Enhanced sampling molecular dynamics simulation captures experimentally suggested intermediate and unfolded states in the folding pathway of Trp-cage miniprotein

Journal of Chemical Physics

Volumn 137, Issue 12, 2012, Pages

  Shao, Qiang ^a   Shi, Jiye ^b   Zhu, Weiliang ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b UCB PHARMA   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EXPERIMENTAL MEASUREMENTS; FOLDING PATHWAY; FORCE FIELDS; MOLECULAR DYNAMICS SIMULATIONS; PHOTO-CIDNP; PROTEIN FOLDING MECHANISMS; SAMPLING METHOD; THERMODYNAMICS PARAMETERS; TRANSIENT STATE;

EXPERIMENTS; MOLECULAR MECHANICS; PROTEIN FOLDING; PROTEINS; THERMODYNAMICS;

MOLECULAR DYNAMICS;

PEPTIDE; TRP CAGE PEPTIDE; TRP-CAGE PEPTIDE;

ARTICLE; CHEMISTRY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN FOLDING;

MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN FOLDING;

EID: 84867027679     PISSN: 00219606     EISSN: None     Source Type: Journal    
DOI: 10.1063/1.4754656     Document Type: Article

References (55)

1. H. Roder and W. Colon, Curr. Opin. Struct. Biol. 7, 15 (1997). 10.1016/S0959-440X(97)80004-8
2. D. J. Brockwell and S. E. Radford, Curr. Opin. Struct. Biol. 17, 30 (2007). 10.1016/j.sbi.2007.01.003
3. J. W. Neidigh, R. M. Fesinmeyer, and N. H. Andersen, Nat. Struct. Biol. 9, 425 (2002). 10.1038/nsb798
4. L. L. Qiu, S. A. Pabit, A. E. Roitberg, and S. J. Hagen, J. Am. Chem. Soc. 124, 12952 (2002). 10.1021/ja0279141
5. L. L. Qiu and S. J. Hagen, Chem. Phys. 312, 325 (2005); 10.1016/j.chemphys.2004.12.002
6. M. R. Bunagan, X. Yang, J. G. Saven, and F. Gai, J. Phys. Chem. B 110, 3759 (2006). 10.1021/jp055288z
7. Z. Ahmed, I. A. Beta, A. V. Mikhonin, and S. A. Asher, J. Am. Chem. Soc. 127, 10943 (2005). 10.1021/ja050664e
8. W. W. Streicher and G. I. Makhatadze, Biochemistry 46, 2876 (2007). 10.1021/bi602424x
9. K. H. Mok, L. T. Kuhn, M. Goez, I. J. Day, J. C. Lin, N. H. Andersen, and P. J. Hore, Nature (London) 447, 106 (2007). 10.1038/nature05728
10. R. H. Zhou, Proc. Natl. Acad. Sci. U.S.A. 100, 13280 (2003). 10.1073/pnas.2233312100
11. J. W. Pitera and W. Swope, Proc. Natl. Acad. Sci. U.S.A. 100, 7587 (2003); 10.1073/pnas.1330954100
12. D. Paschek, S. Hempel, and A. E. Garcia, Proc. Natl. Acad. Sci. U.S.A. 105, 17754 (2008). 10.1073/pnas.0804775105
13. S. Chowdhury, M. C. Lee, and Y. Duan, J. Phys. Chem. B 108, 13855 (2004). 10.1021/jp0478920
14. J. Juraszek and P. G. Bolhuis, Proc. Natl. Acad. Sci. U.S.A. 103, 15859 (2006); 10.1073/pnas.0606692103
15. Z. H. Hu, Y. H. Tang, H. F. Wang, X. Zhang, and M. Lei, Arch. Biochem. Biophys. 475, 140 (2008); 10.1016/j.abb.2008.04.024
16. F. Marinelli, F. Pietrucci, A. Laio, and S. Piana, PloS Comput. Biol. 5, e1000452 (2009). 10.1371/journal.pcbi.1000452
17. R. Day, D. Paschek, and A. E. Garcia, Proteins 78, 1889 (2010). 10.1002/prot.22702
18. H. Neuweiler, S. Doose, and M. Sauer, Proc. Natl. Acad. Sci. U.S.A. 102, 16650 (2005). 10.1073/pnas.0507351102
19. P. Rovo, V. Farkas, O. Hegyi, O. Szolomajer-Csikos, G. K. Toth, and A. Perczel, J. Pept. Sci. 17, 610 (2011). 10.1002/psc.1377
20. P. L. Freddolino, C. B. Harrison, Y. X. Liu, and K. Schulten, Nat. Phys. 6, 751 (2010); 10.1038/nphys1713
21. L. L. Wang, R. A. Friesner, and B. J. Berne, J. Phys. Chem. B 115, 9431 (2011). 10.1021/jp204407d
22. S. Kannan and M. Zacharias, Int. J. Mol. Sci. 10, 1121 (2009). 10.3390/ijms10031121
23. W. J. Son, S. Jang, Y. Pak, and S. Shin, J. Chem. Phys. 126, 104906 (2007). 10.1063/1.2538966
24. F. Ding, S. V. Buldyrev, and N. V. Dokholyan, Biophys. J. 88, 147 (2005). 10.1529/biophysj.104.046375
25. L. L. Duan, Y. Mei, Y. L. Li, Q. G. Zhang, D. W. Zhang, and J. Z. Zhang, Sci. China Chem. 53, 196 (2010). 10.1007/s11426-009-0196-7
26. Y. Duan, C. Wu, S. Chowdhury, M. C. Lee, G. M. Xiong, W. Zhang, R. Yang, P. Cieplak, R. Luo, T. Lee, J. Caldwell, J. M. Wang, and P. Kollman, J. Comput. Chem. 24, 1999 (2003). 10.1002/jcc.10349
27. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling, Proteins 65, 712 (2006). 10.1002/prot.21123
28. W. D. Cornell, P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman, J. Am. Chem. Soc. 117, 5179 (1995). 10.1021/ja00124a002
29. A. Onufriev, D. Bashford, and D. A. Case, Proteins 55, 383 (2004). 10.1002/prot.20033
30. Y. Q. Gao, J. Chem. Phys. 128, 064105 (2008); 10.1063/1.2825614
31. Y. Q. Gao, L. J. Yang, Y. B. Fan, and Q. Shao, Int. Rev. Phys. Chem. 27, 201 (2008). 10.1080/01442350801920334
32. Q. Shao and Y. Q. Gao, J. Chem. Theory Comput. 6, 3750 (2010); 10.1021/ct100436r
33. Q. Shao, H. Y. Wei, and Y. Q. Gao, J. Mol. Biol. 402, 595 (2010); 10.1016/j.jmb.2010.08.037
34. Q. Shao, L. J. Yang, and Y. Q. Gao, J. Chem. Phys. 135, 235104 (2011); 10.1063/1.3668288
35. Q. Shao and Y. Q. Gao, J. Chem. Phys. 135, 135102 (2011); 10.1063/1.3630127
36. L. X. Chen, Q. Shao, Y. Q. Gao, and D. H. Russell, J. Phys. Chem. A 115, 4427 (2011). 10.1021/jp110014j
37. R. M. Culik, A. L. Serrano, M. R. Bunagan, and F. Gai, Angew. Chem., Int. Ed. 50, 10884 (2011). 10.1002/anie.201104085
38. D. A. Case, AMBER 9, University of California, San Francisco, 2006.
39. Q. Shao, L. J. Yang, and Y. Q. Gao, J. Chem. Phys. 130, 195104 (2009). 10.1063/1.3132850
40. J. P. Ryckaert, G. Ciccotti, and H. J. C. Berendsen, J. Comput. Phys. 23, 327 (1977). 10.1016/0021-9991(77)90098-5
41. K. Hukushima and K. Nemoto, J. Phys. Soc. Jpn. 65, 1604 (1996); 10.1143/JPSJ.65.1604
42. Y. Sugita and Y. Okamoto, Chem. Phys. Lett. 314, 141 (1999). 10.1016/S0009-2614(99)01123-9
43. L. J. Yang, Q. Shao, and Y. Q. Gao, J. Chem. Phys. 130, 124111 (2009). 10.1063/1.3097129
44. k values in the ITS method, and the figure of the population of the intermediate, folded, and unfolded states at different temperatures calculated for the simulations using FF03 and FF99SB force fields, and the two-dimensional, three-dimensional free energy profiles for the simulations using three force fields at different temperatures.
45. K. L. Maxwell, D. Wildes, A. Zarrine-Afsar, M. A. de los Rios, A. G. Brown, C. T. Friel, L. Hedberg, J. C. Horng, D. Bona, E. J. Miller, A. Vallee-Belisle, E. R. G. Main, F. Bemporad, L. L. Qiu, K. Teilum, N. D. Vu, A. M. Edwards, I. Ruczinski, F. M. Poulsen, B. B. Kragelund, S. W. Michnick, F. Chiti, Y. W. Bai, S. J. Hagen, L. Serrano, M. Oliveberg, D. P. Raleigh, P. Wittung-Stafshede, S. E. Radford, S. E. Jackson, T. R. Sosnick, S. Marqusee, A. R. Davidson, and K. W. Plaxco, Protein Sci. 14, 602 (2005). 10.1110/ps.041205405
46. S. Ono, N. Nakajima, J. Higo, and H. Nakamura, J. Comput. Chem. 21, 748 (2000); 10.1002/(SICI)1096-987X(20000715)21:9<748::AID-JCC4>3.0.CO;2-2
47. J. Higo, N. Ito, M. Kuroda, S. Ono, N. Nakajima, and H. Nakamura, Protein Sci. 10, 1160 (2001); 10.1110/ps.44901
48. N. Kamiya, J. Higo, and H. Nakamura, Protein Sci. 11, 2297 (2002); 10.1110/ps.0213102
49. M. H. Zaman, M. Y. Shen, R. S. Berry, K. F. Freed, and T. R. Sosnick, J. Mol. Biol. 331, 693 (2003). 10.1016/S0022-2836(03)00765-4
50. D. R. Roe, A. Okur, L. Wickstrom, V. Hornak, and C. Simmerling, J. Phys. Chem. B 111, 1846 (2007); 10.1021/jp066831u
51. A. Okur, L. Wickstrom, and C. Simmerling, J. Chem. Theory Comput. 4, 488 (2008); 10.1021/ct7002308
52. Y. Shang, H. Nguyen, L. Wickstrom, A. Okur, and C. Simmerling, J. Mol. Graphics Modell. 29, 676 (2011). 10.1016/j.jmgm.2010.11.013
53. A. R. Fersht and V. Daggett, Cell 108, 573 (2002). 10.1016/S0092-8674(02) 00620-7
54. U. Mayor, N. R. Guydosh, C. M. Johnson, J. G. Grossmann, S. Sato, G. S. Jas, S. M. V. Freund, D. O. V. Alonso, V. Daggett, and A. R. Fersht, Nature (London) 421, 863 (2003); 10.1038/nature01428
55. K. A. Merchant, R. B. Best, J. M. Louis, I. V. Gopich, and W. A. Eaton, Proc. Natl. Acad. Sci. U.S.A. 104, 1528 (2007). 10.1073/pnas.0607097104