Structural insights into the Trp-cage folding intermediate formation

Chemistry - A European Journal

Volumn 19, Issue 8, 2013, Pages 2628-2640

  Rovõ, Petra ^a   Stráner, Pál ^a   Láng, András ^a   Bartha, István ^a   Huszár, Kristõf ^a   Nyitray, Lászlõ ^a   Perczel, András ^a  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

intermediate states; multistate unfolding; NMR spectroscopy; protein folding; thermal denaturation

Indexed keywords

ACIDIC PH; ACIDIC PH VALUES; COMPUTATIONAL SIMULATION; DECONVOLUTION TECHNIQUES; DYNAMIC INFORMATION; ENERGETIC ASPECT; ENERGY LANDSCAPE; EXPERIMENTAL DATUM; FOLDING INTERMEDIATES; HETERONUCLEAR RELAXATION; IN-SILICO; IN-VITRO; INTERMEDIATE STATE; LABELED PROTEINS; MD SIMULATION; MULTI-STATE; NEUTRAL CONDITIONS; NMR CHEMICAL SHIFTS; NMR MEASUREMENTS; NONLINEAR FITTING METHOD; PEPTIDE BONDS; STRUCTURAL INSIGHTS; STRUCTURAL REARRANGEMENT; TEMPERATURE DEPENDENT; TESTING GROUNDS; THERMAL DENATURATIONS; THERMODYNAMIC PARAMETER; TRANS CONFORMATIONS; UNFOLDING PROCESS;

NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN FOLDING;

PROTEINS;

PEPTIDE; TRP CAGE PEPTIDE; TRP-CAGE PEPTIDE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PROTEIN CONFORMATION; PROTEIN FOLDING; SYNTHESIS; TEMPERATURE; THERMODYNAMICS;

HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PEPTIDES; PROTEIN CONFORMATION; PROTEIN FOLDING; TEMPERATURE; THERMODYNAMICS;

EID: 84873639318     PISSN: 09476539     EISSN: 15213765     Source Type: Journal    
DOI: 10.1002/chem.201203764     Document Type: Article

References (80)

1. A. J. Baldwin, L. E. Kay, Nat. Chem. Biol. 2009, 5, 808-814.
2. D. Eliezer, J. Chung, H. J. Dyson, P. E. Wright, Biochemistry 2000, 39, 2894-2901.
3. S. Ramboarina, C. Redfield, J. Mol. Biol. 2003, 330, 1177-1188.
4. C. Redfield, Methods 2004, 34, 121-132.
5. A. K. Chamberlain, S. Marqusee, Biochemistry 1998, 37, 1736-1742.
6. H. J. Dyson, P. E. Wright, Methods Enzymol. 2001, 339, 258-270.
7. J. R. Gillespie, D. Shortle, J. Mol. Biol. 1997, 268, 158-169
8. J. R. Gillespie, D. Shortle, J. Mol. Biol. 1997, 268, 170-184.
9. S. Meier, M. Blackledge, S. Grzesiek, J. Chem. Phys. 2008, 128, 052204.
10. V. A. Higman, H. I. Rösner, R. Ugolini, L. H. Greene, C. Redfield, L. J. Smith, J. Biomol. NMR 2009, 45, 121-131.
11. A. J. Baldwin, D. F. Hansen, P. Vallurupalli, L. E. Kay, J. Am. Chem. Soc. 2009, 131, 11939-11948.
12. D. M. Korzhnev, T. L. Religa, W. Banachewicz, A. R. Fersht, L. E. Kay, Science 2010, 329, 1312-1316
13. D. M. Korzhnev, R. M. Vernon, T. L. Religa, A. L. Hansen, D. Baker, A. R. Fersht, L. E. Kay, J. Am. Chem. Soc. 2011, 133, 10974-10982.
14. J. Neidigh, R. Fesinmeyer, N. Andersen, Nat. Struct. Biol. 2002, 9, 425-430.
15. L. Qiu, S. Pabit, A. Roitberg, S. Hagen, J. Am. Chem. Soc. 2002, 124, 12952-12953.
16. R. M. Culik, A. L. Serrano, M. R. Bunagan, F. Gai, Angew. Chem. 2011, 123, 11076-11079
17. Angew. Chem. Int. Ed. 2011, 50, 10884-10887.
18. C. Simmerling, B. Strockbine, A. E. Roitberg, J. Am. Chem. Soc. 2002, 124, 11258-11259
19. C. Snow, B. Zagrovic, V. Pande, J. Am. Chem. Soc. 2002, 124, 14548-14549
20. S. Chowdhury, M. Lee, G. Xiong, Y. Duan, J. Mol. Biol. 2003, 327, 711-717
21. J. W. Pitera, W. Swope, Proc. Natl. Acad. Sci. USA 2003, 100, 7587-7592
22. R. Zhou, Proc. Natl. Acad. Sci. USA 2003, 100, 13280-13285
23. M. Ota, M. Ikeguchi, A. Kidera, Proc. Natl. Acad. Sci. USA 2004, 101, 17658-17663
24. A. Linhananta, J. Boer, I. MacKay, J. Chem. Phys. 2005, 122, 114901
25. F. Ding, S. V. Buldyrev, N. V. Dokholyan, Biophys. J. 2005, 88, 147-155
26. L. Ye, H. Chen, T. Liu, Z. Wu, J. Li, R. Zhou, J. Bioinform. Comput. Biol. 2005, 3, 1351-1370
27. D. Paschek, S. Hempel, A. E. García, Proc. Natl. Acad. Sci. USA 2008, 105, 17754-17759
28. Z. Hu, Y. Tang, H. Wang, X. Zhang, M. Lei, Arch. Biochem. Biophys. 2008, 475, 140-147
29. Z. Gattin, S. Riniker, P. J. Hore, K. H. Mok, W. F. van Gunsteren, Protein Sci. 2009, 18, 2090-2099
30. R. Day, D. Paschek, A. Garcia, Proteins 2010, 78, 1889-1899
31. C. Zhang, J. Ma, J. Chem. Phys. 2010, 132, 244101
32. W. Zheng, E. Gallicchio, N. Deng, M. Andrec, R. M. Levy, J. Phys. Chem. B 2011, 115, 1512-1523.
33. J. Juraszek, P. Bolhuis, Proc. Natl. Acad. Sci. USA 2006, 103, 15859-15864
34. J. Juraszek, P. Bolhuis, Biophys. J. 2008, 95, 4246-4257
35. F. Marinelli, F. Pietrucci, A. Laio, S. Piana, PLoS Comput. Biol. 2009, 5, e 1000452.
36. C. A. Jimenez-Cruz, G. I. Makhatadze, A. E. Garcia, Phys. Chem. Chem. Phys. 2011, 13, 17056-17063.
37. H. Neuweiler, S. Doose, M. Sauer, Proc. Natl. Acad. Sci. USA 2005, 102, 16650-16655
38. K. Mok, L. Kuhn, M. Goez, I. Day, J. Lin, N. Andersen, P. Hore, Nature 2007, 447, 106-109
39. A. T. Iavarone, A. Patriksson, D. van der Spoel, J. H. Parks, J. Am. Chem. Soc. 2007, 129, 6726-6735
40. D. Williams, B. Barua, N. Andersen, Org. Biomol. Chem. 2008, 6, 4287-4289
41. D. V. Williams, A. Byrne, J. Stewart, N. H. Andersen, Biochemistry 2011, 50, 1143-1152.
42. Z. Ahmed, I. Beta, A. Mikhonin, S. Asher, J. Am. Chem. Soc. 2005, 127, 10943-10950.
43. B. Barua, J. Lin, V. Williams, P. Kummler, J. Neidigh, N. Andersen, Protein Eng. Des. Sel. 2008, 21, 171-185.
44. P. Hudáky, P. Stráner, V. Farkas, G. Váradi, G. Tõth, A. Perczel, Biochemistry 2008, 47, 1007-1016.
45. P. Rovõ, V. Farkas, O. Hegyi, O. Szolomájer-Csikõs, G. K. Tõth, A. Perczel, J. Pept. Sci. 2011, 17, 610-619.
46. J. Heyda, M. Koz?íšek, L. Bednárova, G. Thompson, J. Konvalinka, J. Vondrášek, P. Jungwirth, J. Phys. Chem. B 2011, 115, 8910-8924.
47. R. L. Baldwin, Fold. Des. 1996, 1, R 1-8.
48. W. Streicher, G. Makhatadze, Biochemistry 2007, 46, 2876-2880.
49. T. L. Religa, J. S. Markson, U. Mayor, S. M. Freund, A. R. Fersht, Nature 2005, 437, 1053-1056.
50. A. Perczel, M. Hollõsi, G. Tusnády, G. Fasman, Protein Eng. 1991, 4, 669-679
51. A. Perczel, K. Park, G. Fasman, Anal. Biochem. 1992, 203, 83-93.
52. Y. Shen, F. Delaglio, G. Cornilescu, A. Bax, J. Biomol. NMR 2009, 44, 213-223.
53. N. Tjandra, S. Feller, R. Pastor, A. Bax, J. Am. Chem. Soc. 1995, 117, 12562-12566.
54. J. García de La Torre, M. L. Huertas, B. Carrasco, J. Magn. Reson. 2000, 147, 138-146.
55. G. Lipari, A. Szabo, J. Am. Chem. Soc. 1982, 104, 4546-4559
56. G. Lipari, A. Szabo, J. Am. Chem. Soc. 1982, 104, 4559-4570
57. G. Clore, A. Szabo, A. Bax, L. Kay, P. Driscoll, A. Gronenborn, J. Am. Chem. Soc. 1990, 112, 4989-4991.
58. J. Peng, G. Wagner, J. Magn. Reson. 1992, 98, 308-332
59. J. Peng, G. Wagner, Biochemistry 1995, 34, 16733-16752.
60. N. Farrow, O. Zhang, A. Szabo, D. Torchia, L. Kay, J. Biomol. NMR 1995, 6, 153-162.
61. J. F. Lefèvre, K. T. Dayie, J. W. Peng, G. Wagner, Biochemistry 1996, 35, 2674-2686.
62. G. Montelione, B. Lyons, S. Emerson, M. Tashiro, J. Am. Chem. Soc. 1992, 114, 10974-10975.
63. M. Scian, J. C. Lin, I. Le Trong, G. I. Makhatadze, R. E. Stenkamp, N. H. Andersen, Proc. Natl. Acad. Sci. USA 2012, 109, 12521-12525.
64. N. L. Fawzi, J. Ying, D. A. Torchia, G. M. Clore, J. Am. Chem. Soc. 2010, 132, 9948-9951.
65. P. Rogne, P. Ozdowy, C. Richter, K. Saxena, H. Schwalbe, L. T. Kuhn, PLoS One 2012, 7, e 41301.
66. T. Kohno, H. Kusunoki, K. Sato, K. Wakamatsu, J. Biomol. NMR 1998, 12, 109-121.
67. J. Marley, M. Lu, C. Bracken, J. Biomol. NMR 2001, 20, 71-75.
68. N. A. Farrow, O. Zhang, J. D. Forman-Kay, L. E. Kay, J. Biomol. NMR 1994, 4, 727-734
69. N. Farrow, R. Muhandiram, A. Singer, S. Pascal, C. Kay, G. Gish, S. Shoelson, T. Pawson, J. Formankay, L. Kay, Biochemistry 1994, 33, 5984-6003.
70. H. Krizova, L. Zidek, M. Stone, M. Novotny, V. Sklenar, J. Biomol. NMR 2004, 28, 369-384.
71. P. Dosset, J. Hus, M. Blackledge, D. Marion, J. Biomol. NMR 2000, 16, 23-28.
72. L. Kay, D. Torchia, A. Bax, Biochemistry 1989, 28, 8972-8979.
73. T. Goddard, D. Kneller, University of California, San Franscisco, 1999.
74. E. Pettersen, T. Goddard, C. Huang, G. Couch, D. Greenblatt, E. Meng, T. Ferrin, J. Comput. Chem. 2004, 25, 1605-1612.
75. D. Van Der Spoel, E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, H. J. Berendsen, J. Comput. Chem. 2005, 26, 1701-1718.
76. A. MacKerell, Jr., D. Bashford, M. Bellott, R. Dunbrack, J. Evanseck, M. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. Lau, C. Mattos, S. Michnick, T. Ngo, D. Nguyen, B. Prodhom, W. Reiher, B. Roux, M. Schlenkrich, J. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, M. Karplus, J. Phys. Chem. B 1998, 102, 3586-3616.
77. W. Jorgensen, J. Chandrasekhar, J. Madura, R. Impey, M. Klein, J. Chem. Phys. 1983, 79, 926-935.
78. X. Daura, K. Gademann, B. Jaun, D. Seebach, W. F. van Gunsteren, A. E. Mark, Angew. Chem. 1999, 111, 249-253
79. Angew. Chem. Int. Ed. 1999, 38, 236-240.
80. W. Kabsch, C. Sander, Biopolymers 1983, 22, 2577-2637.