Probing the free energy landscape of the fast-folding gpW protein by relaxation dispersion NMR

Journal of the American Chemical Society

Volumn 136, Issue 20, 2014, Pages 7444-7451

  Sanchez Medina, Celia ^a   Sekhar, Ashok ^b   Vallurupalli, Pramodh ^b   Cerminara, Michele ^a   Muñoz, Victor ^a   Kay, Lewis E ^a,b,c  

^a CSIC   (Spain)

^b UNIVERSITY OF TORONTO   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DISPERSIONS; FREE ENERGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

CONFORMATIONAL FLUCTUATIONS; CONFORMATIONAL TRANSITIONS; FREE ENERGY LANDSCAPE; MULTIDIMENSIONAL SURFACES; RELAXATION DISPERSION; SECONDARY STRUCTURAL ELEMENTS; SINGLE-DOMAIN PROTEINS; THERMODYNAMICS AND KINETICS;

PROTEINS;

ARTICLE; BACTERIOPHAGE; DISPERSION; ENERGY; LANDSCAPE; LIFESPAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTON NUCLEAR MAGNETIC RESONANCE; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; THERMODYNAMICS;

AC-(GLY-PRO-HYP)3-GLY-PRO-TRP-(GLY-PRO-HYP)4-GLY-GLY-CONH2; PEPTIDE;

NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

EID: 84901044515     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja502705y     Document Type: Article

References (64)

1. Boehr, D. D.; Nussinov, R.; Wright, P. E. Nat. Chem. Biol. 2009, 5, 789-796
2. Frauenfelder, H.; Sligar, S. G.; Wolynes, P. G. Science 1991, 254, 1598-1603
3. Lazaridis, T.; Karplus, M. Biophys. Chem. 2003, 100, 367-395
4. Bai, Y.; Sosnick, T. R.; Mayne, L.; Englander, S. W. Science 1995, 269, 192-197
5. Chamberlain, A. K.; Handel, T. M.; Marqusee, S. Nat. Struct. Mol. Biol. 1996, 3, 782-787
6. Hu, W.; Walters, B. T.; Kan, Z.-Y.; Mayne, L.; Rosen, L. E.; Marqusee, S.; Englander, S. W. Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 7684-7689
7. Bai, Y. Chem. Rev. 2006, 106, 1757-1768
8. Maity, H.; Maity, M.; Krishna, M. M.; Mayne, L.; Englander, S. W. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 4741-4746
9. Hoang, L.; Bédard, S.; Krishna, M. M.; Lin, Y.; Englander, S. W. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 12173-12178
10. Chamberlain, A. K.; Marqusee, S. Adv. Protein Chem. 2000, 53, 283-328
11. Bartlett, A. I.; Radford, S. E. Nat. Struct. Mol. Biol. 2009, 16, 582-588
12. Jackson, S. E. Folding Des. 1998, 3, R81-R91
13. Muñoz, V. Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 395-412
14. Eaton, W. A.; Muñoz, V.; Thompson, P. A.; Henry, E. R.; Hofrichter, J. Acc. Chem. Res. 1998, 31, 745-753
15. Yang, W. Y.; Gruebele, M. Nature 2003, 423, 193-197
16. Naganathan, A. N.; Muñoz, V. J. Am. Chem. Soc. 2005, 127, 480-481
17. Chung, H. S.; McHale, K.; Louis, J. M.; Eaton, W. A. Science 2012, 335, 981-984
18. Garcia-Mira, M. M.; Sadqi, M.; Fischer, N.; Sanchez-Ruiz, J. M.; Muñoz, V. Science 2002, 298, 2191-2195
19. Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Shaw, D. E. Science 2011, 334, 517-520
20. Palmer, A. G.; Kroenke, C. D.; Loria, J. P. Methods Enzymol. 2001, 339, 204-238
21. Mittermaier, A.; Kay, L. E. Science 2006, 312, 224-228
22. Palmer, A. G., III; Massi, F. Chem. Rev. 2006, 106, 1700-1719
23. Robustelli, P.; Kohlhoff, K.; Cavalli, A.; Vendruscolo, M. Structure 2010, 18, 923-933
24. Shen, Y.; Lange, O.; Delaglio, F.; Rossi, P.; Aramini, J. M.; Liu, G.; Eletsky, A.; Wu, Y.; Singarapu, K. K.; Lemak, A. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 4685-4690
25. Korzhnev, D. M.; Religa, T. L.; Banachewicz, W.; Fersht, A. R.; Kay, L. E. Science 2010, 329, 1312-1316
26. Korzhnev, D. M.; Vernon, R. M.; Religa, T. L.; Hansen, A. L.; Baker, D.; Fersht, A. R.; Kay, L. E. J. Am. Chem. Soc. 2011, 133, 10974-10982
27. Neudecker, P.; Robustelli, P.; Cavalli, A.; Walsh, P.; Lundström, P.; Zarrine-Afsar, A.; Sharpe, S.; Vendruscolo, M.; Kay, L. E. Science 2012, 336, 362-366
28. Bouvignies, G.; Vallurupalli, P.; Hansen, D. F.; Correia, B. E.; Lange, O.; Bah, A.; Vernon, R. M.; Dahlquist, F. W.; Baker, D.; Kay, L. E. Nature 2011, 477, 111-114
29. Vallurupalli, P.; Hansen, D. F.; Kay, L. E. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 11766-11771
30. Fung, A.; Li, P.; Godoy-Ruiz, R.; Sanchez-Ruiz, J. M.; Muñoz, V. J. Am. Chem. Soc. 2008, 130, 7489-7495
31. Sborgi, L.; Verma, A.; Muñoz, V.; de Alba, E. PLoS One 2011, 6 e26409
32. Naganathan, A. N.; Doshi, U.; Muñoz, V. J. Am. Chem. Soc. 2007, 129, 5673-5682
33. McConnell, H. M. J. Chem. Phys. 1958, 28, 430-431
34. Millet, O.; Loria, J. P.; Kroenke, C. D.; Pons, M.; Palmer, A. G., III. J. Am. Chem. Soc. 2000, 122, 2867-2877
35. Vallurupalli, P.; Bouvignies, G.; Kay, L. E. J. Phys. Chem. B 2011, 115, 14891-14900
36. Wishart, D. S.; Bigam, C. G.; Holm, A.; Hodges, R. S.; Sykes, B. D. J. Biomol. NMR 1995, 5, 67-81
37. Shen, Y.; Delaglio, F.; Cornilescu, G.; Bax, A. J. Biomol. NMR 2009, 44, 213-223
38. Baldwin, A. J.; Kay, L. E. Nat. Chem. Biol. 2009, 5, 808-814
39. Naganathan, A. N.; Muñoz, V. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 8611-8616
40. Kubelka, J.; Hofrichter, J.; Eaton, W. A. Curr. Opin. Struct. Biol. 2004, 14, 76-88
41. Naganathan, A. N.; Sanchez-Ruiz, J. M.; Muñoz, V. J. Am. Chem. Soc. 2005, 127, 17970-17971
42. Li, P.; Oliva, F. Y.; Naganathan, A. N.; Muñoz, V. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 103-108
43. Kubelka, J.; Henry, E. R.; Cellmer, T.; Hofrichter, J.; Eaton, W. A. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 18655-18662
44. Religa, T. L.; Johnson, C. M.; Vu, D. M.; Brewer, S. H.; Dyer, R. B.; Fersht, A. R. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 9272-9277
45. Neuweiler, H.; Doose, S.; Sauer, M. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 16650-16655
46. Religa, T.; Markson, J.; Mayor, U.; Freund, S.; Fersht, A. Nature 2005, 437, 1053-1056
47. Press, W. H.; Flannery, B. P.; Teukolsky, S. A.; Vetterling, W. T. Numerical Recipes in C; Cambridge University Press: Cambridge, U.K., 1988.
48. Lundström, P.; Teilum, K.; Carstensen, T.; Bezsonova, I.; Wiesner, S.; Hansen, D. F.; Religa, T. L.; Akke, M.; Kay, L. E. J. Biomol. NMR 2007, 38, 199-212
49. Sattler, M.; Schleucher, J.; Griesinger, C. Prog. Nucl. Magn. Reson. Spectrosc. 1999, 34, 93-158
50. Mulder, F. A. A.; Skrynnikov, N. R.; Hon, B.; Dahlquist, F. W.; Kay, L. E. J. Am. Chem. Soc. 2001, 123, 967-975
51. Hansen, D. F.; Vallurupalli, P.; Kay, L. E. J. Phys. Chem. B 2008, 112, 5898-5904
52. Ishima, R.; Torchia, D. A. J. Biomol. NMR 2003, 25, 243-248
53. Vallurupalli, P.; Hansen, D. F.; Lundström, P.; Kay, L. E. J. Biomol. NMR 2009, 45, 45-55
54. Lundström, P.; Hansen, D. F.; Kay, L. E. J. Biomol. NMR 2008, 42, 35-47
55. Lundström, P.; Vallurupalli, P.; Religa, T. L.; Dahlquist, F. W.; Kay, L. E. J. Biomol. NMR 2007, 38, 79-88
56. Skrynnikov, N. R.; Dahlquist, F. W.; Kay, L. E. J. Am. Chem. Soc. 2002, 124, 12352-12360
57. Orekhov, V. Y.; Korzhnev, D. M.; Kay, L. E. J. Am. Chem. Soc. 2004, 126, 1886-1891
58. Bouvignies, G.; Korzhnev, D. M.; Neudecker, P.; Hansen, D. F.; Cordes, M. H.; Kay, L. E. J. Biomol. NMR 2010, 47, 135-141
59. Hansen, D. F.; Vallurupalli, P.; Lundström, P.; Neudecker, P.; Kay, L. E. J. Am. Chem. Soc. 2008, 130, 2667-2675
60. Delaglio, F.; Grzesiek, S.; Vuister, G. W.; Zhu, G.; Pfeifer, J.; Bax, A. J. Biomol. NMR 1995, 6, 277-293
61. Korzhnev, D. M.; Salvatella, X.; Vendruscolo, M.; Di Nardo, A. A.; Davidson, A. R.; Dobson, C. M.; Kay, L. E. Nature 2004, 430, 586-590
62. Kneller, D.; Kuntz, I. J. Cell. Biochem. 1993, 53, 254
63. Desai, T. M.; Cerminara, M.; Sadqi, M.; Muñoz, V. J. Biol. Chem. 2010, 285, 34549-34556
64. Tamiola, K.; Acar, B.; Mulder, F. A. J. Am. Chem. Soc. 2010, 132, 18000-18003