, Sander C. Protein structure comparison by alignment of distance matrices. J Mol Biol 1993;233:123-138.
34. Chothia C, Lesk AM. The relation between the divergence of sequence and structure in proteins. EMBO J 1986;5:823-826.
35. Vriend G. What if - a molecular modeling and drug design program. J Mol Graph 1990;8:52-56.
36. Barnard RJ, Morgan A, Burgoyne RD. Domains of α-SNAP required for the stimulation of exocytosis and for N-ethylmalemide-sensitive fusion protein (NSF) binding and activation. Mol Biol Cell 1996;7:693-701.
37. McGuffin LJ, Bryson K, Jones DT. The PSIPRED protein structure prediction server. Bioinformatics 2000;16:404-405.
38. Marz KE, Lauer JM, Hanson PI. Defining the SNARE complex binding surface of α-SNAP: implications for SNARE complex disassembly. J Biol Chem 2003;278:27000-27008.
39. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 2001;98:10037-10041.
40. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 1988;16:10881-10890.
41. Bahar I, Rader AJ. Coarse-grained normal mode analysis in structural biology. Curr Opin Struct Biol 2005;15:586-592.
42. Ma J. Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. Structure 2005;13:373-380.
43. DeLano WL. The PYMOL molecular graphic system. San Carlos, CA: DeLano Scientific LLC; 2002.
44. Barnard RJ, Morgan A, Burgoyne RD. Stimulation of NSF ATPase activity by α-SNAP is required for SNARE complex disassembly and exocytosis. J Cell Biol 1997;139:875-883.
45. Hanson PI, Roth R, Morisaki H, Jahn R, Heuser JE. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 1997;90:523-535.
46. Scales SJ, Yoo BY, Scheller RH. The ionic layer is required for efficient dissociation of the SNARE complex by α-SNAP and NSF. Proc Natl Acad Sci USA 2001;98:14262-14267.
47. Yu RC, Jahn R, Brunger AT. NSF N-terminal domain crystal structure: models of NSF function. Mol Cell 1999;4:97-107.
48. Thao S, Zhao Q, Kimball T, Steffen E, Blommel PG, Riters M, Newman CS, Fox BG, Wrobel RL. Results from high-throughput DNA cloning of Arabidopsis thaliana target genes using site-specific recombination. J Struct Funct Genomics 2004;5:267-276.
49. Sreenath HK, Bingman CA, Buchan BW, Seder KD, Burns BT, Geetha HV, Jeon WB, Vojtik FC, Aceti DJ, Frederick RO, Phillips GN, Jr, Fox BG. Protocols for production of selenomethionine-labeled proteins in 2-L polyethylene terephthalate bottles using auto-induction medium. Protein Expr Purif 2005;40:256-267.
50. Jeon WB, Aceti DJ, Bingman CA, Vojtik FC, Olson AC, Ellefson JM, McCombs JE, Sreenath HK, Blommel PG, Seder KD, Burns BT, Geetha HV, Harms AC, Sabat G, Sussman MR, Fox BG, Phillips GN, Jr. High-throughput purification and quality assurance of Arabidopsis thaliana proteins for eukaryotic structural genomics. J Struct Funct Genomics 2005;6:143-147.
51. Zolnai Z, Lee PT, Li J, Chapman MR, Newman CS, Phillips GN, Jr, Rayment I, Ulrich EL, Volkman BF, Markley JL. Project management system for structural and functional proteomics: sesame. J Struct Funct Genomics 2003;4:11-23.
52. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-326.
53. Grosse-Kunstleve RW, Adams PD. Substructure search procedures for macromolecular structures. Acta Crystallogr D Biol Crystallogr 2003;59(Part 11):1966-1973.
54. Uson I, Sheldrick GM. Advances in direct methods for protein crystallography. Curr Opin Struct Biol 1999;9:643-648.
55. de la Fortelle E, Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol 1997;276:472-494.
56. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994;50(Part 5):760-763.
57. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004;60:2126-2132.
58. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 1991;47(Part 2):110-119.
59. Kleywegt GJ, Read RJ. Not your average density. Structure 1997;5:1557-1569.
60. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 1997;53(Part 3):240-255.
61. Winn MD, Murshudov GN, Papiz MZ. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol 2003;374:300-321.
62. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. Procheck - a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
63. Lovell SC, Davis IW, Arendall WB, III, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003;50:437-450.
64. Brooks B, Karplus M. Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor. Proc Natl Acad Sci USA 1983;80:6571-6575.
65. Go N, Noguti T, Nishikawa T. Dynamics of a small globular protein in terms of low-frequency vibrational modes. Proc Natl Acad Sci USA 1983;80:3696-3700.
66. Tama F, Brooks CL. Symmetry, form, and shape: guiding principles for robustness in macromolecular machines. Annu Rev Biophys Biomol Struct 2006;35:115-133.
67. Tirion MM. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 1996;77:1905-1908.
68. Kondrashov DA, Van Wynsberghe AW, Bannen RM, Cui Q, Phillips GN, Jr. Protein structural variation in computational models and crystallographic data. Structure 2007;15:169-177.