Role of the unique peptide tail in hyperthermostable Aquifex aeolicus cochaperonin protein 10+

Biochemistry

Volumn 44, Issue 44, 2005, Pages 14385-14395

  Luke, Kathryn ^a   Apiyo, David ^a   Wittung Stafshede, Pernilla ^a  

^a RICE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CALORIMETRY; CRYSTAL ATOMIC STRUCTURE; DISSOCIATION; ELECTRON MICROSCOPY; MOLECULAR BIOLOGY; THERMODYNAMIC STABILITY;

COCHAPERONIN PROTEINS; HEPTAMERS; HOMOLOGY; SUBSTRATE-REFOLDING ACTIVITY;

PROTEINS;

AQUIFEX AEOLICUS COCHAPERONIN PROTEIN 10; CHAPERONIN; MONOMER; PEPTIDE; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AQUIFEX AEOLICUS; ARTICLE; BETA STRAND; BIOPHYSICS; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; DISSOCIATION; ELECTRON MICROSCOPY; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; THERMODYNAMICS; THERMOSTABILITY;

BACTERIA; CHAPERONIN 10; HEAT; MODELS, MOLECULAR; PEPTIDES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; THERMODYNAMICS;

AQUIFEX AEOLICUS; BACTERIA (MICROORGANISMS);

EID: 27644534843     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051131l     Document Type: Article

References (75)

1. Traut, T. W. (1994) Dissociation of enzyme oligomers: a mechanism for allosteric regulation, Crit. Rev. Biochem. Mol. Biol. 29, 125-163.
2. Darnall, D. W., and Klotz, I. M. (1975) Subunit constitution of proteins: a table, Arch. Biochem. Biophys. 166, 651-682.
3. Bodenreider, C., Kellershohn, N., Goldberg, M. E., and Mejean, A. (2002) Kinetic analysis of R67 dihydrofolate reductase folding: from the unfolded monomer to the native tetramer, Biochemistry 41, 14988-14999.
4. Ziegler, M. M., Goldberg, M. E., Chaffotte, A. F., and Baldwin, T. O. (1993) Refolding of luciferase subunits from urea and assembly of the active heterodimer. Evidence for folding intermediates that precede and follow the dimerization step on the pathway to the active form of the enzyme, J. Biol. Chem. 268, 10760-10765.
5. Mann, C. J., Shao, X., and Matthews, C. R. (1995) Characterization of the slow folding reactions of trp aporepressor from Escherichia coli by mutational analysis of prolines and catalysis by a peptidyl-prolyl isomerase, Biochemistry 34, 14573-14580.
6. Waldburger, C. D., Jonsson, T., and Sauer, R. T. (1996) Barriers to protein folding: formation of buried polar interactions is a slow step in acquisition of structure, Proc. Natl. Acad. Sci. U.S.A. 93, 2629-2634.
7. Nichtl, A., Buchner, J., Jaenicke, R., Rudolph, R., and Scheibel, T. (1998) Folding and association of beta-Galactosidase, J. Mol. Biol. 282, 1083-1091.
8. Gloss, L. M., and Matthews, C. R. (1998) Mechanism of folding of the dimeric core domain of Escherichia coli tip repressor: a nearly diffusion-limited reaction leads to the formation of an on-pathway dimeric intermediate, Biochemistry 37, 15990-15999.
9. Doyle, S. M., Braswell, E. H., and Teschke, C. M. (2000) SecA folds via a dimeric intermediate, Biochemistry 39, 11667-11676.
10. Milla, M. E., and Sauer, R. T. (1994) P22 Arc repressor: folding kinetics of a single-domain, dimeric protein, Biochemistry 33, 1125-1133.
11. Srivastava, A. K., and Sauer, R. T. (2000) Evidence for partial secondary structure formation in the transition state for arc repressor refolding and dimerization, Biochemistry 39, 8308-8314.
12. Martin, J., Geromanos, S., Tempst, P., and Hartl, F. U. (1993) Identification of nucleotide-binding regions in the chaperonin proteins GroEL and GroES, Nature 366, 279-282.
13. Todd, M. J., Boudkin, O., Freire, E., and Lorimer, G. H. (1995) GroES and the chaperonin-assisted protein folding cycle: GroES has no affinity for nucleotides, FEBS Lett. 359, 123-125.
14. Burston, S. G., Weissman, J. S., Fair, G. W., Fenton, W. A., and Horwich, A. L. (1996) Release of both native and non-native proteins from a cis-only GroEL ternary complex, Nature 383, 96-99.
15. Shtilerman, M., Lorimer, G. H., and Englander, S. W. (1999) Chaperonin function: folding by forced unfolding, Science 284, 822-825.
16. Athanasas-Platsis, S., Somodevilla-Torres, M. J., Morton, H., and Cavanagh, A. C. (2004) Investigation of the immunocompetent cells that bind early pregnancy factor and preliminary studies of the early pregnancy factor target molecule, Immunol. Cell Biol. 82, 361-369.
17. Cappello, F., Bellafiore, M., David, S., Anzalone, R., and Zummo, G. (2003) Ten kilodalton heat shock protein (HSP10) is overexpressed during carcinogenesis of large bowel and uterine exocervix, Cancer Lett. 196, 35-41.
18. Slavotinek, A. M., and Biesecker, L. G. (2001) Unfolding the role of chaperones and chaperonins in human disease, Trends Genet. 17, 528-535.
19. Coates, A. R. M. (1996) The Chaperonins, Academic Press, London.
20. Cavanagh, A. C., and Morton, H. (1994) The purification of early-pregnancy factor to homogeneity from human platelets and identification as chaperonin 10, Eur. J. Biochem. 222, 551-560.
21. Cavanagh, A. C. (1996) Identification of early pregnancy factor as chaperonin 10: implications for understanding its role, Rev. Reprod. 1, 28-32.
22. Hunt, J. F., Weaver, A. J., Landry, S. J., Gierasch, L., and Deisenhofer, J. (1996) The crystal structure of the GroES co-chaperonin at 2.8 Å resolution, Nature 379, 37-45.
23. Mande, S. C., Mehra, V., Bloom, B. R., and Hol, W. G. (1996) Structure of the heat shock protein chaperonin-10 of Mycobacterium leprae, Science 271, 203-207.
24. Roberts, M. M., Coker, A. R., Fossati, G., Mascagni, P., Coates, A. R., and Wood, S. P. (1999) Crystallization, X-ray diffraction and preliminary structure analysis of Mycobacterium tuberculosis chaperonin 10, Acta Crystallogr., Sect. D: Biol. Crystallogr. 55, 910-914.
25. Hunt, J. F., van der Vies, S. M., Henry, L., and Deisenhofer, J. (1997) Structural adaptations in the specialized bacteriophage T4 co-chaperonin Gp31 expand the size of the Anfinsen cage, Cell 90, 361-371.
26. Numoto, N., Kita, A., and Miki, K. (2005) Crystal structure of the co-chaperonin Cpn10 from Thermus thermophilus HB8, Proteins 58, 498-500.
27. Landry, S. J., Steede, N. K., and Maskos, K. (1997) Temperature dependence of backbone dynamics in loops of human mitochondrial heat shock protein 10, Biochemistry 36, 10975-10986.
28. Guidry, J. J., Shewmaker, F., Maskos, K., Landry, S., and Wittung-Stafshede, P. (2003) Probing the interface in a human co-chaperonin heptamer: Residues disrupting oligomeric unfolded state identified, BMC Biochem. 4, 14.
29. Guidry, J. J., and Wittung-Stafshede, P. (2002) Low stability for monomeric human chaperonin protein 10: Interprotein interactions contribute majority of oligomer stability, Arch. Biochem. Biophys. 405, 280-282.
30. Guidry, J. J., Moczygemba, C. K., Steede, N. K., Landry, S. J., and Wittung-Stafshede, P. (2000) Reversible denaturation of oligomeric human chaperonin 10: denatured state depends on chemical denaturant, Protein Sci. 9, 2109-2117.
31. Boudker, O., Todd, M. J., and Freire, E. (1997) The structural stability of the co-chaperonin GroES, J. Mol. Biol. 272, 770-779.
32. Higurashi, T., Nosaka, K., Mizobata, T., Nagai, J., and Kawata, Y. (1999) Unfolding and refolding of Escherichia coli chaperonin GroES is expressed by a three-state model, J. Mol. Biol. 291, 703-713.
33. Seale, J. W., Gorovits, B. M., Ybarra, J., and Horowitz, P. M. (1996) Reversible oligomerization and denaturation of the chaperonin GroES, Biochemistry 35, 4079-4083.
34. Jaenicke, R., and Bohm, G. (1998) The stability of proteins in extreme environments, Curr. Opin. Struct. Biol. 8, 738-748.
35. Szilagyi, A., and Zavodszky, P. (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey, Struct. Folding Des. 8, 493-504.
36. Rees, D. C., and Adams, M. W. (1995) Hyperthermophiles: taking the heat and loving it, Structure 3, 251-254.
37. Privalov, P. (1997) Thermodynamics of protein Folding, J. Chem. Thermodyn. 29, 447-474.
38. Privalov, P. L., and Makhatadze, G. I. (1993) Contribution of hydration to protein folding thermodynamics. II. The entropy and Gibbs energy of hydration, J. Mol. Biol. 232, 660-679.
39. Beadle, B. M., Baase, W. A., Wilson, D. B., Gilkes, N. R., and Shoichet, B. K. (1999) Comparing the thermodynamic stabilities of a related thermophilic and mesophilic enzyme, Biochemistry 38, 2570-2576.
40. Hollien, J., and Marqusee, S. (1999) A thermodynamic comparison of mesophilic and thermophilic ribonucleases H, Biochemistry 38, 3831-3836.
41. 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.
42. Vogt, G., Woell, S., and Argos, P. (1997) Protein thermal stability, hydrogen bonds, and ion pairs, J. Mol. Biol. 269, 631-643.
43. Guidry, J., and Wittung-Stafshede, P. (2004) First characterization of co-chaperonin protein 10 from hyper-thermophilic Aquifex aeolicus, Biochem. Biophys. Res. Commun. 317, 176-180.
44. Deckert, G., Warren, P. V., Gaasterland, T., Young, W. G., Lenox, A. L., Graham, D. E., Overbeek, R., Snead, M. A., Keller, M., Aujay, M., Huber, R., Feldman, R. A., Short, J. M., Olsen, G. J., and Swanson, R. V. (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus, Nature 392, 353-358.
45. Buchner, J., Schmidt, M., Fuchs, M., Jaenicke, R., Rudolph, R., Schmid, F. X., and Kiefhaber, T. (1991) GroE facilitates refolding of citrate synthase by suppressing aggregation, Biochemistry 30, 1586-1591.
46. Barry, J. K., and Matthews, K. S. (1999) Thermodynamic analysis of unfolding and dissociation in lactose repressor protein, Biochemistry 38, 6520-6528.
47. Bowie, J. U., and Sauer, R. T. (1989) Equilibrium dissociation and unfolding of the Arc repressor dimer, Biochemistry 28, 7139-7143.
48. Dams, T., and Jaenicke, R. (1999) Stability and folding of dihydrofolate reductase from the hyperthermophilic bacterium Thermotoga maritima, Biochemistry 38, 9169-9178.
49. Panse, V. G., Swaminathan, C. P., Aloor, J. J., Surolia, A., and Varadarajan, R. (2000) Unfolding thermodynamics of the tetrameric chaperone, SecB, Biochemistry 39, 2362-2369.
50. Schellman, J. A. (1987) Selective binding and solvent denaturation, Biopolymers 26, 549-559.
51. Smith, J. S., and Scholtz, J. M. (1996) Guanidine hydrochloride unfolding of peptide helices: separation of denaturant and salt effects, Biochemistry 35, 7292-7297.
52. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants, Biochemistry 27, 8063-8068.
53. Santoro, M. M., and Bolen, D. W. (1992) A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range, Biochemistry 31, 4901-4907.
54. Yao, M., and Bolen, D. W. (1995) How valid are denaturant-induced unfolding free energy measurements? Level of conformance to common assumptions over an extended range of ribonuclease A stability, Biochemistry 34, 3771-3781.
55. Makhatadze, G. I., and Privalov, P. L. (1992) Protein interactions with urea and guanidinium chloride. A calorimetric study, J. Mol. Biol. 226, 491-505.
56. Brown, C., Liao, J., and Wittung-Stafshede, P. (2005) Interface mutation in heptameric co-chaperonin protein 10 destabilizes subunits but not interfaces, Arch. Biochem. Biophys. 439, 175-183.
57. Sakane, I., Ikeda, M., Matsumoto, C., Higurashi, T., Inoue, K., Kongo, K., Mizobata, T., and Kawata, Y. (2004) Structural stability of oligomeric chaperonin 10: the role of two beta-strands at the N and C termini in structural stabilization, J. Mol. Biol. 344, 1123-1133.
58. Luke, K., Apiyo, D., and Wittung-Stafshede, P. (2005) Dissecting homo-heptamer thermodynamics by isothermal titration calorimetry: Entropy-driven assembly of co-chaperonin protein 10, Biophys. J. (in press).
59. Velazquez-Campoy, A., Leavitt, S. A., and Freire, E. (2004) Characterization of protein-protein interactions by isothermal titration calorimetry, Methods Mol. Biol. 261, 35-54.
60. Burrows, S. D., Doyle, M. L., Murphy, K. P., Franklin, S. G., White, J. R., Brooks, I., McNulty, D. E., Scott, M. O., Knutson, J. R., Porter, D., and et al. (1994) Determination of the monomer-dimer equilibrium of interleukin-8 reveals it is a monomer at physiological concentrations, Biochemistry 33, 12741-12475.
61. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer. an environment for comparative protein modeling, Electrophoresis 18, 2714-2723.
62. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: An automated protein homology-modeling server, Nucleic Acids Res. 31, 3381-3385.
63. Honig, B., and Nicholls, A. (1995) Classical electrostatics in biology and chemistry, Science 268, 1144-1149.
64. Nicholls, A., Sharp, K. A., and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins 11, 281-296.
65. Lovatt, M., Cooper, A., and Camilleri, P. (1996) Energetics of cyclodextrin-induced dissociation of insulin, Eur. Biophys. J. 24, 354-357.
66. Kumar, S., Tsai, C. J., and Nussinov, R. (2001) Thermodynamic differences among homologous thermophilic and mesophilic proteins, Biochemistry 40, 14152-14165.
67. Robertson, A. D., and Murphy, K. P. (1997) Protein structure and the energetics of protein stability, Chem. Rev. 97, 1251-1267.
68. Abraham, T., Lewis, R. N., Hodges, R. S., and McElhaney, R. N. (2005) Isothermal titration calorimetry studies of the binding of a rationally designed analogue of the antimicrobial peptide gramicidin S to phospholipid bilayer membranes, Biochemistry 44, 2103-2112.
69. Tanford, C. (1978) The hydrophobic effect and the organization of living matter, Science 200, 1012-1018.
70. Xu, D., Lin, S., and Nussinov, R. (1997) Protein binding versus protein folding: The role of hydrophilic bridges in protein associations, J. Mol. Biol. 265, 68-84.
71. Yu, X., VanLoock, M. S., Poplawski, A., Kelman, Z., Xiang, T., Tye, B. K., and Egelman, E. H. (2002) The Methanobacterium thermoautotrophicum MCM protein can form heptameric rings, EMBO Rep. 3, 792-797.
72. Roberts, M. M., Coker, A. R., Fossati, G., Mascagni, P., Coates, A. R., and Wood, S. P. (2003) Mycobacterium tuberculosis chaperonin 10 heptamers self-associate through their biologically active loops, J. Bacteriol. 185, 4172-4185.
73. Zhang, Y. B., Howitt, J., McCorkle, S., Lawrence, P., Springer, K., and Freimuth, P. (2004) Protein aggregation during overexpression limited by peptide extensions with large net negative charge, Protein Expression Purif. 36, 207-216.
74. Zhao, M. W., Zhu, B., Hao, R., Xu, M. G., Eriani, G., and Wang, E. D. (2005) Leucyl-tRNA synthetase from the ancestral bacterium Aquifex aeolicus contains relics of synthetase evolution, EMBO J. 24, 1430-1439.
75. Zondlo, J., Fisher, K. E., Lin, Z., Ducote, K. R., and Eisenstein, E. (1995) Monomer-heptamer equilibrium of the Escherichia coli chaperonin GroES, Biochemistry 34, 10334-10339.