Mechanism of Thermostabilization in a Designed Cold Shock Protein with Optimized Surface Electrostatic Interactions

Journal of Molecular Biology

Volumn 336, Issue 4, 2004, Pages 929-942

  Makhatadze, George I ^a   Loladze, Vakhtang V ^a   Gribenko, Alexey V ^a   Lopez, Maria M ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Circular dichroism; Cold shock proteins; Engineering; Fluorescence; Thermostability

Indexed keywords

BACTERIAL PROTEIN; COLD SHOCK PROTEIN; SINGLE STRANDED DNA; UREA;

ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; CIRCULAR DICHROISM; DIFFERENTIAL SCANNING CALORIMETRY; ENTHALPY; HIGH TEMPERATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SURFACE CHARGE; TEMPERATURE DEPENDENCE; THERMODYNAMICS; THERMOSTABILITY;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 1042298814     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.12.058     Document Type: Article

References (81)

1. Jaenicke R., Bohm G. The stability of proteins in extreme environments. Curr. Opin. Struct. Biol. 8:1998;738-748.
2. Ladenstein R., Antranikian G. Proteins from hyperthermophiles: stability and enzymatic catalysis close to the boiling point of water. Advan. Biochem. Eng. Biotechnol. 61:1998;37-85.
3. Kumar S., Tsai C.J., Nussinov R. Factors enhancing protein thermostability. Protein Eng. 13:2000;179-191.
4. Xiao L., Honig B. Electrostatic contributions to the stability of hyperthermophilic proteins. J. Mol. Biol. 289:1999;1435-1444.
5. Rees D.C., Adams M.W. Hyperthermophiles: taking the heat and loving it. Structure. 3:1995;251-254.
6. Jaenicke R., Schurig H., Beaucamp N., Ostendorp R. Structure and stability of hyperstable proteins: glycolytic enzymes from hyperthermophilic bacterium Thermotoga maritima. Advan. Protein Chem. 48:1996;181-269.
7. Schindelin H., Marahiel M.A., Heinemann U. Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature. 364:1993;164-168.
8. Schindelin H., Jiang W., Inouye M., Heinemann U. Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc. Natl Acad. Sci. USA. 91:1994;5119-5123.
9. Schnuchel A., Wiltscheck R., Czisch M., Herrler M., Willimsky G., Graumann P., et al. Structure in solution of the major cold-shock protein from Bacillus subtilis. Nature. 364:1993;169-171.
10. Mueller U., Perl D., Schmid F.X., Heinemann U. Thermal stability and atomic-resolution crystal structure of the Bacillus caldolyticus cold shock protein. J. Mol. Biol. 297:2000;975-988.
11. Newkirk K., Feng W., Jiang W., Tejero R., Emerson S.D., Inouye M., Montelione G.T. Solution NMR structure of the major cold shock protein (CspA) from Escherichia coli: identification of a binding epitope for DNA. Proc. Natl Acad. Sci. USA. 91:1994;5114-5118.
12. Kremer W., Schuler B., Harrieder S., Geyer M., Gronwald W., Welker C., et al. Solution NMR structure of the cold-shock protein from the hyperthermophilic bacterium Thermotoga maritima. Eur. J. Biochem. 268:2001;2527-2539.
13. Petrosian S.A., Makhatadze G.I. Contribution of proton linkage to the thermodynamic stability of the major cold-shock protein of Escherichia coli CspA. Protein Sci. 9:2000;387-394.
14. Makhatadze G.I., Marahiel M.A. Effect of pH and phosphate ions on self-association properties of the major cold-shock protein from Bacillus subtilis. Protein Sci. 3:1994;2144-2147.
15. Perl D., Schmid F.X. Electrostatic stabilization of a thermophilic cold shock protein. J. Mol. Biol. 313:2001;343-357.
16. Welker C., Bohm G., Schurig H., Jaenicke R. Cloning, overexpression, purification, and physicochemical characterization of a cold shock protein homolog from the hyperthermophilic bacterium Thermotoga maritima. Protein Sci. 8:1999;394-403.
17. Wassenberg D., Welker C., Jaenicke R. Thermodynamics of the unfolding of the cold-shock protein from Thermotoga maritima. J. Mol. Biol. 289:1999;187-193.
18. Martin A., Kather I., Schmid F.X. Origins of the high stability of an in vitro-selected cold-shock protein. J. Mol. Biol. 318:2002;1341-1349.
19. Schindler T., Schmid F.X. Thermodynamic properties of an extremely rapid protein folding reaction. Biochemistry. 35:1996;16833-16842.
20. Schindler T., Graumann P.L., Perl D., Ma S., Schmid F.X., Marahiel M.A. The family of cold shock proteins of Bacillus subtilis. Stability and dynamics in vitro and in vivo. J. Biol. Chem. 274:1999;3407-3413.
21. Pace C.N. Single surface stabilizer. Nature Struct. Biol. 7:2000;345-346.
22. Sanchez-Ruiz J.M., Makhatadze G.I. To charge or not to charge? Trends Biotechnol. 19:2001;132-135.
23. Dominy B.N., Perl D., Schmid F.X., Brooks C.L. III. The effects of ionic strength on protein stability: the cold shock protein family. J. Mol. Biol. 319:2002;541-554.
24. Zhou H.X., Dong F. Electrostatic contributions to the stability of a thermophilic cold shock protein. Biophys. J. 84:2003;2216-2222.
25. Loladze V.V., Ibarra-Molero B., Sanchez-Ruiz J.M., Makhatadze G.I. Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface. Biochemistry. 38:1999;16419-16423.
26. Makhatadze G.I., Loladze V.V., Ermolenko D.N., Chen X., Thomas S.T. Contribution of surface salt bridges to protein stability: guidelines for protein engineering. J. Mol. Biol. 327:2003;1135-1148.
27. Sundd M., Iverson N., Ibarra-Molero B., Sanchez-Ruiz J.M., Robertson A.D. Electrostatic interactions in ubiquitin: stabilization of carboxylates by lysine amino groups. Biochemistry. 41:2002;7586-7596.
28. Mehler E.L., Guarnieri F. A self-consistent, microenvironment modulated screened coulomb potential approximation to calculate pH-dependent electrostatic effects in proteins. Biophys. J. 77:1999;3-22.
29. Mehler E.L., Fuxreiter M., Simon I., Garcia-Moreno E.B. The role of hydrophobic microenvironments in modulating pKa shifts in proteins. Proteins: Struct. Funct. Genet. 48:2002;283-292.
30. Antosiewicz J., McCammon J.A., Gilson M.K. Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238:1994;415-436.
31. as in proteins. Biochemistry. 35:1996;7819-7833.
32. Zaremba S.M., Gregoret L.M. Context-dependence of amino acid residue pairing in antiparallel beta-sheets. J. Mol. Biol. 291:1999;463-479.
33. Hillier B.J., Rodriguez H.M., Gregoret L.M. Coupling protein stability and protein function in Escherichia coli CspA. Fold. Des. 3:1998;87-93.
34. Woody R.W. Aromatic side-chain contributions to the far ultraviolet circular dichroism of peptides and proteins. Biopolymers. 17:1978;1451-1467.
35. Chakrabartty A., Kortemme T., Padmanabhan S., Baldwin R.L. Aromatic side-chain contribution to far-ultraviolet circular dichroism of helical peptides and its effect on measurement of helix propensities. Biochemistry. 32:1993;5560-5565.
36. Vuilleumier S., Sancho J., Loewenthal R., Fersht A.R. Circular dichroism studies of barnase and its mutants: characterization of the contribution of aromatic side chains. Biochemistry. 32:1993;10303-10313.
37. Sreerama N., Manning M.C., Powers M.E., Zhang J.X., Goldenberg D.P., Woody R.W. Tyrosine, phenylalanine, and disulfide contributions to the circular dichroism of proteins: circular dichroism spectra of wild-type and mutant bovine pancreatic trypsin inhibitor. Biochemistry. 38:1999;10814-10822.
38. Sreerama N., Venyaminov S.Y., Woody R.W. Estimation of the number of alpha-helical and beta-strand segments in proteins using circular dichroism spectroscopy. Protein Sci. 8:1999;370-380.
39. Perczel A., Park K., Fasman G.D. Deconvolution of the circular dichroism spectra of proteins: the circular dichroism spectra of the antiparallel beta-sheet in proteins. Proteins: Struct. Funct. Genet. 13:1992;57-69.
40. Woody R.W. Circular dichroism. Methods Enzymol. 246:1995;34-71.
41. Ermolenko D.N., Makhatadze G.I. Bacterial cold-shock proteins. Cell. Mol. Life Sci. 59:2002;1902-1913.
42. Lopez M.M., Yutani K., Makhatadze G.I. Interactions of the major cold shock protein of Bacillus subtilis CspB with single-stranded DNA templates of different base composition. J. Biol. Chem. 274:1999;33601-33608.
43. Lopez M.M., Yutani K., Makhatadze G.I. Interactions of the cold shock protein CspB from Bacillus subtilis with single-stranded DNA. Importance of the T base content and position within the template. J. Biol. Chem. 276:2001;15511-15518.
44. Loladze V.V., Ermolenko D.N., Makhatadze G.I. Heat capacity changes upon burial of polar and nonpolar groups in proteins. Protein Sci. 10:2001;1343-1352.
45. Pace C.N. Measuring and increasing protein stability. Trends Biotechnol. 8:1990;93-98.
46. Santoro M.M., Bolen D.W. A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range. Biochemistry. 31:1992;4901-4907.
47. Yang A.S., Sharp K.A., Honig B. Analysis of the heat capacity dependence of protein folding. J. Mol. Biol. 227:1992;889-900.
48. Lazaridis T., Archontis G., Karplus M. Enthalpic contribution to protein stability: insights from atom-based calculations and statistical mechanics. Advan. Protein Chem. 47:1995;231-306.
49. Makhatadze G.I., Privalov P.L. Energetics of protein structure. Advan. Protein Chem. 47:1995;307-425.
50. 19F NMR. Biochemistry. 41:2002;11670-11680.
51. Loladze V.V., Ermolenko D.N., Makhatadze G.I. Thermodynamic consequences of burial of polar and non-polar amino acid residues in the protein interior. J. Mol. Biol. 320:2002;343-357.
52. Elcock A.H. The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins. J. Mol. Biol. 284:1998;489-502.
53. Becktel W.J., Schellman J.A. Protein stability curves. Biopolymers. 26:1987;1859-1877.
54. Hollien J., Marqusee S. A thermodynamic comparison of mesophilic and thermophilic ribonucleases H. Biochemistry. 38:1999;3831-3836.
55. Beadle B.M., Baase W.A., Wilson D.B., Gilkes N.R., Shoichet B.K. Comparing the thermodynamic stabilities of a related thermophilic and mesophilic enzyme. Biochemistry. 38:1999;2570-2576.
56. Rees D.C., Robertson A.D. Some thermodynamic implications for the thermostability of proteins. Protein Sci. 10:2001;1187-1194.
57. Deutschman W.A., Dahlquist F.W. Thermodynamic basis for the increased thermostability of CheY from the hyperthermophile Thermotoga maritima. Biochemistry. 40:2001;13107-13113.
58. Griko Y.V., Privalov P.L., Sturtevant J.M., Venyaminov S. Cold denaturation of staphylococcal nuclease. Proc. Natl Acad. Sci. USA. 85:1988;3343-3347.
59. Griko Y.V., Privalov P.L., Venyaminov S.Y., Kutyshenko V.P. Thermodynamic study of the apomyoglobin structure. J. Mol. Biol. 202:1988;127-138.
60. Grattinger M., Dankesreiter A., Schurig H., Jaenicke R. Recombinant phosphoglycerate kinase from the hyperthermophilic bacterium Thermotoga maritima: catalytic, spectral and thermodynamic properties. J. Mol. Biol. 280:1998;525-533.
61. Guzman-Casado M., Parody-Morreale A., Robic S., Marqusee S., Sanchez-Ruiz J.M. Energetic evidence for formation of a pH-dependent hydrophobic cluster in the denatured state of Thermus thermophilus ribonuclease H. J. Mol. Biol. 329:2003;731-743.
62. Ermolenko D.N., Thomas S.T., Aurora R., Gronenborn A.M., Makhatadze G.I. Hydrophobic interactions at the Ccap position of the C-capping motif of alpha-helices. J. Mol. Biol. 322:2002;123-135.
63. Ermolenko D.N., Richardson J.M., Makhatadze G.I. Noncharged amino acid residues at the solvent-exposed positions in the middle and at the C terminus of the alpha-helix have the same helical propensity. Protein Sci. 12:2003;1169-1176.
64. Gribenko A., Lopez M.M., Richardson J.M. III, Makhatadze G.I. Cloning, overexpression, purification, and spectroscopic characterization of human S100P. Protein Sci. 7:1998;211-215.
65. Gribenko A.V., Hopper J.E., Makhatadze G.I. Molecular characterization and tissue distribution of a novel member of the S100 family of EF-hand proteins. Biochemistry. 40:2001;15538-15548.
66. Thomas S.T., Loladze V.V., Makhatadze G.I. Hydration of the peptide backbone largely defines the thermodynamic propensity scale of residues at the C′ position of the C-capping box of alpha-helices. Proc. Natl Acad. Sci. USA. 98:2001;10670-10675.
67. Schindelin H., Herrler M., Willimsky G., Marahiel M.A., Heinemann U. Overproduction, crystallization, and preliminary X-ray diffraction studies of the major cold shock protein from Bacillus subtilis, CspB. Proteins: Struct. Funct. Genet. 14:1992;120-124.
68. Gill S.C., von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:1989;319-326.
69. Winder A.F., Gent W.L. Correction of light-scattering errors in spectrophotometric protein determinations. Biopolymers. 10:1971;1243-1251.
70. Stites W.E., Byrne M.P., Aviv J., Kaplan M., Curtis P.M. Instrumentation for automated determination of protein stability. Anal. Biochem. 227:1995;112-122.
71. Loladze V.V., Makhatadze G.I. Removal of surface charge-charge interactions from ubiquitin leaves the protein folded and very stable. Protein Sci. 11:2002;174-177.
72. Lopez M.M., Makhatadze G.I. Differential scanning calorimetry. Methods Mol. Biol. 173:2002;113-119.
73. Lopez M.M., Makhatadze G.I. Major cold shock proteins. CspA from Escherichia coli and CspB from Bacillus subtilis, interact differently with single-stranded DNA templates. Biochim. Biophys. Acta. 1479:2000;196-202.
74. Tanford C., Kirkwood J.G. Theory of protein titration curves. I. General equations for impenetrable spheres. J. Am. Chem. Soc. 79:1957;5333-5339.
75. Ibarra-Molero B., Loladze V.V., Makhatadze G.I., Sanchez-Ruiz J.M. Thermal versus guanidine-induced unfolding of ubiquitin. An analysis in terms of the contributions from charge-charge interactions to protein stability. Biochemistry. 38:1999;8138-8149.
76. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 18:1997;2714-2723.
77. Mezei M. Optimal position of the solute for simulations. J. Comput. Chem. 18:1997;812-815.
78. Fitch C.A., Karp D.A., Lee K.K., Stites W.E., Lattman E.E., Garcia-Moreno E.B. Experimental pK(a) values of buried residues: analysis with continuum methods and role of water penetration. Biophys. J. 82:2002;3289-3304.
79. Schwehm J.M., Fitch C.A., Dang B.N., Garcia-Moreno E.B., Stites W.E. Changes in stability upon charge reversal and neutralization substitution in staphylococcal nuclease are dominated by favorable electrostatic effects. Biochemistry. 42:2003;1118-1128.
80. Lee K.K., Fitch C.A., Garcia-Moreno E.B. Distance dependence and salt sensitivity of pairwise, coulombic interactions in a protein. Protein Sci. 11:2002;1004-1016.
81. Kao Y.H., Fitch C.A., Bhattacharya S., Sarkisian C.J., Lecomte J.T., Garcia-Moreno E.B. Salt effects on ionization equilibria of histidines in myoglobin. Biophys. J. 79:2000;1637-1654.