Glu257 in GroEL is a sensor involved in coupling polypeptide substrate binding to stimulation of ATP hydrolysis

Protein Science

Volumn 15, Issue 6, 2006, Pages 1270-1276

  Danziger, Oded ^a   Shimon, Liat ^a   Horovitz, Amnon ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Allostery; Chaperonins; Cooperativity; Molecular chaperones; Protein folding

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALANINE; CHAPERONE; CHAPERONIN;

ALLOSTERISM; ARTICLE; COOPERATION; HYDROLYSIS; KINETICS; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FOLDING; REDUCTION; STEADY STATE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ALANINE; AMINO ACID SUBSTITUTION; BINDING SITES; GLUTAMIC ACID; GROEL PROTEIN; HYDROLYSIS; KINETICS; LACTALBUMIN; MUTATION; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 33744463129     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062100606     Document Type: Article

References (33)

1. Aharoni, A. and Horovitz, A. 1996. Inter-ring communication is disrupted in the GroEL mutant Arg13 → Gly; Ala126 → Val with known crystal structure. J. Mol. Biol. 258: 732-735.
2. Bartolucci, C., Lamba, D., Grazulis, S., Manakova, E., and Heumann, H. 2005. Crystal structure of wild-type chaperonin GroEL. J. Mol. Biol. 354: 940-951.
3. Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D.C., Joachimiak, A., Horwich, A.L., and Sigler, P.B. 1994. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 371: 578-586.
4. Brocchieri, L. and Karlin, S. 2000. Conservation among HSP60 sequences in relation to structure, function, and evolution. Protein Sci. 9: 476-486.
5. Brune, M., Hunter, J.L., Corrie, J.E.T., and Webb, M.R. 1994. Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment I ATPase. Biochemistry 33: 8262-8271.
6. Brune, M., Hunter, J.L., Howell, S.A., Martin, S.R., Hazlett, T.L., Corrie, J.E.T., and Webb, M.R. 1998. Mechanism of inorganic phosphate interaction with phosphate binding protein from Escherichia coli. Biochemistry 37: 10370-10380.
7. Buckle, A.M., Zahn, R., and Fersht, A.R. 1997. A structural model for GroEL-polypeptide recognition. Proc. Natl. Acad. Sci. 94: 3571-3575.
8. Burston, S.G., Ranson, N.A., and Clarke, A.R. 1995. The origins and consequences of asymmetry in the chaperonin reaction cycle. J. Mol. Biol. 249: 138-152.
9. Chen, L. and Sigler, P.B. 1999. The crystal structure of a GroEL/peptide complex: Plasticity as a basis for substrate diversity. Cell 99: 757-768.
10. Fenton, W.A., Kashi, Y., Furtak, K., and Horwich, A.L. 1994. Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371: 614-619.
11. Flynn, G.C., Chappell, T.G., and Rothman, J.E. 1989. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245: 385-390.
12. Horovitz, A. and Willison, K.R. 2005. Allosteric regulation of chaperonins. Curr. Opin. Struct. Biol. 15: 646-651.
13. Horovitz, A., Bochkareva, E.S., Kovalenko, O., and Girshovich, A.S. 1993. Mutation Ala2 → Ser destabilizes intersubunit interactions in the molecular chaperone GroEL. J. Mol. Biol. 231: 58-64.
14. Horovitz, A., Fridmann, Y., Kafri, G., and Yifrach, O. 2001. Review: Allostery in chaperonins. J. Struct. Biol. 135: 104-114.
15. Hunt, J.F., Weaver, A.J., Landry, S.J., Gierasch, L., and Diesenhofer, J. 1996. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature 379: 37-45.
16. Inobe, T., Makio, T., Takasu-Ishikawa, E., Terada, T.P., and Kuwajima, K. 2001. Nucleotide binding to the chaperonin GroEL: Non-cooperative binding of ATP analogs and ADP, and cooperative effect of ATP. Biochim. Biophys. Acta 1545: 160-173.
17. Kad, N.M., Ranson, N.A., Cliff, M.J., and Clarke, A.R. 1998. Asymmetry, commitment and inhibition in the GroE ATPase cycle impose alternating functions on the two GroEL rings. J. Mol. Biol. 278: 267-278.
18. Kafri, G., Willison, K.R., and Horovitz, A. 2001. Nested allosteric interactions in the cytoplasmic chaperonin containing TCP-1. Protein Sci. 10: 445-449.
19. Koshland Jr., D.E., Némethy, G., and Filmer, D. 1966. Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5: 365-385.
20. McLaughlin, S.H., Smith, H.W., and Jackson, S.E. 2002. Stimulation of the weak ATPase activity of human hsp90 by a client protein. J. Mol. Biol. 315: 787-798.
21. Monod, J., Wyman, J., and Changeux, J.-P. 1965. On the nature of allosteric transitions: A plausible model. J. Mol. Biol. 12: 88-118.
22. Ranson, N.A., Farr, G.W., Roseman, A.M., Gowen, B., Fenton, W.A., Horwich, A.L., and Saibil, H.R. 2001. ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107: 869-879.
23. Rye, H.S., Roseman, A.M., Chen, S., Furtak, K., Fenton, W.A., Saibil, H.R., and Horwich, A.L. 1999. GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings. Cell 97: 325-338.
24. Saibil, H.R., Horwich, A.L., and Fenton, W.A. 2002. Allostery and protein substrate conformational change during GroEL/GroES-mediated protein folding. Adv. Protein Chem. 59: 45-72.
25. Staniforth, R.A., Burston, S.G., Atkinson, T., and Clarke, A.R. 1994. Affinity of chaperonin-60 for a protein substrate and its modulation by nucleotides and chaperonin-10. Biochem. J. 300: 651-658.
26. Thirumalai, D. and Lorimer, G.H. 2001. Chaperonin-mediated protein folding. Annu. Rev. Biophys. Biomol. Struct. 30: 245-269.
27. van der Vaart, A., Ma, J., and Karplus, M. 2004. The unfolding action of GroEL on a protein substrate. Biophys. J. 87: 562-573.
28. Voziyan, P.A. and Fisher, M.T. 2000. Chaperonin-assisted folding of glutamine synthetase under nonpermissive conditions: Off-pathway aggregation propensity does not determine the co-chaperonin requirement. Protein Sci. 9: 2405-2412.
29. Weiss, S., Rossi, R., Pellegrino, M.A., Bottinelli, R., and Geeves, M.A. 2001. Differing ADP release rates from myosin heavy chain isoforms define the shortening velocity of skeletal muscle fibers. J. Biol. Chem. 276: 45902-45908.
30. Yifrach, O. and Horovitz, A. 1995. Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 34: 5303-5308.
31. _. 1996. Allosteric control by ATP of non-folded protein binding to GroEL. J. Mol. Biol. 255: 356-361.
32. _. 1998. Transient kinetic analysis of adenosine 5′-triphosphate binding-induced conformational changes in the allosteric chaperonin GroEL. Biochemistry 37: 7083-7088.
33. _. 2000. Coupling between protein folding and allostery in the GroE chaperonin system. Proc. Natl. Acad. Sci. 97: 1521-1524.