Carboxyl pKa Values, Ion Pairs, Hydrogen Bonding, and the pH-dependence of Folding the Hyperthermophile Proteins Sac7d and Sso7d

Journal of Molecular Biology

Volumn 372, Issue 4, 2007, Pages 992-1008

  Clark, Andrew T ^a   Smith, Kelley ^a   Muhandiram, Ranjith ^b   Edmondson, Stephen P ^a   Shriver, John W ^a  

^a UNIVERSITY OF ALABAMA IN HUNTSVILLE   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

chromatin; electrostatics; hydrogen bonding; ion pairs; sulfolobus

Indexed keywords

BACTERIAL PROTEIN; DNA; PROTEIN SAC7D; PROTEIN SSO7D; UNCLASSIFIED DRUG;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CHROMATIN; HYDROGEN BOND; PH; PKA; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FOLDING; PROTEIN STABILITY; THERMOSTABILITY;

ARCHAEA; SULFOLOBUS;

EID: 34548423250     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.06.089     Document Type: Article

References (108)

1. Edsall J.T., and Wyman J. Biophysical Chemistry (1958), Academic Press, New York
2. Tanford C. Protein denaturation. Part C: theoretical models for the mechanism of denaturation. Advan. Protein Chem. 24 (1970) 1-95
3. Perutz M.F. Electrostatic effects in proteins. Science 201 (1978) 1187-1191
4. Matthew J.B., Gurd F.R.N., Garcia-Moreno B., Flanagan M.A., March K.L., and Shire S.J. pH-dependent processes in proteins. CRC Crit. Rev. Biochem. 18 (1985) 91-197
5. Serrano L., Horovitz A., Avron B., Bycroft M., and Fersht A. Estimating the contribution of engineered surface electrostatic interactions to protein stability by using double-mutant cycles. Biochemistry 29 (1990) 9343-9352
6. Hendsch Z.S., and Tidor B. Do salt-bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3 (1994) 211-226
7. Honig B., and Nicholls A. Classical electrostatics in biology and chemistry. Science 268 (1995) 1144-1149
8. Garcia-Moreno E.B. Probing structural and physical basis of protein energetics linked to protons and salt. Methods Enzymol. 259 (1995) 512-538
9. as in proteins. Biochemistry 35 (1996) 7819-7833
10. Anderson D.E., Becktel W.J., and 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
11. a values of the denatured state are on average 0.4 units lower than those of model compounds. Biochemistry 34 (1995) 9424-9433
12. a values in proteins. Proteins: Struct. Funct. Genet. 48 (2002) 388-403
13. a's of ionizable groups in proteins: atomic detail from a continuum electrostatic model. Biochemistry 29 (1990) 10219-10225
14. Yang A.-S., and Honig B. On the pH dependence of protein stability. J. Mol. Biol. 231 (1993) 459-474
15. Antosiewicz J., McCammon J.A., and Gilson M.K. Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238 (1994) 415-436
16. Warshel A., and Papazyan A. Electrostatic effects in macromolecules: fundamental concepts and practical modeling. Curr. Opin. Struct. Biol. 8 (1998) 211-217
17. Patel S., Mackerell Jr. A.D., and Brooks III C.L. CHARMM fluctuating charge force field for proteins: II protein/solvent properties from molecular dynamics simulations using a nonadditive electrostatic model. J. Comput. Chem. 25 (2004) 1504-1514
18. a values using QM and QM/MM methods. J. Phys. Chem. A 109 (2005) 6634-6643
19. Koehl P. Electrostatics calculations: latest methodological advances. Curr. Opin. Struct. Biol. 16 (2006) 142-151
20. Perutz M.F., and Raidt H. Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2. Nature 255 (1975) 256-259
21. Perl D., Mueller U., Heinemann U., and Schmid F.X. Two exposed amino acid residues confer thermostability on a cold shock protein. Nature Struct. Biol. 7 (2000) 380-383
22. Perl D., and Schmid F.X. Electrostatic stabilization of a thermophilic cold shock protein. J. Mol. Biol. 313 (2001) 343-357
23. Kumar S., and Nussinov R. How do thermophilic proteins deal with heat?. Cell Mol. Life Sci. 58 (2001) 1216-1233
24. Kumar S., and Nussinov R. Close-range electrostatic interactions in proteins. ChemBiochem 3 (2002) 604-617
25. Shiraki K., Nishikori S., Fujiwara S., Imanaka T., and Takagi M. Contribution of protein-surface ion pairs of a hyperthermophilic protein on thermal and thermodynamic stability. J. Biosci. Bioeng. 97 (2004) 75-77
26. Huang S.L., Wu L.C., Huang H.D., Liang H.K., Ko M.T., and Horng J.T. A probabilistic method to correlate ion pairs with protein thermostability. Appl. Bioinformatics 3 (2004) 21-29
27. Dominy B.N., Minoux H., and Brooks III C.L. An electrostatic basis for the stability of thermophilic proteins. Proteins: Struct. Funct. Genet. 57 (2004) 128-141
28. Karlstrom M., Steen I.H., Madern D., Fedoy A.E., Birkeland N.K., and Ladenstein R. The crystal structure of a hyperthermostable subfamily II isocitrate dehydrogenase from Thermotoga maritima. FEBS J. 273 (2006) 2851-2868
29. Tanaka T., Sawano M., Ogasahara K., Sakaguchi Y., Bagautdinov B., Katoh E., et al. Hyper-thermostability of CutA1 protein, with a denaturation temperature of nearly 150 °C. FEBS Letters 580 (2006) 4224-4230
30. Ausili A., Cobucci-Ponzano B., Di Lauro B., D'Avino R., Perugino G., Bertoli E., et al. A comparative infrared spectroscopic study of glycoside hydrolases from extremophilic archaea revealed different molecular mechanisms of adaptation to high temperatures. Proteins: Struct. Funct. Genet. 67 (2007) 991-1001
31. He Y.Z., Fan K.Q., Jia C.J., Wang Z.J., Pan W.B., Huang L., et al. Characterization of a hyperthermostable Fe-superoxide dismutase from hot spring. Appl. Microbiol. Biotechnol. 75 (2007) 367-376
32. Dao-pin S., Anderson D.E., Baase W.A., Dahlquist F.W., and Matthews B.W. Structural and thermodynamic consequences of burying a charged residue within the hydrophobic core of T4 lysozyme. Biochemistry 30 (1991) 11521-11529
33. Waldburger C.D., Schildbach J.F., and Sauer R.T. Are buried salt-bridges important for protein stability and conformational specificity?. Nature Struct. Biol. 2 (1995) 122-128
34. DePrat Gay G., Johnson C.M., and 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
35. Marqusee S., and 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
36. Xiao L., and Honig B. Electrostatic contributions to the stability of hyperthermophilic proteins. J. Mol. Biol. 289 (1999) 1435-1444
37. Elcock A.H. The stability of salt-bridges at high temperatures: implications for hyperthermophilic proteins. J. Mol. Biol. 284 (1998) 489-502
38. de Bakker P.I., Hunenberger P.H., and McCammon J. A. Molecular dynamics simulations of the hyperthermophilic protein sac7d from Sulfolobus acidocaldarius: contribution of salt-bridges to thermostability. J. Mol. Biol. 285 (1999) 1811-1830
39. Kumar S., and Nussinov R. Relationship between ion pair geometries and electrostatic strengths in proteins. Biophys. J. 83 (2002) 1595-1612
40. Kawamura S., Tanaka I., Yamasaki N., and Kimura M. Contribution of a salt-bridge to the thermostability of DNA binding protein HU from Bacillus stearothermophilus determined by site-directed mutagenesis. J. Biochem. (Tokyo) 121 (1997) 448-455
41. Vetriani C., Maeder D.L., Tolliday N., Yip K.S., Stillman T.J., Britton K.L., et al. Protein thermostability above 100 °C: a key role for ionic interactions. Proc. Natl Acad. Sci. USA 95 (1998) 12300-12305
42. Lebbink J.H., Knapp S., van der Oost J., Rice D., Ladenstein R., and de Vos W.M. Engineering activity and stability of Thermotoga maritima glutamate dehydrogenase. II: construction of a 16-residue ion-pair network at the subunit interface. J. Mol. Biol. 289 (1999) 357-369
43. Fabry S., and Hensel R. Purification and characterization of D-glyceraldehyde-3-phosphate dehydrogenase from the thermophilic archaebacterium Methanothermus fervidus. Eur J. Biochem. 165 (1987) 147-155
44. Ermler U., Merckel M., Thauer R., and Shima S. Formylmethanofuran: tetrahydromethanopterin formyltransferase from Methanopyrus kandleri- new insights into salt-dependence and thermostability. Structure 5 (1997) 635-646
45. Oliveberg M., Vuilleumier S., and 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
46. Tan Y.-J., Oliveberg M., Davis B., and Fersht A. Perturbed pKa-values in the denatured states of proteins. J. Mol. Biol. 254 (1995) 980-992
47. Swint-Kruse L., and Robertson A.D. Hydrogen bonds and the pH dependence of ovomucoid third domain stability. Biochemistry 34 (1995) 4724-4732
48. Kuhlman B., Luisi D.L., Young P., and Raleigh D.P. pKa values and the pH dependent stability of the N-terminal domain of L9 as probes of electrostatic interactions in the denatured state. Differentiation between local and nonlocal interactions. Biochemistry 38 (1999) 4896-4903
49. Whitten S.T., and Garcia-Moreno E.B. pH dependence of stability of staphylococcal nuclease: evidence of substantial electrostatic interactions in the denatured state. Biochemistry 39 (2000) 14292-14304
50. Pace C.N., Alston R.W., and Shaw K.L. Charge-charge interactions influence the denatured state ensemble and contribute to protein stability. Protein Sci. 9 (2000) 1395-1398
51. Shaw K.L., Grimsley G.R., Yakovlev G.I., Makarov A.A., and Pace C.N. The effect of net charge on the solubility, activity, and stability of ribonuclease Sa. Protein Sci. 10 (2001) 1206-1215
52. a values for side-chain carboxyl groups of a PGB1 variant explain salt and pH-dependent stability. Biophys. J. 92 (2007) 257-266
53. Tollinger M., Crowhurst K.A., Kay L.E., and Forman-Kay J.D. Site-specific contributions to the pH dependence of protein stability. Proc. Natl Acad. Sci. USA 100 (2003) 4545-4550
54. Lee K.K., Fitch C.A., Lecomte J.T., and Garcia-Moreno E.B. Electrostatic effects in highly charged proteins: salt sensitivity of pKa values of histidines in staphylococcal nuclease. Biochemistry 41 (2002) 5656-5667
55. Grimsley G.R., Shaw K.L., Fee L.R., Alston R. W., Huyghues-Despointes B.M., Thurlkill R.L., et al. Increasing protein stability by altering long-range coulombic interactions. Protein Sci. 8 (1999) 1843-1849
56. Loladze V.V., Ibarra-Molero B., Sanchez-Ruiz J.M., and Makhatadze G.I. Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface. Biochemistry 38 (1999) 16419-16423
57. Spector S., Wang M., Carp S.A., Robblee J., Hendsch Z.S., Fairman R., et al. Rational modification of protein stability by the mutation of charged surface residues. Biochemistry 39 (2000) 872-879
58. Sanchez-Ruiz J.M., and Makhatadze G.I. To charge or not to charge?. Trends Biotechnol. 19 (2001) 132-135
59. Laurents D.V., Huyghues-Despointes B.M., Bruix M., Thurlkill R.L., Schell D., Newsom S., et al. Charge-charge interactions are key determinants of the pK values of ionizable groups in ribonuclease Sa (pI = 3.5) and a basic variant (pI = 10.2). J. Mol. Biol. 325 (2003) 1077-1092
60. Makhatadze G.I., Loladze V.V., Ermolenko D.N., Chen X., and Thomas S.T. Contribution of surface salt-bridges to protein stability: guidelines for protein engineering. J. Mol. Biol. 327 (2003) 1135-1148
61. Lee C.F., Makhatadze G.I., and Wong K.B. Effects of charge-to-alanine substitutions on the stability of ribosomal protein L30e from Thermococcus celer. Biochemistry 44 (2005) 16817-16825
62. Barlow D.J., and Thornton J.M. Ion-pairs in proteins. J. Mol. Biol. 168 (1983) 867-885
63. McCrary B.S., Edmondson S.P., and Shriver J.W. Hyperthermophile protein folding thermodynamics: differential scanning calorimetry and chemical denaturation of Sac7d. J. Mol. Biol. 264 (1996) 784-805
64. Clark A., McCrary B.S., Edmondson S., and Shriver J. Thermodynamics of core hydrophobicity and packing in the hyperthermophile proteins Sac7d and Sso7d. Biochemistry 43 (2004) 2840-2853
65. McCrary B.S., Bedell J., Edmondson S.P., and Shriver J.W. Linkage of protonation and anion binding to the folding of Sac7d. J. Mol. Biol. 276 (1998) 203-224
66. Edmondson S.P., Qiu L., and Shriver J.W. Solution structure of the DNA-binding protein Sac7d from the hyperthermophile Sulfolobus acidocaldarius. Biochemistry 34 (1995) 13289-13304
67. Baumann H., Knapp S., Lundbach T., Ladenstein R., and Hard T. Solution structure and DNA-binding properties of a thermostable protein from the archaeon Sulfolobus solfataricus. Nature Struct. Biol. 1 (1994) 808-819
68. 13C NMR. Biochemistry 35 (1996) 1-6
69. 1H-NMR titration shifts for studies of polypeptide conformation. Biopolymers 18 (1979) 299-311
70. Hermans J., and Scheraga H.A. Structural studies of ribonuclease. V. Reversible change of configuration. J. Am. Chem. Soc. 83 (1961) 3283-3292
71. Tanford C. Protein denaturation. Advan. Protein Chem. 23 (1968) 122-282
72. Hermans J., and Scheraga H.A. Structural studies of ribonuclease. VI. Abnormal ionizable groups. J. Am. Chem. Soc. 83 (1961) 3293-3300
73. Laskowski M.J., and Scheraga H.A. Thermodynamic considerations of protein reactions. I. Modified reactivity of polar groups. J. Am. Chem. Soc. 76 (1954) 6305-6319
74. Warshel A., and Russell S.T. Calculations of electrostatic interactions in biological systems and in solutions. Quart. Rev. Biophys. 17 (1984) 283-422
75. Giletto A., and Pace C.N. Buried, charged, non-ion-paired aspartic acid 76 contributes favorably to the conformational stability of ribonuclease T1. Biochemistry 38 (1999) 13379-13384
76. Joshi M.D., Sidhu G., Nielsen J.E., Brayer G.D., Withers S.G., and McIntosh L.P. Dissecting the electrostatic interactions and pH-dependent activity of a family 11 glycosidase. Biochemistry 40 (2001) 10115-10139
77. Garcia-Mayoral M.F., Perez-Canadillas J.M., Santoro J., Ibarra-Molero B., Sanchez-Ruiz J.M., Lacadena J., et al. Dissecting structural and electrostatic interactions of charged groups in alpha-sarcin. An NMR study of some mutants involving the catalytic residues. Biochemistry 42 (2003) 13122-13133
78. Thurlkill R.L., Grimsley G.R., Scholtz J.M., and Pace C.N. Hydrogen bonding markedly reduces the pK of buried carboxyl groups in proteins. J. Mol. Biol. 362 (2006) 594-604
79. Stigter D., Alonso D.O.V., and Dill K.A. Protein stability: electrostatics and compact denatured states. Proc. Natl Acad. Sci. USA 88 (1991) 4176-4180
80. Elcock A.H. Realistic modeling of the denatured states of proteins allows accurate calculations of the pH dependence of protein stability. J. Mol. Biol. 294 (1999) 1051-1062
81. Schutz C.N., and Warshel A. What are the dielectric "constants" of proteins and how to validate electrostatic models?. Proteins: Struct. Funct. Genet. 44 (2001) 400-417
82. Schaller W., and 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
83. Li H., Robertson A.D., and Jensen J.H. The determinants of carboxyl pKa values in turkey ovomucoid third domain. Proteins: Struct. Funct. Genet. 55 (2004) 689-704
84. a values. Proteins: Struct. Funct. Genet. 61 (2005) 704-721
85. Bundi A., and Wüthrich K. Proton NMR Parameters of the common amino acid residues measured in aqueous solution of the linear tetrapeptides H-Gly-Gly-X-L-Ala-OH. Biopolymers 18 (1979) 285-298
86. Consonni R., Arosio I., Belloni B., Fogolari F., Fusi P., Shehi E., and Zetta L. Investigations of Sso7d catalytic residues by NMR titration shifts and electrostatic calculations. Biochemistry 42 (2003) 1421-1429
87. a of acidic residues in lysozyme. J. Biochem. 118 (1995) 946-952
88. Kao Y.H., Fitch C.A., Bhattacharya S., Sarkisian C.J., Lecomte J.T., and Garcia-Moreno E.B. Salt effects on ionization equilibria of histidines in myoglobin. Biophys. J. 79 (2000) 1637-1654
89. Lee K.K., Fitch C.A., and Garcia-Moreno B. Distance dependence and salt sensitivity of pairwise, coulombic interactions in a protein. Protein Sci. 11 (2002) 1004-1016
90. a values in the ovomucoid third domain to charge replacement at a neighboring residue. Biochemistry 39 (2000) 8067-8072
91. Presta L.G., and Rose G.D. Helix signals in proteins. Science 240 (1988) 1632-1641
92. Aurora R., and Rose G.D. Helix capping. Protein Sci. 7 (1998) 21-38
93. Edmondson S.P., and Shriver J.W. DNA binding proteins Sac7d and Sso7d from Sulfolobus. Methods Enzymol. 334 (2001) 129-145
94. McAfee J., Edmondson S., Datta P., Shriver J., and 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
95. Markley J.L., Bax A., Arata Y., Hilbers C.W., Kaptein R., Sykes B.D., et al. Recommendations for the presentation of NMR structures of proteins and nucleic acids. J. Mol. Biol. 280 (1998) 933-952
96. Kay L.E., Keifer P., and Saarinen T. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114 (1992) 10663-10665
97. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1 beta. Biochemistry 28 (1989) 6150-6156
98. 13C-separated rotating frame Overhauser spectroscopy. J. Biomol. NMR 1 (1991) 13-22
99. 13C enriched proteins. J Biomol. NMR 1 (1991) 99-104
100. Kay L.E., Ikura M., Tschudin R., and Bax A. Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins. J. Magn. Reson. 89 (1990) 496-514
101. 15N spectra of proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29 (1990) 4659-4667
102. Wittekind M., and Mueller G.A. HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resoances in proteins. J. Magn. Reson. ser. B 101 (1993) 201-205
103. Muhandiram D.R., and Kay L.E. Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J. Magn. Reson. ser. B 103 (1994) 203-216
104. 13C magnetization. J. Magn. Reson. ser. B 101 (1993) 114-119
105. 2O samples of proteins. J. Magn. Reson. ser. B 101 (1993) 333-337
106. Wyman J., and Gill S.J. Binding and Linkage: Functional Chemistry of Biological Macromolecules (1990), University Science Books, Mill Valley, CA
107. Gao Y.G., Su S.Y., Robinson H., Padmanabhan S., Lim L., McCrary B.S., et al. The crystal structure of the hyperthermophile chromosomal protein Sso7d bound to DNA. Nature Struct. Biol. 5 (1998) 782-786
108. Krueger J.K., McCrary B.S., Wang A.H., Shriver J. W., Trewhella J., and Edmondson S.P. The solution structure of the Sac7d/DNA complex: a small-angle X-ray scattering study. Biochemistry 38 (1999) 10247-10255