Studying salt effects on protein stability using ribonuclease t1 as a model system

Biophysical Chemistry

Volumn 161, Issue , 2012, Pages 29-38

  Beauchamp, David L ^a   Khajehpour, Mazdak ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Fluorescence; Kirkwood interactions; Protein folding; Salt effects; Salting out

Indexed keywords

RIBONUCLEASE T1; SODIUM CHLORIDE; WATER;

ARTICLE; BINDING AFFINITY; DIELECTRIC CONSTANT; FLUORESCENCE; HALOPHILIC BACTERIUM; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; SOLVATION; SURFACE PROPERTY; THERMODYNAMICS;

OSMOLAR CONCENTRATION; PROTEIN STABILITY; PROTEIN UNFOLDING; RIBONUCLEASE T1; SALTS; THERMODYNAMICS;

EID: 84855976504     PISSN: 03014622     EISSN: 18734200     Source Type: Journal    
DOI: 10.1016/j.bpc.2011.11.004     Document Type: Article

References (56)

1. A. Wegner, and G. Isenberg 12-Fold difference between the critical monomer concentrations of the two ends of actin filaments in physiological salt conditions Proceedings of the National Academy of Sciences of the United States of America 80 1983 4922 4925
2. T. Schlick, B. Li, and W.K. Olson The influence of salt on the structure and energetics of supercoiled DNA Biophysical Journal 67 1994 2146 2166 (Pubitemid 24369640)
3. R.L. Baldwin How Hofmeister ion interactions affect protein stability Biophysical Journal 71 1996 2056 2063 (Pubitemid 26325984)
4. S.N. Timasheff Solvent effects on protein stability Current Opinion in Structural Biology 2 1991 35 39
5. Y. Zhang, and P.S. Cremer Interactions between macromolecules and ions: the Hofmeister series Current Opinion in Chemical Biology 10 2006 658 663 (Pubitemid 44821892)
6. J.G. Kirkwood Acid-base equilibrium in solutions of ampholytes Annals of the New York Academy of Sciences 41 1941 321 328
7. C. Tanford, and J.G. Kirkwood Theory of protein titration curves. I. General equations for impenetrable spheres Journal of the American Chemical Society 79 1957 5333 5339
8. F. Dong, and H.-X. Zhou Electrostatic contributions to T4 lysozyme stability: solvent-exposed charges versus semi-buried salt bridges Biophysical Journal 83 2002 1341 1347 (Pubitemid 34977707)
9. Y.-H. Kao, C.A. Fitch, S. Bhattacharya, C.J. Sarkisian, J.T.J. Lecomte, and B. Garcia-Moreno E Salt effects on ionization equilibria of histidines in myoglobin, Biophys J 79 2000 1637 1654
10. N.A. Simonov, M. Mascagni, and M.O. Fenley Monte Carlo-based linear Poisson-Boltzmann approach makes accurate salt-dependent solvation free energy predictions possible Journal of Chemical Physics 127 2007 185105/185101-185105/ 185106.
11. R. Geney, M. Layten, R. Gomperts, V. Hornak, and C. Simmerling Investigation of salt bridge stability in a generalized born solvent model Journal of Chemical Theory and Computation 2 2006 115 127
12. J.D. Ballin, J.P. Prevas, C.R. Ross, E.A. Toth, G.M. Wilson, and M.T. Record contributions of the histidine side chain and the N-terminal α-amino group to the binding thermodynamics of oligopeptides to nucleic acids as a function of pH Biochemistry 49 2010 2018 2030
13. B. Hribar, N.T. Southall, V. Vlachy, and K.A. Dill How ions affect the structure of water Journal of the American Chemical Society 124 2002 12302 12311 (Pubitemid 35157776)
14. A.S. Thomas, and A.H. Elcock Molecular dynamics simulations of hydrophobic associations in aqueous salt solutions indicate a connection between water hydrogen bonding and the Hofmeister effect Journal of the American Chemical Society 129 2007 14887 14898 (Pubitemid 350230710)
15. R. Piazza Protein interactions and association: an open challenge for colloid science Current Opinion in Colloid and Interface Science 8 2004 515 522 (Pubitemid 38542699)
16. S. Finet, F. Skouri-Panet, M. Casselyn, F. Bonnete, and A. Tardieu The Hofmeister effect as seen by SAXS in protein solutions Current Opinion in Colloid and Interface Science 9 2004 112 116 (Pubitemid 39194145)
17. H.-X. Zhou Interactions of macromolecules with salt ions: an electrostatic theory for the Hofmeister effect Proteins: Structure, Function, and Bioinformatics 61 2005 69 78 (Pubitemid 41262918)
18. X. Huang, and H.-X. Zhou Similarity and difference in the unfolding of thermophilic and mesophilic cold shock proteins studied by molecular dynamics simulations Biophysical Journal 91 2006 2451 2463 (Pubitemid 44511701)
19. S. Spencer Daniel, K. Xu, M. Logan Timothy, and H.-X. Zhou Effects of pH, salt, and macromolecular crowding on the stability of FK506-binding protein: an integrated experimental and theoretical study Journal of Molecular Biology 351 2005 219 232 (Pubitemid 40973796)
20. J. Steyaert A decade of protein engineering on ribonuclease T1. Atomic dissection of the enzyme-substrate interactions European Journal of Biochemistry 247 1997 1 11 (Pubitemid 27319479)
21. C.N. Pace, U. Heinemann, U. Hahn, and W. Saenger Ribonuclease T1: structure, function and stability Angewandte Chemie 103 1991 351 369 (See also Angew Chem, Int Ed Engl, 1991, 1930(1994), 1343-1960)
22. H. Yoshida The ribonuclease T1 family Methods in Enzymology 341 2001 28 41 (Pubitemid 32928517)
23. D.L. Beauchamp, and M. Khajehpour Probing the effect of water-water interactions on enzyme activity with salt gradients: a case-study using ribonuclease t1 The Journal of Physical Chemistry. B 114 2010 16918 16928
24. J.M. Scholtz, G.R. Grimsley, and C.N. Pace Solvent denaturation of proteins and interpretations of the M value Methods in Enzymology 466 2009 549 565
25. C.N. Pace Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods in Enzymology 131 1986 266 280 (Pubitemid 16002205)
26. M.M. Santoro, and D.W. Bolen Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha -chymotrypsin using different denaturants Biochemistry 27 1988 8063 8068
27. J.R. Lakowicz Principles of Fluorescence Spectroscopy 1983
28. S.L.C. Moors, A. Jonckheer, M. De Maeyer, Y. Engelborghs, and A. Ceulemans Tryptophan conformations associated with partial unfolding in ribonuclease T1 Biophysical Journal 97 2009 1778 1786
29. M.C.R. Shastry, and M.R. Eftink Reversible thermal unfolding of ribonuclease T1 in reverse micelles Biochemistry 35 1996 4094 4101 (Pubitemid 26113466)
30. M. Ruoppolo, and R.B. Freedman Refolding by disulfide isomerization: the mixed disulfide between ribonuclease T1 and glutathione as a model refolding substrate Biochemistry 34 1995 9380 9388
31. B. Somogyi, M. Punyiczki, J. Hedstrom, J.A. Norman, F.G. Prendergast, and A. Rosenberg Coupling between external viscosity and the intramolecular dynamics of ribonuclease T1: a two-phase model for the quenching of protein fluorescence Biochimica et Biophysica Acta, Protein Structure and Molecular Enzymology 1209 1994 61 68 (Pubitemid 24351989)
32. Y. Yamamoto, and J. Tanaka Spectroscopic studies on the configurational structures of ribonuclease T1 Biochimica et Biophysica Acta, Protein Structure 207 1970 522 531
33. C.Q. Hu, J.M. Sturtevant, J.A. Thomson, R.E. Erickson, and C.N. Pace Thermodynamics of ribonuclease T1 denaturation Biochemistry 31 1992 4876 4882
34. C.N. Pace, and G.R. Grimsley Ribonuclease T1 is stabilized by cation and anion binding Biochemistry 27 1988 3242 3246
35. C.N. Pace, D.V. Laurents, 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)
36. J. Deswarte, S. De Vos, U. Langhorst, J. Steyaert, and R. Loris The contribution of metal ions to the conformational stability of ribonuclease T1. Crystal versus solution European Journal of Biochemistry 268 2001 3993 4000 (Pubitemid 32868612)
37. J.A. Thomson, B.A. Shirley, G.R. Grimsley, and C.N. Pace Conformational stability and mechanism of folding of ribonuclease T1 Journal of Biological Chemistry 264 1989 11614 11620
38. M.A. de los Rios, and K.W. Plaxco Apparent Debye-Huckel electrostatic effects in the folding of a simple, single domain protein Biochemistry 44 2005 1243 1250 (Pubitemid 40209004)
39. B. Song, J.-H. Cho, and D.P. Raleigh Ionic-strength-dependent effects in protein folding: analysis of rate equilibrium free-energy relationships and their interpretation Biochemistry 46 2007 14206 14214 (Pubitemid 350250314)
40. L.M. Gloss, and B.J. Placek The effect of salts on the stability of the H2A-H2B histone dimer Biochemistry 41 2002 14951 14959 (Pubitemid 35470674)
41. M. Itaya, and Y. Inoue Steady-state kinetic studies of the inhibitory action of zinc on ribonuclease T1 catalysis Biochemistry Journal 207 1982 357 362
42. K. Takahashi, T. Uchida, and F. Egami Ribonuclease T1, structure and function Advances in Biophysics 1 1970 53 98
43. M. Vijayakumar, and M.S. Gopinathan Pair correlation energies and successive ionization potentials of atoms helium through zinc Journal of Chemical Physics 97 1992 6639 6643
44. T. Liu, P.R. Callis, B.H. Hesp, M. de Groot, W.J. Buma, and J. Broos Ionization potentials of fluoroindoles and the origin of nonexponential tryptophan fluorescence decay in proteins Journal of the American Chemical Society 127 2005 4104 4113 (Pubitemid 40411452)
45. J. Ding, H.W. Choe, J. Granzin, and W. Saenger Structure of ribonuclease T1 complexed with zinc(II) at 1.8 Å resolution: a Zn2+.6H2O.carboxylate clathrate Acta Crystallographica Section B: Structural Science B48 1992 185 191
46. L.M. Gloss, T.B. Topping, A.K. Binder, and J.R. Lohman Kinetic folding of Haloferax volcanii and Escherichia coli dihydrofolate reductases: haloadaptation by unfolded state destabilization at high ionic strength Journal of Molecular Biology 376 2008 1451 1462
47. J.A. Schellman The thermodynamics of solvent exchange Biopolymers 34 1994 1015 1026
48. J.A. Schellman Protein stability in mixed solvents: a balance of contact interaction and excluded volume Biophysical Journal 85 2003 108 125 (Pubitemid 36753621)
49. S.N. Timasheff Thermodynamic binding and site occupancy in the light of the Schellman exchange concept Biophysical Chemistry 101-102 2002 99 111 (Pubitemid 35462040)
50. H.-X. Zhou, and F. Dong Electrostatic contributions to the stability of a thermophilic cold shock protein Biophysical Journal 84 2003 2216 2222 (Pubitemid 36373544)
51. J. Srinivasan, M.W. Trevathan, P. Beroza, and D.A. Case Application of a pairwise generalized born model to proteins and nucleic acids. Inclusion of salt effects Theoretical Chemistry Accounts 101 1999 426 434
52. Z. Abbas, M. Gunnarsson, E. Ahlberg, and S. Nordholm Corrected Debye-Hueckel theory of salt solutions: size asymmetry and effective diameters The Journal of Physical Chemistry. B 106 2002 1403 1420 (Pubitemid 35276107)
53. S. Bykov, and S. Asher Raman studies of solution polyglycine conformations The Journal of Physical Chemistry. B 114 2010 6636 6641
54. A.S. Thomas, and A.H. Elcock Molecular dynamics simulations predict a favorable and unique mode of interaction between lithium (Li +) ions and hydrophobic molecules in aqueous solution Journal of Chemical Theory and Computation 7 2011 818 824
55. W.K. Lim, J. Rosgen, and S.W. Englander Urea, but not guanidinium, destabilizes proteins by forming hydrogen bonds to the peptide group Proceedings of the National Academy of Sciences of the United States of America 106 2009 2595 2600
56. C.F. Baes Jr., and R.E. Mesmer The Hydrolysis of Cations 1976