Slow unfolding pathway of hyperthermophilic Tk-RNase H2 examined by pulse proteolysis using the stable protease Tk-subtilisin

Biochemistry

Volumn 51, Issue 45, 2012, Pages 9178-9191

  Okada, Jun ^a   Koga, Yuichi ^a   Takano, Kazufumi ^a,b   Kanaya, Shigenori ^a  

^a OSAKA UNIVERSITY   (Japan)

^b KYOTO PREFECTURAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL REGIONS; CLEAVAGE SITES; DEGRADATION PRODUCTS; EFFECTIVE TOOL; ENZYMATIC ACTIVITIES; GEL ELECTROPHORESIS; GUANIDINE HYDROCHLORIDE; HYPERTHERMOPHILIC; HYPERTHERMOPHILIC ARCHAEON; INTERMEDIATE STRUCTURES; N-TERMINAL SEQUENCING; N-TERMINALS; NATIVE STATE; PROTEIN ENGINEERING; SERINE PROTEASE;

AMINO ACIDS; DEGRADATION; ELECTROPHORESIS; GENETIC ENGINEERING; MASS SPECTROMETRY; PROTEINS; PROTEOLYSIS; SODIUM; SODIUM SULFATE;

GENE ENCODING;

BACTERIAL PROTEIN; GUANIDINE; RIBONUCLEASE H; RIBONUCLEASE H2; SUBTILISIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BIOPHYSICS; CIRCULAR DICHROISM; ENZYME ACTIVITY; ENZYME STRUCTURE; GEL ELECTROPHORESIS; HYPERTHERMOPHILIC ARCHAEON; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN ENGINEERING; PROTEIN UNFOLDING; THERMOCOCCUS KODAKARENSIS;

CIRCULAR DICHROISM; GUANIDINE; KINETICS; PROTEIN REFOLDING; PROTEIN UNFOLDING; PROTEOLYSIS; RIBONUCLEASE H; SUBTILISINS; THERMOCOCCUS;

ARCHAEA; THERMOCOCCUS KODAKARENSIS;

EID: 84869006763     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300973n     Document Type: Article

References (41)

1. Kim, P. S. and Baldwin, R. L. (1990) Intermediates in the folding reactions of small proteins Annu. Rev. Biochem. 59, 631-660
2. Kuwajima, K., Nitta, K., Yoneyama, M., and Sugai, S. (1976) Three-state denaturation of α-lactalbumin by guanidine hydrochloride J. Mol. Biol. 106, 359-373
3. Ptitsyn, O. B. (1995) Molten globule and protein folding Adv. Protein Chem. 47, 83-229
4. Baldwin, R. L., Frieden, C., and Rose, G. D. (2010) Dry molten globule intermediates and the mechanism of protein unfolding Proteins: Struct., Funct., Genet. 78, 2725-2737
5. Arai, M. and Kuwajima, K. (1996) Rapid formation of a molten globule intermediate in refolding of lactalbumin Folding Des. 1, 275-287
6. Udgaonkar, J. B. and Baldwin, R. L. (1988) NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A Nature 335, 694-699
7. Roder, H., Elove, G. A., and Englander, S. W. (1988) Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR Nature 335, 700-704
8. Balbach, J., Forge, V., van, Nuland, N. A., Winder, S. L., Hore, P. J., and Dobson, C. M. (1995) Following protein folding in real time using NMR spectroscopy Nat. Struct. Biol. 2, 865-870
9. Eliezer, D., Jennings, P. A., Wright, P. E., Doniach, S., Hodgson, K. O., and Tsuruta, H. (1995) The radius of gyration of an apomyoglobin folding intermediate Science 270, 487-488
10. Arai, M., Ikura, T., Semisotnov, G. V., Kihara, H., Amemiya, Y., and Kuwajima, K. (1998) Kinetic refolding of β-lactoglobulin. Studies by synchrotron X-ray scattering, and circular dichroism, absorption and fluorescence spectroscopy J. Mol. Biol. 275, 149-162
11. Serrano, L., Matouschek, A., and Fersht, A. R. (1992) The folding of an enzyme. III. Structure of the transition state for unfolding of barnase analysed by a protein engineering procedure J. Mol. Biol. 224, 805-818
12. Cavagnero, S., Debe, D. A., Zhou, Z. H., Adams, M. W. W., and Chan, S. I. (1998) Kinetic role of electrostatic interactions in the unfolding of hyperthermophilic and mesophilic rubredoxins Biochemistry 37, 3369-3376
13. Ogasahara, K., Nakamura, M., Nakura, S., Tsunasawa, S., Kato, I., Yoshimoto, T., and Yutani, K. (1998) 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 Biochemistry 37, 17537-17544
14. Dams, T. and Jaenicke, R. (1999) Stability and folding of dihydrofolate reductase from the hyperthermophilic bacterium Thermotoga maritime Biochemistry 38, 9169-9178
15. Kaushik, J. K., Ogasahara, K., and Yutani, K. (2002) The unusually slow relaxation kinetics of the folding-unfolding of pyrrolidone carboxyl peptidase from a hyperthermophile Pyrococcus furiosus J. Mol. Biol. 316, 991-1003
16. Jaswal, S. S., Sohl, J. L., Dans, J. H., and Agard, D. A. (2002) Energetic landscape of α-lytic protease optimizes longevity through kinetic stability Nature 415, 343-346
17. Zeeb, M., Lipps, G., Lilie, H., and Balbach, J. (2004) Folding and association of an extremely stable dimeric protein from Sulfolobus islandicus J. Mol. Biol. 336, 227-240
18. Forrer, P., Chang, C., Ott, D., Wlodawer, A., and Pluckthun, A. (2004) Kinetic stability and crystal structure of the viral capside protein SHP J. Mol. Biol. 344, 179-193
19. Wittung-Stafshede, P. (2004) Slow unfolding explains high stability of thermostable ferredoxins: Common mechanism governing thermostability? Biochim. Biophys. Acta 1700, 1-4
20. Duy, C. and Fitter, J. (2005) Thermostability of irreversible unfolding α-amylases analyzed by unfolding kinetics J. Biol. Chem. 280, 37360-37365
21. Kaushik, J. K., Iimura, S., Ogasahara, K., Yamagata, Y., Segawa, S., and Yutani, K. (2006) Completely buried, non-ion-paired glutamic acid contributes favorably to the conformational stability of pyrrolidone carboxyl peptidases from hyperthermophiles Biochemistry 45, 7100-7112
22. Mishra, R., Olofsson, L., Karlsson, M., Carlsson, U., Nicholls, I. A., and Hammarstrom, P. (2008) A conformationally isoformic thermophilic protein with high kinetic unfolding barriers Cell. Mol. Life Sci. 65, 827-839
23. Costas, M., Rodriguez-Larrea, D., De Maria, L., Borchert, T. V., Gomez-Puyou, A., and Sanchez-Ruiz, J. M. (2009) Between-species variation in the kinetic stability of TIM proteins linked to solvation-barrier free energies J. Mol. Biol. 385, 924-937
24. Iimura, S., Yagi, H., Ogasahara, K., Akutsu, H., Noda, Y., Segawa, S., and Yutani, K. (2004) Unusually slow denaturation and refolding process of pyrrolidone carcoxyl peptidase from a hyper-thermophile are highly cooperative: Real-time NMR studies Biochemistry 43, 11906-11915
25. Mukaiyama, A., Takano, K., Haruki, M., Morikawa, M., and Kanaya, S. (2004) Kinetically robust monomeric protein from a hyperthermophile Biochemistry 43, 13859-13866
26. Mukaiyama, A. and Takano, K. (2009) Slow unfolding of monomeric proteins from hyperthermophiles with reversible unfolding Int. J. Mol. Sci. 10, 1369-1385
27. Dong, H., Mukaiyama, A., Tadokoro, T., Koga, Y., Takano, K., and Kanaya, S. (2008) Hydrophobic effect on the stability and folding of a hyperthermophilic protein J. Mol. Biol. 378, 264-272
28. Takano, K., Higashi, R., Okada, J., Mukaiyama, A., Tadokoro, T., Koga, Y., and Kanaya, S. (2008) Proline effect on the thermostability and slow unfolding of a hyperthermophilic protein J. Biochem. 145, 79-85
29. Okada, J., Okamoto, T., Mukaiyama, A., Tadokoro, T., You, D. J., Koga, Y., Takano, K., and Kanaya, S. (2010) Evolution and thermodynamics of slow unfolding of hyperstable monomeric proteins BMC Evol. Biol. 10, 207
30. 2+-induced folding J. Biol. Chem. 282, 8246-8255
31. Laemmli, U. K. (1970) Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 Nature 227, 680-685
32. Goodwin, T. W. and Morton, R. A. (1946) The spectrophotometric determination of tyrosine and tryptophan in proteins Biochem. J. 40, 628-632
33. Schägger, H. (2006) Tricine-SDS-PAGE Nat. Protoc. 1, 16-22
34. Santoro, M. M. and Bolen, B. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants Biochemistry 27, 8063-8068
35. Park, C. and Marqusee, S. (2005) Pulse proteolysis: A simple method for quantitative determination of protein stability and ligand binding Nat. Methods 2, 207-212
36. Na, Y. R. and Park, C. (2009) Investigating protein unfolding kinetics by pulse proteolysis Protein Sci. 18, 268-276
37. Chang, Y. and Park, C. (2009) Mapping transient partial unfolding by protein engineering and native-state proteolysis J. Mol. Biol. 393, 543-556
38. Kim, M. S., Song, J., and Park, C. (2009) Determining protein stability in cell lysates by pulse proteolysis and Western blotting Protein Sci. 18, 1051-1059
39. Semisotnov, G. V., Rodionova, N. A., Kutyshenko, V. P., Ebert, B., Blanck, J., and Ptitsyn, O. B. (1987) Sequential mechanism of refolding of carbonic anhydrase B FEBS Lett. 224, 9-13
40. Kuwajima, K. (1989) The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure Proteins: Struct., Funct., Genet. 6, 87-103
41. Muroya, A., Tsuchiya, D., Ishikawa, M., Haruki, M., Morikawa, M., Kanaya, S., and Morikawa, K. (2001) Catalytic center of an archaeal type 2 ribonuclease H as revealed by X-ray crystallographic and mutational analyses Protein Sci. 10, 707-714