Unusually slow denaturation and refolding processes of pyrrolidone carboxyl peptidase from a hyperthermophile are highly cooperative: Real-time NMR studies

Biochemistry

Volumn 43, Issue 37, 2004, Pages 11906-11915

  Iimura, Satoshi ^a   Yagi, Hiromasa ^b   Ogasahara, Kyoko ^b   Akutsu, Hideo ^b   Noda, Yasuo ^a   Segawa, Shin Ichi ^a   Yutani, Katsuhide ^a,c  

^a KWANSEI GAKUIN UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c RIKEN HARIMA INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; PHASE TRANSITIONS; PHYSIOLOGY; PROTEINS; REACTION KINETICS; STRUCTURE (COMPOSITION);

DENATURATION; HYPERTHERMOPROFILE; REFOLDING PROCESSES;

NUCLEAR MAGNETIC RESONANCE;

5 OXOPROLYL PEPTIDASE; BACTERIAL ENZYME; NITROGEN 15;

ARTICLE; CIRCULAR DICHROISM; ENZYME DENATURATION; ENZYME SUBSTRATE; ESCHERICHIA COLI; ISOTOPE LABELING; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTON NUCLEAR MAGNETIC RESONANCE; PYROCOCCUS FURIOSUS;

ARCHAEAL PROTEINS; CIRCULAR DICHROISM; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN RENATURATION; PYROCOCCUS FURIOSUS; PYROGLUTAMYL-PEPTIDASE I; THERMODYNAMICS; TIME FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; POSIBACTERIA; PYROCOCCUS; PYROCOCCUS FURIOSUS;

EID: 4644309000     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048762k     Document Type: Article

References (53)

1. Backmann, J., and Schafer, G. (2001) Thermodynamic analysis of hyperthermostable oligomeric proteins, Methods Enzymol. 334, 328-342.
2. Rees, D. (2001) Crystallographic analyses of hyperthermophilic proteins, Methods Enzymol. 334, 423-437.
3. Yutani, K., Takano, K., and Funahashi, J. (1999) Evaluation of some factors that contribute to conformational stability of a protein using database of stability/structure, in Old and New Views of Protein Folding (Kuwajima, K., and Arai, M., Eds.) pp 175-184, Elsevier Science B.V., Amsterdam.
4. Jaenicke, R. (2000) Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity?, Proc. Natl Acad. Sci. U.S.A. 97, 2962-2964.
5. Wrba, A., Schweiger, A., Schultes, V., Jaenicke, R., and Zavodsky, P. (1990) Extremely thermostable D-glyceraldehyde-3-phosphate dehydrogenase from the eubacterium Thermotoga maritima, Biochemistry 29, 7584-7592.
6. Klump, H., Di Ruggiero, J., Kessel, M., Park, J. B., Adams, M. W., and Robb, F. T. (1992) Glutamate dehydrogenase from the hyperthermophile Pyrococcus furiosus. Thermal denaturation and activation, J. Biol. Chem. 267, 22681-22685.
7. Laderman, K. A., Davis, B. R., Krutzsch, H. C., Lewis, M. S., Griko, Y. V., Privalov, P. L., and Anfinsen, C. B. (1993) The purification and characterization of an extremely thermostable α-amylase from the hyperthermophilic archaebacterium Pyrococcus furiosus, J. Biol. Chem. 268, 24394-24401.
8. McAfee, J. G., Edmondson, S. P., Zegar, I., and Shriver, J. W. (1996) Equilibrium DNA binding of Sac7d protein from the hyperthermophile Sulfolobus acidocaldarius: fluorescence and circular dichroism studies, Biochemistry 35, 4034-4045.
9. DeDecker, B. S., O'Brien, R., Fleming, P. J., Geiger, J. H., Jackson, S. P., and Sigler, P. B. (1996) The crystal structure of a hyperthermophilic archaeal TATA-box binding protein, J. Mol. Biol. 264, 1072-1084.
10. Pfeil, W., Geierich, U. Kleemann, G. R., and Sterner, R. (1997) Ferredoxin from the hyperthermophile Thermotoga maritima is stable beyond the boiling point of water, J. Mol. Biol. 272, 591-596.
11. Pappenberger, G., Schurig, H., and Jaenicke, R. (1997) Disruption of an ionic network leads to accelerated thermal denaturation of D-glyceraldehyde-3- phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima, J. Mol. Biol. 274, 676-683.
12. 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 pyrrolidone carboxyl peptidase from a hyperthermophile, Pyrococcus furiosus: Equilibrium and kinetic studies of guanidine hydrochloride-induced unfolding and refolding, Biochemistry 37, 17537-17544.
13. Cavagnero, S., Debe, D. A., Zhou, Z. H., Adams, M. W., and Chan, S. I. (1998) Kinetic role of electrostatic interactions in the unfolding of hyperthermophilic and mesophilic rubredoxins, Biochemistry 37, 3369-3376.
14. Pothekin, S. A., Ogasahara, K., and Yutani, K. (2000) Transition state of heat denaturation of methionine aminopeptidase from a hyperthermophile, J. Therm. Anal. Calorim. 62, 111-122.
15. Nojima, H., Hon-Nami, K., Oshima, T., and Noda, H. (1978) Reversible thermal unfolding of thermostable cytochrome c-552, J. Mol. Biol. 122, 33-42.
16. McCrary, B. S., Edmondson, S. P., and Shriver, J. W. (1996) Hyperthermophile protein folding thermodynamics: differential scanning calorimetry and chemical denaturation of Sac7d, J. Mol. Biol. 264, 784-805.
17. Knapp, S., Karshikoff, A., Berndt, K. D., Christova, P., Atanssov, B., and Ladenstein, R. (1996) Thermal unfolding of the DNA-binding protein Sso7d from the hyperthermophile Sulfolobus solfataricus, J. Mol. Biol. 264, 1132-1144.
18. Consalvi, V., Chiaraluce, R., Giangiacomo, L., Scandurra, R., Christova, P., Karshikoff, A., Knapp, S., and Ladenstein, R. (2000) Thermal unfolding and conformational stability of the recombinant domain II of glutamate dehydrogenase from the hyperthermophile Thermotoga maritima, Protein Eng. 13, 501-507.
19. 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.
20. Ogasahara, K., Khechinashvili, N. N., Nakamura, M., Yoshimoto, T., and Yutani, K. (2001) Thermal stability of pyrrolidone carboxyl peptidases from the hyperthermophilic Archaeon, Pyrococcus furiosus, Eur. J. Biochem. 268, 3233-3242.
21. Shortle, D., and Ackerman, M. S. (2001) Persistence of native-like topology in a denatured protein in 8 M urea, Science 293, 487-489.
22. Tsunasawa, S., Nakura, S., Tanigawa, T., and Kato, I. (1998) Pyrrolidone carboxyl peptidase from the hyperthermophilic archaeon Pyrococcus furiosus: Cloning and overexpression in Echerichia coli of the gene, and its application to protein sequence analysis, J. Biochem. 124, 778-783.
23. Kay, L., Keifer, E. P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
24. Schulman, B. A., Kim, P. S., Dobson, C. M., and Redfield, C. (1997) A residue-specific NMR view of the non-cooperative unfolding of a molten globule, Nat. Struct. Biol. 4, 630-634.
25. Yutani, K., Ogasahara, K., Suzuki, M., and Sugino, Y. (1979) Comparison of denaturation by guanidine hydrochloride of the wild-type tryptophan synthase α-Subunit of E. coli and two mutant proteins (Glu49 → Met or Gln), J. Biochem. 85, 915-921.
26. Roy, M., and Jennings, P. A. (2003) Real-time NMR kinetics provide global and residue-specific information on the Non-cooperative unfolding of the beta-trefoil protein, interleukin-1beta, J. Mol. Biol. 328, 693-703.
27. Steegborn, C., Schneider-Hassloff, H., Zeeb, M., and Balbach, J. (2000) Cooperativity of a protein folding reaction probed at multiple chain positions by real-time 2D NMR spectroscopy, Biochemistry 39, 7910-7919.
28. Mizuguchi, M., Kroon, G. J., Wright, P. E., and Dyson, H. J. (2003) Folding of a beta-sheet protein monitored by real-time NMR spectroscopy, J. Mol. Biol. 328, 1161-1171.
29. Koide, S., Dyson, H. J., and Wright, P. E. (1993) Characterization of a folding intermediate of apoplastocyanin trapped by proline isomerization, Biochemistry 32, 12299-12310.
30. Ogasahara, K., Matsushita, E., and Yutani, K., (1993) Further examination of the intermediate states in the denaturation of the tryptophan synthase α subunit: Evidence that the equilibrium denaturation intermediate is a molten globule, J. Mol. Biol. 234, 1197-1206.
31. Yutani, K., Ogasahara, K., and Kuwajima, K. (1992) The absence of the thermal transition in apo-α-lactalbumin in the molten globule state: A study by differential scanning microcalorimetry, J. Mol. Biol. 228, 347-350.
32. Ohgushi, M., and Wada, A. (1983) Molten-globule state: a compact form of globular protein with mobile side chain, FEBS Lett. 164, 21-24.
33. Brockwell, D. J., Smith, D. A., and Radford, S. E. (2000) Protein folding mechanisms: new methods and emerging ideas, Curr. Opin. Struct. Biol. 10, 16-25.
34. Roder, H., and Colon, W. (1997) Kinetic role of early intermediates in protein folding, Curr. Opin. Struct. Biol. 7, 15-28.
35. Singleton, M. R., Ksupov, M. N., and Littlechild, J. A. (1999) X-ray structure of pyrrolidone carboxyl peptidase from the hyperthermophilic archaeon Thermococcus litoralis, Structure 7, 237-244.
36. Sokabe, M., Kawamura, T., Sakai, N., Yao, M., Watanabe, N., and Tanaka, I. (2002) The X-ray crystal structure of pyrrolidone-carboxylate peptidase from hyperthermophilic archaea Pyrococcus horikoshii, J. Struct. Funct. Genomics 2, 145-54.
37. Odagaki, Y., Hayashi, A., Okada, K., Hirotsu, K., Kabashima, T., Ito, K., Yoshimoto, Y., Tsuru, D., Sato, M., and Clardy, J. (1999) The crystal structure of pyroglutamyl peptidase I from Bacillus amyloliquefaciens reveals a new structure for a cysteine protease, Structure 7, 399-411.
38. Balbach, J., and Schmid, F. X. (2000) Proline isomerization and its catalysis in protein folding, Mechanisms of Protein Folding (Pain, R. H., Ed.) pp 212-249, Oxford University Press, Oxford.
39. Tanaka, H., Chinami, M., Mizushima, T., Ogasahara, K., Ota, M., Tsukihara, T., and Yutani, K. (2001) X-ray crystalline structures of pyrrolidone carboxyl peptidase from a hyperthermophile, Pyrococcus furiosus, and its cys-free mutant, J. Biochem. 130, 107-118.
40. Wuthrich, K. (1994) NMR assignments as a baias for structural characterization of denatured states of globular proteins, Curr. Opin. Struct. Biol. 4, 93-99.
41. Mayor, U., Grossmann, J. G., Foster, N. W., Freund, S. M., and Fersht, A. R. (2003) The denatured state of engrailed homeodomain under denaturing and native conditions, J. Mol. Biol. 333, 977-991.
42. Tafer, H., Hiller, S., Hilty, C., Fernandez, C., and Wuthrich, K. (2004) Nonrandom structure in the urea-unfolded Escherichia coli outer membrane protein X (OmpX), Biochemistry 43, 860-869.
43. Plaxco, K. W., Simons, K. T., and Baker, D. (1998) Contact order, transition state placement and the refolding rates of single domain proteins, J. Mol. Biol. 277, 985-994.
44. Dobson, C. M., Sali, A., and Karplus, M. (1998) Protein Folding: A Perspective from Theory and Experiment, Angew. Chem., Int. Ed. Engl. 37, 868-893.
45. Dobson, C. M. (2000) The nature and significance of protein folding, in Mechanisms of Protein Folding (Pain, R. H., Ed.) pp 1-33, Oxford University Press, Oxford.
46. Bryngelson, J. D., Onuchic, J. N., Socci, N. D., and Wolynes, P. G. (1995) Funnels, pathways, and the energy landscape of protein folding: a synthesis, Proteins 21, 167-195.
47. Dill, K. A., Phillips, A. T., and Rosen, J. B. (1997) Protein structure and energy landscape dependence on sequence using a continuous energy function, J. Comput. Biol. 4, 227-239.
48. Baum, J., Dobson, C. M., Evans, P. A., and Hanley, C. (1989) Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea pig α-lactalbumin, Biochemistry 28, 7-13.
49. Gutin, A. M., Abkevich, V. I., and Shakhnovich, E. I. (1995) Is burst hydrophobic collapse necessary for protein folding?, Biochemistry 34, 3066-3076.
50. Dinner, A. R., Sali, A., Smith, L. J., Dobson, C. M., and Karplus, M. (2000) Understanding protein folding via free-energy surfaces from theory and experiment, Trends Biochem Sci. 25, 331-339.
51. Matagne, A., Jamin, M., Chung, E. W., Robinson, C. V., Radford, S. E., and Dobson, C. M. (2000) Thermal unfolding of an intermediate is associated with non-Arrhenius kinetics in the folding of hen lysozyme, J. Mol. Biol. 297, 193-210.
52. Sali, A., Shakhnovich, E., and Karplus, M. (1994) How does a protein fold?, Nature 369, 248-251.
53. Eyring (1935) The activated complex and the absolute rate of chemical reactions, Chem. Phys. Rev. 17, 65-77.