Molecular dynamics simulation of aqueous urea solution: Is urea a structure breaker?

Journal of Physical Chemistry B

Volumn 118, Issue 40, 2014, Pages 11757-11768

  Bandyopadhyay, Dibyendu ^a   Mohan, Sadhana ^a   Ghosh, Swapan K ^a   Choudhury, Niharendu ^a  

^a BHABHA ATOMIC RESEARCH CENTRE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR DYNAMICS SIMULATIONS; STRUCTURE-BREAKERS; UREA SOLUTIONS;

UREA; WATER;

CHEMISTRY; HYDROGEN BOND; MOLECULAR DYNAMICS;

HYDROGEN BONDING; MOLECULAR DYNAMICS SIMULATION; UREA; WATER;

EID: 84907899929     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp505147u     Document Type: Article

References (96)

1. Tanford, C. Contribution of Hydrophobic Interactions to the Stability of the Globular Conformation of Proteins J. Am. Chem. Soc. 1962, 84 (22) 4240-4247
2. Brandts, J. F.; Hunt, L. Thermodynamics of Protein Denaturation. III. Denaturation of Ribonuclease in Water and in Aqueous Urea and Aqueous Ethanol Mixtures J. Am. Chem. Soc. 1967, 89, 4826
3. Yancey, P. H.; Clark, M. E.; Hand, S. C.; Bowlus, R. D.; Somero, G. N. Living with Water Stress: Evolution of Osmolyte Systems Science 1982, 217, 1214-1222
4. Schellman, J. A. A Simple Model for Salvation in Mixed Solvents: Applications to the Stabilization and Destabilization of Macromolecular Structures Biophys. Chem. 1990, 37 (1-3) 121-140
5. Watlaufer, D. B.; Malik, S. K.; Stoller, L.; Coffin, R. L. Nonpolar Group Participation in the Denaturation of Proteins by Urea and Guanidinium Salts. Model Compound Studies J. Am. Chem. Soc. 1964, 86, 508-514
6. Bruning, W.; Holtzer, A. The Effect of Urea on Hydrophobic Bonds: the Critical Micelle Concentration of n -Dodecyltrimethylammonium Bromide in Aqueous Solutions of Urea J. Am. Chem. Soc. 1961, 83, 4865-4866
7. Schick, M. J. Effect of Electrolyte and Urea on Micelle Formation J. Phys. Chem. 1964, 68, 3585-3592
8. Vanzi, F.; Madan, B.; Sharp, K. Effect of the Protein Denaturants Urea and Guanidinium on Water Structure: A Structural and Thermodynamic Study J. Am. Chem. Soc. 1998, 120, 10748-10753
9. Kallies, B. Coupling of Solvent and Solute Dynamics-Molecular Dynamics Simulations of Aqueous Urea Solutions with Different Intramolecular Potentials Phys. Chem. Chem. Phys. 2002, 4, 86-95
10. Mountain, R. D.; Thirumalai, D. Importance of Excluded Volume on the Solvation of Urea in Water J. Phys. Chem. B 2004, 108, 6826-6831
11. Felitsky, D. J.; Record, M. T. Application of the Local-Bulk Partitioning and Competitive Binding Models to Interpret Preferential Interactions of Glycine Betaine and Urea with Protein Surface Biochemistry 2004, 43, 9276-9288
12. Batchelor, J. D.; Olteanu, A.; Tripathy, A.; Pielak, G. J. Impact of Protein Denaturants and Stabilizers on Water Structure J. Am. Chem. Soc. 2004, 126, 1958-1961
13. Zou, Q.; Habermann-Rottinghaus, S. M.; Murphy, K. P. Urea Effects on Protein Stability: Hydrogen Bonding and the Hydrophobic Effect Proteins: Struct., Funct. Genet. 1998, 31, 107-115
14. Wallqvist, A.; Covell, D. G.; Thirumalai, D. Hydrophobic Interactions in Aqueous Urea Solutions with Implications for the Mechanism of Protein Denaturation J. Am. Chem. Soc. 1998, 120, 427-428
15. Felitsky, D. J.; Record, M. T. Thermal and Urea-Induced Unfolding of the Marginally Stable LAC Repressor DNA-Binding Domain: A Model System for Analysis of Solute Effects on Protein Processes Biochemistry 2003, 42, 2202-2217
16. Tobi, D.; Elber, R.; Thirumalai, D. The Dominant Interaction between Peptide and Urea Is Electrostatic in Nature: A Molecular Dynamics Study Biopolymers 2003, 68, 359-369
17. Klimov, D. K.; Straub, J. E.; Thirumalai, D. Aqueous Urea Solution Destabilizes A?16-22 Oligomers Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 14760-14765
18. OBrien, E. P.; Dima, R. I.; Brooks, B.; Thirumalai, D. Interactions between Hydrophobic and Ionic Solutes in Aqueous Guanidinium Chloride and Urea Solutions: Lessons for Protein Denaturation Mechanism J. Am. Chem. Soc. 2007, 129, 7346-7353
19. Das, A.; Mukhopadhyay, C. Atomistic Mechanism of Protein Denaturation by Urea J. Phys. Chem. B 2008, 112, 7903-7908
20. Hua, L.; Zhou, R.; Thirumalai, D.; Berne, B. J. Urea Denaturation by Stronger Dispersion Interactions with Proteins than Water Implies a 2-Stage Unfolding Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 16928-16933
21. Stumpe, M. C.; Grubmüller, H. Urea Impedes the Hydrophobic Collapse of Partially Unfolded Proteins Biophys. J. 2009, 96, 3744-3752
22. Zangi, R.; Zhou, R.; Berne, B. J. Ureas Action on Hydrophobic Interactions J. Am. Chem. Soc. 2009, 131, 1535-1541
23. Canchi, D. R.; Paschek, D.; García, A. E. Equilibrium Study of Protein Denaturation by Urea J. Am. Chem. Soc. 2010, 132, 2338-2344
24. Ma, L.; Pegram, L.; Record, M. T.; Cui, Q. Preferential Interactions between Small Solutes and the Protein Backbone: A Computational Analysis Biochemistry 2010, 49, 1954-1962
25. Berteotti, A.; Barducci, A.; Parrinello, M. Effect of Urea on the ?-Hairpin Conformational Ensemble and Protein Denaturation Mechanism J. Am. Chem. Soc. 2011, 133, 17200-17206
26. Guinn, E. J.; Pegram, L. M.; Capp, M. W.; Pollock, M. N.; Record, M. T. Quantifying Why Urea Is a Protein Denaturant, Whereas Glycine Betaine Is a Protein Stabilizer Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16932-16937
27. Zhou, R.; Li, J.; Hua, L.; Yang, Z.; Berne, B. J. Comment on Urea-Mediated Protein Denaturation: A Consensus View J. Phys. Chem. B 2011, 115, 1323-1326
28. England, J. L.; Haran, G. Role of Solvation Effects in Protein Denaturation: From Thermodynamics to Single Molecules and Back Annu. Rev. Phys. Chem. 2011, 62, 257-277
29. Schellman, J. A. Macromolecular Binding Biopolymers 1975, 14, 999-1018
30. Schellman, J. A. Selective Binding and Solvent Denaturation Biopolymers 1987, 26, 549-559
31. Muller, N. A Model for the Partial Reversal of Hydrophobic Hydration by Addition of a Urea-like Cosolvent J. Phys. Chem. 1990, 94, 3856-3859
32. Schellman, J. A. A Simple Model for Solvation in Mixed Solvents: Applications to the Stabilization and Destabilization of Macromolecular Structures Biophys. Chem. 1990, 37, 121-140
33. Graziano, G. How Does Trimethylamine N-Oxide Counteract the Denaturing Activity of Urea? Phys. Chem. Chem. Phys. 2011, 13, 17689-17695
34. Yang, Z.; Xiu, P.; Shi, B.; Hua, L.; Zhou, R. Coherent Microscopic Picture for Urea-Induced Denaturation of Proteins J. Phys. Chem. B 2012, 116, 8856-8862
35. Pazos, I. M.; Gai, F. Solutes Perspective on How Trimethylamine Oxide, Urea, and Guanidine Hydrochloride Affect Waters Hydrogen Bonding Ability J. Phys. Chem. B 2012, 116, 12473-12478
36. Canchi, D. R.; García, A. E. Backbone and Side-Chain Contributions in Protein Denaturation by Urea Biophys. J. 2011, 100, 1526-1533
37. Rezus, Y. L. A.; Bakker, H. J. Effect of Urea on the Structural Dynamics of Water Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 18417-18420
38. Frank, H. S.; Franks, F. Structural Approach to the Solvent Power of Water for Hydrocarbons; Urea as a Structure Breaker J. Chem. Phys. 1968, 48, 4746-4757
39. Wei, H.; Fan, Y.; Gao, Y. Q. Effects of Urea, Tetramethyl Urea, and Trimethylamine N -Oxide on Aqueous Solution Structure and Solvation of Protein Backbones: A Molecular Dynamics Simulation Study J. Phys. Chem. B 2010, 114, 557-568
40. Bennion, B.; Daggett, V. The Molecular Basis for the Chemical Denaturation of Proteins by Urea Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 5142-5147
41. Caballero-Herrera, A.; Nordstrand, K.; Berndt, K. D.; Nilsson, L. Effect of Urea on Peptide Conformation in Water: Molecular Dynamics and Experimental Characterization Biophys. J. 2005, 89, 842-857
42. Das, A.; Mukhopadhyay, C. Urea-Mediated Protein Denaturation: A Consensus View J. Phys. Chem. B 2009, 113, 12816-12824
43. Guo, F.; Friedman, J. M. Osmolyte-Induced Perturbations of Hydrogen Bonding between Hydration Layer Waters: Correlation with Protein Conformational Changes J. Phys. Chem. B 2009, 113, 16632-16642
44. Zhang, Y.; Cremer, P. S. Chemistry of Hofmeister Anions and Osmolytes Annu. Rev. Phys. Chem. 2010, 61, 63-83
45. Kokubo, H.; Roesgen, J.; Bolen, D. W.; Pettitt, B. M. Molecular Basis of the Apparent Near Ideality of Urea Solutions Biophys. J. 2007, 93, 3392-3407
46. Kokubo, H.; Pettitt, B. M. Preferential Solvation in Urea Solutions at Different Concentrations: Properties from Simulation Studies J. Phys. Chem. B 2007, 111, 5233-5242
47. Shimizu, A.; Fumino, K.; Yukiyasu, K.; Taniguchi, Y. NMR Studies on Dynamic Behavior of Water Molecule in Aqueous Denaturant Solutions at 25°C: Effects of Guanidine Hydrochloride, Urea and Alkylated Ureas J. Mol. Liq. 2000, 85, 269-278
48. Funkner, S.; Havenith, M.; Schwaab, G. Urea, a Structure Breaker? Answers from THz Absorption Spectroscopy J. Phys. Chem. B 2012, 116, 13374-13380
49. Sharp, K. A.; Madan, B.; Manas, E.; Vanderkooi, J. M. Water Structure Changes Induced by Hydrophobic and Polar Solutes Revealed by Simulations and Infrared Spectroscopy J. Chem. Phys. 2001, 114, 1791-1796
50. Sharp, K. A.; Vanderkooi, J. M. Water in the Half Shell: Structure of Water, Focusing on Angular Structure and Solvation Acc. Chem. Res. 2010, 43, 231-239
51. Kuffel, A.; Zielkiewicz, J. The Hydrogen Bond Network Structure within the Hydration Shell around Simple Osmolytes: Urea, Tetramethylurea, and Trimethylamine-N-oxide, Investigated Using Both a Fixed Charge and a Polarizable Water Model J. Chem. Phys. 2010, 133, 035102(1-8)
52. Soper, A. K.; Ricci, M. A. Structures of High-Density and Low-Density Water Phys. Rev. Lett. 2000, 84, 2881-2884
53. Xu, L.; Kumar, P.; Buldyrev, S. V.; Chen, S.-H.; Poole, P. H.; Sciortino, F.; Stanley, H. E. Relation between the Widom Line and the Dynamic Crossover in Systems with a Liquid-Liquid Phase Transition Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 16558-16562
54. Huang, C.; Wikfeldt, K. T.; Tokushima, T.; Nordlund, D.; Harada, Y.; Bergmann, U.; Niebuhr, M.; Weiss, T. M.; Horikawa, Y.; Leetmaa, M.; Ljungberg, M. P.; Takahasi, O.; Lenz, A.; Ojamae, L.; Lyubartsev, A. P.; Shin, S.; Pettersson, L. G. M.; Nilsson, A. The Inhomogeneous Structure of Water at Ambient Conditions Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 15214-15218
55. Clark, G. N. I.; Hura, G. L.; Teixeira, J.; Soper, A. K.; Head-Gordon, T. Small-Angle Scattering and the Structure of Ambient Liquid Water Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 14003-14007
56. Soper, A. K.; Teixeira, J.; Head-Gordon, T. Is Ambient Water Inhomogeneous on the Nanometer-Length Scale? Proc. Natl. Acad. Sci. U.S.A. 2010, 107, E44-1
57. Bandyopadhyay, D.; Mohan, S.; Ghosh, S. K.; Choudhury, N. Correlation of Structural Order, Anomalous Density, and Hydrogen Bonding Network of Liquid Water J. Phys. Chem. B 2013, 117, 8831-8843
58. Walrafen, G. E. Raman Spectral Studies of the Effects of Urea and Sucrose on Water Structure J. Chem. Phys. 1966, 44, 3726-3727
59. Sacco, A.; Holz, M. NMR Studies on Hydrophobic Interactions in Solution Part2. - Temperature and Urea Effect on the Self-Association of Ethanol in Water J. Chem. Soc., Faraday Trans. 1997, 93, 1101-1104
60. Hammes, G. G.; Schimmel, P. R. An Investigation of Water-Urea and Water-Urea-Polyethylene Glycol Interactions J. Am. Chem. Soc. 1967, 89, 442-446
61. Chen, X.; Sagle, L. B.; Cremer, P. S. Urea Orientation at Protein Surfaces J. Am. Chem. Soc. 2007, 129, 15104-15105
62. Soper, A. K.; Castner, E. W.; Luzar, A. Impact of Urea on Water Structure: A Clue to Its Properties as a Denaturant? Biophys. Chem. 2003, 105, 649-666
63. Hayashi, Y.; Katsumoto, Y.; Omori, S.; Kishii, N.; Yasuda, A. Liquid Structure of the Urea-Water System Studied by Dielectric Spectroscopy J. Phys. Chem. B 2007, 111, 1076-1080
64. Carr, J. K.; Buchanan, L. E.; Schmidt, J. R.; Zanni, M. T.; Skinner, J. L. Structure and Dynamics of Urea/Water Mixtures Investigated by Vibrational Spectroscopy and Molecular Dynamics Simulation J. Phys. Chem. B 2013, 117, 13291-13300
65. Tsai, J.; Gerstein, M.; Levitt, M. Keeping the Shape but Changing the Charges: A Simulation Study of Urea and Its Iso-steric Analogs J. Chem. Phys. 1996, 104, 9417
66. Berkowitz, M. L.; Vaisman, I. I. Local Structural Order and Molecular Associations in Water-DMSO Mixtures. Molecular Dynamics Study J. Am. Chem. Soc. 1992, 114, 7889-7896
67. Aastrand, P.-O.; Wallqvist, A.; Karlstroem, G. Molecular Dynamics Simulations of 2 m Aqueous Urea Solutions J. Phys. Chem. 1994, 98, 8224-8233
68. Weerasinghe, S.; Smith, P. E. A Kirkwood-Buff Derived Force Field for Mixtures of Urea and Water J. Phys. Chem. B 2003, 107, 3891-3898
69. aq at 25 C J. Am. Chem. Soc. 1980, 102, 4287-4294
70. Kuharski, R. A.; Rossky, P. J. Molecular Dynamics Study of Solvation in Urea-Water Solution J. Am. Chem. Soc. 1984, 106, 5786-5793
71. Almarza, J.; Rincon, L.; Bahsas, A.; Brito, F. Molecular Mechanism for the Denaturation of Proteins by Urea Biochemistry 2009, 48, 7608-7613
72. Stumpe, M. C.; Grubmuller, H. Aqueous Urea Solutions: Structure, Energetics, and Urea Aggregation J. Phys. Chem. B 2007, 111, 6220-6228
73. Chitra, R.; Smith, P. E. Molecular Association in Solution: A Kirkwood-Buff Analysis of Sodium Chloride, Ammonium Sulfate, Guanidinium Chloride, Urea, and 2,2,2-Trifluoroethanol in Water J. Phys. Chem. B 2002, 106, 1491-1500
74. Yamazaki, T.; Kovalenko, A.; Murashov, V. V.; Patey, G. N. Ion Solvation in a Water-Urea Mixture J. Phys. Chem. B 2010, 114, 613-619
75. Hansen, J.-P.; McDonald, I. Theory of Simple Liquids, 2 nd ed.; Academic Press: New York, 1986.
76. Idrissi, A.; Gerard, M.; Damay, P.; Kiselev, M.; Puhovsky, Y.; Cinar, E.; Lagant, P.; Vergoten, G. The Effect of Urea on the Structure of Water: A Molecular Dynamics Simulation J. Phys. Chem. B 2010, 114, 4731-4738
77. Abascal, J. L. F.; Vega, C. A General Purpose Model for the Condensed Phases of Water: TIP4P/2005 J. Chem. Phys. 2005, 123, 234505-1-234505-12
78. Allen, M. P.; Tildesley, D. J. Computer Simulation of Liquids; Oxford University Press: New York, 1987.
79. Parrinello, M.; Rahman, A. Polymorphic Transitions in Single Crystals: A New Molecular Dynamics Method J. Appl. Phys. 1981, 52, 7182-7190
80. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81, 3684
81. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A Linear Constraint Solver for Molecular Simulations J. Comput. Chem. 1997, 18, 1463-1472
82. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An N log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
83. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A Smooth Particle Mesh Ewald Potential J. Chem. Phys. 1995, 103, 8577-8592
84. Van Der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. C. GROMACS: Fast, Flexible, and Free J. Comput. Chem. 2005, 26, 1701-1718
85. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447
86. Errington, J. R.; Debenedetti, P. G. Relationship between Structural Order and the Anomalies of Liquid Water Nature 2001, 409, 318-321
87. Yan, Z.; Buldyrev, S. V.; Kumar, P.; Giovambattista, N.; Debenedetti, P. G.; Stanley, H. E. Structure of the First- and Second-Neighbor Shells of Simulated Water: Quantitative Relation to Translational and Orientational Order Phys. Rev. E 2007, 76, 051201
88. Pearlman, D. A.; Case, D. A.; Caldwell, J. W.; Ross, W. S.; Cheatham, T. E., III; DeBolt, Steve; Ferguson, D.; Seibel, G.; Kollman, P. AMBER, a Package of Computer Programs for Applying Molecular Mechanics, Normal Mode Analysis, Molecular Dynamics and Free Energy Calculations to Simulate the Structural and Energetic Properties of Molecules Comput. Phys. Commun. 1995, 91, 1-41
89. Sokoli, F.; Idrissi, A.; Perera, A. Concentrated Aqueous Urea Solutions: A Molecular Dynamics Study of Different Models J. Chem. Phys. 2002, 116, 1636-1646
90. Sarma, R.; Paul, S. Trimethylamine- N -oxides Effect on Polypeptide Solvation at High Pressure: A Molecular Dynamics Simulation Study J. Phys. Chem. B 2013, 117, 9056-9066
91. Horinek, D.; Netz, R. R. Can Simulations Quantitatively Predict Peptide Transfer Free Energies to Urea Solutions? Thermodynamic Concepts and Forcefield Limitations J. Phys. Chem. A 2011, 115, 6125-6136
92. Booth, J.; Abbott, S.; Shimizu, S. Mechanism of Hydrophobic Drug Solubilization by Small Molecule Hydrotropes J. Phys. Chem. B 2012, 116, 14915-14921
93. Choudhury, N. On the Manifestation of Hydrophobicity at the Nanoscale J. Phys. Chem. B 2008, 112, 6296-6300
94. Choudhury, N. Dynamics of Water at the Nanoscale Hydrophobic Confinement J. Chem. Phys. 2010, 132, 064505
95. Guinn, E. J.; Schwinefus, J. J.; Cha, H. K.; McDevitt, J. L.; Merker, W. E.; Ritzer, R.; Muth, G. W.; Engelsgjerd, S. W.; Mangold, K. E.; Thompson, P. J.; Kerins, M. J.; Record, M. T., Jr. Quantifying Functional Group Interactions That Determine Urea Effects on Nucleic Acid Helix Formation J. Am. Chem. Soc. 2013, 135, 5828-5838
96. Priyakumar, U. D.; Hyeon, C.; Thirumalai, D.; MacKerell, A. D., Jr. Urea Destabilizes RNA by Forming Stacking Interactions and Multiple Hydrogen Bonds with Nucleic Acid Bases J. Am. Chem. Soc. 2009, 131, 17759-17761