Comparative study of hydration shell dynamics around a hyperactive antifreeze protein and around ubiquitin

Journal of Chemical Physics

Volumn 141, Issue 22, 2014, Pages

  Duboué Dijon, Elise ^a   Laage, Damien ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINS; HYDRATION; HYDROGEN BONDS; ICE; MOLECULAR DYNAMICS; MOLECULES; SHELLS (STRUCTURES);

BIOCHEMICAL FUNCTIONS; COMPARATIVE STUDIES; CONFINEMENT EFFECTS; DYNAMICAL HETEROGENEITIES; HETEROGENEOUS ENSEMBLES; HYDRATION SHELL STRUCTURE; MOLECULAR DYNAMICS SIMULATIONS; REORIENTATION DYNAMICS;

PROTEINS;

ANTIFREEZE PROTEIN; ICE; INSECT PROTEIN; UBIQUITIN; WATER;

ANIMAL; CHEMISTRY; COMPARATIVE STUDY; HUMAN; HYDROGEN BOND; LEPIDOPTERA; MOLECULAR DYNAMICS;

ANIMALS; ANTIFREEZE PROTEINS; HUMANS; HYDROGEN BONDING; ICE; INSECT PROTEINS; LEPIDOPTERA; MOLECULAR DYNAMICS SIMULATION; UBIQUITIN; WATER;

EID: 84918532011     PISSN: 00219606     EISSN: None     Source Type: Journal    
DOI: 10.1063/1.4902822     Document Type: Article

References (101)

1. B. Halle, Philos. Trans. R. Soc. London, Ser. B 359, 1207 (2004). 10.1098/rstb.2004.1499
2. S. K. Pal and A. H. Zewail, Chem. Rev. 104, 2099 (2004). 10.1021/cr020689l
3. P. Ball, Chem. Rev. 108, 74 (2008). 10.1021/cr068037a
4. Y. Levy and J. N. Onuchic, Annu. Rev. Biophys. Biomol. Struct. 35, 389 (2006). 10.1146/annurev.biophys.35.040405.102134
5. B. Bagchi, Chem. Rev. 105, 3197 (2005). 10.1021/cr020661+
6. A. C. Fogarty, E. Duboué-Dijon, F. Sterpone, J. T. Hynes, and D. Laage, Chem. Soc. Rev. 42, 5672 (2013). 10.1039/c3cs60091b
7. C. Mattea, J. Qvist, and B. Halle, Biophys. J. 95, 2951 (2008). 10.1529/biophysj.108.135194
8. R. G. Bryant, C. R. Phys. 11, 128 (2010). 10.1016/j.crhy.2010.06.013
9. S. K. Pal, J. Peon, and A. H. Zewail, Proc. Natl. Acad. Sci. U.S.A. 99, 1763 (2002). 10.1073/pnas.042697899
10. T. Li, A. A. Hassanali, Y.-T. Kao, D. Zhong, and S. J. Singer, J. Am. Chem. Soc. 129, 3376 (2007). 10.1021/ja0685957
11. J. T. King, E. J. Arthur, C. L. Brooks III, and K. J. Kubarych, J. Phys. Chem. B 116, 5604 (2012). 10.1021/jp300835k
12. B. Born, S. J. Kim, S. Ebbinghaus, M. Gruebele, and M. Havenith, Faraday Discuss. 141, 161 (2009). 10.1039/b804734k
13. K. Wood, M. Plazanet, F. Gabel, B. Kessler, D. Oesterhelt, D. J. Tobias, G. Zaccai, and M. Weik, Proc. Natl. Acad. Sci. U.S.A. 104, 18049 (2007). 10.1073/pnas.0706566104
14. D. Russo, J. Ollivier, and J. Teixeira, Phys. Chem. Chem. Phys. 10, 4968 (2008). 10.1039/b807551b
15. M.-C. Bellissent-Funel, J.-M. Zanotti, and S. H. Chen, Faraday Discuss. 103, 281 (1996). 10.1039/fd9960300281
16. K. Mazur, I. A. Heisler, and S. R. Meech, J. Phys. Chem. A 116, 2678 (2011). 10.1021/jp2074539
17. L. Comez, L. Lupi, A. Morresi, M. Paolantoni, P. Sassi, and D. Fioretto, J. Phys. Chem. Lett. 4, 1188 (2013). 10.1021/jz400360v
18. R. Abseher, H. Schreiber, and O. Steinhauser, Prot.: Struct., Funct., Genet. 25, 366 (1996). 10.1002/(SICI)1097-0134(199607)25:3<366::AID-PROT8>3.0.CO;2-D
19. V. A. Makarov, B. K. Andrews, P. E. Smith, and B. M. Pettitt, Biophys. J. 79, 2966 (2000). 10.1016/S0006-3495(00)76533-7
20. A. E. García and G. Hummer, Prot.: Struct., Funct., Bioinf. 38, 261 (2000). 10.1002/(SICI)1097-0134(20000215)38:3<261::AID-PROT3>3.0.CO;2-Q
21. M. Tarek and D. J. Tobias, Phys. Rev. Lett. 89, 275501 (2002). 10.1103/PhysRevLett.89.275501
22. A. R. Bizzarri and S. Cannistraro, J. Phys. Chem. B 106, 6617 (2002). 10.1021/jp020100m
23. M. Marchi, F. Sterpone, and M. Ceccarelli, J. Am. Chem. Soc. 124, 6787 (2002). 10.1021/ja025905m
24. F. Pizzitutti, M. Marchi, F. Sterpone, and P. J. Rossky, J. Phys. Chem. B 111, 7584 (2007). 10.1021/jp0717185
25. M. Tarek and D. J. Tobias, Biophys. J. 79, 3244 (2000). 10.1016/S0006-3495(00)76557-X
26. M. Heyden and D. J. Tobias, Phys. Rev. Lett. 111, 218101 (2013). 10.1103/PhysRevLett.111.218101
27. V. Conti Nibali, G. DAngelo, A. Paciaroni, D. J. Tobias, and M. Tarek, J. Phys. Chem. Lett. 5, 1181 (2014). 10.1021/jz500023e
28. F. Sterpone, G. Stirnemann, and D. Laage, J. Am. Chem. Soc. 134, 4116 (2012). 10.1021/ja3007897
29. A. C. Fogarty and D. Laage, J. Phys. Chem. B 118, 7715 (2014). 10.1021/jp409805p
30. D. Laage, G. Stirnemann, F. Sterpone, R. Rey, and J. T. Hynes, Annu. Rev. Phys. Chem. 62, 395 (2011). 10.1146/annurev.physchem.012809.103503
31. D. Laage, G. Stirnemann, F. Sterpone, and J. T. Hynes, Acc. Chem. Res. 45, 53 (2012). 10.1021/ar200075u
32. D. Wen and R. A. Laursen, Biophys. J. 63, 1659 (1992). 10.1016/S0006-3495(92)81750-2
33. Y. Yeh and R. E. Feeney, Chem. Rev. 96, 601 (1996). 10.1021/cr950260c
34. H. Chao, M. E. Houston, R. S. Hodges, C. M. Kay, B. D. Sykes, M. C. Loewen, P. L. Davies, and F. D. Sönnichsen, Biochemistry 36, 14652 (1997). 10.1021/bi970817d
35. M. E. Houston Jr., H. Chao, R. S. Hodges, B. D. Skyes, C. M. Kay, F. D. Sonnichsen, M. C. Loewen, and P. L. Davies, J. Biol. Chem. 273, 11714 (1998). 10.1074/jbc.273.19.11714
36. A. D. J. Haymet, L. G. Ward, and M. M. Harding, J. Am. Chem. Soc. 121, 941 (1999). 10.1021/ja9801341
37. J. D. Madura, K. Baran, and A. Wierzbicki, J. Mol. Recognit. 13, 101 (2000). 10.1002/(SICI)1099-1352(200003/04)13:2<101::AID-JMR493>3.0.CO;2-9
38. N. Pertaya, C. B. Marshall, C. L. DiPrinzio, L. Wilen, E. S. Thomson, J. S. Wettlaufer, P. L. Davies, and I. Braslavsky, Biophys. J. 92, 3663 (2007). 10.1529/biophysj.106.096297
39. H. Nada and Y. Furukawa, J. Phys. Chem. B 112, 7111 (2008). 10.1021/jp711977g
40. H. Nada and Y. Furukawa, Polym. J. 44, 690 (2012). 10.1038/pj.2012.13
41. Y. Celik, R. Drori, N. Pertaya-Braun, A. Altan, T. Barton, M. Bar-Dolev, A. Groisman, P. L. Davies, and I. Braslavsky, Proc. Natl. Acad. Sci. U.S.A. 110, 1309 (2013). 10.1073/pnas.1213603110
42. S. Ebbinghaus, K. Meister, M. B. Prigozhin, A. L. Devries, M. Havenith, J. Dzubiella, and M. Gruebele, Biophys. J. 103, L20 (2012). 10.1016/j.bpj.2012.06.013
43. S. Wang, N. Amornwittawat, V. Juwita, Y. Kao, J. G. Duman, T. A. Pascal, W. A. Goddard, and X. Wen, Biochemistry 48, 9696 (2009). 10.1021/bi901283p
44. K. A. Sharp and J. M. Vanderkooi, Acc. Chem. Res. 43, 231 (2010). 10.1021/ar900154j
45. J. A. Raymond and A. L. DeVries, Proc. Natl. Acad. Sci. U.S.A. 74, 2589 (1977). 10.1073/pnas.74.6.2589
46. R. A. Nistor, T. E. Markland, and B. J. Berne, J. Phys. Chem. B 118, 752 (2014). 10.1021/jp408832b
47. D. R. Nutt and J. C. Smith, J. Am. Chem. Soc. 130, 13066 (2008). 10.1021/ja8034027
48. N. Smolin and V. Daggett, J. Phys. Chem. B 112, 6193 (2008). 10.1021/jp710546e
49. U. S. Midya and S. Bandyopadhyay, J. Phys. Chem. B 118, 4743 (2014). 10.1021/jp412528b
50. A. Kuffel, D. Czapiewski, and J. Zielkiewicz, J. Chem. Phys. 141, 055103 (2014). 10.1063/1.4891810
51. C. P. Garnham, R. L. Campbell, and P. L. Davies, Proc. Natl. Acad. Sci. U.S.A. 108, 7363 (2011). 10.1073/pnas.1100429108
52. K. Modig, J. Qvist, C. B. Marshall, P. L. Davies, and B. Halle, Phys. Chem. Chem. Phys. 12, 10189 (2010). 10.1039/c002970j
53. K. Meister, S. Ebbinghaus, Y. Xu, J. G. Duman, A. DeVries, M. Gruebele, D. M. Leitner, and M. Havenith, Proc. Natl. Acad. Sci. U.S.A. 110, 1617 (2013). 10.1073/pnas.1214911110
54. S. Vijay-Kumar, C. E. Bugg, and W. J. Cook, J. Mol. Biol. 194, 531 (1987). 10.1016/0022-2836(87)90679-6
55. E. K. Leinala, P. L. Davies, and Z. Jia, Structure 10, 619 (2002). 10.1016/S0969-2126(02)00745-1
56. W. Humphrey, A. Dalke, and K. Schulten, J. Mol. Graph. 14, 33 (1996). 10.1016/0263-7855(96)00018-5
57. A. D. MacKerell Jr., D. Bashford, M. Bellott, R. L. Dunbrack Jr., J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, and S. Ha, J. Phys. Chem. B 102, 3586 (1998). 10.1021/jp973084f
58. J. L. F. Abascal and C. Vega, J. Chem. Phys. 123, 234505 (2005). 10.1063/1.2121687
59. G. Stirnemann and D. Laage, J. Chem. Phys. 137, 031101 (2012). 10.1063/1.4737390
60. E. Duboué-Dijon, A. C. Fogarty, and D. Laage, J. Phys. Chem. B 118, 1574 (2014). 10.1021/jp408603n
61. J. C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kale, and K. Schulten, J. Comput. Chem. 16, 1781 (2005). 10.1002/jcc.20289
62. T. Darden, D. York, and L. Pedersen, J. Chem. Phys. 98, 10089 (1993). 10.1063/1.464397
63. J. Qvist, C. Mattea, E. P. Sunde, and B. Halle, J. Chem. Phys. 136, 204505 (2012). 10.1063/1.4720941
64. D. Laage and J. T. Hynes, Science 311, 832 (2006). 10.1126/science.1122154
65. D. Laage and J. T. Hynes, J. Phys. Chem. B 112, 14230 (2008). 10.1021/jp805217u
66. G. Ruocco, M. Sampoli, and R. Vallauri, J. Chem. Phys. 96, 6167 (1992). 10.1063/1.462889
67. J. R. Errington and P. G. Debenedetti, Nature (London) 409, 318 (2001). 10.1038/35053024
68. http://dx.doi.org/10.1063/1.4902822.
69. J. R. Schmidt, S. T. Roberts, J. J. Loparo, A. Tokmakoff, M. D. Fayer, and J. L. Skinner, Chem. Phys. 341, 143 (2007). 10.1016/j.chemphys.2007.06.043
70. N. V. Nucci, M. S. Pometun, and A. J. Wand, J. Am. Chem. Soc. 133, 12326 (2011). 10.1021/ja202033k
71. J. Tian and A. E. García, J. Chem. Phys. 134, 225101 (2011). 10.1063/1.3592712
72. V. P. Denisov and B. Halle, J. Mol. Biol. 245, 682 (1995). 10.1006/jmbi.1994.0055
73. E. Persson and B. Halle, J. Am. Chem. Soc. 130, 1774 (2008). 10.1021/ja0775873
74. N. V. Nucci, M. S. Pometun, and A. J. Wand, Nat. Struct. Mol. Biol. 18, 245 (2011). 10.1038/nsmb.1955
75. B. Halle, J. Chem. Phys. 119, 12372 (2003). 10.1063/1.1625632
76. J. R. Jabusch and H. F. Deutsch, Arch. Biochem. Biophys. 238, 170 (1985). 10.1016/0003-9861(85)90153-5
77. F. Sterpone, G. Stirnemann, J. T. Hynes, and D. Laage, J. Phys. Chem. B 114, 2083 (2010). 10.1021/jp9119793
78. J. Qvist, E. Persson, C. Mattea, and B. Halle, Faraday Discuss. 141, 131 (2009). 10.1039/b806194g
79. L. R. Winther, J. Qvist, and B. Halle, J. Phys. Chem. B 116, 9196 (2012). 10.1021/jp304982c
80. J. Qvist and B. Halle, J. Am. Chem. Soc. 130, 10345 (2008). 10.1021/ja802668w
81. L. A. Graham, Y.-C. Liou, V. K. Walker, and P. L. Davies, Nature (London) 388, 727 (1997). 10.1038/41908
82. G. L. Fletcher, C. L. Hew, and P. L. Davies, Annu. Rev. Physiol. 63, 359 (2001). 10.1146/annurev.physiol.63.1.359
83. J. G. Duman, Annu. Rev. Physiol. 63, 327 (2001). 10.1146/annurev.physiol.63.1.327
84. Y.-C. Liou, A. Tocilj, P. L. Davies, and Z. Jia, Nature (London) 406, 322 (2000). 10.1038/35018604
85. N. Prabhu and K. Sharp, Chem. Rev. 106, 1616 (2006). 10.1021/cr040437f
86. A. B. Siemer, K.-Y. Huang, and A. E. McDermott, Proc. Natl. Acad. Sci. U.S.A. 107, 17580 (2010). 10.1073/pnas.1009369107
87. Y. Xu, R. Gnanasekaran, and D. M. Leitner, J. At. Mol. Opt. Phys. 2012, 1 (2012). 10.1155/2012/125071
88. F. Sicheri and D. S. C. Yang, Nature (London) 373, 427 (1995). 10.1038/375427a0
89. Z. Jia and P. L. Davies, Trends Biochem. Sci. 27, 101 (2002). 10.1016/S0968-0004(01)02028-X
90. M. E. Daley and B. D. Sykes, Protein Sci. 12, 1323 (2003). 10.1110/ps.0369503
91. H. Nguyen, L. Le, and T. B. Ho, J. Chem. Phys. 140, 225101 (2014). 10.1063/1.4881895
92. S. P. Graether, M. J. Kuiper, S. M. Gagné, V. K. Walker, Z. Jia, B. D. Sykes, and P. L. Davies, Nature (London) 406, 325 (2000). 10.1038/35018610
93. C. Yang and K. A. Sharp, Proteins 59, 266 (2005). 10.1002/prot.20429
94. T. Sun, F.-H. Lin, R. L. Campbell, J. S. Allingham, and P. L. Davies, Science 343, 795 (2014). 10.1126/science.1247407
95. B. Halle, J. Phys. Chem. B 118, 10806 (2014). 10.1021/jp5083467
96. J. Baardsnes, L. H. Kondejewski, R. S. Hodges, H. Chao, C. Kay, and P. L. Davies, FEBS Lett. 463, 87 (1999). 10.1016/S0014-5793(99)01588-4
97. A. L. Devries and Y. Lin, BBA-Protein Struct. 495, 388 (1977). 10.1016/0005-2795(77)90395-6
98. S. M. Gruenbaum, C. J. Tainter, L. Shi, Y. Ni, and J. L. Skinner, J. Chem. Theory Comput. 9, 3109 (2013). 10.1021/ct400292q
99. C. J. Tainter, L. Shi, and J. L. Skinner, J. Chem. Phys. 140, 134503 (2014). 10.1063/1.4869293
100. A. C. Fogarty, E. Duboué-Dijon, D. Laage, and W. H. Thompson, J. Chem. Phys. 141, 18C523 (2014). 10.1063/1.4896983
101. B. Zelent, M. A. Bryan, K. A. Sharp, and J. M. Vanderkooi, Biophys. Chem. 141, 222 (2009). 10.1016/j.bpc.2009.02.002