Observing the osmophobic effect in action at the single molecule level

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 7, 2011, Pages 2214-2223

  Aioanei, Daniel ^a   Tessari, Isabella ^b   Bubacco, Luigi ^b   Samorì, Bruno ^a,c   Brucale, Marco ^a,c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c CNR   (Italy)

Author keywords

Force spectroscopy; Osmolytes; Protein folding; Single molecule; Unfolding transition state

Indexed keywords

GLOBULAR PROTEIN; GLYCEROL;

ARTICLE; ENERGY TRANSFER; MOLECULE; OSMOPHOBIC EFFECT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; THERMODYNAMICS;

GLYCEROL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; OSMOLAR CONCENTRATION; PROTECTIVE AGENTS; PROTEIN FOLDING; PROTEIN UNFOLDING; PROTEINS; THERMODYNAMICS;

EID: 79958767217     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23045     Document Type: Article

References (77)

1. Peter W. Hochachka GNS. Biochemical adaptation: mechanism and process in physiological evolution. USA: Oxford University Press; 2002.
2. Rose GD, Fleming PJ, Banavar JR, Maritan A. A backbone-based theory of protein folding. Proc Natl Acad Sci USA 2006; 103: 16623-16633.
3. Bolen DW. Protein Stabilization by naturally occurring osmolytes. In: Murphy KP, editor. Protein structure, stability, and folding. Volume 168, Methods in Molecular Biology: Humana Press, Totowa, New Jersey, 2001. p 17-36.
4. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN. Living with water stress: evolution of osmolyte systems. Science 1982; 217: 1214-1222.
5. Bolen DW, Baskakov IV. The osmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol 2001; 310: 955-963.
6. Kumar R. Role of naturally occurring osmolytes in protein folding and stability. Arch Biochem Biophys 2009; 491: 1-6.
7. Holthauzen LM, Bolen DW. Mixed osmolytes: the degree to which one osmolyte affects the protein stabilizing ability of another. Protein Sci 2007; 16: 293-298.
8. Banavar JR, Maritan A. Physics of proteins. Annu Rev Biophys Biomol Struct 2007; 36: 261-280.
9. Bolen DW, Rose GD. Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu Rev Biochem 2008; 77: 339-362.
10. Wu P, Bolen DW. Osmolyte-induced protein folding free energy changes. Proteins 2006; 63: 290-296.
11. Auton M, Bolen DW. Application of the transfer model to understand how naturally occurring osmolytes affect protein stability. Methods Enzymol 2007; 428: 397-418.
12. Auton M, Bolen DW. Predicting the energetics of osmolyte-induced protein folding/unfolding. Proc Natl Acad Sci USA 2005; 102: 15065-15068.
13. Baskakov I, Bolen DW. Forcing thermodynamically unfolded proteins to fold. J Biol Chem 1998; 273: 4831-4834.
14. Street TO, Bolen DW, Rose GD. A molecular mechanism for osmolyte-induced protein stability. Proc Natl Acad Sci USA 2006; 103: 13997-14002.
15. Yiu CP, Mateu MG, Fersht AR. Protein folding transition states: elicitation of Hammond effects by 2, 2, 2-trifluoroethanol. Chembiochem 2000; 1: 49-55.
16. Garcia-Manyes S, Dougan L, Fernandez JM. Osmolyte-induced separation of the mechanical folding phases of ubiquitin. Proc Natl Acad Sci USA 2009; 106: 10540-10545.
17. Dougan L, Feng G, Lu H, Fernandez JM. Solvent molecules bridge the mechanical unfolding transition state of a protein. Proc Natl Acad Sci USA 2008; 105: 3185-3190.
18. Pradeep L, Udgaonkar JB. Osmolytes induce structure in an early intermediate on the folding pathway of barstar. J Biol Chem 2004; 279: 40303-40313.
19. Silow M, Oliveberg M. High concentrations of viscogens decrease the protein folding rate constant by prematurely collapsing the coil. J Mol Biol 2003; 326: 263-271.
20. Lin SL, Zarrine-Afsar A, Davidson AR. The osmolyte trimethylamine-N-oxide stabilizes the Fyn SH3 domain without altering the structure of its folding transition state. Protein Sci 2009; 18: 526-536.
21. Mukaiyama A, Koga Y, Takano K, Kanaya S. Osmolyte effect on the stability and folding of a hyperthermophilic protein. Proteins 2008; 71: 110-118.
22. Russo AT, Rosgen J, Bolen DW. Osmolyte effects on kinetics of FKBP12 C22A folding coupled with prolyl isomerization. J Mol Biol 2003; 330: 851-866.
23. Cao Y, Li H. Polyprotein of GB1 is an ideal artificial elastomeric protein. Nat Mater 2007; 6: 109-114.
24. Sandal M, Benedetti F, Brucale M, Gomez-Casado A, Samori B. Hooke: an open software platform for force spectroscopy. Bioinformatics 2009; 25: 1428-1430.
25. Walcott S. The load dependence of rate constants. J Chem Phys 2008; 128: 215101.
26. Hänggi P, Talkner P, Borkovec M. Reaction-rate theory: fifty years after Kramers. Rev Modern Phys 1990; 62: 251.
27. Aioanei D, Samori B, Brucale M. Maximum likelihood estimation of protein kinetic parameters under weak assumptions from unfolding force spectroscopy experiments. Phys Rev E Stat Nonlin Soft Matter Phys 2009; 80(6 Pt 1): 061916.
28. Dougan L, Koti AS, Genchev G, Lu H, Fernandez JM. A single-molecule perspective on the role of solvent hydrogen bonds in protein folding and chemical reactions. Chemphyschem 2008; 9: 2836-2847.
29. Cao Y, Lam C, Wang M, Li H. Nonmechanical protein can have significant mechanical stability. Angew Chem Int Ed Engl 2006; 45: 642-645.
30. Cheng N-S. Formula for the Viscosity of a Glycerol-Water Mixture. Ind Eng Chem Res 2008; 47: 3285-3288.
31. Pirzer T, Hugel T. Atomic force microscopy spring constant determination in viscous liquids. Rev Sci Instrum 2009; 80: 035110.
32. Sader J. Frequency response of cantilever beams immersed in viscous fluids with applications to the atomic force microscope. J Appl Phys 1998; 84: 64-76.
33. Nicu CBaL. Viscosity measurements based on experimental investigations of composite cantilever beam eigenfrequencies in viscous media. Rev Sci Instrum 2000; 71: 5.
34. Christopher T. Gibson DJJ, Anderson C, Abell C, Rayment T. Method to determine the spring constant of atomic force microscope cantilevers. Rev Sci Instrum 2004; 75: 3.
35. Liu R, Roman M, Yang G. Correction of the viscous drag induced errors in macromolecular manipulation experiments using atomic force microscope. Rev Sci Instrum 2010; 81: 063703.
36. Vinogradova OI, Butt HJ, Yakubov GE, Feuillebois Fc. Dynamic effects on force measurements. I. Viscous drag on the atomic force microscope cantilever. Rev Sci Instrum 2001; 72: 2330-2339.
37. Janovjak H, Struckmeier J, Muller DJ. Hydrodynamic effects in fast AFM single-molecule force measurements. Eur Biophys J 2005; 34: 91-96.
38. Glasstone S. The theory of rate processes: the kinetics of chemical reactions, viscosity, diffusion and electrochemical phenomena. New York: McGraw-Hill Book Company, Inc; 1941. 611p.
39. Wako H, Saitô N. Statistical mechanical theory of the protein conformation. I. General considerations and the application to homopolymers. J Phys Soc Jpn 1978; 44: 1931.
40. Wako H, Saitô Nobuhiko. Statistical mechanical theory of the protein conformation. II. Folding pathway for protein. J Phys Soc Jpn 1978; 44: 1939.
41. Munoz V, Thompson PA, Hofrichter J, Eaton WA. Folding dynamics and mechanism of beta-hairpin formation. Nature 1997; 390: 196-199.
42. Munoz V, Eaton WA. A simple model for calculating the kinetics of protein folding from three-dimensional structures. Proc Natl Acad Sci USA 1999; 96: 11311-11316.
43. Imparato A, Pelizzola A, Zamparo M. Ising-like model for protein mechanical unfolding. Phys Rev Lett 2007; 98: 148102.
44. Imparato A, Pelizzola A, Zamparo M. Protein mechanical unfolding: a model with binary variables. J Chem Phys 2007; 127: 145105.
45. Bruscolini P, Pelizzola A. Exact solution of the Munoz-Eaton model for protein folding. Phys Rev Lett 2002; 88(25 Pt 1): 258101.
46. Bruscolini P, Pelizzola A, Zamparo M. Downhill versus two-state protein folding in a statistical mechanical model. J Chem Phys 2007; 126: 215103.
47. Imparato A, Pelizzola A. Mechanical unfolding and refolding pathways of ubiquitin. Phys Rev Lett 2008; 100: 158104.
48. Caraglio M, Imparato A, Pelizzola A. Pathways of mechanical unfolding of FnIII(10): low force intermediates. J Chem Phys 2010; 133: 065101.
49. Wang A, Bolen DW. A naturally occurring protective system in urea-rich cells: mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry 1997; 36: 9101-9108.
50. Qu Y, Bolen CL, Bolen DW. Osmolyte-driven contraction of a random coil protein. Proc Natl Acad Sci USA 1998; 95: 9268-9273.
51. Bernado P, Blackledge M, Sancho J. Sequence-specific solvent accessibilities of protein residues in unfolded protein ensembles. Biophys J 2006; 91: 4536-4543.
52. Estrada J, Bernado P, Blackledge M, Sancho J. ProtSA: a web application for calculating sequence specific protein solvent accessibilities in the unfolded ensemble. BMC Bioinform 2009; 10: 104.
53. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000; 28: 235-242.
54. Gallagher T, Alexander P, Bryan P, Gilliland GL. Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR. Biochemistry 1994; 33: 4721-4729.
55. Chen VB, Arendall WB, 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010; 66(Pt 1): 12-21.
56. Lindman S, Xue WF, Szczepankiewicz O, Bauer MC, Nilsson H, Linse S. Salting the charged surface: pH and salt dependence of protein G B1 stability. Biophys J 2006; 90: 2911-2921.
57. Kumar S, Li MS. Biomolecules under mechanical force. Phys Rep 2010; 486(1-2): 1-74.
58. Odaert B, Jean F, Boutillon C, Buisine E, Melnyk O, Tartar A, Lippens G. Synthesis, folding, and structure of the beta-turn mimic modified B1 domain of streptococcal protein G. Protein Sci 1999; 8: 2773-2783.
59. Li H, Cao Y. Protein mechanics: from single molecules to functional biomaterials. Acc Chem Res 2010; 43: 1331-1341.
60. Lv S, Dudek DM, Cao Y, Balamurali MM, Gosline J, Li H. Designed biomaterials to mimic the mechanical properties of muscles. Nature 2010; 465: 69-73.
61. Ramirez-Alvarado M, Cocco MJ, Regan L. Mutations in the B1 domain of protein G that delay the onset of amyloid fibril formation in vitro. Protein Sci 2003; 12: 567-576.
62. Ramirez-Alvarado M, Merkel JS, Regan L. A systematic exploration of the influence of the protein stability on amyloid fibril formation in vitro. Proc Natl Acad Sci USA 2000; 97: 8979-8984.
63. Gronenborn AM, Filpula DR, Essig NZ, Achari A, Whitlow M, Wingfield PT, Clore GM. A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science 1991; 253: 657-661.
64. Alexander P, Fahnestock S, Lee T, Orban J, Bryan P. Thermodynamic analysis of the folding of the streptococcal protein G IgG-binding domains B1 and B2: why small proteins tend to have high denaturation temperatures. Biochemistry 1992; 31: 3597-3603.
65. Alexander P, Orban J, Bryan P. Kinetic analysis of folding and unfolding the 56 amino acid IgG-binding domain of streptococcal protein G. Biochemistry 1992; 31: 7243-7248.
66. Smith CK, Withka JM, Regan L. A thermodynamic scale for the beta-sheet forming tendencies of the amino acids. Biochemistry 1994; 33: 5510-5517.
67. Smith CK, Regan L. Guidelines for protein design: the energetics of beta sheet side chain interactions. Science 1995; 270: 980-982.
68. Park SH, O'Neil KT, Roder H. An early intermediate in the folding reaction of the B1 domain of protein G contains a native-like core. Biochemistry 1997; 36: 14277-14283.
69. Park SH, Shastry MC, Roder H. Folding dynamics of the B1 domain of protein G explored by ultrarapid mixing. Nat Struct Biol 1999; 6: 943-947.
70. Merkel JS, Regan L. Aromatic rescue of glycine in beta sheets. Fold Des 1998; 3: 449-455.
71. Merkel JS, Sturtevant JM, Regan L. Sidechain interactions in parallel beta sheets: the energetics of cross-strand pairings. Structure 1999; 7: 1333-1343.
72. Raible M, Evstigneev M, Bartels FW, Eckel R, Nguyen-Duong M, Merkel R, Ros R, Anselmetti D, Reimann P. Theoretical analysis of single-molecule force spectroscopy experiments: heterogeneity of chemical bonds. Biophys J 2006; 90: 3851-3864.
73. Aioanei D, Lv S, Tessari I, Rampioni A, Bubacco L, Li H, Samorì B, Brucale M. Single-Molecule-Level Evidence for the Osmophobic Effect Angewandte Chemie Int. Ed. EnglDOI: 10.1002/anie.201006714.
74. Paci E, Clarke J, Steward A, Vendruscolo M, Karplus M. Self-consistent determination of the transition state for protein folding: application to a fibronectin type III domain. Proc Natl Acad Sci USA 2003; 100: 394-399.
75. Main ER, Jackson SE. Does trifluoroethanol affect folding pathways and can it be used as a probe of structure in transition states? Nat Struct Biol 1999; 6: 831-835.
76. Frank H. HEaMJPJ. The Kinetic Basis of Molecular Biology. London: Wiley: Chapman & Hall; 1954. 874p.
77. Meng FG, Hong YK, He HW, Lyubarev AE, Kurganov BI, Yan YB, Zhou HM. Osmophobic effect of glycerol on irreversible thermal denaturation of rabbit creatine kinase. Biophys J 2004; 87: 2247-2254.