Simplicity within the complexity: Bilateral impact of DMSO on the functional and unfolding patterns of α-chymotrypsin

Biophysical Chemistry

Volumn 175-176, Issue , 2013, Pages 17-27

  Tretyakova, Tatyana ^a,b   Shushanyan, Mikhael ^a,b   Partskhaladze, Tamar ^a   Makharadze, Maya ^b   Van Eldik, Rudi ^c   Khoshtariya, Dimitri E ^a,b,c  

^a TBILISI STATE UNIVERSITY   (Georgia)

^b Georgia   (Georgia)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Chymotrypsin; Differential scanning calorimetry; Dimethyl sulfoxide; Dynamic potentiometry; Michaelis Menten kinetics; Protein's local global stability

Indexed keywords

CHYMOTRYPSIN A; DIMETHYL SULFOXIDE; LYSOZYME;

ACIDITY; ARTICLE; CALORIMETRY; CATALYSIS; DIFFERENTIAL SCANNING CALORIMETRY; ENZYME KINETICS; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; MELTING POINT; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN UNFOLDING; TEMPERATURE; THERMODYNAMICS;

CALORIMETRY; CATALYTIC DOMAIN; CHYMOTRYPSIN; DIMETHYL SULFOXIDE; HYDROGEN-ION CONCENTRATION; KINETICS; PROTEIN STABILITY; PROTEIN UNFOLDING; THERMODYNAMICS;

EID: 84875060561     PISSN: 03014622     EISSN: 18734200     Source Type: Journal    
DOI: 10.1016/j.bpc.2013.02.006     Document Type: Article

References (118)

1. A.R. Fersht Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding 2nd ed. 1998 Freeman New York
2. M. Wolf-Watz, V. Thai, K.A. Henzler-Wildman, G. Hadjipavlou, E.Z. Eisenmesser, and D. Kern Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair Nature Structural & Molecular Biology 11 2004 945 949 (Pubitemid 39315297)
3. 19F NMR studies Journal of Molecular Biology 345 2005 599 610 (Pubitemid 39575927)
4. K. Teilum, J.G. Olsen, and B.B. Kragelund Protein stability, flexibility and function Biochimica et Biophysica Acta 1814 2011 969 976
5. A.N. Morozov, and D.C. Chatfield Chloroperoxidase-catalyzed epoxidation of cis-β-methylstyrene: distal pocket flexibility tunes catalytic reactivity Journal of Physical Chemistry B 116 2012 12905 12914
6. Z. Amini-Bayat, S. Hosseinkhani, R. Jafari, and K. Khajeh Relationship between stability and flexibility in the most flexible region of Photinus pyralis luciferase Biochimica et Biophysica Acta 1824 2012 350 358
7. J.N. Onuchic, H. Nymeyer, A.E. Garcia, J. Chahine, and N.D. Socci The energy landscape theory of protein folding: insights into folding mechanisms and scenarios Advances in Protein Chemistry 53 2000 87 152 (Pubitemid 34194293)
8. A. Warshel, and W. Parson Dynamics of biochemical and biophysical reactions: insight from computer simulations Quarterly Reviews of Biophysics 34 2001 563 679 (Pubitemid 34127275)
9. C.M. Dobson Protein folding and misfolding Nature (London) 426 2003 884 890 (Pubitemid 38056880)
10. O. Miyashita, J.N. Onuchic, and P.G. Wolynes Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins Proceedings of the National Academy of Sciences of the United States of America 100 2003 12570 12575 (Pubitemid 37339939)
11. J.N. Onuchic, and P.G. Wolynes Theory of protein folding Current Opinion in Structural Biology 14 2004 70 75 (Pubitemid 38249595)
12. D.E. Khoshtariya, T.D. Dolidze, S. Seyfert, D. Sarauli, G. Lee, and R. van Eldik Kinetic, thermodynamic and mechanistic patterns for free (unbound) cytochrome c at Au/SAM junctions. Impact of electronic coupling, hydrostatic pressure, and stabilizing/denaturing additives Chemistry - A European Journal 12 2006 7041 7056 (Pubitemid 44450131)
13. M. Shushanyan, D.E. Khoshtariya, T. Tretyakova, M. Makharadze, and R. van Eldik Diverse role of conformational dynamics in carboxypeptidase A-driven peptide and ester hydrolyses. Disclosing the "perfect induced fit" and "protein local unfolding" pathways by altering protein stability Biopolymers 95 2011 852 870
14. D.E. Khoshtariya, M. Shushanian, R. Sujashvili, M. Makharadze, E. Tabuashvili, and G. Getashvili Enzymatic activity of α-chymotrypsin in the urea-induced molten-globule-like state: a combined kinetic/thermodynamic study Journal of Biological Physics and Chemistry (Basel) 3 2003 2 11
15. M. Shushanyan, R. Sujashvili, E. Tabuashvili, M. Makharadze, G. Getashvili, and D.E. Khoshtariya Kinetic and thermodynamic manifestations of thermally induced molten-globule-like state of α-chymotrypsin Journal of Biological Physics and Chemistry (Basel) 6 2006 51 55
16. K.A. Henzler-Wildman, V. Thai, M. Lei, M. Ott, M. Wolf-Watz, T. Fenn, E. Pozharski, M.A. Wilson, G.A. Petsko, M. Karplus, C.G. Hübner, and D. Kern Intrinsic motions along an enzymatic reaction trajectory Nature (London) 450 2007 838 844 (Pubitemid 350231334)
17. A.V. Pisliakova, J. Caoa, S.C.L. Kamerlina, and A. Warshel Enzyme millisecond conformational dynamics do not catalyze the chemical step Proceedings of the National Academy of Sciences of the United States of America 106 2009 17359 17364
18. D.E. Khoshtariya, J. Wei, H. Liu, H. Yue, and D.H. Waldeck The charge-transfer mechanism for cytochrome c adsorbed on nanometer thick films. Distinguishing frictional control from conformational gating Journal of the American Chemical Society 125 2003 7704 7714 (Pubitemid 36750292)
19. D) Journal of Biological Physics and Chemistry (Basel) 5 2005 103 110
20. D.E. Khoshtariya, T.D. Dolidze, M. Shushanyan, K.L. Davis, D.H. Waldeck, and R. van Eldik Fundamental signatures of short- and long-range electron transfer for azurin functionalized at Au/alkanethiol SAM junctions Proceedings of the National Academy of Sciences of the United States of America 107 2010 2757 2762
21. P.L. Privalov, and N.N. Khechinashvili A thermodynamic approach to the problem of stabilization of globular protein structure: a calorimetric study Journal of Molecular Biology 86 1974 665 684
22. N.N. Khechinashvili, J. Janin, and F. Rodier Thermodynamics of the temperature-induced unfolding of globular proteins Protein Science 4 1995 1315 1324
23. E. Freire, W.W. van Osdol, O.L. Mayorga, and J.M. Sanches-Ruiz Calorimetricaly determined dynamics of complex unfolding transitions in proteins Annual Review of Biophysics and Biophysical Chemistry 19 1990 159 188 (Pubitemid 20205622)
24. J.M. Sanches-Ruiz Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry Biophysical Journal 61 1992 921 935
25. C. La Rosa, D. Milardi, D. Grasso, R. Guzzi, and L. Sporteli Thermodynamics of the thermal unfolding of azurin The Journal of Physical Chemistry 99 1995 14864 14870
26. H. Weingärtner, C. Cabrele, and C. Herrmann How ionic liquids can help to stabilize native proteins Physical Chemistry Chemical Physics 2012 10.1039/c1cp21947b
27. M. Arai, and K. Kuwajima Role of the molten globule state in protein folding Advances in Protein Chemistry 53 2000 209 282 (Pubitemid 34194295)
28. P.L. Privalov, and S.A. Potekhin Scanning microcalorimetry in studying temperature-induced changes in proteins Methods in Enzymology 131 1986 4 51 (Pubitemid 16002194)
29. D. Martin, A. Weise, and H.-J. Niclas The solvent dimethyl sulfoxide Angewandte Chemie, International Edition 6 1967 318 334
30. Z.-W. Yu, and P.J. Quinn Dimethyl sulphoxide: a review of applications in cell biology Bioscience Reports 14 1994 259 281
31. K. Capriotti, and J.A. Capriotti Dimethyl sulfoxide: history, chemistry, and clinical utility in dermatology The Journal of Clinical and Aesthetic Dermatology 5 2012 24 26
32. A.N. Rajeshwara, and V. Prakash Structural stability of lipase from wheat germ International Journal of Peptide and Protein Research 44 1994 435 440 (Pubitemid 24367481)
33. S. Rajendran, C. Radha, and V. Prakash Mechanism of solvent-induced thermal stabilization of alfa-amylase from Bacillus amyloliquefaciens International Journal of Peptide and Protein Research 45 1995 122 128
34. K. Hamaguchi Structure of muramidase (lysosyme). VIII. Effect of dimethyl sulfoxide on the stability of muramidase Journal of Biochemistry (Tokyo) 56 1964 441 449
35. M. Kotik, S.E. Radford, and C.M. Dobson Comparison of the refolding of hen lysozyme from dimethyl sulfoxide and guanidinium chloride Biochemistry 34 1995 1714 1724
36. I.K. Voets, W.A. Cruz, C. Moitzi, P. Lindner, E.P.G. Areas, and P. Schurtenberger DMSO-induced denaturation of hen egg white lysozyme The Journal of Physical Chemistry. B 114 2010 11875 11883
37. R.L. Perlman, and J. Wolff Dimethyl sulfoxide: an inhibitor of liver alcohol dehydrogenase Science (Washington) 160 1968 317 319
38. M. Banasik, and K. Ueda Dual inhibitory effects of dimethyl sulfoxide on poly(adp-ribose) synthetase Journal of Enzyme Inhibition 14 1999 239 250 (Pubitemid 29141432)
39. O. Almarsson, and A.M. Klibanov Remarkable activation of enzymes in nonaqueous aqueous media by denaturing organic cosolvents Biotechnology and Bioengineering 1996 4987 4992
40. H.J. Zhang, X.R. Sheng, X.M. Pan, and J.M. Zhou Activation of adenylate kinase by denaturants is due to the increasing conformational flexibility at its active sites Biochemical and Biophysical Research Communications 113 1983 348 352
41. A. Steinschneider, and K. Druck Ribonuclease properties and activity in the presence of dimethylsulfoxide Biochimica et Biophysica Acta 287 1972 77 89
42. J.E. Lovelock, and M.W.H. Bishop Prevention of freezing damage to living cells by dimethyl sulphoxide Nature (London) 183 1959 1394 1395
43. E. Jaspard Role of protein-solvent interactions in refolding: effects of cosolvent additives on the renaturation of porcine pancreatic elastase at various pHs Archives of Biochemistry and Biophysics 375 2000 220 228 (Pubitemid 30158378)
44. W.-B. Ou, Y.-D. Park, and H.-M. Zhou Effect of osmolytes as folding aids on creatine kinase refolding pathway The International Journal of Biochemistry & Cell Biology 34 2002 136 147 (Pubitemid 34112523)
45. S.-H. Kim, Y.-B. Yan, and H.-M. Zhou Role of osmolytes as chemical chaperones during the refolding of aminoacylase Biochemistry and Cell Biology 84 2006 30 38
46. B. Zerner, and M.L. Bender The kinetic consequences of the acyl-enzyme mechanism for the reactions of specific substrates with chymotrypsin Journal of the American Chemical Society 86 1964 3669 3674
47. N.L. Eremeev Interaction of α-chymotrypsin with dimethyl sulfoxide: a change of substrate could "change" the interaction mechanism Bioorganicheskaia Khimiia 29 2003 479 485
48. C.L. Tsou Conformational flexibility of enzyme active sites Science 262 1993 380 381
49. C.L. Tsou Active site flexibility in enzyme catalysis Annals of the New York Academy of Sciences 864 1998 1 8
50. J. Bhalla, G.B. Storchan, C.M. MacCarthy, V.N. Uversky, and O. Tcherkasskaya Local flexibility in molecular function paradigm Molecular & Cellular Proteomics 5 2006 1212 1223 (Pubitemid 44103393)
51. D.E. Khoshtariya, V.V. Topolev, and L.I. Krishtalik Study of proton transfer in enzymatic hydrolysis by the method of temperature dependence of kinetic isotope effect. I. α-chymotrypsin catalyzed hydrolysis of N-acetyl- and N-benzyl-l-tyrosine ethyl esters Bioorganicheskaia Khimiia 4 1978 1341 1351
52. D.E. Khoshtariya Study of proton transfer in enzymatic hydrolysis by the method of temperature dependence of kinetic isotope effect. II. β-trypsin catalyzed hydrolysis of N-benzoyl-l-arginine ethyl ester Bioorganicheskaia Khimiia 4 1978 1673 1677
53. L.Z. Holland, M. McFall-Ngai, and G.N. Somero Evolution of lactate dehydrogenase-A homologs of barracuda fishes (Genus Sphyraena) from different thermal environments: differences in kinetic properties and thermal stability are due to amino acid substitutions outside the active site Biochemistry 36 1997 3207 3215 (Pubitemid 27142393)
54. P.A. Fields, and G.N. Somero Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes Proceedings of the National Academy of Sciences of the United States of America 95 1998 11476 11481 (Pubitemid 28450154)
55. F. Conejero-Lara, A.I. Azuaga, and P.L. Mateo Differential scanning calorimetry of thermolysin and its 255-316 and 205-316 C-terminal fragments Reactive and Functional Polymers 34 1997 113 120 (Pubitemid 127402518)
56. F. Conejero-Lara, V. De Filippis, A. Fontana, and P.L. Mateo The thermodynamics of the unfolding of an isolated protein subdomain: the 255-316 C-terminal fragment of thermolysin FEBS Letters 344 1994 154 156 (Pubitemid 24154629)
57. J. Wen, K. Arthur, L. Chemmalil, S. Muzammil, J. Gabrielson, and Y. Jiang Applications of differential scanning calorimetry for thermal stability analysis of proteins: qualification of DSC Journal of Pharmaceutical Sciences 101 2012 955 964
58. D.E. Khoshtariya, M. Makharadze, G. Getashvili, and M. Zaalishvili On the DSC rate performance for a three-state thermal denaturation of globular proteins Bulletin of the Georgian National Academy of Sciences 164 2001 535 537
59. D.E. Khoshtariya, and N.G. Goguadze Conformationally-adiabatic process of deacylation of N-acetyl-l-tyrosile-α-chymotrypsin Bioorganicheskaia Khimiia 11 1985 1621 1626
60. D.E. Khoshtariya, N.G. Goguadze, and J. Ulstrup Kinetic manifestation of conformational dynamics accompanying enzymatic hydrolysis of benzoyl-glycyl-phenillactate by carcoxypeptidase A Bioorganicheskaia Khimiia 17 1991 618 625
61. Y. Fujita, S. Izumiguchi, and Y. Noda Effect of dimethylsulfoxide and its homologues on the thermal denaturation of lysozyme as measured by differential scanning calorimetry International Journal of Peptide and Protein Research 19 1982 25 31
62. A. Torreggiani, M.D. Foggia, L. Manco, A. De Maio, S.A. Markarian, and S. Bonora Effect of sulfoxides on the thermal denaturation of hen lysozyme: a calorimetric and Raman study Journal of Molecular Structure 891 2008 115 122
63. T. Arakawa, Y. Kita, and S.N. Timasheff Protein precipitation and denaturation by dimethyl sulfoxide Biophysical Chemistry 131 2007 62 70 (Pubitemid 350047519)
64. Y. Fujita, A. Miyanaga, and Y. Noda Effect of alcohols on the thermal denaturation of lysozyme as measured by differential scanning calorimetry Bulletin of the Chemical Society of Japan 52 1979 3659 3662
65. G. Velicelebi, and J.M. Sturtevant Thermodynamics of the denaturation of lysozyme in alcohol-water mixtures Biochemistry 18 1979 1180 1186
66. P. Attri, P. Venkatesu, and M.J. Lee Influence of osmolytes and denaturants on the structure and enzyme activity of alpha-chymotrypsin The Journal of Physical Chemistry. B 114 2010 1471 1478
67. A. Kumar, P. Attri, and P. Venkatesu Effect of polyols on the native structure of alpha-chymotrypsin: a comparable study Thermochimica Acta 536 2012 55 62
68. H. Jóhannesson, V.P. Denisov, and B. Halle Dimethyl sulfoxide binding to globular proteins: a nuclear magnetic relaxation dispersion study Protein Science 6 1997 1756 1763 (Pubitemid 27333078)
69. S. Bhattacharjya, and P. Balaram Effects of organic solvents on protein structures: observation of a structured helical core in hen egg-white lysozyme in aqueous dimethylsulfoxide Proteins 29 1997 492 507 (Pubitemid 27520202)
70. A. Giugliarelli, M. Paolantoni, A. Morresi, and P. Sassi Denaturation and preservation of globular proteins: the role of DMSO The Journal of Physical Chemistry. B 116 2012 13361 13367
71. Y.J. Zhen, and R.L. Ornstein A molecular dynamics and quantum mechanics analysis of the effect of DMSO on enzyme structure and dynamics: subtilisin Journal of the American Chemical Society 118 1996 4175 4180 (Pubitemid 26175187)
72. S. Roy, B. Jana, and B. Bagchi Dimethyl sulfoxide induced structural transformations and non-monotonic concentration dependence of conformational fluctuation around active site of lysozyme The Journal of Chemical Physics 136 115103 2012 1 10
73. γ. Crystallographic study using peptide chloromethyl ketones as site-specific inhibitors Biochemistry 10 1971 3728 3739
74. J.C. Powers, B.L. Baker, J. Browb, and B.K. Chelm Inhibition of chymotrypsin A-alpha with N-acyl- and N-peptidyl-2-phenylethylamines. Subsite binding free energies Journal of the American Chemical Society 96 1974 238 243
75. D.M. Segal Kinetic investigation of the crystallographically deduced binding subsites of bovine chymotrypsin Aγ Biochemistry 11 1972 349 356
76. S.A. Bizzozero, W.K. Baumann, and H. Dutler Kinetic investigation of the α-chymotrypsin-catalyzed hydrolysis of peptide-ester substrates European Journal of Biochemistry 58 1975 167 176
77. 1′ Biochimica et Biophysica Acta 438 1976 495 502
78. S.N. Timasheff, and G. Xie Preferential interactions of urea with lysozyme and their linkage to protein denaturation Biophysical Chemistry 105 2003 421 448 (Pubitemid 37123076)
79. B.J. Bennion, and V. Daggett Counteraction of urea-induced protein denaturation by trimethylamine N-oxide: a chemical chaperone at atomic resolution Proceedings of the National Academy of Sciences of the United States of America 101 2004 6433 6438 (Pubitemid 38585991)
80. A. Kumar, and P. Venkatesu Overview of the stability of α-chymotrypsin in different solvent media Chemical Reviews 112 2012 4283 4307
81. P.J. Rossky Protein denaturation by urea: slash and bond Proceedings of the National Academy of Sciences of the United States of America 105 2008 16825 16826
82. L. Hua, R. Zhou, D. Thirumalai, and B.J. Berne Urea denaturation by stronger dispersion interactions with proteins than water implies a two-stage unfolding Proceedings of the National Academy of Sciences of the United States of America 105 2008 16928 16933
83. S.C. Mande, and M.E. Sobhia Structural characterization of protein-denaturant interactions: crystal structures of hen egg-white lysozyme in complex with DMSO and guanidinium chloride Protein Engineering 13 2000 133 141 (Pubitemid 30151045)
84. P.H. Yancey, and G.N. Somero Methylamine osmoregulatory solutes of elasmobranch fishes counteract urea inhibition of enzymes The Journal of Experimental Zoology 212 1980 205 213
85. H. Frauenfelder, G.A. Petsko, and D. Tsernoglou Temperature-dependent X-ray diffraction as a probe of protein structural dynamics Nature (London) 280 1979 558 563
86. P.J. Artymiuk, C.C.F. Blake, D.E.P. Grace, S.J. Oatley, D.C. Phillips, and M.J.E. Sternberg Crystallographic studies of the dynamic properties of lysozyme Nature (London) 280 1979 563 568
87. E.R. Birnbaum, F. Abbott, J.E. Gomez, and D.W. Darnall The calcium ion binding site in bovine chymotrypsin A Archives of Biochemistry and Biophysics 179 1977 469 476 (Pubitemid 8067827)
88. F. Adebodun, and F. Jordan Multinuclear magnetic resonance studies on the calcium(II) binding site in trypsin, chymotrypsin, and subtilisin Biochemistry 28 1989 7524 7531 (Pubitemid 19238100)
89. E. Fioretti, M. Angeletti, G. Lupidi, and M. Coletta Heterotropic modulation of the protease-inhibitor-recognition process: cations effect the binding properties of α-chymotrypsin European Journal of Biochemistry 225 1994 459 465 (Pubitemid 24306273)
90. K. Kar, B. Alex, and N. Kishore Thermodynamics of the interactions of calcium chloride with α-chymotrypsin The Journal of Chemical Thermodynamics 34 2002 319 336
91. J.J. Birktoft, and D.M. Blow Structure of crystalline α-chymotrypsin. V. the atomic structure of tosyl-α-chymotrypsin at 2 Å resolution Journal of Molecular Biology 68 1972 187 240
92. C.N. Pace Conformational stability of globular proteins Trends in Biochemical Sciences 15 1990 14 17 (Pubitemid 20033184)
93. N. Ui Isoelectric points and conformation of proteins. II Isoelectric focusing of α-chymotrypsin and its inactive derivative Biochimica et Biophysica Acta 229 1971 582 589
94. S.N. Timasheff The control of protein stability and association by weak interactions with water. How do solvent affect these processes? Annual Review of Biophysics and Biomolecular Structure 22 1993 67 97 (Pubitemid 23180317)
95. C.N. Pace, D.V. Laurence, and J.A. Thomson pH dependence of the urea and guanidine hydrochloride denaturation of ribonuclease A and ribonuclease T1 Biochemistry 29 1990 2564 2572 (Pubitemid 20100853)
96. A.-S. Yang, and B. Honig On the pH dependence of protein stability Journal of Molecular Biology 231 1993 459 474 (Pubitemid 23188265)
97. A.H. Elcock Realistic modelling of the denatured states of proteins allows accurate calculations of the pH dependence of protein stability Journal of Molecular Biology 294 1999 1051 1062 (Pubitemid 30000394)
98. G.I. Makhatadze, and P.L. Privalov Contribution of hydration to protein folding thermodynamics. I. The enthalpy of hydration Journal of Molecular Biology 232 1993 639 659 (Pubitemid 23251184)
99. G.I. Makhatadze, and P.L. Privalov Energetics of protein structure Advances in Protein Chemistry 47 1995 307 425
100. S.S. Stickler, A.V. Gribenko, A.V. Gribenko, T.R. Keiffer, J. Tomilson, T. Reihle, V.V. Loladze, and G.I. Makhatadze Protein stability and surface electrostatics: a charged relationship Biochemistry 45 2006 2761 2766 (Pubitemid 43334524)
101. A.G. Gvritishvili, A.V. Gribenko, and G.I. Makhatadze Cooperativity of complex salt bridges Protein Science 17 2008 1285 1290 (Pubitemid 351930926)
102. V.M. Dadarlat, and C.B. Post Contribution of charged groups to the enthalpic stabilization of the folded states of globular proteins The Journal of Physical Chemistry. B 112 2008 6159 6167
103. L. Xiao, and B. Honig Electrostatic contributions to the stability of hyperthermophilic proteins Journal of Molecular Biology 289 1999 1435 1444 (Pubitemid 29296715)
104. G.R. Grimsley, K.I. Shaw, L.R. Fee, R.W. Alston, B.M.P. Huyghes-Despointes, R.L. Thurlkill, J.M. Scholtz, and C.N. Pace Increasing protein stability by altering long-range coulombic interactions Protein Science 8 1999 1843 1849 (Pubitemid 29430484)
105. G. Careri Cooperative charge fluctuations by migrating protons in globular proteins Progress in Biophysics and Molecular Biology 70 1998 223 249 (Pubitemid 28487614)
106. D.E. Khoshtariya, E. Hansen, R. Leecharoen, and G.C. Walker Probing protein hydration by the difference HO-H (HO-D) vibrational spectroscopy: interfacial percolation network involving highly polarizable water-water hydrogen bonds Journal of Molecular Liquids 105 2003 13 36
107. B. Bagchi Water dynamics in the hydration layer around proteins and micelles Chemical Reviews 105 2005 3197 3219 (Pubitemid 41430808)
108. V.A. Sirotkin, and A.V. Khadiulina Hydration of α-chymotrypsin: excess partial enthalpies of water and enzyme Thermochimica Acta 522 2011 205 210
109. A. Wada, and H. Nakamura Nature of the charge distribution in proteins Nature (London) 293 1981 757 758 (Pubitemid 12241937)
110. 2O): a dynamic model emerging from near-infrared DO-D stretching overtone studies Journal of Molecular Liquids 96 97 2002 45 63 (Pubitemid 34228399)
111. 2O) from difference vibrational spectroscopy The Journal of Physical Chemistry. B 108 2004 14796 14799
112. N.N. Khechinashvili, S.A. Volchkov, A.V. Kabanov, and G. Barone Thermal stability of proteins does not correlate with the energy of intramolecular interactions Biochimica et Biophysica Acta 1784 2008 1830 1834
113. J.L. England, and G. Haran Role of solvation effects in protein denaturation: from thermodynamics to single molecules and back Annual Review of Physical Chemistry 62 2011 257 277
114. J. Bush, and G.I. Makhatadze Statistical analysis of protein structures suggests that buried ionisable residues in proteins are hydrogen bonded or form salt bridges Proteins 79 2011 2027 2032
115. M. Ohgushi, and A. Wada Molten-globule state: a compact form of globular proteins with mobile side chains FEBS Letters 164 1983 21 24
116. O.B. Ptytsin The molten globule state T.E. Creighton, Protein Folding 1992 Freeman New York 243 300
117. Y.V. Griko, and P.L. Privalov Thermodynamic puzzle of apomyoglobin unfolding Journal of Molecular Biology 235 1994 1318 1325 (Pubitemid 24148934)
118. Y.V. Griko Energetic basis of structural stability in the molten globule state: α-lactalbumin Journal of Molecular Biology 297 2000 1259 1268