Protein folding and unfolding by Escherichia coli chaperones and chaperonins

Current Opinion in Microbiology

Volumn 3, Issue 2, 2000, Pages 197-202

  Gottesman, Max E ^a   Hendrickson, Wayne A ^b  

^a Columbia University ^*  (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CHAPERONIN; HEAT SHOCK PROTEIN 90;

CRYSTAL STRUCTURE; DNA PROTEIN COMPLEX; ENZYME SUBUNIT; ESCHERICHIA COLI; NONHUMAN; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0034025903     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(00)00075-8     Document Type: Review

References (49)

1. Zhu X., Zhao X., Burkholder W.F., Gragerov A., Ogata C.M., Gottesman M.E., Hendrickson W.A. Structural analysis of substrate binding by the molecular chaperone DnaK. Science. 272:1996;1606-1614.
2. Wang H., Kurochkin A.V., Pang Y., Hu W., Flynn G.C., Zuiderweg E.R. NMR solution structure of the 21 kDa chaperone protein DnaK substrate binding domain. a preview of chaperone-protein interaction Biochemistry. 37:1998;7929-7940.
3. Harrison C.J., Hayer-Hartl M., Di Liberto M, Hartl F., Kuriyan J. Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science. 276:1997;431-435.
4. Flaherty K.M., DeLuca-Flaherty C., McKay D.B. Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature. 346:1990;623-628.
5. Sriram M., Osipiuk J., Freeman B.C., Morimoto R.I., Joachimiak A. Human Hsp70 molecular chaperone binds two calcium ions within the ATPase domain. Structure. 5:1997;403-414.
6. Stebbins C.E., Russo A.A., Schneider C., Rosen N., Hartl F.U., Pavletich N.P. Crystal structure on an Hsp90-geldanamycin complex. targeting of a protein chaperone by an antitumor agent Cell. 89:1997;239-250.
7. Prodromou C., Roe S.M., Piper P.W., Pearl L.H. A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone. Nat Struct Biol. 4:1997;477-482.
8. Dutta R., Inouye M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci. 25:2000;24-28.
9. Pellecchia M., Szyperski T., Wall D., Georgopoulos C., Wuthrich K. NMR structure of the J-domain and the Gly/Phe-rich region of the Escherichia coli DnaJ chaperone. J Mol Biol. 260:1996;236-250.
10. Huang K., Flanagan J.M., Prestegard J.H. The influence of C-terminal extension on the structure of the 'J-domain' in E. coli DnaJ. Protein Sci. 8:1999;203-214.
11. Qian Y.Q., Patel D., Hartl F.U., McColl D.J. Nuclear magnetic resonance solution structure of the human hsp40 (HDJ-1) J-domain. J Mol Biol. 260:1996;224-235.
12. Szabo A., Korszun R., Hartl F.U., Flanagan J. A zinc finger-like domain of the molecular chaperone DnaJ is involved in binding to denatured protein substrates. EMBO J. 15:1996;408-417.
13. de Crouy-Chanel A., Kohiyama M., Richarme G. Interaction of DnaK with native proteins and membrane proteins correlates with their accessible hydrophobicity. Gene. 30:1999;163-170.
14. Blaszczak A., Georgopoulos C., Liberek K. On the mechanism of FtsH-dependent degradation of the sigma 32 transcriptional regulator of Escherichia coli and the role of the DnaK chaperone machine. Mol Microbiol. 1:1999;157-166.
15. Shotland Y., Koby S., Teff D., Mansur N., Oren D.A., Tatematsu K., Tomoyasu T., Kessel M., Bukau B., Ogura T., Oppenheim A.B. Proteolysis of the phage lambda CII regulatory protein by FtsH (HflB) of Escherichia coli. Mol Microbiol. 24:1997;1303-1310.
16. Gaitanaris G.A., Vysokanov A., Gottesman M.E., Gragerov A. Successive action of Escherichia coli chaperones in vivo. Mol Microbiol. 14:1994;861-870.
17. Slepenkov S.V., Witt S.N. Peptide-induced conformational changes in the molecular chaperone DnaK. Biochemistry. 37:1998;16749-16756.
18. Slepenkov S.V., Witt S.N. Kinetics of the reactions of the Escherichia coli molecular chaperone DnaK with ATP: evidence that a three-step reaction precedes ATP hydrolysis. Biochemistry. 37:1998;1015-1024.
19. Montgomery D.L., Morimoto R.I., Gierasch L.M. Mutations in the substrate binding domain of the Escherichia coli 70 kDa molecular chaperone, DnaK, which alter substrate affinity or interdomain coupling. J Mol Biol. 286:1999;915-932. A DnaK mutant (K414I) that affects coupling between the ATPase and peptide domains is described. The K414I mutation lies close to the linker region to the ATPase domain. K414I has elevated ATPase activity and reduced peptide-stimulated ATPase activity, ATP-induced changes in tryptophan fluorescence, and ATP-induced peptide release.
20. Suh W.C., Burkholder W.F., Lu C.Z., Zhao X., Gottesman M.E., Gross C.A. Interaction of the Hsp70 molecular chaperone, DnaK, with its cochaperone DnaJ. Proc Natl Acad Sci USA. 95:1998;15223-15228. Allele-specific suppression analysis and biochemical studies show that DnaJ binds to at least two sites on DnaK: under the ATPase domain in a cleft between its two subdomains and at or near the pocket of substrate binding. Binding to the ATPase domain involves the J-domain of DnaJ.
21. Laufen T., Mayer M.P., Beisel C., Klostermeier D., Mogk A., Reinstein J., Bukau B. Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc Natl Acad Sci USA. 96:1999;5452-5457. At low concentrations, DnaJ efficient stimulation of DnaK ATPase requires a protein substrate of DnaK, indicating a synergistic action of DnaJ and substrate. Peptide substrates were poorly effective, suggesting a mechanism to prevent peptide "jamming" of the substrate domain.
22. 2+. Implications for the mechanism of nucleotide exchange. J Biol Chem. 270:1995;26282-26285.
23. Zylicz M., Wawrzynow A., Marszalek J., Liberek K., Banecki B., Konieczny I., Blaszczak A., Barski P., Jakobkiewicz J., Gonciarz-Swiatek M.et al. Role of chaperones in replication of bacteriophage lambda DNA. Bukau B. Molecular Chaperones and Folding Catalysts. 1999;Harwood Academic Publishers, Amsterdam, The Netherlands.
24. Zolkiewski M. ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J Biol Chem. 274:1999;28083-28086.
25. Mogk A., Tomoyasu T., Goloubinoff P., Rudiger S., Roder D., Langen H., Bukau B. Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 18:1999;6934-6949. DnaK prevents aggregation of proteins during denaturation and acts cooperatively with ClpB to solubilize aggregates of denatured proteins.
26. Goloubinoff P., Mogk A., Zvi A.P., Tomoyasu T., Bukau B. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci USA. 96:1999;13732-71373.
27. Motohashi K., Watanabe Y., Yohda M., Yoshida M. Heat-inactivated proteins are rescued by the DnaK. J-GrpE set and ClpB chaperones. Proc Natl Acad Sci USA. 96:1999;7184-7189.
28. Deuerling E., Schulze-Specking A., Tomoyasu T., Mogk A., Bukau B. Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature. 400:1999;693-696.
29. Caldas T., Laalami S., Richarme G. Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2. J Biol Chem. 275:2000;855-860.
30. Nadeau K., Das A., Walsh C.T. Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J Biol Chem. 268:1993;1479-1487.
31. 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 2.8Å Nature. 371:1994;578-586.
32. Boisvert D.C., Wang J., Otwinowski Z., Horwich A.L., Sigler P.B. The 2.4Å crystal structure of the bacterial chaperonin GroEL complexed with ATP gamma S. Nat Sruct Biol. 3:1996;170-177.
33. Buckle A.M., Zahn R., Fersht A.R. A structural model for GroEL-polypeptide recognition. Proc Natl Acad Sci USA. 94:1997;3571-3575.
34. Chen L., Sigler P.B. The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. Cell. 99:1999;757-768. Non-native conformations of diverse protein substrates bind to the apical domains surrounding the opening of the central cavity of the GroEL double toroid. The crystal structures of the complexes formed by a strongly bound peptide with the isolated apical domain, and with GroEL were determined. The peptide interacts with the groove between paired α helices in a manner similar to that of the GroES mobile loop. The tight promiscuous binding of non-native substrates and their release into the shielded cis assembly can be accounted for by various modes of molecular plasticity.
35. Hunt J.F., Weaver A.J., Landry S.J., Gierasch L., Deisenhofer J. The crystal structure of the GroES co-chaperonin at 2.8Å resolution. Nature. 379:1996;37-45.
36. Roseman A.M., Chen S., White H., Braig K., Saibil H.R. The chaperonin ATPase cycle. mechanism of allosteric switching and movements of substrate-binding domains in GroEL Cell. 87:1996;241-251.
37. Xu Z., Horawich A.L., Sigler P.B. The crystal structure of the asymmetric GroEL-GroEs-(ADP)7 chaperonin complex. Nature. 388:1997;741-750.
38. Houry W.A., Frishman D., Eckerskorn C., Lottspeich F., Hartl F.U. Identification of in vivo substrates of the chaperonin GroEL. Nature. 402:1999;147-154. GroEL interacts strongly with approximately 300 newly translated polypeptides, some of which are structurally unstable and repeatedly rebind to GroEL. GroEL substrates consist preferentially of two or more domains with αβ-folds, which contain α-helices and buried β-sheets with extensive hydrophobic surfaces.
39. Wang Z., Feng Hp, Landry S.J., Maxwell J., Gierasch L.M. Basis of substrate binding by the chaperonin GroEL. Biochemistry. 38:1999;12537-12546.
40. Chatellier J., Buckle A.M., Fersht A.R. GroEL recognises sequential and non-sequential linear structural motifs compatible with extended beta-strands and alpha-helices. J Mol Biol. 292:1999;163-172. GroEL can bind a wide range of structures, from extended β-strands and α-helices to folded states, with exposed side-chains. The binding site can accommodate substrates of approximately 18 residues when in a helical or seven residues when in an extended conformation. In addition to holding folding intermediates via contacts with many motifs, GroEL promotes unfolding by binding an extended sequential conformation of the substrate.
41. Horwich A.L., Weber-Ban E.U., Finley D. Chaperone rings in protein folding and degradation. Proc Natl Acad Sci USA. 96:1999;11033-11040.
42. Rye H.S., Roseman A.M., Chen S., Furtak K., Fenton W.A., Saibil H.R., Horwich A.L. GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings. Cell. 97:1999;325-338. Hydrolysis of ATP within the cis ring of GroEL reorients the apical domains of the trans ring, allowing the binding of non-native polypeptide or GroES to the trans ring. Subsequently, formation of a new cis-ternary complex proceeds on the open trans ring. Polypeptide binds first, which stimulates the ATP-dependent dissociation of the cis complex, followed by GroES binding. GroEL alternates its rings as folding-active cis complexes, hydrolysing seven ATPs per folding cycle.
43. Sakikawa C., Taguchi H., Makino Y., Yoshida M. On the maximum size of proteins to stay and fold in the cavity of GroEL underneath GroES. J Biol Chem. 274:1999;21251-21256.
44. Wynn R.M., Song J.L., Chuang D.T. GroEL/GroES promote Dissociation/Reassociation cycles of a heterodimeric intermediate during alpha(2)beta(2) protein assembly. Iterative annealing at the quaternary structure level. J Biol Chem. 275:2000;2786-2794.
45. Kandror O., Sherman M., Goldberg A. Rapid degradation of an abnormal protein in Escherichia coli proceeds through repeated cycles of association with GroEL. J Biol Chem. 274:1999;37743-37749.
46. Horwich A.L., Weber-Ban E.U., Finley D. Chaperone rings in protein folding and degradation. Proc Natl Acad Sci USA. 96:1999;11033-11040.
47. Pak M., Hoskins J.R., Singh S.K., Maurizi M.R., Wickner S. Concurrent chaperone and protease activities of ClpAP and the requirement for the N-terminal ClpA ATP binding site for chaperone activity. J Biol Chem. 274:1999;19316-19322. Chaperone and protease activities occur concurrently in ClpAP complexes, as seen in a single round of binding of the phage P1 RepA protein to ClpAP and ATP-dependent release.
48. Weber-Ban E.U., Reid B.G., Miranker A.D., Horwich A.L. Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature. 401:1999;90-93. ClpA can unfold stable, native proteins in the presence of ATP. This was demonstrated using a stable monomeric protein, the green fluorescent protein GFP, tagged with an 11-amino-acid carboxy-terminal recognition peptide, which is responsible for recruiting truncated proteins to ClpAP for degradation.
49. Wang J., Hartling J.A., Flanagan J.M. The structure of ClpP at 2.3Å resolution suggests a model for ATP-dependent proteolysis. Cell. 91:1997;447-456.