How do thermophilic proteins and proteomes withstand high temperature?

Biophysical Journal

Volumn 101, Issue 1, 2011, Pages 217-227

  Sawle, Lucas ^a   Ghosh, Kingshuk ^a  

^a UNIVERSITY OF DENVER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME;

ARTICLE; BACTERIUM; CHEMISTRY; ENTROPY; GROWTH, DEVELOPMENT AND AGING; HEAT; METABOLISM; PROTEIN FOLDING; PROTEIN STABILITY; STRUCTURAL HOMOLOGY;

BACTERIA; ENTROPY; HOT TEMPERATURE; PROTEIN FOLDING; PROTEIN STABILITY; PROTEOME; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 80052449370     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.05.059     Document Type: Article

References (72)

1. S. Kumar, and R. Nussinov How do thermophilic proteins deal with heat? Cell. Mol. Life Sci. 58 2001 1216 1233 (Pubitemid 32844095)
2. A. Razvi, and J.M. Scholtz Lessons in stability from thermophilic proteins Protein Sci. 15 2006 1569 1578
3. R. Jaenicke Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc. Natl. Acad. Sci. USA 97 2000 2962 2964 (Pubitemid 30183236)
4. J.L. England, B.E. Shakhnovich, and E.I. Shakhnovich Natural selection of more designable folds: a mechanism for thermophilic adaptation Proc. Natl. Acad. Sci. USA 100 2003 8727 8731 (Pubitemid 36899166)
5. I.N. Berezovsky, and E.I. Shakhnovich Physics and evolution of thermophilic adaptation Proc. Natl. Acad. Sci. USA 102 2005 12742 12747 (Pubitemid 41279436)
6. R. Ladenstein Heat capacity, configurational entropy, and the role of ionic interactions in protein thermostability Biotechnol., Biotechnol. Equip. 22 2008 612 619 (Pubitemid 351422063)
7. M. Mevarech, F. Frolow, and L.M. Gloss Halophilic enzymes: proteins with a grain of salt Biophys. Chem. 86 2000 155 164 (Pubitemid 30665604)
8. R. Jaenicke, and G. Böhm The stability of proteins in extreme environments Curr. Opin. Struct. Biol. 8 1998 738 748 (Pubitemid 29004672)
9. S. Kumar, C.J. Tsai, and R. Nussinov Thermodynamic differences among homologous thermophilic and mesophilic proteins Biochemistry 40 2001 14152 14165 (Pubitemid 33081618)
10. R. Singleton Jr. , and R.E. Amelunxen Proteins from thermophilic microorganisms Bacteriol. Rev. 37 1973 320 342
11. H.X. Zhou Toward the physical basis of thermophilic proteins: linking of enriched polar interactions and reduced heat capacity of unfolding Biophys. J. 83 2002 3126 3133
12. A. Razvi, and J.M. Scholtz A thermodynamic comparison of HPr proteins from extremophilic organisms Biochemistry 45 2006 4084 4092
13. S. Robic, and M. Guzman-Casado S. Marqusee Role of residual structure in the unfolded state of a thermophilic protein Proc. Natl. Acad. Sci. USA 100 2003 11345 11349 (Pubitemid 37205937)
14. K. Ratcliff, J. Corn, and S. Marqusee Structure, stability, and folding of ribonuclease H1 from the moderately thermophilic Chlorobium tepidum: comparison with thermophilic and mesophilic homologues Biochemistry 48 2009 5890 5898
15. H. Fu, and G. Grimsley C.N. Pace Increasing protein stability: importance of ΔC(p) and the denatured state Protein Sci. 19 2010 1044 1052
16. G. Graziano Is there a relationship between protein thermal stability and the denaturation heat capacity change? J. Therm. Anal. Calorim. 93 2008 429 438
17. B.W. Matthews, H. Nicholson, and W.J. Becktel Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding Proc. Natl. Acad. Sci. USA 84 1987 6663 6667
18. C. Liu, Y. Yang, and V. Licata Thermodynamic and structural origins for the extreme stability of Taq DNA polymerase Biophys. J. 96 2009 330a
19. M. Wallgren, and J. Adén M. Wolf-Watz Extreme temperature tolerance of a hyperthermophilic protein coupled to residual structure in the unfolded state J. Mol. Biol. 379 2008 845 858
20. J. Fitter, and S. Haber-Pohlmeier Structural stability and unfolding properties of thermostable bacterial α-amylases: a comparative study of homologous enzymes Biochemistry 43 2004 9589 9599 (Pubitemid 38993809)
21. K.A. Scott, and D.O. Alonso V. Daggett Conformational entropy of alanine versus glycine in protein denatured states Proc. Natl. Acad. Sci. USA 104 2007 2661 2666 (Pubitemid 46327936)
22. I. Berezovsky, W. Chen, P. Choi, and E. Shakhnovich Entropic stabilization of proteins and its proteomic consequences PLOS Comput. Biol. 1 2005 e47
23. A.H. Elcock The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins J. Mol. Biol. 284 1998 489 502 (Pubitemid 28542468)
24. J.-H. Cho, S. Sato, and D.P. Raleigh Thermodynamics and kinetics of non-native interactions in protein folding: a single point mutant significantly stabilizes the N-terminal domain of L9 by modulating non-native interactions in the denatured state J. Mol. Biol. 338 2004 827 837 (Pubitemid 38507425)
25. M. Ge, X.-Y. Xia, and X.-M. Pan Salt bridges in the hyperthermophilic protein Ssh10b are resilient to temperature increases J. Biol. Chem. 283 2008 31690 31696
26. S. Kumar, C.J. Tsai, and R. Nussinov Factors enhancing protein thermostability Protein Eng. 13 2000 179 191 (Pubitemid 30237592)
27. S. Kumar, B. Ma, C. Tsai, and R. Nussinov Electrostatic strengths of salt bridges in thermophilic and mesophilic glutamate dehydrogenase monomers Proteins 38 2000 368 383 (Pubitemid 30112440)
28. B.N. Dominy, and D. Perl C.L. Brooks 3rd The effects of ionic strength on protein stability: the cold shock protein family J. Mol. Biol. 319 2002 541 554 (Pubitemid 34729478)
29. B.N. Dominy, H. Minoux, and C.L. Brooks 3rd An electrostatic basis for the stability of thermophilic proteins Proteins 57 2004 128 141 (Pubitemid 39195889)
30. C.F. Lee, and M.D. Allen K.B. Wong Electrostatic interactions contribute to reduced heat capacity change of unfolding in a thermophilic ribosomal protein l30e J. Mol. Biol. 348 2005 419 431 (Pubitemid 40462106)
31. V. Rosato, N. Pucello, and G. Giuliano Evidence for cysteine clustering in thermophilic proteomes Trends Genet. 18 2002 278 281 (Pubitemid 34607109)
32. S. Chakravarty, and R. Varadarajan Elucidation of factors responsible for enhanced thermal stability of proteins: a structural genomics based study Biochemistry 41 2002 8152 8161 (Pubitemid 34655184)
33. R. Das, and M. Gerstein The stability of thermophilic proteins: a study based on comprehensive genome comparison Funct. Integr. Genomics. 1 2000 76 88
34. G. Saelensminde, O. Halskau Jr. , and I. Jonassen Amino acid contacts in proteins adapted to different temperatures: hydrophobic interactions and surface charges play a key role Extremophiles 13 2009 11 20
35. U. Bastolla, and L. Demetrius Stability constraints and protein evolution: the role of chain length, composition and disulfide bonds Protein Eng. Des. Sel. 18 2005 405 415 (Pubitemid 41219887)
36. J. Gu, and V.J. Hilser Sequence-based analysis of protein energy landscapes reveals nonuniform thermal adaptation within the proteome Mol. Biol. Evol. 26 2009 2217 2227
37. A.D. Robertson, and K.P. Murphy Protein structure and the energetics of protein stability Chem. Rev. 97 1997 1251 1268
38. K. Ghosh, and K.A. Dill Computing protein stabilities from their chain lengths Proc. Natl. Acad. Sci. USA 106 2009 10649 10654
39. P.L. Privalov, and N.N. Khechinashvili A thermodynamic approach to the problem of stabilization of globular protein structure: a calorimetric study J. Mol. Biol. 86 1974 665 684
40. P.L. Privalov Stability of proteins: small globular proteins Adv. Protein Chem. 33 1979 167 241
41. R.L. Baldwin Temperature dependence of the hydrophobic interaction in protein folding Proc. Natl. Acad. Sci. USA 83 1986 8069 8072 (Pubitemid 17182445)
42. A.J. Doig, and D.H. Williams Why water-soluble, compact, globular proteins have similar specific enthalpies of unfolding at 110 degrees C Biochemistry 31 1992 9371 9375
43. K.P. Murphy, P.L. Privalov, and S.J. Gill Common features of protein unfolding and dissolution of hydrophobic compounds Science 247 1990 559 561
44. L. Fu, and E. Freire On the origin of the enthalpy and entropy convergence temperatures in protein folding Proc. Natl. Acad. Sci. USA 89 1992 9335 9338
45. K.P. Murphy, and S.J. Gill Solid model compounds and the thermodynamics of protein unfolding J. Mol. Biol. 222 1991 699 709
46. J. Hollien, and S. Marqusee Structural distribution of stability in a thermophilic enzyme Proc. Natl. Acad. Sci. USA 96 1999 13674 13678
47. S. Kumar, and R. Nussinov Experiment-guided thermodynamic simulations on reversible two-state proteins: implications for protein thermostability Biophys. Chem. 111 2004 235 246 (Pubitemid 39389142)
48. S. Kumar, C.J. Tsai, and R. Nussinov Temperature range of thermodynamic stability for the native state of reversible two-state proteins Biochemistry 42 2003 4864 4873 (Pubitemid 36532038)
49. K. Shiraki, and S. Nishikori T. Imanaka Comparative analyses of the conformational stability of a hyperthermophilic protein and its mesophilic counterpart Eur. J. Biochem. 268 2001 4144 4150 (Pubitemid 32862874)
50. C.-H. Chen, and L. Roth D. Berns Thermodynamics elucidation of the structural stability of a thermophilic protein Biophys. Chem. 50 1994 313 321 (Pubitemid 24167294)
51. K. Ghosh, and K. Dill Cellular proteomes have broad distributions of protein stability Biophys. J. 99 2010 3996 4002
52. J. Zhang Protein-length distributions for the three domains of life Trends Genet. 16 2000 107 109 (Pubitemid 30122341)
53. P. Chen, and E.I. Shakhnovich Thermal adaptation of viruses and bacteria Biophys. J. 98 2010 1109 1118
54. D.A. Ratkowsky, J. Olley, and T. Ross Unifying temperature effects on the growth rate of bacteria and the stability of globular proteins J. Theor. Biol. 233 2005 351 362 (Pubitemid 40093594)
55. J. Clarke, and A.M. Hounslow V. Daggett The effects of disulfide bonds on the denatured state of barnase Protein Sci. 9 2000 2394 2404 (Pubitemid 32105722)
56. C.N. Pace, R.W. Alston, and K.L. Shaw Charge-charge interactions influence the denatured state ensemble and contribute to protein stability Protein Sci. 9 2000 1395 1398 (Pubitemid 30602294)
57. D. Shortle, H.S. Chan, and K.A. Dill Modeling the effects of mutations on the denatured states of proteins Protein Sci. 1 1992 201 215 (Pubitemid 23007287)
58. K.A. Dill, and D. Shortle Denatured states of proteins Annu. Rev. Biochem. 60 1991 795 825
59. S. Miyazawa, and R.L. Jernigan Protein stability for single substitution mutants and the extent of local compactness in the denatured state Protein Eng. 7 1994 1209 1220 (Pubitemid 24319399)
60. D. Shortle The denatured state (the other half of the folding equation) and its role in protein stability FASEB J. 10 1996 27 34 (Pubitemid 26035503)
61. D. Shortle, and M.S. Ackerman Persistence of native-like topology in a denatured protein in 8 M urea Science 293 2001 487 489 (Pubitemid 32679075)
62. K. Lindorff-Larsen, and S. Kristjansdottir M. Vendruscolo Determination of an ensemble of structures representing the denatured state of the bovine acyl-coenzyme a binding protein J. Am. Chem. Soc. 126 2004 3291 3299 (Pubitemid 38380732)
63. B.E. Bowler Thermodynamics of protein denatured states Mol. Biosyst. 3 2007 88 99 (Pubitemid 46155471)
64. C. Nick Pace, and B.M. Huyghues-Despointes G.R. Grimsley Urea denatured state ensembles contain extensive secondary structure that is increased in hydrophobic proteins Protein Sci. 19 2010 929 943
65. K. Watanabe, and Y. Suzuki Protein thermostabilization by proline substitutions J. Mol. Catal. B. Enzym. 4 1998 167 180 (Pubitemid 28303932)
66. S.R. Trevino, and S. Schaefer C.N. Pace Increasing protein conformational stability by optimizing beta-turn sequence J. Mol. Biol. 373 2007 211 218 (Pubitemid 47390718)
67. G. Nemethy, S. Leach, and H. Scheraga The influence of amino acid side chains on the free energy of helix-coil transitions J. Phys. Chem. 70 1966 998 1004
68. A.J. Rader Thermostability in rubredoxin and its relationship to mechanical rigidity Phys. Biol. 7 2009 16002
69. D.R. Livesay, and D.J. Jacobs Conserved quantitative stability/ flexibility relationships (QSFR) in an orthologous RNase H pair Proteins 62 2006 130 143 (Pubitemid 43063011)
70. K. Dietz Darwinian fitness, evolutionary entropy and directionality theory Bioessays 27 2005 1097 1101 (Pubitemid 43076135)
71. L. Demetrius, S. Legendre, and P. Harremöes Evolutionary entropy: a predictor of body size, metabolic rate and maximal life span Bull. Math. Biol. 71 2009 800 818
72. D. Benson, I. Karsch-Mizrachi, D. Lipman, J. Ostell, and D. Wheeler GenBank Nucleic Acids Res. 31 2005 23 27