Studying "invisible" excited protein states in slow exchange with a major state conformation

Journal of the American Chemical Society

Volumn 134, Issue 19, 2012, Pages 8148-8161

  Vallurupalli, Pramodh ^a   Bouvignies, Guillaume ^a   Kay, Lewis E ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL EXCHANGE; CHEMICAL EXCHANGE SATURATION TRANSFER; CONFORMATIONAL EXCHANGE; EXCHANGE PARAMETERS; EXCITED-STATE LIFETIME; FIELD STRENGTHS; FOLDING TRANSITION; FUNCTION OF FREQUENCY; GROUND-STATE CONFORMATIONS; PEAK INTENSITY; RELAXATION DISPERSION;

CHEMICAL SHIFT; CONFORMATIONS; DISPERSIONS; EXPERIMENTS; FREQUENCY ALLOCATION; MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

EXCITED STATES;

15 NITROGEN CHEMICAL EXCHANGE SATURATION MAGNETIC RESONANCE SPECTROSCOPY; ARTICLE; CONFORMATIONAL TRANSITION; DISPERSION; EXCITATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MAGNETIC FIELD; MAGNETISM; NITROGEN NUCLEAR MAGNETIC RESONANCE; OSCILLATION; POLARIZATION; PROTEIN CONFORMATION; PROTEIN TRANSPORT; THERMODYNAMICS;

CARRIER PROTEINS; HUMANS; KINETICS; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; REPRODUCIBILITY OF RESULTS;

EID: 84862061967     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja3001419     Document Type: Article

References (77)

1. Austin, R. H.; Beeson, K. W.; Eisenstein, L.; Frauenfelder, H.; Gunsalus, I. C. Biochemistry 1975, 14, 5355-5373
2. Frauenfelder, H.; Sligar, S. G.; Wolynes, P. G. Science 1991, 254, 1598-1603
3. Xie, X. S. J. Chem. Phys. 2002, 117, 11024-11032
4. English, B. P.; Min, W.; van Oijen, A. M.; Lee, K. T.; Luo, G.; Sun, H.; Cherayil, B. J.; Kou, S. C.; Xie, X. S. Nat. Chem. Biol. 2006, 2, 87-94
5. Karplus, M. J. Phys. Chem. B 2000, 104, 11-27
6. Boehr, D. D.; Nussinov, R.; Wright, P. E. Nat. Chem. Biol. 2009, 5, 789-796
7. Clore, G. M.; Iwahara, J. Chem. Rev. 2009, 109, 4108-4139
8. Sugase, K.; Dyson, H. J.; Wright, P. E. Nature 2007, 447, 1021-1025
9. Fraser, J. S.; Clarkson, M. W.; Degnan, S. C.; Erion, R.; Kern, D.; Alber, T. Nature 2009, 462, 669-673
10. 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
11. Korzhnev, D. M.; Religa, T. L.; Banachewicz, W.; Fersht, A. R.; Kay, L. E. Science 2010, 329, 1312-1316
12. Bouvignies, G.; Hansen, D. F.; Vallurupalli, P.; Kay, L. E. J. Am. Chem. Soc. 2011, 133, 1935-1945
13. Palmer, A. G., III; Kroenke, C. D.; Loria, J. P. Methods Enzymol. 2001, 339, 204-238
14. Palmer, A. G., III. Chem. Rev. 2004, 104, 3623-3640
15. Mittermaier, A.; Kay, L. E. Science 2006, 312, 224-228
16. Meiboom, S.; Gill, D. Rev. Sci. Instrum. 1958, 29, 688-691
17. Carr, H. Y.; Purcell, E. M. Phys. Rev. 1954, 94, 630-638
18. 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
19. Hansen, D. F.; Vallurupalli, P.; Lundstrom, P.; Neudecker, P.; Kay, L. E. J. Am. Chem. Soc. 2008, 130, 2667-2675
20. Ishima, R.; Wingfield, P. T.; Stahl, S. J.; Kaufman, J. D.; Torchia, D. A. J. Am. Chem. Soc. 1998, 120, 10534-10542
21. Loria, J. P.; Rance, M.; Palmer, A. G., III. J. Am. Chem. Soc. 1999, 121, 2331-2332
22. Lundstrom, P.; Hansen, D. F.; Kay, L. E. J. Biomol. NMR 2008, 42, 35-47
23. Lundstrom, P.; Hansen, D. F.; Vallurupalli, P.; Kay, L. E. J. Am. Chem. Soc. 2009, 131, 1915-1926
24. Lundstrom, P.; Lin, H.; Kay, L. E. J. Biomol. NMR 2009, 44, 139-155
25. Hansen, A. L.; Kay, L. E. J. Biomol. NMR 2011, 50, 347-355
26. Mulder, F. A.; Skrynnikov, N. R.; Hon, B.; Dahlquist, F. W.; Kay, L. E. J. Am. Chem. Soc. 2001, 123, 967-975
27. Skrynnikov, N. R.; Mulder, F. A.; Hon, B.; Dahlquist, F. W.; Kay, L. E. J. Am. Chem. Soc. 2001, 123, 4556-4566
28. Vallurupalli, P.; Hansen, D. F.; Stollar, E.; Meirovitch, E.; Kay, L. E. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 18473-18477
29. Hansen, D. F.; Vallurupalli, P.; Kay, L. E. J. Am. Chem. Soc. 2008, 130, 8397-8405
30. Vallurupalli, P.; Hansen, D. F.; Kay, L. E. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 11766-11771
31. Vallurupalli, P.; Bouvignies, G.; Kay, L. E. J. Phys. Chem. B 2011, 115, 14891-14900
32. Farrow, N. A.; Zhang, O.; Forman-Kay, J. D.; Kay, L. E. J. Biomol. NMR 1994, 4, 727-734
33. Neudecker, P.; Lundstrom, P.; Kay, L. E. Biophys. J. 2009, 96, 2045-2054
34. Forsén, S.; Hoffman, R. A. J. Chem. Phys. 1963, 39, 2892-2901
35. Fawzi, N. L.; Ying, J.; Ghirlando, R.; Torchia, D. A.; Clore, G. M. Nature 2011, 480, 268-72
36. Bertini, I.; Ciurli, S.; Dikiy, A.; Gasanov, R.; Luchinat, C.; Martini, G.; Safarov, N. J. Am. Chem. Soc. 1999, 121, 2037-2046
37. Ward, K. M.; Aletras, A. H.; Balaban, R. S. J. Magn. Reson. 2000, 143, 79-87
38. Zhou, J. Y.; van Zijl, P. C. M. Prog. Nucl. Magn. Reson. Spectrosc. 2006, 48, 109-136
39. Hansen, D. F.; Led, J. J. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 1738-1743
40. Gupta, R. K.; Redfield, A. G. Science 1970, 169, 1204-1206
41. Cayley, P. J.; Albrand, J. P.; Feeney, J.; Roberts, G. C.; Piper, E. A.; Burgen, A. S. Biochemistry 1979, 18, 3886-3895
42. van Zijl, P. C. M.; Yadav, N. N. Magn. Reson. Med. 2011, 65, 927-948
43. Jemth, P.; Day, R.; Gianni, S.; Khan, F.; Allen, M.; Daggett, V.; Fersht, A. R. J. Mol. Biol. 2005, 350, 363-378
44. Loria, J. P.; Rance, M.; Palmer, A. G., III. J. Biomol. NMR 1999, 15, 151-155
45. Palmer, A. G., III; Grey, M. J.; Wang, C. Methods Enzymol. 2005, 394, 430-465
46. Korzhnev, D. M.; Kloiber, K.; Kanelis, V.; Tugarinov, V.; Kay, L. E. J. Am. Chem. Soc. 2004, 126, 3964-3973
47. Millet, O.; Loria, J. P.; Kroenke, C. D.; Pons, M.; Palmer, A. G. J. Am. Chem. Soc. 2000, 122, 2867-2877
48. Zhou, J. Y.; Wilson, D. A.; Sun, P. Z.; Klaus, J. A.; van Zijl, P. C. M. Magn. Reson. Med. 2004, 51, 945-952
49. Roell, S. A.; Dreher, W.; Leibfritz, D. J. Magn. Reson. 1998, 132, 96-101
50. Farrow, N. A.; Muhandiram, R.; Singer, A. U.; Pascal, S. M.; Kay, C. M.; Gish, G.; Shoelson, S. E.; Pawson, T.; Forman-Kay, J. D.; Kay, L. E. Biochemistry 1994, 33, 5984-6003
51. Morris, G. A.; Freeman, R. J. Am. Chem. Soc. 1979, 101, 760-762
52. Pervushin, K.; Riek, R.; Wider, G.; Wuthrich, K. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 12366-12371
53. Goldman, M. J. Magn. Reson. 1984, 60, 437-452
54. Levitt, M. H. J. Magn. Reson. 1982, 50, 95-110
55. Rance, M.; Loria, J. P.; Palmer, A. G., III. J. Magn. Reson. 1999, 136, 92-101
56. Kay, L. E.; Keifer, P.; Saarinen, T. J. Am. Chem. Soc. 1992, 114, 10663-10665
57. Schleucher, J.; Sattler, M.; Griesinger, C. Angew. Chem., Int. Ed. Engl. 1993, 32, 1489-1491
58. Marion, D.; Ikura, M.; Tschudin, R.; Bax, A. J. Magn. Reson. 1989, 85, 393-399
59. Shaka, A. J.; Keeler, J.; Frenkiel, T.; Freeman, R. J. Magn. Reson. 1983, 52, 335-338
60. 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
61. Grey, M. J.; Tang, Y.; Alexov, E.; McKnight, C. J.; Raleigh, D. P.; Palmer, A. G., III. J. Mol. Biol. 2006, 355, 1078-1094
62. Jemth, P.; Gianni, S.; Day, R.; Li, B.; Johnson, C. M.; Daggett, V.; Fersht, A. R. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 6450-6455
63. Clore, G. M.; Roberts, G. C. K.; Gronenborn, A.; Birdsall, B.; Feeney, J. J. Magn. Reson. 1981, 45, 151-161
64. Tamiola, K.; Acar, B.; Mulder, F. A. J. Am. Chem. Soc. 2010, 132, 18000-18003
65. Farrow, N. A.; Zhang, O.; Forman-Kay, J. D.; Kay, L. E. Biochemistry 1995, 34, 868-878
66. Palmer, A. G., III; Massi, F. Chem. Rev. 2006, 106, 1700-1719
67. Wagner, G.; DeMarco, A.; Wuthrich, K. Biophys. Struct. Mech. 1976, 2, 139-158
68. Montelione, G. T.; Wagner, G. J. Am. Chem. Soc. 1989, 111, 3096-3098
69. Clore, G. M.; Driscoll, P. C.; Wingfield, P. T.; Gronenborn, A. M. Biochemistry 1990, 29, 7387-7401
70. Clore, G. M.; Omichinski, J. G.; Gronenborn, A. M. J. Am. Chem. Soc. 1991, 113, 4350-4351
71. Mittermaier, A.; Kay, L. E. J. Am. Chem. Soc. 2001, 123, 6892-6903
72. Guenneugues, M.; Berthault, P.; Desvaux, H. J. Magn. Reson. 1999, 136, 118-126
73. Hansen, D. F.; Vallurupalli, P.; Kay, L. E. J. Phys. Chem. B 2008, 112, 5898-5904
74. Delaglio, F.; Grzesiek, S.; Vuister, G. W.; Zhu, G.; Pfeifer, J.; Bax, A. J. Biomol. NMR 1995, 6, 277-293
75. Available at http://pound.med.utoronto.ca/software.html.
76. Goddard, T. D.; Kneller, D. G. SPARKY 3 University of California: San Francisco, 2008.
77. McConnell, H. M. J. Chem. Phys. 1958, 28, 430-431