Unfolded protein ensembles, folding trajectories, and refolding rate prediction

Journal of Chemical Physics

Volumn 139, Issue 12, 2013, Pages

  Das, A ^a   Sin, B K ^a   Mohazab, A R ^a,b   Plotkin, S S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Recon Instruments 100 ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; COVALENT BONDS; SULFUR COMPOUNDS;

CLUSTERING PROPERTIES; COMPUTATIONAL ANALYSIS; CONFORMATIONAL ENSEMBLE; DISORDERED PROTEINS; GEOMETRICAL PROPERTY; PHYSIOLOGICAL CONDITION; RESIDUAL DIPOLAR COUPLINGS; ROOT MEAN SQUARED DEVIATIONS;

PROTEINS;

POLYMER; PROTEIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CLUSTER ANALYSIS; GENETICS; HUMAN; KINETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN UNFOLDING;

CLUSTER ANALYSIS; HUMANS; KINETICS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; POLYMERS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN UNFOLDING; PROTEINS;

EID: 84885458042     PISSN: 00219606     EISSN: None     Source Type: Journal    
DOI: 10.1063/1.4817215     Document Type: Article

References (118)

1. J. Deisenhofer, O. Epp, K. Miki, R. Huber, and H. Michel, Nature (London) 318, 618 (1985). 10.1038/318618a0
2. D. A. Doyle, J. M. Cabral, R. A. Pfuetzner, A. Kuo, J. M. Gulbis, S. L. Cohen, B. T. Chait, and R. MacKinnon, Science 280, 69 (1998). 10.1126/science.280.5360.69
3. P. Agre, L. S. King, M. Yasui, W. B. Guggino, O. P. Ottersen, Y. Fujiyoshi, A. Engel, and S. Nielsen, J. Physiol. 542, 3 (2002). 10.1113/jphysiol.2002.020818
4. N. Ban, P. Nissen, J. Hansen, P. B. Moore, and T. A. Steitz, Science 289, 905 (2000). 10.1126/science.289.5481.905
5. A. P. Carter, W. M. Clemons, D. E. Brodersen, R. J. Morgan-Warren, B. T. Wimberly, and V. Ramakrishnan, Nature (London) 407, 340 (2000). 10.1038/35030019
6. F. Schluenzen, A. Tocilj, R. Zarivach, J. Harms, M. Gluehmann, D. Janell, A. Bashan, H. Bartels, I. Agmon, F. Franceschi, and A. Yonath, Cell 102, 615 (2000). 10.1016/S0092-8674(00)00084-2
7. A. L. Gnatt, P. Cramer, J. Fu, D. A. Bushnell, and R. D. Kornberg, Science 292, 1876 (2001). 10.1126/science.1059495
8. J. A. Pitcher, N. J. Freedman, and R. J. Lefkowitz, Annu. Rev. Biochem. 67, 653 (1998). 10.1146/annurev.biochem.67.1.653
9. V. Cherezov, D. M. Rosenbaum, M. A. Hanson, S. G. Rasmussen, F. S. Thian, T. S. Kobilka, H.-J. Choi, P. Kuhn, W. I. Weis, B. K. Kobilka, and R. C. Stevens, Science 318, 1258 (2007). 10.1126/science.1150577
10. P. E. Wright and H. J. Dyson, J. Mol. Biol. 293, 321 (1999). 10.1006/jmbi.1999.3110
11. V. N. Uversky, J. R. Gillespie, and A. L. Fink, Proteins: Struct., Funct., Bioinf. 41, 415 (2000). 10.1002/1097-0134(20001115)41:3<415::AID- PROT130>3.0.CO;2-7
12. A. K. Dunker, J. D. Lawson, C. J. Brown, R. M. Williams, P. Romero, J. S. Oh, C. J. Oldfield, A. M. Campen, C. M. Ratliff, K. W. Hipps, J. Ausio, M. Nissen, R. Reeves, C. Kang, C. R. Kissinger, R. W. Bailey, M. D. Griswold, W. Chiu, E. C. Garner, and Z. Obradovic, J. Mol. Graphics Modell. 19, 26 (2001). 10.1016/S1093-3263(00)00138-8
13. P. Tompa, Trends Biochem. Sci. 27, 527 (2002). 10.1016/S0968-0004(02) 02169-2
14. H. J. Dyson and P. E. Wright, Nat. Rev. Mol. Cell Biol. 6, 197 (2005). 10.1038/nrm1589
15. A. K. Dunker, C. Oldfield, J. Meng, P. Romero, J. Yang, J. Chen, V. Vacic, Z. Obradovic, and V. Uversky, BMC Genomics 9, S1 (2008). 10.1186/1471-2164-9-S2-S1
16. P. E. Wright and H. J. Dyson, Curr. Opin. Struct. Biol. 19, 31 (2009). 10.1016/j.sbi.2008.12.003
17. I. Baskakov and D. W. Bolen, J. Biol. Chem. 273, 4831 (1998). 10.1074/jbc.273.9.4831
18. P. Bernadó, C. W. Bertoncini, C. Griesinger, M. Zweckstetter, and M. Blackledge, J. Am. Chem. Soc. 127, 17968 (2005). 10.1021/ja055538p
19. X. Wang, A. Vitalis, M. A. Wyczalkowski, and R. V. Pappu, Proteins: Struct., Funct., Bioinf. 63, 297 (2006). 10.1002/prot.20761
20. N. G. Sgourakis, Y. Yan, S. A. McCallum, C. Wang, and A. E. Garcia, J. Mol. Biol. 368, 1448 (2007). 10.1016/j.jmb.2007.02.093
21. A. Vitalis, X. Wang, and R. V. Pappu, Biophys. J. 93, 1923 (2007). 10.1529/biophysj.107.110080
22. O. O. Olubiyi and B. Strodel, J. Phys. Chem. B 116, 3280 (2012). 10.1021/jp2076337
23. S. Æ. Jónsson, S. Mohanty, and A. Irbäck, Proteins: Struct., Funct., Bioinf. 80, 2169 (2012). 10.1002/prot.24107
24. A. K. Jha, A. Colubri, K. F. Freed, and T. R. Sosnick, Proc. Natl. Acad. Sci. U.S.A. 102, 13099 (2005). 10.1073/pnas.0506078102
25. P. Bernadó, L. Blanchard, P. Timmins, D. Marion, R. W. H. Ruigrok, and M. Blackledge, Proc. Natl. Acad. Sci. U.S.A. 102, 17002 (2005). 10.1073/pnas.0506202102
26. J. B. Udgaonkar, Arch. Biochem. Biophys. 531, 24 (2013). 10.1016/j.abb.2012.10.003
27. K. W. Plaxco, K. T. Simons, and D. Baker, J. Mol. Biol. 277, 985 (1998). 10.1006/jmbi.1998.1645
28. Y. Zhang, BMC Bioinf. 9, 40 (2008). 10.1186/1471-2105-9-40
29. N. S. Bogatyreva, A. A. Osypov, and D. N. Ivankov, Nucleic Acids Res. 37, D342 (2009). 10.1093/nar/gkn696
30. A. R. Mohazab and S. S. Plotkin, PloS ONE 8, e53642 (2013). 10.1371/journal.pone.0053642
31. D. W. Farrell, K. Speranskiy, and M. F. Thorpe, Proteins: Struct., Funct., Bioinf. 78, 2908 (2010). 10.1002/prot.22810
32. M. Lal, Mol. Phys. 17, 57 (1969). 10.1080/00268976900100781
33. N. Madras and A. D. Sokal, J. Stat. Phys. 50, 109 (1988). 10.1007/BF01022990
34. S. Hadizadeh, A. Linhananta, and S. S. Plotkin, Macromolecules 44, 6182 (2011). 10.1021/ma200454e
35. G. Favrin, A. Irback, and F. Sjunnesson, J. Chem. Phys. 114, 8154 (2001). 10.1063/1.1364637
36. N. Go and H. A. Scheraga, Macromolecules 3, 178 (1970). 10.1021/ma60014a012
37. L. R. Dodd, T. D. Boone, and D. N. Theodorou, Mol. Phys. 78, 961 (1993). 10.1080/00268979300100641
38. D. Hoffmann and E.-W. Knapp, Eur. Biophys. J. 24, 387 (1996), see http://dx.doi.org/10.1007/BF00576711. 10.1007/BF00576711
39. M. R. Betancourt, J. Chem. Phys. 123, 174905 (2005), see http://link.aip.org/link/?JCP/123/174905/1. 10.1063/1.2102896
40. P. Rotkiewicz and J. Skolnick, J. Comput. Chem. 29, 1460 (2008). 10.1002/jcc.20906
41. J. Maupetit, R. Gautier, and P. Tufféry, Nucleic Acids Res. 34, W147 (2006). 10.1093/nar/gkl289
42. B. Zagrovic, C. D. Snow, S. Khaliq, M. R. Shirts, and V. S. Pande, J. Mol. Biol. 323, 153 (2002). 10.1016/S0022-2836(02)00888-4
43. M. N. Rosenbluth and A. W. Rosenbluth, J. Chem. Phys. 23, 356 (1955). 10.1063/1.1741967
44. P. Grassberger, Phys. Rev. E 56, 3682 (1997). 10.1103/PhysRevE.56.3682
45. K. J. Kohlhoff, P. Robustelli, A. Cavalli, X. Salvatella, and M. Vendruscolo, J. Am. Chem. Soc. 131, 13894 (2009). 10.1021/ja903772t
46. M. Zweckstetter, Nat. Protoc. 3, 679 (2008). 10.1038/nprot.2008.36
47. See supplementary material at http://dx.doi.org/10.1063/1.4817215 E-JCPSA6-139-022336 for supporting figures, tables, and description.
48. RMSD values for backbone and all heavy atoms were also examined and gave similar results.
49. W. Humphrey, A. Dalke, and K. Schulten, J. Mol. Graphics 14, 33 (1996). 10.1016/0263-7855(96)00018-5
50. Y. Zhang and J. Skolnick, Nucleic Acids Res. 33, 2302 (2005). 10.1093/nar/gki524
51. A. Zemla, Nucleic Acids Res. 31, 3370 (2003). 10.1093/nar/gkg571
52. J. P. Rodrigues, M. Levitt, and G. Chopra, Nucleic Acids Res. 40, W323 (2012). 10.1093/nar/gks376
53. S. S. Plotkin, Proc. Natl. Acad. Sci. U.S.A. 104, 14899 (2007). 10.1073/pnas.0607833104
54. A. R. Mohazab and S. S. Plotkin, J. Phys. Condens. Matter 20, 244133 (2008). 10.1088/0953-8984/20/24/244133
55. A. R. Mohazab and S. S. Plotkin, Biophys. J. 95, 5496 (2008). 10.1529/biophysj.108.135046
56. B. Thiruv, G. Quon, S. Saldanha, and B. Steipe, BMC Struct. Biol. 5, 12 (2005). 10.1186/1472-6807-5-12
57. L. Hou, H. Shao, Y. Zhang, H. Li, N. K. Menon, E. B. Neuhaus, J. M. Brewer, I.-J. L. Byeon, D. G. Ray, M. P. Vitek, T. Iwashita, R. A. Makula, A. B. Przybyla, and M. G. Zagorski, J. Am. Chem. Soc. 126, 1992 (2004). 10.1021/ja036813f
58. A. De Simone, A. Cavalli, S.-T. D. Hsu, W. Vranken, and M. Vendruscolo, J. Am. Chem. Soc. 131, 16332 (2009). 10.1021/ja904937a
59. G. Lipari and A. Szabo, J. Am. Chem. Soc. 104, 4546 (1982). 10.1021/ja00381a009
60. N. G. Sgourakis, M. Merced-Serrano, C. Boutsidis, P. Drineas, Z. Du, C. Wang, and A. E. Garcia, J. Mol. Biol. 405, 570 (2011). 10.1016/j.jmb.2010.10.015
61. O. Tcherkasskaya and V. N. Uversky, Proteins: Struct., Funct., Bioinf. 44, 244 (2001). 10.1002/prot.1089
62. S. Doniach, Chem. Rev. 101, 1763 (2001). 10.1021/cr990071k
63. H. Hofmann, A. Soranno, A. Borgia, K. Gast, D. Nettels, and B. Schuler, Proc. Natl. Acad. Sci. U.S.A. 109, 16155 (2012). 10.1073/pnas.1207719109
64. C. Tanford, K. Kawahara, and S. Lapanje, J. Biol. Chem. 241, 1921 (1966).
65. D. K. Wilkins, S. B. Grimshaw, V. Receveur, C. M. Dobson, J. A. Jones, and L. J. Smith, Biochemistry 38, 16424 (1999). 10.1021/bi991765q
66. J. E. Kohn, I. S. Millett, J. Jacob, B. Zagrovic, T. M. Dillon, N. Cingel, R. S. Dothager, S. Seifert, P. Thiyagarajan, T. R. Sosnick, M. Z. Hasan, V. S. Pande, I. Ruczinski, S. Doniach, and K. W. Plaxco, Proc. Natl. Acad. Sci. U.S.A. 101, 12491 (2004). 10.1073/pnas.0403643101
67. P. J. Flory, Principles of Polymer Chemistry (Cornell University Press, Ithaca, 1953).
68. V. N. Uversky, Protein Sci. 11, 739 (2002). 10.1110/ps.4210102
69. B. Hammouda, Adv. Polymer Sci. 106, 87 (1993). 10.1007/BFb0025862
70. R. B. Best, B. Li, A. Steward, V. Daggett, and J. Clarke, Biophys. J. 81, 2344 (2001). 10.1016/S0006-3495(01)75881-X
71. D. Brockwell, E. Paci, R. Zinober, G. Beddard, P. Olmsted, D. Smith, R. Perham, and S. Radford, Nat. Struct. Biol. 10, 731 (2003). 10.1038/nsb968
72. D. Shortle, K. T. Simons, and D. Baker, Proc. Natl. Acad. Sci. U.S.A. 95, 11158 (1998); see also http://www.sbg.bio.ic.ac.uk/maxcluster. 10.1073/pnas.95.19.11158
73. C. W. Bertoncini, Y.-S. Jung, C. O. Fernandez, W. Hoyer, C. Griesinger, T. M. Jovin, and M. Zweckstetter, Proc. Natl. Acad. Sci. U.S.A. 102, 1430 (2005). 10.1073/pnas.0407146102
74. M. Doi and S. F. Edwards, The Theory of Polymer Dynamics (Oxford University Press, Oxford, 1986), Chap..
75. D. Nettels, I. V. Gopich, A. Hoffmann, and B. Schuler, Proc. Natl. Acad. Sci. U.S.A. 104, 2655 (2007). 10.1073/pnas.0611093104
76. F. Krieger, B. Fierz, O. Bieri, M. Drewello, and T. Kiefhaber, J. Mol. Biol. 332, 265 (2003). 10.1016/S0022-2836(03)00892-1
77. J. Kubelka, J. Hofrichter, and W. A. Eaton, Curr. Opin. Struct. Biol. 14, 76 (2004). 10.1016/j.sbi.2004.01.013
78. K. W. Plaxco, K. T. Simons, I. Ruczinski, and D. Baker, Biochemistry 39, 11177 (2000). 10.1021/bi000200n
79. M. M. Gromiha and S. Selvaraj, J. Mol. Biol. 310, 27 (2001). 10.1006/jmbi.2001.4775
80. A. Y. Istomin, D. J. Jacobs, and D. R. Livesay, Protein Sci. 16, 2564 (2007). 10.1110/ps.073124507
81. B. Harihar and S. Selvaraj, Biopolymers 91, 928 (2009). 10.1002/bip.21281
82. T. Zou and S. B. Ozkan, Phys. Biol. 8, 066011 (2011). 10.1088/1478-3975/8/6/066011
83. H. Zhou and Y. Zhou, Biophys. J. 82, 458 (2002). 10.1016/S0006-3495(02) 75410-6
84. D. N. Ivankov, S. O. Garbuzynskiy, E. Alm, K. W. Plaxco, D. Baker, and A. V. Finkelstein, Protein Sci. 12, 2057 (2003). 10.1110/ps.0302503
85. M. Rustad and K. Ghosh, J. Chem. Phys. 137, 205104 (2012). 10.1063/1.4767567
86. D. Thirumalai, J. Phys. I 5, 1457 (1995). 10.1051/jp1:1995209
87. S. S. Plotkin, J. Wang, and P. G. Wolynes, J. Chem. Phys. 106, 2932 (1997). 10.1063/1.473355
88. A. R. Dinner and M. Karplus, Nat. Struct. Biol. 8, 21 (2001). 10.1038/83003
89. S. S. Plotkin and J. N. Onuchic, J. Chem. Phys. 116, 5263 (2002). 10.1063/1.1449866
90. B. Oztop, M. R. Ejtehadi, and S. S. Plotkin, Phys. Rev. Lett. 93, 208105 (2004). 10.1103/PhysRevLett.93.208105
91. U. Bastolla, P. Bruscolini, and J. L. Velasco, Proteins: Struct., Funct., Bioinf. 80, 2287 (2012). 10.1002/prot.24118
92. N. Koga and S. Takada, J. Mol. Biol. 313, 171 (2001). 10.1006/jmbi.2001.5037
93. C. Micheletti, Proteins: Struct., Funct., Bioinf. 51, 74 (2003). 10.1002/prot.10342
94. Z. Ouyang and J. Liang, Protein Sci. 17, 1256 (2008). 10.1110/ps.034660.108
95. H. Gong, D. G. Isom, R. Srinivasan, and G. D. Rose, J. Mol. Biol. 327, 1149 (2003). 10.1016/S0022-2836(03)00211-0
96. D. Ivankov and A. Finkelstein, Proc. Natl. Acad. Sci. U.S.A. 101, 8942 (2004). 10.1073/pnas.0402659101
97. P. Bruscolini, A. Pelizzola, and M. Zamparo, Phys. Rev. Lett. 99, 038103 (2007). 10.1103/PhysRevLett.99.038103
98. J.-T. Huang, J.-P. Cheng, and H. Chen, Proteins: Struct., Funct., Bioinf. 67, 12 (2007). 10.1002/prot.21282
99. M. M. Gromiha, J. Chem. Inf. Model. 45, 494 (2005). 10.1021/ci049757q
100. H.-B. Shen, J.-N. Song, and K.-C. Chou, J. Biomed. Sci. Eng. 2, 136 (2009). 10.4236/jbise.2009.23024
101. L. Chang, J. Wang, and W. Wang, Phys. Rev. E 82, 051930 (2010). 10.1103/PhysRevE.82.051930
102. A. D. Miranker and C. M. Dobson, Curr. Opin. Struct. Biol. 6, 31 (1996). 10.1016/S0959-440X(96)80092-3
103. D. Eliezer, P. A. Jennings, P. E. Wright, S. Doniach, K. O. Hodgson, and H. Tsuruta, Science 270, 487 (1995). 10.1126/science.270.5235.487
104. A. Dasgupta and J. B. Udgaonkar, J. Mol. Biol. 403, 430 (2010). 10.1016/j.jmb.2010.08.046
105. C. Magg and F. X. Schmid, J. Mol. Biol. 335, 1309 (2004). 10.1016/j.jmb.2003.11.050
106. B. Anil, Y. Li, J.-H. Cho, and D. P. Raleigh, Biochemistry 45, 10110 (2006). 10.1021/bi060636o
107. K. H. Mok, L. T. Kuhn, M. Goez, I. J. Day, J. C. Lin, N. H. Andersen, and P. Hore, Nature (London) 447, 106 (2007). 10.1038/nature05728
108. M. Sadqi, L. J. Lapidus, and V. Muñoz, Proc. Natl. Acad. Sci. U.S.A. 100, 12117 (2003). 10.1073/pnas.2033863100
109. Y. Duan and P. A. Kollman, Science 282, 740 (1998). 10.1126/science.282. 5389.740
110. J. D. Bryngelson and P. G. Wolynes, Biopolymers 30, 177 (1990). 10.1002/bip.360300117
111. S. S. Plotkin and J. N. Onuchic, Q. Rev. Biophys. 35, 111 (2002). 10.1017/S0033583502003761
112. S. S. Plotkin and J. N. Onuchic, Q. Rev. Biophys. 35, 205 (2002). 10.1017/S0033583502003785
113. G. Ziv, D. Thirumalai, and G. Haran, Phys. Chem. Chem. Phys. 11, 83 (2009). 10.1039/b813961j
114. N. D. Socci and J. N. Onuchic, J. Chem. Phys. 103, 4732 (1995). 10.1063/1.470610
115. A. M. Gutin, V. I. Abkevich, and E. I. Shakhnovich, Biochemistry 34, 3066 (1995). 10.1021/bi00009a038
116. Z. Guo and D. Thirumalai, Biopolymers 36, 83 (1995). 10.1002/bip. 360360108
117. A. R. Fersht, Curr. Opin. Struct. Biol. 5, 79 (1995). 10.1016/0959-440X(95)80012-P
118. M. Gromiha, A. Thangakani, and S. Selvaraj, Nucleic Acids Res. 34, W70 (2006). 10.1093/nar/gkl043