Slow unfolded-state structuring in acyl-CoA binding protein folding revealed by simulation and experiment

Journal of the American Chemical Society

Volumn 134, Issue 30, 2012, Pages 12565-12577

  Voelz, Vincent A ^a,i   Jäger, Marcus ^b   Yao, Shuhuai ^c   Chen, Yujie ^d,j   Zhu, Li ^d,e   Waldauer, Steven A ^d,k   Bowman, Gregory R ^a,l   Friedrichs, Mark ^f   Bakajin, Olgica ^b,g   Lapidus, Lisa J ^d   Weiss, Shimon ^h   Pande, Vijay S ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e SOUTHEAST UNIVERSITY   (China)

^f Stanford University   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ Temple University   (United States)

^j Cornell University   (United States)

^k UNIVERSITY OF ZURICH   (Switzerland)

^l UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACYL-COA BINDING PROTEINS; ATOMISTIC SIMULATIONS; BINDING PROTEINS; COMPLEX NETWORKS; DENATURED STATE; FAST KINETICS; FOLDING INTERMEDIATES; FOLDING KINETICS; FOLDING PATHWAY; FOLDING REACTIONS; FOLDING TIME; HUMAN DISEASE; HYDROPHOBIC CORE; LONG-RANGE STRUCTURES; MARKOV STATE MODELS; META-STABLE STATE; MIXING EXPERIMENTS; MOLECULAR DYNAMICS TRAJECTORIES; NETWORK MODELS; SIDE-CHAINS; SIMULATION STUDIES; SINGLE-MOLECULE; TIME-RESOLVED; TIME-SCALES; TWO-STATE FOLDERS; ULTRA-FAST;

FARM BUILDINGS; KINETICS; MOLECULAR DYNAMICS; PROTEIN FOLDING; PROTEINS; REACTION INTERMEDIATES; REACTION KINETICS;

EXPERIMENTS;

ACYL COENZYME A; CYSTEINE; DIAZEPAM BINDING INHIBITOR; TRYPSIN;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIDDEN MARKOV MODEL; HYDROPHOBICITY; LAMINAR FLOW; MOLECULAR DYNAMICS; MONTE CARLO METHOD; MUTATION; PARTICLE SIZE; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN UNFOLDING; SIMULATION; SITE DIRECTED MUTAGENESIS; UNFOLDED STATE STRUCTURE;

ANIMALS; CATTLE; DIAZEPAM BINDING INHIBITOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MARKOV CHAINS; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN UNFOLDING;

EID: 84864495493     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja302528z     Document Type: Article

References (68)

1. Kragelund, B. B.; Osmark, P.; Neergaard, T. B.; Schiødt, J.; Kristiansen, K.; Knudsen, J.; Poulsen, F. M. Nat. Struct. Mol. Biol. 1999, 6, 594
2. Teilum, K.; Poulsen, F. M.; Akke, M. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 6877
3. Bruun, S. W.; Iešmantavičius, V.; Danielsson, J.; Poulsen, F. M. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 13306
4. Kristjansdottir, S.; Lindorff-Larsen, K.; Fieber, W.; Dobson, C. M.; Vendruscolo, M.; Poulsen, F. M. J. Mol. Biol. 2005, 347, 1053
5. Laurence, T. A.; Kong, X.; Jager, M.; Weiss, S. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 17348
6. Hertzog, D. E.; Michalet, X.; Jager, M.; Kong, X. X.; Santiago, J. G.; Weiss, S.; Bakajin, O. Anal. Chem. 2004, 76, 7169
7. Teilum, K.; Maki, K.; Kragelund, B. B.; Poulsen, F. M.; Roder, H. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 9807
8. Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Shaw, D. E. Science 2011, 334, 517
9. Shaw, D. E.; Chao, J. C.; Eastwood, M. P.; Gagliardo, J.; Grossman, J. P.; Ho, C. R.; Lerardi, D. J. Commun. ACM 2008, 51, 91
10. Shaw, D. E.; Maragakis, P.; Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Eastwood, M. P.; Bank, J. A.; Jumper, J. M.; Salmon, J. K.; Shan, Y.; Wriggers, W. Science 2010, 330, 341
11. Voelz, V. A.; Bowman, G. R.; Beauchamp, K. A.; Pande, V. S. J. Am. Chem. Soc. 2010, 132, 1526
12. Bowman, G. R.; Voelz, V. A.; Pande, V. S. J. Am. Chem. Soc. 2011, 133, 664
13. Teilum, K.; Kragelund, B. B.; Poulsen, F. M. J. Mol. Biol. 2002, 324, 349
14. Jager, M.; Michalet, X.; Weiss, S. Protein Sci. 2005, 14, 2059
15. Kapanidis, A. N.; Lee, N. K.; Laurence, T. A.; Doose, S.; Margeat, E.; Weiss, S. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 8936
16. Hoffmann, A.; Kane, A. S.; Nettels, D.; Hertzog, D. E.; Baumgärtel, P.; Lengefeld, J.; Reichardt, G.; Horsley, D. A.; Seckler, R.; Bakajin, O.; Schuler, B. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 105
17. Hofmann, H.; Golbik, R. P.; Ott, M.; Hubner, C. G.; Ulbrich-Hofmann, R. J. Mol. Biol. 2008, 376, 597
18. McCarney, E. R.; Werner, J. H.; Bernstein, S. L.; Ruczinski, I.; Makarov, D. E.; Goodwin, P. M.; Plaxco, K. W. J. Mol. Biol. 2005, 352, 672
19. van der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen], H. J. C. J. Comput. Chem. 2005, 26, 1701
20. Friedrichs, M. S.; Eastman, P.; Vaidyanathan, V.; Houston, M.; Legrand, S.; Beberg, A. L.; Ensign, D. L.; Bruns, C. M.; Pande, V. S. J. Comput. Chem. 2009, 30, 864
21. Shirts, M.; Pande, V. Science 2000, 290, 1903
22. Wang, J.; Cieplak, P.; Kollman, P. A. J. Comput. Chem. 2000, 21, 1049
23. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M. L.; Xiong, G.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T.; Caldwell, J.; Wang, J.; Kollman, P. J. Comput. Chem. 2003, 24, 1999
24. Onufriev, A.; Bashford, D.; Case, D. Proteins: Struct., Funct., Bioinf. 2004, 55, 383
25. Voelz, V. A.; Singh, V. R.; Wedemeyer, W. J.; Lapidus, L. J.; Pande, V. S. J. Am. Chem. Soc. 2010, 132, 4702
26. Ziv, G.; Haran, G. J. Am. Chem. Soc. 2009, 131, 2942
27. Liu, Z.; Reddy, G.; O'Brien, E. P.; Thirumalai, D. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 7787
28. Ziv, G.; Thirumalai, D.; Haran, G. Phys. Chem. Chem. Phys. 2009, 11, 83
29. Sherman, E.; Haran, G. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 11539
30. Jha, A. K.; Colubri, A.; Zaman, M. H.; Koide, S.; Sosnick, T. R.; Freed, K. F. Biochemistry 2005, 44, 9691
31. Miyazawa, S.; Jernigan, R. L. Protein Eng. 1993, 6, 267
32. Shirts, M. R.; Chodera, J. D. J. Chem. Phys. 2008, 129, 124105
33. Bowman, G. R.; Huang, X.; Pande, V. S. Methods 2009, 49, 197
34. Deuflhard, P.; Weber, M. Linear Algebra Appl. 2005, 398, 161
35. Bacallado, S.; Chodera, J. D.; Pande, V. J. Chem. Phys. 2009, 131, 045106
36. Chodera, J. D.; Singhal, N.; Pande, V. S.; Dill, K. A.; Swope, W. C. J. Chem. Phys. 2007, 126, 155101
37. Noé, F.; Fischer, S. Curr. Opin. Struct. Biol. 2008, 18, 154
38. Bowman, G. R.; Pande, V. S. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 10890
39. Singhal, N.; Snow, C. D.; Pande, V. S. J. Chem. Phys. 2004, 121, 415
40. Berezhkovskii, A.; Hummer, G.; Szabo, A. J. Chem. Phys. 2009, 130, 205102
41. Metzner, P.; Schütte, C.; Vanden-Eijnden, E. Multiscale Model. Simul. 2009, 7, 1192
42. Noé, F.; Schütte, C.; Vanden-Eijnden, E.; Reich, L.; Weikl, T. R. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 19011
43. Buchete, N.-V.; Hummer, G. J. Phys. Chem. B 2008, 112, 6057
44. Bowman, G. R.; Beauchamp, K. A.; Boxer, G.; Pande, V. S. J. Chem. Phys. 2009, 131, 124101
45. Huang, F.; Rajagopalan, S.; Settanni, G.; Marsh, R. J.; Armoogum, D. A.; Nicolaou, N.; Bain, A. J.; Lerner, E.; Haas, E.; Ying, L.; Fersht, A. R. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 20758
46. Schuler, B.; Eaton, W. A. Curr. Opin. Struct. Biol. 2008, 18, 16
47. Lindorff-Larsen, K.; Trbovic, N.; Maragakis, P.; Piana, S.; Shaw, D. E. J. Am. Chem. Soc. 2012, 134, 3787
48. Buscaglia, M.; Schuler, B.; Lapidus, L. J.; Eaton, W. A.; Hofrichter, J. J. Mol. Biol. 2003, 332, 9
49. Waldauer, S. A.; Bakajin, O.; Lapidus, L. J. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 13713
50. Lane, T. J.; Bowman, G. R.; Beauchamp, K.; Voelz, V. A.; Pande, V. S. J. Am. Chem. Soc. 2011, 133, 18413
51. Chodera, J. D.; Swope, W. C.; Pitera, J. W.; Dill, K. A. Multiscale Model. Simul. 2006, 5, 1214
52. Ihalainen, J. A.; Paoli, B.; Muff, S.; Backus, E. H. G.; Bredenbeck, J.; Woolley, G. A.; Caflisch, A.; Hamm, P. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 9588
53. Rao, F.; Caflisch, A. J. Mol. Biol. 2004, 342, 299
54. Pande, V. S. Phys. Rev. Lett. 2010, 105, 198101
55. Kabsch, W.; Sander, C. Biopolymers 1983, 2, 2577
56. Modig, K.; Jürgensen, V. W.; Lindorff-Larsen, K.; Fiebera, W.; Bohrb, H. G.; Poulsen, F. M. FEBS Lett. 2007, 581, 4965
57. Camilloni, C.; De Simone, A.; Vranken, W. F.; Vendruscolo, M. Biochemistry 2012, 51, 2224
58. Camilloni, C.; Broglia, R. A.; Tiana, G. J. Chem. Phys. 2011, 134, 045105
59. Fitzkee, N. C.; Rose, G. D. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 12497
60. Voelz, V. A.; Pande, V. S. Proteins: Struct., Funct., Bioinf. 2012, 80, 342
61. Mulligan, V. K.; Hadley, K. C.; Chakrabartty, A. Anal. Biochem. 2012, 421, 181
62. Noé, F.; Doose, S.; Daidone, I.; Löllmann, M.; Sauer, M.; Chodera, J. D.; Smith, J. C. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 4822
63. Pirchi, M.; Ziv, G.; Riven, I.; Cohen, S. S.; Zohar, N.; Barak, Y.; Haran, G. Nat. Commun. 2011, 2, 493
64. Stigler, J.; Ziegler, F.; Gieseke, A.; Gebhardt, C. M.; Rief, M. Science 2011, 334, 512
65. Sadqi, M.; Lapidus, L. J.; Muñoz, V. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 12117
66. Dasgupta, A.; Udgaonkar, J. B. J. Mol. Biol. 2010, 403, 430
67. Haran, G. Curr. Opin. Struct. Biol. 2012, 22, 14
68. Hagen, S. J.; Eaton, W. A. J. Mol. Biol. 2000, 301, 1019