Insight into the molecular mechanisms of protein stabilizing osmolytes from global force-field variations

Journal of Physical Chemistry B

Volumn 117, Issue 28, 2013, Pages 8310-8321

  Schneck, Emanuel ^a,b,d   Horinek, Dominik ^b,c   Netz, Roland R ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF REGENSBURG   (Germany)

^d INSTITUT LAUE LANGEVIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; FREE ENERGY; HYDROPHOBICITY; OPTIMIZATION;

EXPERIMENTAL VALUES; HYDROPHOBIC GROUPS; HYDROPHOBIC INTERACTIONS; MOLECULAR MECHANISM; POLYGLYCINE CHAINS; THERMODYNAMIC AND STRUCTURAL PROPERTIES; WATER-SOLUBLE MOLECULE; WORKING MECHANISMS;

PROTEINS;

EID: 84880518790     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp400790f     Document Type: Article

References (58)

1. Arakawa, T.; Timasheff, S. N. The Stabilization of Proteins by Osmolytes Biophys. J. 1985, 47, 411-414
2. Brown, A. D.; Simpson, J. R. Water Relations of Sugar-Tolerant Yeasts: The Role of Intracellular Polyols J. Gen. Microbiol. 1972, 72, 589-591
3. Somero, G. N. From Dogfish to Dogs: Trimethylamines Protect Proteins from Urea Physiology 1986, 1, 9-12
4. 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
5. Lippert, K.; Galinski, E. A. Enzyme Stabilization by Ectoine-Type Compatible Solutes: Protection against Heating, Freezing, and Drying Appl. Microbiol. Biotechnol. 1992, 37, 61-65
6. Santoro, M. M.; Liu, Y.; Khan, S. M. A.; Hou, L.-X.; Bolen, D. W. Increased Thermal Stability of Proteins in the Presence of Naturally Occurring Osmolytes Biochemistry 1992, 31, 5278-5283
7. Lee, J. C.; Timasheff, S. N. The Stabilization of Proteins by Sucrose J. Biol. Chem. 1981, 256, 7193-7201
8. Tanford, C. Isothermal Unfolding of Globular Proteins in Aqueous Urea Solutions J. Am. Chem. Soc. 1964, 86, 2050-2059
9. O'Brien, E. P.; Ziv, G.; Haran, G.; Brooks, B. R.; Thirumalai, D. Effects of Denaturants and Osmolytes on Proteins Are Accurately Predicted by the Molecular Transfer Model Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 13403-13408
10. Lin, T.-Y.; Timasheff, S. N. Why Do Some Organisms Use a Urea-Methylamine Mixture as Osmolyte? Thermodynamic Compensation of Urea and Trimethylamine N-Oxide Interactions with Protein Biochemistry 1994, 33, 12695-12701
11. Auton, M.; Bolen, D. W. Additive Transfer Free Energies of the Peptide Backbone Unit That Are Independent of the Model Compound and the Choice of Concentration Scale Biochemistry 2004, 43, 1329-1342
12. Hu, C. Y.; Kokubo, H.; Lynch, G. C.; Bolen, D. W.; Pettitt, B. M. Backbone Additivity in the Transfer Model of Protein Solvation Protein Sci. 2010, 19, 1011-1022
13. Greene, R. F., Jr.; Pace, C. N. Urea and Guanidine Hydrochloride Denaturation of Ribonuclease, Lysozyme, Alpha-Chymotrypsin, and Beta-Lactoglobulin J. Biol. Chem. 1974, 249, 5388-5393
14. Parsegian, V. A.; Rand, R. P.; Rau, D. C. Osmotic Stress, Crowding, Preferential Hydration, and Binding: A Comparison of Perspectives Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 3987-3992
15. Athawale, M. V.; Dordick, J. S.; Garde, S. Osmolyte Trimethylamine-N- Oxide Does Not Affect the Strength of Hydrophobic Interactions: Origin of Osmolyte Compatibility Biophys. J. 2004, 89, 858-866
16. Bennion, B. J.; Daggett, V. Counteraction of Urea-Induced Protein Denaturation by Trimethylamine N-Oxide: A Chemical Chaperone at Atomic Resolution Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 6433-6438
17. Cho, S. S.; Reddy, G.; Straub, J. E.; Thirumalai, D. Entropic Stabilization of Proteins by Tmao J. Phys. Chem. B 2011, 115, 13401-13407
18. Gilman-Politi, R.; Harries, D. Unraveling the Molecular Mechanism of Enthalpy Driven Peptide Folding by Polyol Osmolytes J. Chem. Theory Comput. 2011, 7, 3816-3828
19. 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
20. Zou, Q.; Bennion, B. J.; Daggett, V.; Murphy, K. P. The Molecular Mechanism of Stabilization of Proteins by Tmao and Its Ability to Counteract the Effects of Urea J. Am. Chem. Soc. 2002, 124, 1192-1202
21. Stumpe, M. C.; Grubmüller, H. Urea Impedes the Hydrophobic Collapse of Partially Unfolded Proteins Biophys. J. 2009, 96, 3744-3752
22. Xie, G.; Timasheff, S. N. The Thermodynamic Mechanism of Protein Stabilization by Trehalose Biophys. Chem. 1997, 64, 25-43
23. O'Connor, T. F.; Debenedetti, P. G.; Carbeck, J. D. Simultaneous Determination of Structural and Thermodynamic Effects of Carbohydrate Solutes on the Thermal Stability of Ribonuclease A J. Am. Chem. Soc. 2004, 126, 11794-11795
24. Politi, R.; Harries, D. Enthalpically Driven Peptide Stabilization by Protective Osmolytes Chem. Commun. 2010, 46, 6449-6451
25. Canchi, D. R.; Jayasimha, P.; Rau, D. C.; Makhatadze, G. I.; Garcia, A. E. Molecular Mechanism for the Preferential Exclusion of Tmao from Protein Surfaces J. Phys. Chem. B 2012, 116, 12095-12104
26. Street, T. O.; Bolen, D. W.; Rose, G. D. A Molecular Mechanism for Osmolyte-Induced Protein Stability Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 13997-14002
27. Horinek, D.; Netz, R. R. Can Simulations Quantitatively Predict Peptide Transfer Free Energies to Urea Solutions? Thermodynamic Concepts and Force Field Limitations J. Phys. Chem. A 2011, 115, 6125-6136
28. Rösgen, J.; Pettitt, B. M.; Bolen, D. W. Uncovering the Basis for Nonideal Behavior of Biological Molecules Biochemistry 2004, 43, 14472-14484
29. 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
30. Berendsen, H. J. C.; Grigera, J. R.; Straatsma, T. P. The Missing Term in Effective Pair Potentials J. Phys. Chem. 1987, 91, 6269-6271
31. Miyamoto, S.; Kollman, P. A. Settle: An Analytical Version of the Shake and Rattle Algorithms for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
32. 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
33. Hoover, W. G. Canonical Dynamics: Equilibrium Phase-Space Distributions Phys. Rev. A 1985, 31, 1695-1697
34. Parrinello, M.; Rahman, A. Polymorphic Transitions in Single Crystals: A New Molecular Dynamics Method J. Appl. Phys. 1981, 52, 7182
35. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An Nlog(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089
36. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G.; Smooth, A. Particle Mesh Ewald Method J. Chem. Phys. 1995, 103, 8577
37. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M., Jr.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules J. Am. Chem. Soc. 1995, 117, 5179-5197
38. 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
39. Besler, B. H.; Merz, K. M., Jr.; Kollman, P. A. Atomic Charges Derived from Semiempirical Methods J. Comput. Chem. 1990, 11, 431-439
40. Singh, U. C.; Kollman, P. A. An Approach to Computing Electrostatic Charges for Molecules J. Comput. Chem. 1984, 5, 129-145
41. Kast, K. M.; Brickmann, J.; Kast, S. M.; Berry, R. S. Binary Phases of Aliphatic N-Oxides and Water: Force Field Development and Molecular Dynamics Simulation J. Phys. Chem. A 2003, 107, 5342-5351
42. Hub, J. S.; de Groot, B. L.; van der Spoel, D. G-Wham-a Free Weighted Histogram Analysis Implementation Including Robust Error and Autocorrelation Estimates J. Chem. Theory Comput. 2010, 6, 3713-3720
43. Kirkwood, J. G.; Buff, F. P. The Statistical Mechanical Theory of Solutions. I J. Chem. Phys. 1951, 19, 774-777
44. Courtenay, E. S.; Capp, M. W.; Anderson, C. F.; Record, M. T., Jr. Vapor Pressure Osmometry Studies of Osmolyte-Protein Interactions: Implications for the Action of Osmoprotectants in Vivo and for the Interpretation of "Osmotic Stress" Experiments in Vitro Biochemistry 2000, 39, 4455-4471
45. Wang, A.; Bolen, D. W. A Naturally Occurring Protective System in Urea-Rich Cells: Mechanism of Osmolyte Protection of Proteins against Urea Denaturation Biochemistry 1997, 36, 9101-9108
46. Handbook of Chemistry and Physics; CRC: Boca Raton, FL, 1986.
47. Kozak, J. J.; Knight, W. S.; Kauzmann, W. Solute-Solute Interactions in Aqueous Solutions J. Chem. Phys. 1968, 48, 675-686
48. Macaskill, J. B.; Robinson, R. A.; Bates, R. G. Osmotic Coefficients and Activity Coefficients of Guanidinium Chloride in Concentrated Aqueous Solutions at 25 C J. Chem. Eng. Data 1977, 22, 411-412
49. Rösgen, J.; Pettitt, B. M.; Bolen, D. W. Protein Folding, Stability, and Solvation Structure in Osmolyte Solutions Biophys. J. 2005, 89, 2988-2997
50. Di Michele, A.; Freda, M.; Onori, G.; Paolantoni, M.; Santucci, A.; Sassi, P. Modulation of Hydrophobic Effect by Cosolutes J. Phys. Chem. B 2006, 110, 21077-21085
51. Garrod, J. E.; Herrington, T. M. Apparent Molar Volumes and Temperatures of Maximum Density of Dilute Aqueous Sucrose Solutions J. Phys. Chem. 1970, 74, 363-370
52. Tyrrell, W. J. V.; Kennerley, M. Viscosity B-Coefficients between 5 and 20 for Glycolamide, Glycine, and N-Methylated Glycines in Aqueous Sotution J. Chem. Soc. A 1968, 2724-2728
53. Tanford, C. The Hydrophobic Effect: Formation of Micelles and Biological Membranes; John Wiley: New York, 1973.
54. Pettitt, B. M.; Rossky, P. J. Alkali Halides in Water: Ion-Solvent Correlations and Ion-Ion Potentials of Mean Force at Infinite Dilution J. Chem. Phys. 1986, 84, 5836-5844
55. Sukenik, S.; Sapir, L.; Gilman-Politi, R.; Harries, D. Diversity in the Mechanisms of Cosolute Action on Biomolecular Processes Faraday Discuss. 2013, 160, 225-237
56. Tanford, C. Contribution of Hydrophobic Interactions to the Stability of the Globular Conformation of Proteins J. Am. Chem. Soc. 1962, 84, 4240-4247
57. Hu, C. Y.; Lynch, G. C.; Kokubo, H.; Pettitt, B. M. Trimethylamine N-Oxide Influence on the Backbone of Proteins: An Oligoglycine Model Proteins 2009, 78, 695-704
58. Pace, C. N.; Marshall, H. F., Jr. A Comparison of the Effectiveness of Protein Denaturants for B-Lactoglobulin and Ribonuclease Arch. Biochem. Biophys. 1980, 199, 270-276