Asymmetry, commitment and inhibition in the GroE ATPase cycle impose alternating functions on the two GroEL rings

Journal of Molecular Biology

Volumn 278, Issue 1, 1998, Pages 267-278

  Kad, Neil M ^a   Ranson, Neil A ^a   Cliff, Matthew J ^a   Clarke, Anthony R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Chaperonin; GroE; Non competitive inhibition; Protein folding; Transient kinetics

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CHAPERONIN; GLUCOSE; HEXOKINASE; NUCLEOTIDE;

ARTICLE; ENZYME INHIBITION; HYDROLYSIS; KINETICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 0032562652     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1704     Document Type: Article

References (38)

1. 2 hetero-oligomer. Proc. Natl Acad. Sci. USA. 92:1995;12021-12025
2. Badcoe I.G., Smith C.J., Wood S., Halsall D.J., Holbrook J.J., Lund P., Clarke A.R. Binding of a chaperonin to the folding intermediates of lactate dehydrogenase. Biochemistry. 30:1991;9195-9200
3. Bochkareva E.S., Girshovich A.S. ATP induces non-identity of two rings in chaperonin GroEL. J. Biol. Chem. 269:1994;23869-23971
4. Bochkareva E.S., Lissin N.M., Flynn G.C., Rothman J.E., Girshovich A.S. Positive co-operativity in the functioning of molecular chaperone GroEL. J. Biol. Chem. 267:1992;11637-11644
5. Braig K., Otwinowski Z., Hegde R., Boisvert D.C., Joachimiak A., Horwich A.L., Sigler P.B. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å Nature. 371:1994;578-586
6. Burston S.G., Ranson N.A., Clarke A.R. The origins and consequences of asymmetry in the chaperonin reaction cycle. J. Mol. Biol. 249:1995;138-152
7. Burston S.G., Weissman J.S., Farr G.W., Fenton W.A., Horwich A.L. Native and non-native forms of a protein substrate are released from a cis-only form of GroEL. Nature. 383:1996;96-99
8. Chandrasekhar G.N., Tilly K., Woolford C., Hendrix R., Georgopoulos C. Purification and properties of the GroES morphogenetic protein of Escherichia coli. J. Biol. Chem. 261:1986;. 12424-12419
9. Chen S., Roseman A.M., Hunter A.S., Wood S.P., Burston S.G., Ranson N.A., Clarke A.R., Saibil H.R. Location of a folding protein and shape changes in GroEL-GroES complexes imaged by cryo-electron microscopy. Nature. 371:1994;261-264
10. Fayet O., Ziegelhoffer T., Georgopoulos C.M. The GroES and GroEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J. Bacteriol. 171:1989;1379-1385
11. Fisher M.T. The rates of commitment renaturation of rhodanese and glutamine synthetase in the presence of the GroE chaperonins. J. Biol. Chem. 269:1994;29589-29601
12. Gray T.E., Fersht A.R. Co-operativity in ATP hydrolysis by GroEL is increased by GroES. FEBS Letters. 292:1991;254-258
13. Goloubinoff P., Gatenby A.A., Lorimer G.H. GroE heat shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers inEscherichia coli. Nature. 337:1989;44-47
14. Hayer-Hartl M.K., Martin J., Hartl F.U. Asymmetrical interaction of GroEL and GroES in the ATPase cycle of assisted protein-folding. Science. 269:1995;836-841
15. Hemmingsen S.M., Woolford C., Van der Vies S.M., Tilly K., Dennis D.T., Georgopolous C.P., Hendrix R.W., Ellis R.J. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature. 333:1988;330-334
16. Hunt J.F., Weaver A.J., Landry S.J., Gierasch L., Deisenhofer J. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature. 379:1996;37-45
17. Jackson G.S., Staniforth R.A., Halsall D.J., Atkinson T., Holbrook J.J., Clarke A.R., Burston S.G. Binding and hydrolysis of nucleotides in the chaperonin catalytic cycle implications for the mechanisms of assisted protein folding. Biochemistry. 32:1993;2554-2563
18. Kouyama T., Mihashi K. Fluorimetry study of N-1-pyrene-iodoacetamide-labelled F-actin-local structural change of actin promoter both on polymerization and on binding of heavy-meromyosin. Eur. J. Biochem. 144:1981;33-38
19. Llorca O., Marco S., Carrascosa J.L., Valpuesta J.M. The formation of symmetrical GroEL-GroES complexes in the presence of ATP. FEBS Letters. 345:1994;181-186
20. Martin J., Langer T., Boteva R., Schramel A., Horwich A.L., Hartl F.U. Chaperonin-mediated protein folding at the surface of GroEL through a "molten-globule"-like intermediate. Nature. 352:1991;36-42
21. Martin J., Mayhew M., Langer T., Hartl F.U. The reaction cycle of GroEL and GroES in chaperonin-assisted protein folding. Nature. 366:1993;228-233
22. Mayhew M., da Silva A.C.R., Martin J., Erdjument-Bromage H., Tempst P., Hartl F.U. Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature. 379:1996;420-426
23. Ranson N.A., Dunster N.J., Burston S.G., Clarke A.R. Chaperonins can reverse the early aggregation steps when a protein misfolds. J. Mol. Biol. 250:1995;581-586
24. Ranson N.A., Burston S.G., Clarke A.R. Binding, encapsulation and ejection; substrate dynamics during a chaperonin-assisted folding reaction. J. Mol. Biol. 266:1997;656-664
25. Roseman A., Chen S., White H., Braig K., Saibil H. The chaperonin ATPase cycle mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell. 87:1996;241-251
26. Rye H.S., Burston S.G., Fenton W.A., Beecham J.M., Xu Z., Sigler P.B., Horwich A.L. Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature. 388:1997;792-798
27. Saibil H., Dong Z., Wood S., auf der Mauer A. Binding of chaperonins. Nature. 353:1991;25-26
28. Schmidt M., Rutkat K., Rachel R., Pfeifer G., Jaenicke R., Viitanen P.V., Lorimer G.H., Buchner J. Symmetric complexes of GroE chaperonins as part of the functional cycle. Science. 265:1994;656-659
29. Staniforth R.A., Burston S.G., Atkinson T., Clarke A.R. Affinity of chaperonin-60 for a protein substrate and its modulation by nucleotides and chaperonin-10. Biochem. J. 300:1994;651-658
30. Taguchi H., Yoshida M. Chaperonin release the substrate protein in a form with tendency to aggregate and ability to rebind to chaperonin. FEBS Letters. 359:1995;195-198
31. Todd M.J., Viitanen P.V., Lorimer G.H. Dynamics of the chaperonin ATPase implications for facilitated protein folding. Science. 265:1994;659-666
32. Weissman J.S., Kashi Y., Fenton W.A., Horwich A.L. GroEL-mediated protein folding proceeds by multiple rounds of binding and release of non-native forms. Cell. 78:1994;693-702
33. Weissman J.S., Hohl C.M., Kovalenko O., Kashi Y., Chen S., Braig K., Saibil H.R., Fenton W.A., Horwich A.L. Mechanism of GroEL action productive release of polypeptide from a sequestered position under GroES. Cell. 83:1995;577-587
34. Weissman J.S., Rye H.S., Fenton W.A., Beecham J.M., Horwich A.L. Characterisation of the active intermediate of a GroEL-GroES mediated protein folding reaction. Cell. 84:1996;481-490
35. 7 chaperonin complex. Nature. 388:1997;741-750
36. Yifrach O., Horovitz A. Two lines of allosteric communications in the oligomeric chaperonin GroEL are revealed by the single mutation Arg196 → Ala. J. Mol. Biol. 243:1994;397-401
37. Yifrach O., Horovitz A. Nested co-operativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry. 34:1995;5303-5308
38. Yifrach O., Horovitz A. Allosteric control by ATP of non-folded protein binding to GroEL. J. Mol. Biol. 255:1996;356-361