Comparative study of protein unfolding in aqueous urea and dimethyl sulfoxide solutions: Surface polarity, solvent specificity, and sequence of secondary structure melting

Journal of Physical Chemistry B

Volumn 118, Issue 21, 2014, Pages 5691-5697

  Roy, Susmita ^a   Bagchi, Biman ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTER SIMULATION; DIMETHYL SULFOXIDE; MELTING; METABOLISM; ORGANIC SOLVENTS; SOLVENTS; UREA;

COMPARATIVE STUDIES; COSOLVENTS; DIMETHYL SULFOXIDE (DMSO); PROTEIN UNFOLDING; SECONDARY STRUCTURES; SOLVENT ENVIRONMENTS; SURFACE POLARITIES; UREA SOLUTIONS;

PROTEINS;

BACTERIAL PROTEIN; CHYMOTRYPSIN INHIBITOR 2; DIMETHYL SULFOXIDE; IGG FC-BINDING PROTEIN, STREPTOCOCCUS; NEUROFILAMENT PROTEIN; PEPTIDE; PEPTIDE FRAGMENT; PROTEIN; UBIQUITIN; UREA; VEGETABLE PROTEIN; VILLIN HEADPIECE SUBDOMAIN PEPTIDE;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; COMPARATIVE STUDY; COMPUTER SIMULATION; HORDEUM; HUMAN; PROTEIN SECONDARY STRUCTURE; PROTEIN UNFOLDING;

ANIMALS; BACTERIAL PROTEINS; CHICKENS; COMPUTER SIMULATION; DIMETHYL SULFOXIDE; HORDEUM; HUMANS; MODELS, MOLECULAR; NEUROFILAMENT PROTEINS; PEPTIDE FRAGMENTS; PEPTIDES; PLANT PROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; PROTEINS; UBIQUITIN; UREA;

EID: 84901654339     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp5037348     Document Type: Article

References (66)

1. Bagchi, B. Water in Biological and Chemical Processes: From Structure and Dynamics to Function; Cambridge University Press, London, U.K., 2013.
2. Levinthal, C. Are There Pathways for Protein Folding? J. Chim. Phys. 1968, 65, 44-45
3. Levinthal, C. How to Fold Graciously. In Mossbauer Spectroscopy in Biological System, Proceedings of a Meeting Held at Allerton House, Monticello, IL, March 17 and 18, 1969; De-Brunner, P.; Tsibris, J.; Munck, E., Eds.; University of Illinois Press: Urbana, IL, 1969; pp 22-24.
4. Zwanzig, R.; Szabo, A.; Bagchi, B. Levinthal's Paradox Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 20-22
5. Bryngelson, J. D.; Wolynes, P. G. Intermediates and Barrier Crossing in a Random Energy Model (with Applications to Protein Folding) J. Phys. Chem. 1989, 93, 6902-6915
6. Leopold, P. E.; Montal, M.; Onuchic, J. N. Protein Folding Funnels: A Kinetic Approach to the Sequence-Structure Relationship Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 8721-8725
7. Bryngelson, J. D.; Onuchic, J. N.; Socci, N. D.; Wolynes, P. G. Funnels, Pathways, and the Energy Landscape of Protein Folding: A Synthesis Proteins: Struct., Funct., Genet. 1995, 21, 167-195
8. Onuchic, J. N.; Wolynes, P. G. Theory of Protein Folding Curr. Opin. Struct. Biol. 2004, 14, 70-75 (Pubitemid 38249595)
9. Chan, H. S.; Dill, K. A. Polymer Principles in Protein Structure and Stability Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 447-490
10. Dill, K.; Chan, H. S. From Levinthal to Pathways to Funnels Nat. Struct. Biol. 1997, 4, 10-19 (Pubitemid 27020916)
11. Chan, H. S.; Dill, K. A. Protein Folding in the Landscape Perspective: Chevron Plots and Non-Arrhenius Kinetics Proteins 1998, 30, 2-33 (Pubitemid 28036107)
12. Karplus, M. The Levinthal Paradox: Yesterday and Today Folding Des. 1997, 2, S69-S75
13. Sali, A.; Shakhnovich, E.; Karplus, M. How Does a Protein Fold? Nature 1994, 369, 248-251 (Pubitemid 24154805)
14. Karplus, M.; Weaver, D. L. Protein-Folding Dynamics Nature 1976, 260, 404-406
15. Honeycutt, J. D.; Thirumalai, D. Metastability of the Folded States of Globular Proteins Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 3526-3529
16. Wolynes, P. G.; Onuchic, J. N.; Thirumalai, D. Navigating the Folding Routes Science 1995, 267, 1619-1620
17. Wales, D. J. The Energy Landscape as a Unifying Theme in Molecular Science Philos. Trans. R. Soc., A 2005, 363, 357-377 (Pubitemid 40180202)
18. Wales, D. J.; Bogdan, T. V. Potential Energy and Free Energy Landscapes J. Phys. Chem. B 2006, 110, 20765-20776 (Pubitemid 44797331)
19. Carr, J. M.; Wales, D. J. Global Optimization and Folding Pathways of Selected α-Helical Proteins J. Chem. Phys. 2005, 123, 23490
20. Baldwin, R. L. The Nature of Protein Folding Pathways: The Classical versus the New View J. Biomol. NMR 1995, 5, 103-109
21. Baldwin, R. L. Competing Unfolding Pathways Nat. Struct. Biol. 1997, 4, 965-966 (Pubitemid 27525800)
22. Fersht, A. R.; Itzhaki, L. S.; elMasry, N. F.; Matthews, J. M.; Otzen, D. E. Single versus Parallel Pathways of Protein Folding and Fractional Formation of Structure in the Transition State Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 10426-10429 (Pubitemid 24329010)
23. Fersht, A. R. Optimization of Rates of Protein Folding: The Nucleation-Condensation Mechanism and Its Implications Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 10869-10873
24. Oliveberg, M.; Tan, Y. J.; Fersht, A. R. Negative Activation Enthalpies in the Kinetics of Protein Folding Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 8926-8929
25. Pande, V. S.; Grosberg, A. Yu.; Tanaka, T.; Rokhsar, D. S. Pathways for Protein Folding: Is a New View Needed? Curr. Opin. Struct. Biol. 1998, 8, 68-79 (Pubitemid 28107917)
26. Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Shaw, D. E. How Fast-Folding Proteins Fold Science 2011, 334, 517-520
27. 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. 2003, 100, 5142-5147
28. Camilloni, C.; Rocco, A. G.; Eberini, I.; Gianazza, E.; Broglia, R. A.; Tiana, G. Urea and Guanidinium Chloride Denature Protein L in Different Ways in Molecular Dynamics Simulations Biophys. J. 2008, 94, 4654-61
29. Rocco, A. G.; Mollica, L.; Ricchiuto, P.; Baptista, A. M.; Gianazza, E.; Eberini, I. Characterization of the Protein Unfolding Processes Induced by Urea and Temperature Biophys. J. 2008, 94, 2241-51
30. Maity, H.; Maity, M.; Englander, S. W. How Cytochrome C Folds, and Why: Submolecular Foldon Units and Their Stepwise Sequential Stabilization J. Mol. Biol. 2004, 343, 223-233 (Pubitemid 39277460)
31. Krishna, M. M. G.; Maity, H.; Rumbley, J. N.; Lin, Y.; Englander, S. W. Order Steps in the Cytochrome C Folding Pathway: Evidence for a Sequential Stabilization Mechanism J. Mol. Biol. 2006, 359, 1410-1419 (Pubitemid 43903495)
32. Krishna, M. M. G.; Englander, S. W. A Unified Mechanism for Protein Folding: Predetermined Pathways with Optional Errors Protein Sci. 2007, 16, 449-464 (Pubitemid 46327556)
33. Kim, S.; Chung, J. K.; Kwak, K.; Bren, K. L.; Bagchi, B.; Fayer, M. D. Native and Unfolded Cytochrome c-Comparison of Dynamics Using 2D-IR Vibrational Echo Spectroscopy J. Phys. Chem. B 2008, 112, 10054-10063
34. 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
35. Tobi, D.; Elber, R.; Thirumalai, D. The Dominant Interaction between Peptide and Urea Is Electrostatic in Nature: A Molecular Dynamics Simulation Study Biopolymers 2003, 68, 359-369 (Pubitemid 36342872)
36. O'Brien, 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 (Pubitemid 46980813)
37. Das, A.; Mukhopadhyay, C. Urea-Mediated Protein Denaturation: A Consensus View J. Phys. Chem. B 2009, 113, 12816-12824
38. 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, 1323-1328
39. 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
40. Caflisch, A.; Karplus, M. Structural Details of Urea Binding to Barnase: A Molecular Dynamics Analysis Structure 1999, 7, 477-488 (Pubitemid 29230482)
41. Roy, S.; Jana, B.; Bagchi, B. Dimethyl Sulfoxide Induced Structural Transformations and Non-Monotonic Concentration Dependence of Conformational Fluctuation around Active Site of Lysozyme J. Chem. Phys. 2012, 136, 115103/1-10
42. Jackson, M.; Mantsch, H. H. Beware of Proteins in DMSO Biochim. Biophys. Acta 1991, 1078, 231-5
43. Huang, P.; Dong, A.; Caughey, W. S. Effects of Dimethyl Sulfoxide, Glycerol, and Ethylene Glycol on Secondary Structures of Cytochrome c and Lysozyme as Observed by Infrared Spectroscopy J. Pharm. Sci. 1995, 84, 387-392
44. Roy, S.; Bagchi, B. Chemical Unfolding of Chicken Villin Headpiece in Aqueous Dimethyl Sulfoxide Solution: Cosolvent Concentration Dependence, Pathway, and Microscopic Mechanism J. Phys. Chem. B 2013, 117, 4488-4502
45. Tretyakova, T.; Shushanyan, M.; Partskhaladze, T.; Makharadze, M.; van Eldik, R.; Khoshtariya, D. E. Simplicity within the Complexity: Bilateral Impact of DMSO on the Functional and Unfolding Patterns of α-Chymotrypsin Biophys. Chem. 2013, 175-176, 17-27
46. Batista, A. N.; Batista, J. M., Jr.; Bolzani, V. S.; Furlan, M.; Blanch, E. W. Selective DMSO-Induced Conformational Changes in Proteins from Raman Optical Activity Phys. Chem. Chem. Phys. 2013, 15, 20147-20152
47. Piana, S.; Lindorff-Larsen, K.; Shaw, D. E. Atomic-Level Description of Ubiquitin Folding Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 5915-5920
48. Larios, E.; Yang, W. Y.; Schulten, K.; Gruebele, M. A Similarity Measure for Partially Folded Proteins: Application to Unfolded and Native-like Conformation Fluctuations Chem. Phys. 2004, 307, 217-225
49. Yang, W. Y.; Pitera, J. W.; Swope, W. C.; Gruebele, M. Heterogeneous Folding of the Trpzip Hairpin: Full Atom Simulation and Experiment J. Mol. Biol. 2004, 336, 241-251 (Pubitemid 38102345)
50. Larios, E.; Li, J. S.; Schulten, K.; Kihara, H.; Gruebele, M. Multiple Probes Reveal a Native-like Intermediate during Low-Temperature Refolding of Ubiquitin J. Mol. Biol. 2004, 340, 115-125 (Pubitemid 38739441)
51. Gronenborn, A. M.; Filpula, D. R.; Essig, N. Z.; Achari, A.; Whitlow, M.; Wingfield, P. T.; Clore, G. M. A Novel, Highly Stable Fold of the Immunoglobulin Binding Domain of Streptococcal Protein G Science 1991, 253, 657-661 (Pubitemid 21917198)
52. McPhalen, C. A.; James, M. N. Crystal and Molecular Structure of the Serine Proteinase Inhibitor CI-2 from Barley Seeds Biochemistry 1987, 26, 261-269
53. Wikstrom, M.; Drakenberg, T.; Forsen, S.; Sjobring, U.; Bjorck, L. Three-Dimensional Solution Structure of an Immunoglobulin Light Chain-Binding Domain of Protein L. Comparison with the IgG-Binding Domains of Protein G Biochemistry 1994, 33, 14011-14017 (Pubitemid 24382342)
54. Vijay-Kumar, S.; Bugg, C. E.; Cook, W. J. Structure of Ubiquitin Refined at 1.8 Å Resolution J. Mol. Biol. 1987, 194, 531-544
55. Oostenbrink, C.; Villa, A.; Mark, A. E.; van Gunsteren, W. F. A Biomolecular Force Field Based on the Free Enthalpy of Hydration and Solvation: The GROMOS Force-Field Parameter Sets 53A5 and 53A6 Comput. Chem. 2004, 25, 1656-1676
56. Liu, H. Y.; Müller-Plathe, F.; van Gunsteren, W. F. A Force Field for Liquid Dimethyl Sulfoxide and Physical Properties of Liquid Dimethyl Sulfoxide Calculated Using Molecular Dynamics Simulation J. Am. Chem. Soc. 1995, 117, 4363-4366
57. Geerke, D. P.; Oostenbrink, C.; van der Vegt, N. F. A.; van Gunsteren, W. F. An Effective Force Field for Molecular Dynamics Simulations of Dimethyl Sulfoxide and Dimethyl Sulfoxide-Water Mixtures J. Phys. Chem. B 2004, 108, 1436-1445
58. Smith, L. J.; Berendsen, H. J. C.; van Gunsteren, W. F. Computer Simulation of Urea-Water Mixtures: A Test of Force Field Parameters for Use in Biomolecular Simulation J. Phys. Chem. B 2004, 108, 1065-1071
59. Berendsen, H. J. C.; Grigera, J. R.; Straatsma, T. P. The Missing Term in Effective Pair Potentials J. Phys. Chem. 1987, 89, 6269-6271
60. Hoover, W. G. Canonical Dynamics: Equilibrium Phase-Space Distributions Phys. Rev. A 1985, 31, 1695-1697
61. Nose, S. A Unified Formulation of the Constant Temperature Molecular Dynamics Methods J. Chem. Phys. 1984, 81, 511-519
62. Parinello, M.; Rahman, A. Polymorphic Transitions in Single Crystals: A New Molecular Dynamics Method J. Appl. Phys. 1981, 52, 7182-7190 (Pubitemid 12456820)
63. Frenkel, D.; Smit, B. Understanding Molecular Simulation: From Algorithms to Applications, 2 nd ed.; Academic Press: San Diego, CA, 2002.
64. Roy, S.; Banerjee, S.; Biyani, N.; Jana, B.; Bagchi, B. Theoretical and Computational Analysis of Static and Dynamic Anomalies in Water-DMSO Binary Mixture at Low DMSO Concentrations J. Phys. Chem. B 2010, 115, 685-692
65. Banerjee, S.; Roy, S.; Bagchi, B. Enhanced Pair Hydrophobicity in Water-DMSO Binary Mixture at Low DMSO Concentration J. Phys. Chem. B 2010, 114, 12875-12882
66. Roy, S.; Bagchi, B. Solvation Dynamics of Tryptophan in Water-Dimethyl Sulfoxide Binary Mixture: In Search of Molecular Origin of Composition Dependent Multiple Anomalies J. Chem. Phys. 2013, 139, 034308/1-10