Evolution and thermodynamics of the slow unfolding of hyperstable monomeric proteins

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Okada, Jun ^a   Okamoto, Tomohiro ^a   Mukaiyama, Atsushi ^a   Tadokoro, Takashi ^a   You, Dong Ju ^a   Chon, Hyongi ^a   Koga, Yuichi ^a   Takano, Kazufumi ^a,b   Kanaya, Shigenori ^a  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENETIC ANALYSIS; PROTEIN; THERMODYNAMICS;

AQUIFEX AEOLICUS; ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SULFOLOBUS; SULFOLOBUS TOKODAII; THERMOCOCCUS; THERMOCOCCUS KODAKARENSIS; THERMOTOGA MARITIMA; THERMUS THERMOPHILUS;

ARCHAEAL PROTEIN; BACTERIAL PROTEIN; RIBONUCLEASE H; RIBONUCLEASE HI; RIBONUCLEASE HII;

ARTICLE; CIRCULAR DICHROISM; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SULFOLOBUS; TEMPERATURE; THERMODYNAMICS; THERMOTOGA MARITIMA;

ARCHAEAL PROTEINS; BACTERIAL PROTEINS; CIRCULAR DICHROISM; EVOLUTION, MOLECULAR; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASE H; SULFOLOBUS; TEMPERATURE; THERMODYNAMICS; THERMOTOGA MARITIMA;

EID: 77954338351     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-207     Document Type: Article

References (68)

1. The stability of proteins in extreme environments. R Jaenicke G Bohm, Curr Opin Struct Biol 1998 8 738 748 10.1016/S0959-440X(98)80094-8 9914256
2. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. C Vieille GJ Zeikus, Microbiol Mol Biol Rev 2001 65 1 43 10.1128/MMBR.65.1.1-43.2001 11238984
3. Some like it hot: The molecular determinants of protein thermostability. D Perl FX Schmid, ChemBioChem 2002 3 39 44 10.1002/1439-7633(20020104)3:1<39: :AID-CBIC39>3.0.CO;2-D 17590951
4. Lessons in stability from thermophilic proteins. A Razvi JM Scholtz, Protein Sci 2006 15 1569 1578 10.1110/ps.062130306 16815912
5. Kinetic role of electrostatic interactions in the unfolding of hyperthermophilic and mesophilic rubredoxins. S Cavagnero DA Debe ZH Zhou MWW Adams SI Chan, Biochemsitry 1998 37 3369 3376 10.1021/bi9721795 (Pubitemid 28125564)
6. The unusually slow unfolding rate causes the high stability of pyroolidone carboxyl peptidase from a hyperthermophilile Pyrococcus furiosus: Equilibrium and kinetic studies of guanidine hydrochloride-induced unfolding and refolding. K Ogasahara M Nakamura S Nakura S Tsunasawa I Kato T Yoshimoto K Yutani, Biochemistry 1998 37 17537 17544 10.1021/bi9814585 9860869
7. Stability and folding of dihydrofolate reductase from the hyperthermophilic bacterium Thermotoga maritima. T Dams R Jaenicke, Biochemistry 1999 38 9169 9178 10.1021/bi990635e 10413491
8. The unusually slow relaxation kinetics of the folding-unfolding of pyrrolidone carboxyl peptidase from a hyperthermophile. Pyrococcus furiosus. JK Kaushik K Ogasahara K Yutani, J Mol Biol 2002 316 991 1003 10.1006/jmbi.2001. 5355 11884137
9. Energetic landscape of alpha-lytic protease optimizes longevity through kinetic stability. SS Jaswal JL Sohl JH Dans DA Agard, Nature 2002 415 343 346 10.1038/415343a 11797014
10. Unusually slow denaturation and refolding process of pyrrolidone carcoxyl peptidase from a hyper-thermophile are highly cooperative: Real-time NMR studies. S Iimura H Yagi K Ogasahara H Akutsu Y Noda S Segawa K Yutani, Biochemistry 2004 43 11906 11915 10.1021/bi048762k 15362877
11. Folding and association of an extremely stable dimeric protein from Sulfolobus islandicus. M Zeeb G Lipps H Lilie J Balbach, J Mol Biol 2004 336 227 240 10.1016/j.jmb.2003.12.003 14741218
12. Kinetic stability and crystal structure of the viral capside protein SHP. P Forrer C Chang D Ott A Wlodawer A Plückthun, J Mol Biol 2004 344 179 193 10.1016/j.jmb.2004.09.030 15504410
13. Slow unfolding explains high stability of thermostable ferredoxins: common mechanism governing thermostability? P Wittung-Stafshede, Biochim Biophys Acta 2004 1700 1 4 15210118
14. Thermostability of irreversible unfolding alpha-amylases analyzed by unfolding kinetics. C Duy J Fitter, J Biol Chem 2005 280 37360 37365 10.1074/jbc.M507530200 16150692
15. Completely buried, non-ion-paired glutamic acid contributes favorably to the conformational stability of pyrrolidone carboxyl peptidases from hyperthermophiles. JK Kaushik S Iimura K Ogasahara Y Yamagata S Segawa K Yutani, Biochemistry 2006 45 7100 7112 10.1021/bi052610n 16752900
16. A conformationally isoformic thermophilic protein with high kinetic unfolding barriers. R Mishra L Olofsson M Karlsson U Carlsson IA Nicholls P Hammarström, Cell Mol Life Sci 2008 65 827 839 10.1007/s00018-008-7517-4 18217202
17. Between-species variation in the kinetic stability of TIM proteins linked to solvation-barrier free energies. M Costas D Rodríguez-Larrea L De Maria TV Borchert A Gámez-Puyou JM Sanchez-Ruiz, J Mol Biol 2009 385 924 937 10.1016/j.jmb.2008.10.056 18992756
18. Hydrophobic effect on the stability and folding of a hyperthermophilic protein. H Dong A Mukaiyama T Tadokoro Y Koga K Takano S Kanaya, J Mol Biol 2008 378 264 272 10.1016/j.jmb.2008.02.039 18353366
19. Kinetically robust monomeric protein from a hyperthermophile. A Mukaiyama K Takano M Haruki M Morikawa S Kanaya, Biochemistry 2004 43 13859 13866 10.1021/bi0487645 15504048
20. A thermodynamic comparison of mesophilic and thermophilic ribonucleases H. J Hollien S Marqusee, Biochemistry 1999 38 3831 3836 10.1021/bi982684h 10090773
21. Comparison of the folding processes of T. thermophilus and E. coli ribonucleases H. J Hollien S Marqusee, J Mol Biol 2002 316 327 340 10.1006/jmbi.2001.5346 11851342
22. Thermodynamic stability and folding of proteins from hyperthermophilic organisms. KA Luke CL Higgins P Wittung-Stafshede, FEBS J 2007 274 4023 4033 10.1111/j.1742-4658.2007.05955.x 17683332
23. Slow unfolding of monomeric proteins from hyperthermophiles with reversible unfolding. A Mukaiyama K Takano, Int J Mol Sci 2009 10 1369 1385 10.3390/ijms10031369 19399254
24. Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. D Perl C Welker T Schindler K Schröder MA Marahiel R Janicke FX Schmid, Nature Struct Biol 1998 5 229 235 10.1038/nsb0398-229 9501917
25. The effect of ionic strength on protein stability: The cold shock protein family. BN Dominy D Perl FX Schmid CLIII Brooks, J Mol Biol 2002 319 541 554 10.1016/S0022-2836(02)00259-0 12051927
26. Role of entropy in protein thermostability: folding kinetics of a hyperthermophilic cold shock protein at high temperatures using 19F NMR. B Schuler W Kremer HR Kalbitzer R Jaenicke, Biochemistry 2002 41 11670 11680 10.1021/bi026293l 12269809
27. Extreme temperature tolerance of a hyperthermophilic protein coupled to residual structure in the unfolded state. M Wallgren J Adén O Pylypenko T Mikaelsson LB Johansson A Rak M Wolf-Watz, J Mol Biol 2008 379 845 858 10.1016/j.jmb.2008.04.007 18471828
28. 2+-dependent RNase HIII from Bacillus subtilis: Classification of RNase H into these families. N Ohtani M Haruki M Morikawa RJ Crouch M Itaya S Kanaya, Biochemistry 1999 38 605 618 10.1021/bi982207z 9888800
29. Molecular diversities of RNase H. N Ohtani M Haruki M Morikawa S Kanaya, J Biosci Bioeng 1999 88 12 19 10.1016/S1389-1723(99)80168-6 16232566
30. Recombining the structures of HIV integrase, RuvC and RNase H. W Yang TA Steitz, Structure 1995 3 131 134 10.1016/S0969-2126(01)00142-3 7735828
31. Folding pathway of Escherichia coli ribonucrease H: A circular dichroism, fluorescence and NMR study. K Yamasaki K Ogasahara K Yutani M Oobatake S Kanaya, Biochemistry 1995 34 16552 16562 10.1021/bi00051a003 8527428
32. Structural and thermodynamic analyses of Escherichia coli RNase HI variant with quintuple thermostabilizing mutations. M Haruki M Tanaka T Motegi T Tadokoro Y Koga K Takano S Kanaya, FEBS J 2007 274 5815 5825 10.1111/j.1742-4658.2007.06104.x 17944939
33. The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions. TM Raschke S Marqusee, Naure Struct Biol 1997 4 298 304 10.1038/nsb0497-298 (Pubitemid 27157202)
34. Confirmation of the hierarchical folding of RNase H: A protein engineering study. TM Raschke J Kho S Marqusee, Naure Struct Biol 1999 6 825 831 10.1038/12277 (Pubitemid 29415173)
35. Destabilization of the Escherichia coli RNase H kinetic intermediate: Switching between a two-state and three-state folding mechanism. GM Spudich EJ Miller S Marquesee, J Mol Biol 2004 335 609 618 10.1016/j.jmb.2003.10.052 14672667
36. The high-resolution NMR structure of the early folding intermediate of the Thermus thermophilus ribonuclease H. Z Zhou H Feng R Ghirlando Y Bai, J Mol Biol 2008 384 531 539 10.1016/j.jmb.2008.09.044 18848567
37. A hyperthermophilic protein acquires function at the cost of stability. A Mukaiyama M Haruki M Ota Y Koga K Takano S Kanaya, Biochemistry 2006 45 12673 12679 10.1021/bi060907v 17042484
38. Osmolyte effect on the stability and folding of a hyperthermophilic protein. A Mukaiyama Y Koga K Takano S Kanaya, Proteins: Struct Funct Bioinf 2008 71 110 118 10.1002/prot.21660 (Pubitemid 351358595)
39. Proline effect on the thermostability and slow unfolding of a hyperthermophilic protein. K Takano R Higashi J Okada A Mukaiyama T Tadokoro Y Koga S Kanaya, J Biochem 2008 145 79 85 10.1093/jb/mvn144 18977771
40. Effect of the disease-causing mutations identified in human ribonuclease (RNase) H2 on the activities and stabilities of yeast RNase H2 and archaeal RNase HII. MS Rohman Y Koga K Takano H Chon RJ Crouch S Kanaya, FEBS J 2008 275 4836 4849 10.1111/j.1742-4658.2008.06622.x 18721139
41. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. CR Woese O Kandler ML Wheelis, Proc Natl Acad Sci USA 1990 87 4576 4579 10.1073/pnas.87.12.4576 2112744
42. Structural details of ribonuclease H from Escherichia coli as refined to an atomic resolution. K Katayanagi M Miyagawa M Matsushima M Ishikawa S Kanaya H Nakamura M Ikehara T Matsuzaki K Morikawa, J Mol Biol 1992 223 1029 1052 10.1016/0022-2836(92)90260-Q 1311386
43. Crystal structure of ribonuclease H from Thermus thermophilus HB8 refined at 2.8 resolution. K Ishikawa M Okumura K Katayanagi S Kimura S Kanaya H Nakamura K Morikawa, J Mol Biol 1993 230 529 542 10.1006/jmbi.1993.1169 8385228
44. Crystal structure of type 1 ribonuclease H from hyperthermophilic archaeon Sulfolobus tokodaii: role of arginine 118 and C-terminal anchoring. DJ You H Chon Y Koga K Takano S Kanaya, Biochemistry 2007 461 1494 1503
45. Catalytic center of an archaeal type2 ribonuclease H as revealed by X-ray crystallographic and mutational analyses. A Muroya D Tsuchiya M Ishikawa M Haruki M Morikawa S Kanaya K Morikawa, Protein Sci 2001 10 707 714 10.1110/ps.48001 11274461
46. Structural, thermodynamic, and mutational analyses of a psychrotrophic RNase HI. T Tadokoro DJ You Y Abe H Chon H Matsumura Y Koga K Takano S Kanaya, Biochemistry 2007 46 7460 7468 10.1021/bi7001423 17536836
47. Remarkable stabilization of a psychrotrophic RNase HI by a combination of thermostabilizing mutations identified by the suppressor mutation method. T Tadokoro K Matsushita Y Abe MS Rohman Y Koga K Takano S Kanaya, Biochemistry 2008 47 8040 8047 10.1021/bi800246e 18616283
48. Destabilization of psychrotrophic RNase HI in a localized fashion as revealed by mutational and X-ray crystallographic analyses. MS Rohman T Tadokoro C Angkawidjaja Y Abe H Matsumura Y Koga K Takano S Kanaya, FEBS J 2009 276 603 613 10.1111/j.1742-4658.2008.06811.x 19120449
49. Reversible thermal unfolding of thermostable phosphoglycerate kinase. Thermostability associated with mean zero enthalpy change. H Nojima A Ikai T Oshima H Noda, J Mol Biol 1977 116 429 442 10.1016/0022-2836(77)90078-X 338921
50. A thermodynamic comparison of HPr proteins from extremophilic organisms. A Razvi JM Scholtz, Biochemistry 2006 45 4084 4092 10.1021/bi060038+ 16566582
51. Hyperthermophile protein folding thermodynamics: Differential scanning calorimetry and chemical denaturation of Sac7d. BS McCrary SP Edmondson JW Shriver, J Mol Biol 1996 264 784 805 10.1006/jmbi.1996.0677 8980686
52. Thermodynamic stability of archaeal histones. WT Li RA Grayling K Sandman S Edmondson JW Shriver JN Reeve, Biochemistry 1998 37 10563 10572 10.1021/bi973006i 9692945
53. Recombinant phosphoglycerate kinase from the hyperthermophilic bacterium Thermotoga maritima: Catalytic, spectral and thermodynamic properties. M Grättinger A Dankesreiter H Schurig R Jaenicke, J Mol Biol 1998 280 525 533 10.1006/jmbi.1998.1861 9665854
54. Thermodynamic basis for the increased thermostability of CheY from the hyperthermophile Thermotoga maritima. WA Deutschman FW Dahlquist, Biochemistry 2001 40 13107 13113 10.1021/bi010665t 11669649
55. Electrostatic interactions contribute reduced heat capacity change of unfolding in a thermophilic ribosomal protein L30e. CF Lee MD Allen M Bycroft KD Wong, J Mol Biol 2005 348 419 431 10.1016/j.jmb.2005.02.052 15811378
56. Identification of RNase HII from psychrotrophic bacterium. Shewanella sp, SIB1 as a high-activity type RNase H. H Chon T Tadokoro N Ohtani Y Koga K Takano S Kanaya, FEBS J 2006 273 2264 2275 10.1111/j.1742-4658.2006.05241.x 16650002
57. Physics and evolution of thermophilic adaptation. IN Berezovsky EI Shakhnovich, Proc Natl Acad Sci USA 2005 102 12742 12747 10.1073/pnas.0503890102 16120678
58. Environment specific substitution tables for thermophilic proteins. K Mizuguchi M Sele MV Cubellis, BMC Bioinformatics 2007 8 Suppl 1 15 10.1186/1471-2105-8-S1-S15 17430559
59. Are the parameters of various stabilization factors estimated from mutant human lysozymes compatible with other proteins? J Funahashi K Takano K Yutani, Protein Eng 2001 14 127 134 10.1093/protein/14.2.127 11297670
60. Structure, stability, and folding of ribonuclease H1 from the moderately thermophilic Chlorobium tepidum: comparison with thermophilic and mesophilic homologues. K Ratcliff J Corn S Marqusee, Biochemistry 2009 48 5890 5898 10.1021/bi900305p 19408959
61. Crystallization and preliminary crystallographic analysis of type 1 RNase H from the hyperthermophilic archaeon Sulfolobus tokodaii 7. DJ You H Chon Y Koga K Takano S Kanaya, Acta Crystallogr Sect F Struct Biol Cryst Commun 2006 62 781 784 10.1107/S1744309106024420 16880556
62. The spectrophotometric determination of tyrosine and tryptophan in proteins. TW Goodwin RA Morton, Biochem J 1946 40 628 632
63. Measuring and increasing protein stability. CN Pace, Trends Biotechnol 1990 8 93 98 10.1016/0167-7799(90)90146-O 1367432
64. Hydrogen ion buffers for biological research. NE Good GD Winget W Winter TN Connolly S Izawa RMM Singh, Biochemistry 1966 5 467 477 10.1021/bi00866a011 5942950
65. Mutational and structural-based analyses of the osmolyte effect on protein stability. K Takano M Saito M Morikawa S Kanaya, J Biochem 2004 135 701 708 10.1093/jb/mvh085 15213245
66. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesufonyl alpha-chymotrypsin using different denaturants. MM Santoro BW Bolen, Biochemistry 1988 27 8063 8068 10.1021/bi00421a014 3233195
67. Protein thermostabilization requires a fine-tuned placement of surface-charged residues. DJ You S Fukuchi K Nishikawa Y Koga K Takano S Kanaya, J Biochem 2007 142 507 516 10.1093/jb/mvm157 17761696
68. PyMOL User's Guide. WL DeLano, DeLano Scientific San Carlos, California 2004