Beyond the random coil: Stochastic conformational switching in intrinsically disordered proteins

Structure

Volumn 19, Issue 4, 2011, Pages 566-576

  Choi, Ucheor B ^a,b   McCann, James J ^b   Weninger, Keith R ^a   Bowen, Mark E ^b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; COMPLEXIN; GLUTAMATE RECEPTOR; INTRINSICALLY DISORDERED PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEUROLIGIN; POLYMER; SNAP 25 PROTEIN; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UNCLASSIFIED DRUG;

ARTICLE; CELL FUNCTION; CYTOSOL; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIPID BILAYER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; STOCHASTIC MODEL; SYNAPSE VESICLE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR DYNAMICS SIMULATION; NERVE TISSUE PROTEINS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEINS; R-SNARE PROTEINS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; REPRODUCIBILITY OF RESULTS; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 79953838275     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.01.011     Document Type: Article

References (57)

1. D.D. Boehr, R. Nussinov, and P.E. Wright The role of dynamic conformational ensembles in biomolecular recognition Nat. Chem. Biol. 5 2009 789 796
2. E. Boukobza, A. Sonnenfeld, and G. Haran Immobilization in surface-tethered lipid vesicles as a new tool for single biomolecule spectroscopy J. Phys. Chem. B 105 2001 12165 12170 (Pubitemid 35338375)
3. M.E. Bowen, K. Weninger, J. Ernst, S. Chu, and A.T. Brunger Single-molecule studies of synaptotagmin and complexin binding to the SNARE complex Biophys. J. 89 2005 690 702 (Pubitemid 41098319)
4. A.T. Brunger Structure and function of SNARE and SNARE-interacting proteins Q. Rev. Biophys. 38 2005 1 47 (Pubitemid 43338671)
5. H. Chen, and E. Rhoades Fluorescence characterization of denatured proteins Curr. Opin. Struct. Biol. 18 2008 516 524
6. X. Chen, D.R. Tomchick, E. Kovrigin, D. Arac, M. Machius, T.C. Sudhof, and J. Rizo Three-dimensional structure of the complexin/SNARE complex Neuron 33 2002 397 409 (Pubitemid 34158843)
7. U.B. Choi, P. Strop, M. Vrljic, S. Chu, A.T. Brunger, and K.R. Weninger Single-molecule FRET-derived model of the synaptotagmin 1-SNARE fusion complex Nat. Struct. Mol. Biol. 17 2010 318 324
8. A.A. Deniz, T.A. Laurence, G.S. Beligere, M. Dahan, A.B. Martin, D.S. Chemla, P.E. Dawson, P.G. Schultz, and S. Weiss Single-molecule protein folding: diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2 Proc. Natl. Acad. Sci. USA 97 2000 5179 5184 (Pubitemid 30313692)
9. K.A. Dill, and D. Shortle Denatured states of proteins Annu. Rev. Biochem. 60 1991 795 825
10. H.J. Dyson, and P.E. Wright Coupling of folding and binding for unstructured proteins Curr. Opin. Struct. Biol. 12 2002 54 60 (Pubitemid 34142721)
11. D. Eliezer Biophysical characterization of intrinsically disordered proteins Curr. Opin. Struct. Biol. 19 2009 23 30
12. J.F. Ellena, B. Liang, M. Wiktor, A. Stein, D.S. Cafiso, R. Jahn, and L.K. Tamm Dynamic structure of lipid-bound synaptobrevin suggests a nucleation-propagation mechanism for trans-SNARE complex formation Proc. Natl. Acad. Sci. USA 106 2009 20306 20311
13. T.H. Evers, E.M.W.M. van Dongen, A.C. Faesen, E.W. Meijer, and M. Merkx Quantitative understanding of the energy transfer between fluorescent proteins connected via flexible peptide linkers Biochemistry 45 2006 13183 13192 (Pubitemid 44707679)
14. D. Fasshauer, D. Bruns, B. Shen, R. Jahn, and A.T. Brunger A structural change occurs upon binding of syntaxin to SNAP-25 J. Biol. Chem. 272 1997 4582 4590 (Pubitemid 27078540)
15. A.C. Ferreon, Y. Gambin, E.A. Lemke, and A.A. Deniz Interplay of alpha-synuclein binding and conformational switching probed by single-molecule fluorescence Proc. Natl. Acad. Sci. USA 106 2009 5645 5650
16. J.P. Flory Statistical mechanics of chain molecules 1969 Interscience New York
17. I. Gopich, and A. Szabo Theory of photon statistics in single-molecule Forster resonance energy transfer J. Chem. Phys. 122 2005 14707
18. A.I.U. Grosberg, A.R. Khokhlov, and V.S. Pande Statistical Physics of Macromolecules 2002 AIP Press New York
19. T. Hayashi, G.M. Thomas, and R.L. Huganir Dual palmitoylation of NR2 subunits regulates NMDA receptor trafficking Neuron 64 2009 213 226
20. J. Hazzard, T.C. Sudhof, and J. Rizo NMR analysis of the structure of synaptobrevin and of its interaction with syntaxin J. Biomol. NMR 14 1999 203 207 (Pubitemid 29396479)
21. A. Hoffmann, A. Kane, D. Nettels, D.E. Hertzog, P. Baumgärtel, J. Lengefeld, G. Reichardt, D.A. Horsley, R. Seckler, O. Bakajin, and B. Schuler Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy Proc. Natl. Acad. Sci. USA 104 2007 105 110 (Pubitemid 46067992)
22. M. Irie, Y. Hata, M. Takeuchi, K. Ichtchenko, A. Toyoda, K. Hirao, Y. Takai, T.W. Rosahl, and T.C. Sudhof Binding of neuroligins to PSD-95 Science 277 1997 1511 1515 (Pubitemid 27449240)
23. J.E. Kohn, I.S. Millett, J. Jacob, B. Zagrovic, T.M. Dillon, N. Cingel, R.S. Dothager, S. Seifert, P. Thiyagarajan, and T.R. Sosnick Random-coil behavior and the dimensions of chemically unfolded proteins Proc. Natl. Acad. Sci. USA 101 2004 12491 12496 (Pubitemid 39122051)
24. C.G. Lau, and R.S. Zukin NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders Nat. Rev. Neurosci. 8 2007 413 426 (Pubitemid 46789232)
25. T.A. Laurence, X. Kong, M. Jager, and S. Weiss Probing structural heterogeneities and fluctuations of nucleic acids and denatured proteins Proc. Natl. Acad. Sci. USA 102 2005 17348 17353 (Pubitemid 41740869)
26. H. Lee, K.H. Mok, R. Muhandiram, K.H. Park, J.E. Suk, D.H. Kim, J. Chang, Y.C. Sung, K.Y. Choi, and K.H. Han Local structural elements in the mostly unstructured transcriptional activation domain of human p53 J. Biol. Chem. 275 2000 29426 29432 (Pubitemid 32043817)
27. A.H. Mao, S.L. Crick, A. Vitalis, C.L. Chicoine, and R.V. Pappu Net charge per residue modulates conformational ensembles of intrinsically disordered proteins Proc. Natl. Acad. Sci. USA 107 2010 8183 8188
28. J.A. Marsh, and J.D. Forman-Kay Sequence determinants of compaction in intrinsically disordered proteins Biophys. J. 98 2010 2383 2390
29. J.J. McCann, U.B. Choi, L. Zheng, K. Weninger, and M.E. Bowen Optimizing methods to recover absolute FRET efficiency from immobilized single molecules Biophys. J. 99 2010 961 970
30. E.R. McCarney, J.H. Werner, S.L. Bernstein, I. Ruczinski, D.E. Makarov, P.M. Goodwin, and K.W. Plaxco Site-specific dimensions across a highly denatured protein; a single molecule study J. Mol. Biol. 352 2005 672 682 (Pubitemid 41225477)
31. K.A. Merchant, R.B. Best, J.M. Louis, I.V. Gopich, and W.A. Eaton Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations Proc. Natl. Acad. Sci. USA 104 2007 1528 1533 (Pubitemid 46214624)
32. X. Michalet, S. Weiss, and M. Jager Single-molecule fluorescence studies of protein folding and conformational dynamics Chem. Rev. 106 2006 1785 1813 (Pubitemid 43792781)
33. S. Muller-Spath, A. Soranno, V. Hirschfeld, H. Hofmann, S. Ruegger, L. Reymond, D. Nettels, and B. Schuler Charge interactions can dominate the dimensions of intrinsically disordered proteins Proc. Natl. Acad. Sci. USA 107 2010 14609 14614
34. D. Nettels, I.V. Gopich, A. Hoffmann, and B. Schuler Ultrafast dynamics of protein collapse from single-molecule photon statistics Proc. Natl. Acad. Sci. USA 104 2007 2655 2660 (Pubitemid 46327935)
35. E.P. O'Brien, G. Morrison, B.R. Brooks, and D. Thirumalai How accurate are polymer models in the analysis of Forster resonance energy transfer experiments on proteins? J. Chem. Phys. 130 2009 10
36. L. Pauling, and R.B. Corey The pleated sheet, a new layer configuration of polypeptide chains Proc. Natl. Acad. Sci. USA 37 1951 251 256
37. A. Paz, T. Zeev-Ben-Mordehai, M. Lundqvist, E. Sherman, E. Mylonas, L. Weiner, G. Haran, D.I. Svergun, F.A. Mulder, J.L. Sussman, and I. Silman Biophysical characterization of the unstructured cytoplasmic domain of the human neuronal adhesion protein neuroligin 3 Biophys. J. 95 2008 1928 1944
38. K. Ritchie, R. Iino, T. Fujiwara, K. Murase, and A. Kusumi The fence and picket structure of the plasma membrane of live cells as revealed by single molecule techniques Mol. Membr. Biol. 20 2003 13 18 (Pubitemid 36460641)
39. T.J. Ryan, R.D. Emes, S.G.N. Grant, and N.H. Komiyama Evolution of NMDA receptor cytoplasmic interaction domains: implications for organisation of synaptic signalling complexes BMC Neurosci. 9 2008 14
40. J.J. Sakon, and K.R. Weninger Detecting the conformation of individual proteins in live cells Nat. Methods 7 2010 203 205
41. L.E. Sass, C. Lanyi, K. Weninger, and D.A. Erie Single-molecule FRET TACKLE reveals highly dynamic mismatched DNA-MutS complexes Biochemistry 49 2010 3174 3190
42. B. Schuler, E.A. Lipman, and W.A. Eaton Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy Nature 419 2002 743 747 (Pubitemid 35177962)
43. F. Seiler, J. Malsam, J.M. Krause, and T.H. Sollner A role of complexin-lipid interactions in membrane fusion FEBS Lett. 583 2009 2343 2348
44. T.C. Sudhof Neuroligins and neurexins link synaptic function to cognitive disease Nature 455 2008 903 911
45. D.S. Talaga, W.L. Lau, H. Roder, J. Tang, Y. Jia, W.F. DeGrado, and R.M. Hochstrasser Dynamics and folding of single two-stranded coiled-coil peptides studied by fluorescent energy transfer confocal microscopy Proc. Natl. Acad. Sci. USA 97 2000 13021 13026
46. S.F. Traynelis, L.P. Wollmuth, C.J. McBain, F.S. Menniti, K.M. Vance, K.K. Ogden, K.B. Hansen, H. Yuan, S.J. Myers, R. Dingledine, and D. Sibley Glutamate Receptor Ion Channels: Structure, Regulation, and Function Pharmacol. Rev. 62 2010 405 496
47. C.J. Tsai, B. Ma, Y.Y. Sham, S. Kumar, and R. Nussinov Structured disorder and conformational selection Proteins 44 2001 418 427 (Pubitemid 32762067)
48. V.N. Uversky What does it mean to be natively unfolded? Eur. J. Biochem. 269 2002 2 12 (Pubitemid 34107333)
49. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochim. Biophys. Acta 1804 2010 1231 1264
50. V. Vacic, V. Uversky, A.K. Dunker, and S. Lonardi Composition Profiler: a tool for discovery and visualization of amino acid composition differences BMC Bioinformatics 8 2007 211
51. A. Vitalis, X. Wang, and R.V. Pappu Quantitative characterization of intrinsic disorder in polyglutamine: insights from analysis based on polymer theories Biophys. J. 93 2007 1923 1937 (Pubitemid 47437577)
52. S. Vucetic, C.J. Brown, A.K. Dunker, and Z. Obradovic Flavors of protein disorder Proteins 52 2003 573 584 (Pubitemid 37034155)
53. Z. Wang, K.W. Plaxco, and D.E. Makarov Influence of local and residual structures on the scaling behavior and dimensions of unfolded proteins Biopolymers 86 2007 321 328 (Pubitemid 47067549)
54. K. Weninger, M.E. Bowen, U.B. Choi, S. Chu, and A.T. Brunger Accessory proteins stabilize the acceptor complex for synaptobrevin, the 1:1 syntaxin/SNAP-25 complex Structure 16 2008 308 320 (Pubitemid 351222650)
55. D.K. Wilkins, S.B. Grimshaw, V. Receveur, C.M. Dobson, J.A. Jones, and L.J. Smith Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38 1999 16424 16431
56. H.-X. Zhou Polymer models of protein stability, folding, and interactions Biochemistry 43 2004 2141 2154 (Pubitemid 38279959)
57. H.-X. Zhou From induced fit to conformational selection: a continuum of binding mechanism controlled by the timescale of conformational transitions Biophys. J. 98 2010 L15 L17