Linkage of protonation and anion binding to the folding of Sac7d

Journal of Molecular Biology

Volumn 276, Issue 1, 1998, Pages 203-224

  McCrary, Bradford S ^a   Bedell, Jennifer ^a   Edmondson, Stephen P ^a   Shriver, John W ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calorimetry; Circular dichroism; Hyperthermophile; Protein stability; Sulfolobus

Indexed keywords

ANION; BACTERIAL PROTEIN; CHLORIDE; RECOMBINANT PROTEIN;

ARTICLE; CIRCULAR DICHROISM; DIFFERENTIAL SCANNING CALORIMETRY; ENTHALPY; GRAM NEGATIVE BACTERIUM; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN FOLDING; TEMPERATURE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SULFOLOBUS; SULFOLOBUS ACIDOCALDARIUS;

EID: 0032512877     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1500     Document Type: Article

References (114)

1. Abe Y., Ueda T., Iwashita H., Hashimoto Y., Motoshima H., Tanaka Y., Imoto T. Effect of salt concentration on the pKa of acidic residues in lysozyme. J. Biochem. 118:1995;946-952
2. Anderson D.E., Becktel W.J., Dahlquist F.W. pH-induced denaturation of proteins a single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme. Biochemistry. 29:1990;2403-2408
3. Antosiewicz J., McCammon J.A., Gilson M.K. Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238:1994;415-436
4. Aune K., Tanford C. Thermodynamics of the denaturation of lysozyme by guanidine hydrochloride II. Dependence on denaturant concentration at 25°C. Biochemistry. 8:1969;4586-4590
5. Baker B.M., Murphy K.P. Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys. J. 71:1996;2049-2055
6. Baldwin R.L. How Hofmeister ion interactions affect protein stability. Biophys. J. 71:1996;2056-2063
7. Barrick D., Hughson F.M., Baldwin R.L. Molecular mechanism of acid denaturation the role of histidine residues in the partial unfolding of apomyoglobin. J. Mol. Biol. 237:1994;588-601
8. Bartik K., Redfield C., Dobson C.M. Measurement of the individual pKa values of acidic residues of hen and turkey lysozymes by two-dimensional 1H NMR. Biophys. J. 66:1994;1180-1184
9. Bevington P.R., Robinson D.K. Data Reduction and Error Analysis for the Physical Sciences. 1992;McGraw-Hill, New York
10. Brandts J.F., Lin L.-N. Study of strong to ultratight protein interactions using differential scanning calorimetry. Biochemistry. 29:1990;6927-6940
11. Breitung J., Schmitz R.A., Stetter K.O., Thauer R.K. N5, N10-methylenetetrahydromethanopterin cyclohydrolase from the extreme thermophile Methanopyrus kanderli increase of catalytic efficiency (kcat/Km) and thermostability in the presence of salts. Arch. Microbiol. 156:1991;517-524
12. Catanzano F., Giancola C., Graziano G., Barone G. Temperature-induced denaturation of ribonuclease S a thermodynamic study. Biochemistry. 35:1996;13378-13385
13. Cavagnero S., Zhou Z.H., Adams M.W.W., Chan S.I. Response of rubredoxin from Pyrococcus furiosus to environmental changes implications for the origin of hyperthermostability. Biochemistry. 34:1995;9865-9873
14. Chan M.K., Mukund S., Kletzin A., Adams M.W.W., Rees D. Structure of a hyperthermophilic tungsopterin enzyme, aldehyde ferredoxin oxidoreductase. Science. 267:1995;1463-1469
15. Cohn E.J., Edsall J.T. Proteins, Amino Acids and Peptides as Ions and Dipolar Ions. 1943;Reinhold Publishing, New York
16. Collins K.D., Washabaugh M.W. The Hofmeister effect and the behaviour of water at interfaces. Quart. Rev. Biophys. 4:1985;323-422
17. DeDecker B., O'Brien R., Fleming P., Geiger J., Jackson S., Sigler P. The crystal structure of a hyperthermophile archael TATA-box binding protein. J. Mol. Biol. 264:1996;1072-1084
18. DeLauder S., Mauro J., Poulos T., Williams J., Schwarz F. Thermodynamics of hydrogen cyanide and hydrogen fluoride binding to cytochrome c peroxidase and its Asn-82 → Asp mutant. Biochem. J. 302:1994;437-442
19. DePrat Gay G., Johnson C.M., Fersht A.R. Contribution of a proline residue and a salt bridge to the stability of a type I reverse turn in chymotrypsin inhibitor-2. Protein Eng. 7:1994;103-108
20. di Cera E. Thermodynamic Theory of Site-specific Binding Processes in Biological Macromolecules. 1995;Cambridge University Press, Cambridge, UK
21. Edmondson S.P., Qiu L., Shriver J.W. Solution structure of the DNA-binding protein Sac7d from the hyperthermophile Sulfolobus acidocaldarius. Biochemistry. 34:1995;13289-13304
22. Edsall J.T., Wyman J. Biophysical Chemistry. 1958;Academic Press, New York
23. Eftink M. Use of multiple spectroscopic methods to monitor equilibrium unfolding of proteins. Methods Enzymol. 259:1995;487-512
24. Eftink M., Anusiem A.C., Biltonen R.L. Enthalpy-entropy compensation and heat capacity changes for protein-ligand interactions general thermodynamic models and data for the binding of nucleotides to ribonuclease A. Biochemistry. 22:1983;3884-3896
25. Fink A., Calciano L., Goto Y., Kurotsu T., Palleros D. Classification of acid denaturation of proteins intermediates and unfolded states. Biochemistry. 33:1994;12504-12511
26. Fink A.L. Compact intermediate states in protein folding. Annu. Rev. Biophys. Biomol. Struct. 24:1995;495-522
27. Flogel M., Albert A., Biltonen R. The magnitude of electrostatic interactions in inhibitor binding and during catalysis by ribonuclease A. Biochemistry. 14:1975;2616-2621
28. Freire E. Differential scanning calorimetry. Shirley B. Protein Stability and Folding. 1995;Humana Press, Totowa, NJ
29. Freire E., Biltonen R. Statistical mechanical deconvolution of thermal transitions in macromolecules. I. Theory and application to homogeneous systems. Biopolymers. 17:1978;463-479
30. Garcia-Moreno B. Estimating binding constants for site-specific interactions between monovalent ions and proteins. Methods Enzymol. 240:1994;645-667
31. Garcia-Moreno E.B. Probing structural and physical basis of protein energetics linked to protons and salt. Methods Enzymol. 259:1995;512-538
32. Gast K., Damaschun H., Misselwitz R., Müller-Frome M., Zirwer D., Damaschun G. Compactness of protein molten globules temperature-induced structural changes of the apomyoglobin folding intermediate. Eur. Biophys. J. 23:1994;297-305
33. Gjerde D.T., Schmuchler G., Fritz J.S. Anion chromatography with low conductivity elements. II. J. Chromatog. 187:1980;35-45
34. Goto Y., Takahashi N., Fink A. Mechanism of acid-induced folding of proteins. Biochemistry. 29:1990;3480-3488
35. Grayling R.A., Becktel W.J., Reeve J.N. Structure and stability of histone HMf from the hyperthermophilic archaeon Methanothermus fervidus. Biochemistry. 34:1995;8441-8448
36. Guinto E.R., Di Cera E. Large heat capacity change in a protein - monovalent cation interaction. Biochemistry. 35:1996;8800-8804
37. Hagihara Y., Aimoto S., Fink A., Goto Y. Guanidine hydrochloride-induced folding of proteins. J. Mol. Biol. 231:1993;180-184
38. Hagihara Y., Tan Y., Goto Y. Comparison of the conformational stability of the molten globule and native states of horse cytochrome c. J. Mol. Biol. 237:1994;336-348
39. Hamada D., Kidokoro S.-I., Fukada H., Takahashi K., Goto Y. Salt-induced formation of the molten globule state of cytochrome c studied by isothermal titration calorimetry. Proc. Natl Acad. Sci. USA. 91:1994;10325-10329
40. Haynie D., Freire E. Structural energetics of the molten globule state. Proteins: Struct. Funct. Genet. 16:1993;115-140
41. Haynie D.T., Freire E. Estimation of the folding/unfolding energetics of marginally stable proteins using differential scanning calorimetry. Anal. Biochem. 216:1994;33-41
42. Henning M., Darimont B., Sterner R., Kirschner K., Jansonius J.N. 2.0 Å structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus possible determinants of protein stability. Structure. 3:1995;1295-1306
43. Hensel R., König H. Thermoadaptation of methanogenic bacteria by intracellular ion concentration. FEMS Microbiol. Letters. 49:1988;75-79
44. Honig B., Yang A.-S. Free energy balance in protein folding. Advan. Protein Chem. 46:1995;27-58
45. Horovitz A., Serrano L., Avron B., Bycroft M., Fersht A. Strength and co-operativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 216:1991;1031-1044
46. Hu C.Q., Sturtevant J. A differential scanning calorimetric study of the binding of sulfate ion and of cibacron blue F3GA to yeast phosphoglycerate kinase. Biochemistry. 28:1989;813-818
47. Imada K., Sato M., Tanaka N., Katsube Y., Matuura Y., Oshima T. Three-dimensional structure of a highly thermostable enzyme, 3-isopropylmalate dehydrogenase of Thermus thermophilus at 2.2 Å resolution. J. Mol. Biol. 222:1991;725-738
48. Ionescu R.M., Eftink M.R. Global analysis of the acid-induced and urea-induced unfolding of staphylococcal nuclease and two of its variants. Biochemistry. 36:1997;1129-1140
49. Jackson S.E., Moracci M., elMasry N., Johnson C.M., Fersht A.R. Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor. Biochemistry. 32:1993;11259-11269
50. Jencks W.P. Catalysis in Chemistry and Enzymology. 1969;McGraw-Hill, New York
51. Jennings P.A., Wright P.E. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science. 262:1993;892-896
52. Kamath U., Shriver J. Characterization of thermotropic state changes in myosin subfragment-1 and heavy meromyosin by UV difference spectroscopy. J. Biol. Chem. 264:1989;5586-5592
53. Kataoka M., Hagihara Y., Mihara K., Goto Y. Molten globule of cytochrome-c studied by small angle X-ray scattering. J. Mol. Biol. 229:1993;591-596
54. Kauzman W. Some factors in the interpretation of protein denaturation. Advan. Protein Chem. 14:1955;1-63
55. Kelly C., Nishiyama M., Ohnishi Y., Beppu T., Birktoft J. Determinants of protein thermostability observed in the 1.9 Å crystal structure of malate dehydrogenase from the thermophilic bacterium Thermus flavus. Biochemistry. 32:1993;3913-3922
56. Kelly R.M., Peeples T.L., Halio S.B., Rinker K.D., Duffaud G.D. Extremely thermophilic microorganisms metabolic strategies, genetic characteristics, and biotechnological potential. Ann. N. Y. Acad. Sci. 745:1994;409-425
57. Knapp S., Karshikoff A., Berndt K.D., Christova P., Atanasov B., Ladenstein R. Thermal unfolding of the DNA-binding protein Sso7d from the hyperthermophile Sulfolobus solfataricus. J. Mol. Biol. 264:1996;1132-1144
58. Korndörfer I., Steipe B., Huber R., Tomschy A., Jaenicke R. The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima at 2.5 Å resolution. J. Mol. Biol. 246:1995;511-521
59. Korolev S., Nayal M., Barnes W., Di Cera E., Waksman G. Crystal structure of the large fragment of Thermus aquaticus DNA polymerase I at 2.5 Å resolution structural basis for thermostability. Proc. Natl Acad. Sci. 92:1995;9264-9268
60. Linderström-Lang K. The ionization of proteins. Compt. Rend. Trav. Lab. Carlsberg, ser. Chim. 15:1924;1-29
61. Liu Y., Sturtevant J.M. Significant discrepancies between van't Hoff and calorimetric enthalpies. II. Protein Sci. 4:1995;2559-2561
62. Liu Y., Sturtevant J.M. The observed change in heat capacity accompanying the thermal unfolding of proteins depends on the composition of the solution and on the method employed to change the temperature of unfolding. Biochemistry. 35:1996;3059-3062
63. Lovrien R., Sturtevant J.M. Calorimetric determination of the enthalpies of binding of ions to deionized bovine serum albumin. Biochemistry. 10:1971;3811-3815
64. Lumry R., Biltonen R., Brandts J. Validity of the "two-state" hypothesis for conformational transitions of proteins. Biopolymers. 4:1966;917-944
65. Marqusee S., Sauer R.T. Contributions of a hydrogen bond/salt bridge network to the stability of secondary and tertiary structure in lambda repressor. Protein Sci. 3:1994;2217-2225
66. Matthew J.B., Gurd F.R.N., Garcia-Moreno B., Flanagan M.A., March K.L., Shire S.J. pH-dependent processes in proteins. CRC Crit. Rev. Biochem. 18:1985;91-197
67. McAfee J., Edmondson S., Datta P., Shriver J., Gupta R. Gene cloning, sequencing, expression, and characterization of the Sac7 DNA-binding proteins from the extremely thermophilic archaeon Sulfolobus acidocaldarius. Biochemistry. 34:1995;10063-10077
68. McCrary B.S., Edmondson S.P., Shriver J.W. Hyperthermophile protein folding thermodynamics differential scanning calorimetry and chemical denaturation of Sac7d. J. Mol. Biol. 264:1996;784-805
69. Monera O., Kay C., Hodges R. Protein denaturation with guanidine hydrochloride or urea provides a different estimate of stability depending on the contributions of electrostatic interactions. Protein Science. 3:1994;1984-1991
70. Naghibi H., Tamura A., Sturtevant J.M. Significant discrepancies between van't Hoff and calorimetric enthalpies. Proc. Natl Acad. Sci. USA. 92:1995;5597-5599
71. Nicholson E.M., Scholtz J.M. Conformational stability of the Escherichia coli HPr protein test of the linear extrapolation method and a thermodynamic characterization of cold denaturation. Biochemistry. 35:1996;11369-11378
72. Oda Y., Yamasaki T., Nagayama K., Kanaya S., Kuroda Y., Nakamura H. Individual ionization constants of all the carboxyl groups in ribonuclease HI from Escherichia coli determined by NMR. Biochemistry. 33:1994;5275-5284
73. Ohgushi M., Wada A. "Molten-globule state" a compact form of globular proteins with mobile side chains. FEBS Letters. 164:1983;21-24
74. Oliveberg M., Vuilleumier S., Fersht A. Thermodynamic study of the acid denaturation of barnase and its dependence on ionic strength evidence for residual electrostatic interactions in the acid/thermally denatured state. Biochemistry. 33:1994;8826-8832
75. Oliveberg M., Arcus V., Fersht A.R. pKa values of carboxyl groups in the native and denatured states of barnase: the pKa values of the denatured state are on average 0. 4 units lower than those of model compounds. Biochemistry. 34:1995;9424-9433
76. Pace C.N. The stability of globular proteins. CRC Crit. Rev. Biochem. 3:1975;1-43
77. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131:1986;266-280
78. Pace C.N., Grimsley G.R. Ribonuclease T1 is stabilized by cation and anion binding. Biochemistry. 27:1988;3242-3246
79. Pace C.N., Laurents D. A new method for determining the heat capacity change for protein folding. Biochemistry. 28:1989;2520-2525
80. Pace C.N., Laurents D.V., Thomson J.A. pH dependence of the urea and guanidine hydrochloride denaturation of ribonuclease A and ribonuclease T1. Biochemistry. 29:1990;2564-2572
81. Pace C.N., Shirley B.A., McNutt M., Gajiwala K. Forces contributing to the conformational stability of proteins. FASEB J. 10:1996;75-83
82. Perutz M.F. Electrostatic effects in proteins. Science. 201:1978;1187-1191
83. Potter J.D., Hsu F.-J., Pownall H. Thermodynamics of Ca + 2 binding to troponin-C. J. Biol. Chem. 252:1977;2452-2454
84. Press W., Flannery B., Teukolsky S., Vetterling W. Numerical Recipes: The Art of Scientific Computing (Fortran Version). 1989;Cambridge University Press, Cambridge
85. Privalov P. Stability of proteins. Small globular proteins. Advan. Protein. Chem. 33:1979;167-241
86. Privalov P., Khechinashvili N. A thermodynamic approach to the problem of stabilization of globular protein structure a calorimetric study. J. Mol. Biol. 86:1974;665-684
87. Privalov P., Griko Y., Venyaminov S., Kutyshenko V. Cold denaturation of myoglobin. J. Mol. Biol. 190:1986;487-498
88. Ptitsyn O.B. Molten globule and protein folding. Advan. Protein Chem. 47:1995;83-229
89. Ramsay G.D., Eftink M.R. Analysis of multidimensional spectroscopic data to monitor unfolding of proteins. Methods Enzymol. 240:1994;615-645
90. Record J.M.T., Anderson C.F., Lohman T.M. Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids the roles of ion association or release, screening, and ion effects on water activity. Quart. Rev. Biophys. 11:1978;103-178
91. Ripoll D., Vorobjev Y., Liwo A., Vila J., Scheraga H. Coupling between folding and ionization equilibria effects of pH on the conformational preferences of polypeptides. J. Mol. Biol. 264:1996;770-783
92. Schaller W., Robertson A.D. pH, ionic strength, and temperature dependences of ionization equilibria for the carboxyl groups in turkey ovomucoid third domain. Biochemistry. 34:1995;4714-4723
93. Schellman J.A. Selective binding and solvent denaturation. Biopolymers. 26:1987;549-559
94. Scholtz J.M. Conformational stability of HPr the histidine-containing phosphocarrier protein from Bacillus subtilis. Protein Sci. 4:1995;35-43
95. Scholz S., Sonnenbichler J., Schäfer W., Hensel R. Di-myo-inositol-1,1'-phosphate a new inositol phosphate isolated from Pyrococcus woesei. FEBS Letters. 306:1992;239-242
96. Spassov V., Karshikoff A.D., Ladenstein R. The optimization of protein-solvent interactions thermostability and the role of hydrophobic and electrostatic interactions. Protein Sci. 4:1995;1516-1527
97. Straume M., Freire E. Two-dimensional differential scanning calorimetry simultaneous resolution of intrinsic protein structural energetics and ligand binding interactions by global linkage analysis. Anal. Biochem. 203:1992;259-268
98. Sturtevant J. Heat capacity and entropy changes in processes involving proteins. Proc. Natl Acad. Sci. USA. 74:1977;2236-2240
99. Sturtevant J. Biochemical applications of differential scanning calorimetry. Annu. Rev. Phys. Chem. 38:1987;463-488
100. Swint-Kruse L., Robertson A.D. Hydrogen bonds and the pH dependence of ovomucoid third domain stability. Biochemistry. 34:1995;4724-4732
101. Szilagyi A., Zavodszky P. Structural basis for the extreme thermostability of D-glyceraldehyde-3-phosphate dehydrogenase from Thermotoga maritima analysis based on homology modelling. Protein Eng. 8:1995;779-789
102. Tanford C. Protein denaturation. Advan. Protein Chem. 23:1968;122-282
103. Tanford C. Protein denaturation part C theoretical models for the mechanism of denaturation. Advan. Protein Chem. 24:1970;1-95
104. Viguera A.R., Martinez J.C., Filimonov V.V., Mateo P.L., Serrano L. Thermodynamic and kinetic analysis of the SH3 domain of spectrin shows a two-state folding transition. Biochemistry. 33:1994;2142-2150
105. Wang P., Oscarson J.L., Gillespie S.E., Izatt R.M., Cao H. Thermodynamics of Protonation of Amino Acid Carboxylate Groups from 50 to 125°C. J. Sol. Chem. 25:1996;243-266
106. Wintrode P.L., Makhatadze G.I., Privalov P. Thermodynamics of ubiquitin unfolding. Proteins: Struct. Funct. Genet. 18:1994;246-253
107. Wyman J., Gill S.J. Binding and Linkage: Functional Chemistry of Biological Macromolecules. 1990;University Science Books, Mill Valley, CA
108. Xie D., Bhakuni V., Freire E. Calorimetric determination of the energetics of the molten globule intermediate in protein folding apo-α-lactalbumin. Biochemistry. 30:1991;10673-10678
109. Yang A.-S., Honig B. On the pH dependence of protein stability. J. Mol. Biol. 231:1993;459-474
110. Yao M., Bolen D.W. How valid are denaturant-induced unfolding free energy measurements? Level of conformance to common assumptions over an extended range of ribonuclease A stability. Biochemistry. 34:1995;3771-3781
111. Yip K.S.P., Stillman T.J., Britton K.L., Artymiuk P.J., Baker P.J., Sekelnikova S.E., Engel P.C., Pasquo A., Chiaraluce R., Consalvi V., Scandurra R., Rice D.W. The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion pair networks in maintaining enzyme stability at extreme temperatures. Structure. 3:1995;1147-1158
112. Privalov P. Stability of proteins. Small globular proteins. Advan. Protein. Chem. 33:1979;167-241
113. Straume M., Freire E. Two-dimensional differential scanning calorimetry simultaneous resolution of intrinsic protein structural energetics and ligand binding interactions by global linkage analysis. Anal. Biochem. 203:1992;259-268
114. Wyman J., Gill S.J. Binding and Linkage: Functional Chemistry of Biological Macromolecules. 1990;University Science Books, Mill Valley, CA