A thermodynamic comparison of HPr proteins from extremophilic organisms

Biochemistry

Volumn 45, Issue 13, 2006, Pages 4084-4092

  Razvi, Abbas ^a   Scholtz, J Martin ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOCHEMISTRY; CONFORMATIONS; CORRELATION THEORY; SOLVENTS; THERMODYNAMIC STABILITY;

BACILLUS SUBTILIS (BS); EXTREMOPHILIC ORGANISMS; HISTIDINE CONTAINING PHOSPHOCARRIER PROTEIN (HPR); THERMAL DENATURATION;

PROTEINS;

BACTERIAL PROTEIN; PROTEIN HPR; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS; BACILLUS HALODURANS; BACILLUS SUBTILIS; ELECTRICITY; GEOBACILLUS STEAROTHERMOPHILUS; NONHUMAN; OCEANOBACILLUS IHEYENSIS; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STABILITY; STREPTOCOCCUS THERMOPHILUS; THERMODYNAMICS; THERMOSTABILITY;

AMINO ACID SEQUENCE; BACILLACEAE; BACILLUS; BACILLUS STEAROTHERMOPHILUS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CLONING, MOLECULAR; ENZYME STABILITY; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; PROTEIN CONFORMATION; PROTEIN DENATURATION; SEQUENCE ALIGNMENT; SODIUM CHLORIDE; STREPTOCOCCUS THERMOPHILUS; THERMODYNAMICS;

BACILLUS (BACTERIUM); BACILLUS HALODURANS; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); GEOBACILLUS STEAROTHERMOPHILUS; OCEANOBACILLUS IHEYENSIS; STREPTOCOCCUS THERMOPHILUS;

EID: 33645554971     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060038+     Document Type: Article

References (73)

1. Anfinsen, C. B., Haber, E., Sela, M., and White, F. H., Jr. (1961) The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain, Proc. Natl. Acad. Sci. U.S.A. 47, 1309-1314.
2. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains, Science 181, 223-230.
3. Sterner, R., and Liebl, W. (2001) Thermophilic adaptation of proteins, Crit. Rev. Biochem. Mol. Biol. 36, 39-106.
4. Jaenicke, R. (1998) What ultrastable globular proteins teach us about protein stabilization, Biochemistry (Moscow, Russ. Ed.) 63, 312-321.
5. Vieille, C., and Zeikus, J. G. (1996) Thermozymes: identifying molecular determinants of protein structural and functional stability, Trends Biotechnol. 14, 183-190.
6. Rees, D. C., and Adams, M. W. (1995) Hyperthermophiles: taking the heat and loving it, Structure 3, 251-254.
7. Somero, G. N. (1995) Proteins and temperature, Annu. Rev. Physiol. 57, 43-68.
8. Argos, P., Rossman, M. G., Grau, U. M., Zuber, H., Frank, G., and Tratschin, J. D. (1979) Thermal stability and protein structure, Biochemistry 18, 5698-5703.
9. Bougault, C. M., Eidsness, M. K., and Prestegard, J. H. (2003) Hydrogen bonds in rubredoxins from mesophilic and hyperthermophilic organisms, Biochemistry 42, 4357-4372.
10. Tanner, J. J., Hecht, R. M., and Krause, K. L. (1996) Determinants of enzyme thermostability observed in the molecular structure of Thermus aquaticus D-glyceraldehyde-3-phosphate dehydrogenase at 2.5 Å resolution, Biochemistry 35, 2597-2609.
11. Britton, K. L., Baker, P. J., Borges, K. M., Engel, P. C., Pasquo, A., Rice, D. W., Robb, F. T., Scandurra, R., Stillman, T. J., and Yip, K. S. (1995) Insights into thermal stability from a comparison of the glutamate dehydrogenases from Pyrococcus furiosus and Thermococcus litoralis, Eur. J. Biochem. 229, 688-695.
12. Perl, D., Mueller, U., Heinemann, U., and Schmid, F. X. (2000) Two exposed amino acid residues confer thermostability on a cold shock protein, Nat. Struct. Biol. 7, 380-383.
13. Criswell, A. R., Bae, E., Stec, B., Konisky, J., and Phillips, G. N., Jr. (2003) Structures of thermophilic and mesophilic adenylate kinases from the genus Methanococcus, J. Mol. Biol. 330, 1087-1099.
14. Petsko, G. A. (2001) Structural basis of thermostability in hyperthermophilic proteins, or "there's more than one way to skin a cat", Methods Enzymol. 334, 469-478.
15. Jaenicke, R. (1991) Protein stability and molecular adaptation to extreme conditions, Eur. J. Biochem. 202, 715-728.
16. Booth, I. R. (1985) Regulation of cytoplasmic pH in bacteria, Microbiol. Rev. 49, 359-378.
17. Yancey, P. H., Clark, M. E., Hand, S. C., Bowlus, R. D., and Somero, G. N. (1982) Living with water stress: evolution of osmolyte systems, Science 217, 1214-1222.
18. Timasheff, S. N. (1993) The control of protein stability and association by weak interactions with water: how do solvents affect these processes? Annu. Rev. Biophys. Biomol. Struct. 22, 67-97.
19. Timasheff, S. N. (2002) Protein hydration, thermodynamic binding, and preferential hydration, Biochemistry 41, 13473-13482.
20. Horikoshi, K. (1999) Alkaliphiles: some applications of their products for biotechnology, Microbiol. Mol. Biol. Rev. 63, 735-750.
21. Vieille, C., and Zeikus, G. J. (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability, Microbiol. Mol. Biol. Rev. 65, 1-43.
22. Arnold, F. H., Wintrode, P. L., Miyazaki, K., and Gershenson, A. (2001) How enzymes adapt: lessons from directed evolution, Trends Biochem. Sci. 26, 100-106.
23. Wintrode, P. L., and Arnold, F. H. (2000) Temperature adaptation of enzymes: lessons from laboratory evolution, Adv. Protein Chem. 55, 161-225.
24. Van den Burg, B., Vriend, G., Veltman, O. R., Venema, G., and Eijsink, V. G. (1998) Engineering an enzyme to resist boiling, Proc. Natl. Acad. Sci. U.S.A. 95, 2056-2060.
25. Hollien, J., and Marqusee, S. (1999) A thermodynamic comparison of mesophilic and thermophilic ribonucleases H, Biochemistry 38, 3831-3836.
26. Deutschman, W. A., and Dahlquist, F. W. (2001) Thermodynamic basis for the increased thermostability of CheY from the hyperthermophile Thermotoga maritima, Biochemistry 40, 13107-13113.
27. Lee, C. F., Allen, M. D., Bycroft, M., and Wong, K. B. (2005) Electrostatic interactions contribute to reduced heat capacity change of unfolding in a thermophilic ribosomal protein 130e, J. Mol. Biol. 348, 419-431.
28. Cheung, Y. Y., Lam, S. Y., Chu, W. K., Allen, M. D., Bycroft, M., and Wong, K. B. (2005) Crystal structure of a hyperthermophilic archaeal acylphosphatase from Pyrococcus horikoshii-structural insights into enzymatic catalysis, thermostability, and dimerization, Biochemistry 44, 4601-4611.
29. Kreig, N. R., and Holt, J. G. (1984) Bergey's Manual of Systematic Bacteriology, 1st ed., Vol. 2, Williams & Wilkins, Baltimore, MD.
30. Esser, A. F., and Souza, K. A. (1974) Correlation between thermal death and membrane fluidity in Bacillus stearothermophilus, Proc. Natl. Acad. Sci. U.S.A. 71, 4111-4115.
31. Takami, H., Nakasone, K., Takaki, Y., Maeno, G., Sasaki, R., Masui, N., Fuji, F., Hirama, C., Nakamura, Y., Ogasawara, N., Kuhara, S., and Horikoshi, K. (2000) Complete genome sequence of the alkaliphilic bacteriumBacillus halodurans and genomic sequence comparison with Bacillus subtilis, Nucleic Acids Res. 28, 4317-4331.
32. Takami, H., and Horikoshi, K. (1999) Reidentification of facultatively alkaliphilic Bacillus sp. C-125 to Bacillus halodurans, Biosci. Biotechnol. Biochem. 63, 943-945.
33. Lu, J., Nogi, Y., and Takami, H. (2001) Oceanobacillus iheyensis gen. nov., sp. nov., a deep-sea extremely halotolerant and alkaliphilic species isolated from a depth of 1050 m on the Iheya Ridge, FEMS Microbiol. Lett. 205, 291-297.
34. Meadow, N. D., Fox, D. K., and Roseman, S. (1990) The bacterial phosphoenolpyruvate: glycose phosphotransferase system, Annu. Rev. Biochem. 59, 497-542.
35. Scholtz, J. M. (1995) Conformational stability of HPr: the histidine-containing phosphocarrier protein from Bacillus subtilis, Protein Sci. 4, 35-43.
36. Nicholson, E. M., and Scholtz, J. M. (1996) Conformational stability of the Escherichia coli HPr protein: test of the linear extrapolation method and a thermodynamic characterization of cold denaturation, Biochemistry 35, 11369-11378.
37. Van Nuland, N. A., Meijberg, W., Warner, J., Forge, V., Scheek, R. M., Robillard, G. T., and Dobson, C. M. (1998) Slow cooperative folding of a small globular protein HPr, Biochemistry 37, 622-637.
38. Sridharan, S., Razvi, A., Scholtz, J. M., and Sacchettini, J. C. (2005) The HPr proteins from the thermophile Bacillus stearothermophilus can form domain-swapped dimers, J. Mol. Biol. 346, 919-931.
39. Herzberg, O., Reddy, P., Sutrina, S., Saier, M. H., Jr., Reizer, J., and Kapadia, G. (1992) Structure of the histidine-containing phosphocarrier protein HPr from Bacillus subtilis at 2.0 Å resolution, Proc. Natl. Acad. Sci. U.S.A. 89, 2499-2503.
40. Anderson, J. W., Bhanot, P., Georges, F., Klevit, R. E., and Waygood, E. B. (1991) Involvement of the carboxy-terminal residue in the active site of the histidine-containing protein, HPr, of the phosphoenolpyruvate: sugar phosphotransferase system of Escherichia coli, Biochemistry 30, 9601-9607.
41. Lai, X., and Ingram, L. O. (1995) Discovery of a ptsHI operon, which includes a third gene (ptsT), in the thermophile Bacillus stearothermophilus, Microbiology 141 (Pt. 6), 1443-1449.
42. Howorka, S., and Bayley, H. (1998) Improved protocol for high-throughput cysteine scanning mutagenesis, BioTechniques 25, 764-772.
43. Kalia, A., Rattan, A., and Chopra, P. (1999) A method for extraction of high-quality and high-quantity genomic DNA generally applicable to pathogenic bacteria, Anal. Biochem. 275, 1-5.
44. Waygood, E. B., Reiche, B., Hengstenberg, W., and Lee, J. S. (1987) Characterization of mutant histidine-containing proteins of the phosphoenolpyruvate:sugar phosphotransferase system of Escherichia coli and Salmonella typhimurium, J. Bacteriol. 169, 2810-2818.
45. Grimsley, G. R., Huyghues-Despointes, B. M. P., Pace, C. N., and Scholtz, J. M. (2003) Measuring the conformational stability of a protein, in Purifying Proteins for Proteomics: A Laboratory Manual (Simpson, R. J., Ed.) pp 535-566, Cold Spring Harbor Press, Cold Spring Harbor, NY.
46. Becktel, W. J., and Schellman, J. A. (1987) Protein stability curves, Biopolymers 26, 1859-1877.
47. Pace, C. N., and Laurents, D. V. (1989) A new method for determining the heat capacity change for protein folding, Biochemistry 28, 2520-2525.
48. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22, 4673-4680.
49. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling, Electrophoresis 18, 2714-2723.
50. Nojima, H., Ikai, A., Oshima, T., and Noda, H. (1977) Reversible thermal unfolding of thermostable phosphoglycerate kinase. Thermostability associated with mean zero enthalpy change, J. Mol. Biol. 116, 429-442.
51. Li, W. T., Grayling, R. A., Sandman, K., Edmondson, S., Shriver, J. W., and Reeve, J. N. (1998) Thermodynamic stability of archaeal histones, Biochemistry 37, 10563-10572.
52. Somero, G. N. (1978) Temperature adaptation of enzymes-biological optimization through structure-function compromises, Annu. Rev. Ecol. Syst. 9, 1-29.
53. Zavodszky, P., Kardos, J., Svingor, and Petsko, G. A. (1998) Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins, Proc. Natl. Acad. Sci. U.S.A. 95, 7406-7411.
54. Jaenicke, R. (2000) Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc. Natl. Acad. Sci. U.S.A. 97, 2962-2964.
55. Akke, M. (2004) Out of hot water, Nat. Struct. Mol. Biol. 11, 912-913.
56. Wolf-Watz, M., Thai, V., Henzler-Wildman, K., Hadjipavlou, G., Eisenmesser, E. Z., and Kern, D. (2004) Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair, Nat. Struct. Mol. Biol. 11, 945-949.
57. Eisenmesser, E. Z., Millet, O., Labeikovsky, W., Korzhnev, D. M., Wolf-Watz, M., Bosco, D. A., Skalicky, J. J., Kay, L. E., and Kern, D. (2005) Intrinsic dynamics of an enzyme underlies catalysis, Nature 438, 117-121.
58. Varley, P. G., and Pain, R. H. (1991) Relation between stability, dynamics and enzyme activity in 3-phosphoglycerate kinases from yeast and Thermus thermophilus, J. Mol. Biol. 220, 531-538.
59. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding, Protein Sci. 4, 2138-2148.
60. Guzman-Casado, M., Parody-Morreale, A., Robic, S., Marqusee, S., and Sanchez-Ruiz, J. M. (2003) Energetic evidence for formation of a pH-dependent hydrophobic cluster in the denatured state of Thermus thermophilus ribonuclease H, J. Mol. Biol. 329, 731-743.
61. Robic, S., Guzman-Casado, M., Sanchez-Ruiz, J. M., and Marqusee, S. (2003) Role of residual structure in the unfolded state of a thermophilic protein, Proc. Natl. Acad. Sci. U.S.A. 100, 11345-11349.
62. Chakravarty, S., and Varadarajan, R. (2002) Elucidation of factors responsible for enhanced thermal stability of proteins: a structural genomics based study, Biochemistry 41, 8152-8161.
63. Szilagyi, A., and Zavodszky, P. (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey, Structure 8, 493-504.
64. Karshikoff, A., and Ladenstein, R. (2001) Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads, Trends Biochem. Sci. 26, 550-556.
65. Xiao, L., and Honig, B. (1999) Electrostatic contributions to the stability of hyperthermophilic proteins, J. Mol. Biol. 289, 1435-1444.
66. Spassov, V. Z., Karshikoff, A. D., and Ladenstein, R. (1995) The optimization of protein-solvent interactions: thermostability and the role of hydrophobic and electrostatic interactions, Protein Sci. 4, 1516-1527.
67. Perutz, M. F. (1978) Electrostatic effects in proteins, Science 201, 1187-1191.
68. Elcock, A. H. (1998) The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins, J. Mol. Biol. 284, 489-502.
69. Fukuchi, S., Yoshimune, K., Wakayama, M., Moriguchi, M., and Nishikawa, K. (2003) Unique amino acid composition of proteins in halophilic bacteria, J. Mol. Biol. 327, 347-357.
70. Kuntz, I. D., Jr., and Kauzmann, W. (1974) Hydration of proteins and polypeptides, Adv. Protein Chem. 28, 239-345.
71. Dym, O., Mevarech, M., and Sussman, J. L. (1995) Structural features that stabilize halophilic malate dehydrogenase from an archaebacterium, Science 267, 1344-1346.
72. Rao, J. K., and Argos, P. (1981) Structural stability of halophilic proteins, Biochemistry 20, 6536-6543.
73. Kohn, W. D., Kay, C. M., and Hodges, R. S. (1995) Protein destabilization by electrostatic repulsions in the two-stranded alpha-helical coiled-coil/leucine zipper, Protein Sci. 4, 237-250.