Protein folding in the cytoplasm of Escherichia coli: Requirements for the DnaK-DnaJ-GrpE and GroEL-GroES molecular chaperone machines

Molecular Microbiology

Volumn 21, Issue 6, 1996, Pages 1185-1196

  Thomas, Jeffrey G ^a   Baneyx, François ^a  

^a University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN FOLDING;

ESCHERICHIA COLI;

EID: 0029786163     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1996.651436.x     Document Type: Article

References (61)

1. Anfinsen, C.B. (1973) Principles that govern the folding of protein chains. Science 181: 223-230.
2. Ayling, A., and Baneyx, F. (1996) Influence of the GroE molecular chaperone machine on the in vitro refolding of Escherichia coli β-galactosidase. Protein Sci 5: 478-487.
3. Baker, T.A., Grossman, A.D., and Gross, C.A. (1984) A gene regulating the heat shock response in Escherichia coli also affects proteolysis. Proc Natl Acad Sd USA 81: 6779-6783.
4. Baneyx, F., and Gatenby, A.A. (1992) A mutation in GroEL interferes with protein folding by reducing the rate of discharge of sequestered polypeptides. J Biol Chem 267: 11637-11644.
5. Braig, K., Otwinowski, Z., Hedge, R., Boisvert, D.C., Joachimiak, A., Norwich, A.L., and Sigler, P.B. (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 371: 578-586.
6. Breton, J., La Fiura, A., Bertolero, F., Orsini, G., Valsasina, B., Ziliotto, R., De Filippis, V., Polverino de Laureto, P., and Fontana, A. (1995) Structure, stability and biological properties of a N-terminally truncated form of recombinant human interleukin-6 containing a single disulphide bond. Eur J Biochem 227: 573-581.
7. Buchner, J., Pastan, I., and Brinkmann, U. (1992) A method for increasing the yield of properly folded recombinant fusion proteins: single-chain immunotoxins from renaturation of bacterial inclusion bodies. Anal Biochem 205: 263-270.
8. + oxidoreductase in Escherichia coli requires GroE molecular chaperones. J Biol Chem 267: 15537-15541.
9. Ellis, R.J., and van der Vies, S.M. (1991) Molecular chaperones. Annu Rev Biochem 60: 321-347.
10. Escher, A., and Szalay, A.A. (1993) GroE-mediated folding of bacterial luciferases in vivo. Mol Gen Genet 238: 65-73.
11. Fink, A.L. (1995) Compact intermediate states in protein folding. Annu Rev Biophys Biomol Struct 24: 495-522.
12. Gaitanaris, G.A., Vysokanov, A., Hung, S.-C., Gottesman, M.E., and Gragerov, A. (1994) Successive action of Escherichia coli chaperones in vivo. 14: 861-869.
13. Georgopoulos, C., and Welch, W.J. (1993) Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol 9: 601-634.
14. Georgopoulos, C., Ang, D., Liberek, L., and Zylicz, M. (1990) Properties of the Escherichia coli heat shock proteins and their role in bacteriophage λ. growth. In Stress Proteins in Biology and Medicine. Morimoto, R., Tissieres, A., and Georgopoulos, C. (eds). Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press, pp. 191-221.
15. Goloubinoff, P., Gatenby, A.A., and Lorimer, G.H. (1989) GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature 337: 44-47.
16. Gragerov, A.L., Martin, E.S., Krupenko, M.A., Kashlev, M.V., and Nikiforov, V.G. (1991) Protein aggregation and inclusion body formation in Escherichia coli rpoH mutant defective in heat shock protein induction. FEBS Lett 291: 222-224.
17. Gragerov, A.L., Nudler, E., Komissarova, N., Gaitanaris, G.A., Gottesman, M.E., and Nikiforov, V.G. (1992) Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc Natl Acad Sci USA 89: 10341-10344.
18. Gross, C.A. (1996) Function and regulation of the heat shock proteins. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. 2nd edn. Neidhardt, F.C. (ed.). Washington DC: American Society for Microbiology, pp. 1382-1399.
19. Gross, C.A., Straus, D.B., Erickson, J.W., and Yura, T. (1990) The function and regulation of heat shock proteins in Escherichia coli. In Stress Proteins in Biology and Medicine. Morimoto, R., Tissieres, A., and Georgopoulos, C. (eds). Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press, pp. 167-190.
20. Hartl, F.U., and Martin, J. (1995) Molecular chaperones in cellular protein folding. Curr Opin Struct Biol 5: 92-102.
21. Horwich, A.L., Low, K.B., Fenton, W.A., Hirshfield, I.N., and Furtak, K. (1993) Folding in vivo of bacterial cytoplasmic proteins: role of GroEL. Cell 74: 909-917.
22. Kanemori, M., Mori, H., and Yura, T. (1994) Effects of reduced levels of GroE chaperones on protein metabolism: enhanced synthesis of heat shock proteins during steady-state growth of Escherichia coli. J Bacteriol 176: 4235-4242.
23. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M.K., and Hartl, F.U. (1992) Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356: 683-689.
24. Lee, S.C., Choi, Y.C., and Yu, M.-H. (1990) Effect of the N-terminal hydrophobic sequence of hepatitis B virus surface antigen on the folding and assembly of hybrid β-galactosidase in Escherichia coli. Eur J Biochem 187: 417-424.
25. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C., and Zylicz, M. (1991a) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sd USA 88: 2874-2878.
26. Liberek, K., Skowyra, D., Zylicz, M., Johnson, C., and Georgopoulos, C. (1991b) The Escherichia coli DnaK chaperone, the 70kDa heat shock protein eukaryotic equivalent, changes conformation upon ATP hydrolysis thus triggering its dissociation from a bound target protein. J Biol Chem 266: 14491-14496.
27. 32 heat shock transcriptional regulator. Proc Natl Acad Sci USA 92: 6224-6228.
28. Lorimer, G.H. (1996) A quantitative assessment of the role of the chaperonin proteins in protein folding in vivo. FASEB J 10: 5-9.
29. Mayhew, M., da Silva, A.C., Martin, J., Erdjument-Bromage, H., Tempst, P., and Hartl, F.U. (1996) Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature 379: 420-426.
30. McCarty, J.S., Buchberger, A., Reinstein, J., and Bukau, B. (1995) The role of ATP in the functional cycle of the DnaK chaperone system. J Mol Biol 249: 126-137.
31. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press, pp. 352-355.
32. Mitraki, A., and King, J. (1989) Protein folding intermediates and inclusion body formation. Biotechnology 7: 690-697.
33. Neidhardt, F.C., and VanBogelen, R.A. (1987) The heat shock response. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington DC: American Society for Microbiology, pp. 1334-1345.
34. 32, the Escherichia coli heat shock transcription factor. Protein Expr Purif 4: 425-433.
35. Pierce, J., and Gutteridge, S. (1985) Large-scale preparation of ribulosebisphosphate carboxylase from a recombinant system in Escherichia coli characterized by extreme plasmid instability. Appl Environ Microbiol 49: 1094-1100.
36. Pullen, J.K., Liang, S.M., Blake, M.S., Mates, S., and Tai, J.Y. (1995) Production of Haemophilus influenzae type-b porin in Escherichia coli and its folding into the trimeric form. Gene 152: 85-88.
37. Rudolph, R., and Lilie, H. (1996) In vitro folding of inclusion body proteins. FASEB J 10: 49-56.
38. Schröder, H., Langer, T., Hartl, F.-U., and Bukau, B. (1993) DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J 12: 4137-4144.
39. Sherman, M.Y., and Goldberg, A.L. (1992a) Involvement of the chaperonin DnaK in the rapid degradation of mutant protein in Escherichia coli. EMBO J 11: 71-77.
40. Sherman, M.Y., and Goldberg, A.L. (1992b) Heat shock in Escherichia coli alters the protein-binding properties of the chaperonin groEL by inducing its phosphorylation. Nature 357: 167-169.
41. Sherman, M.Y., and Goldberg, A.L. (1993) Heat shock of Escherichia coli increases binding of dnaK (the hsp70 homolog) to polypeptides by promoting its phosphorylation. Proc Natl Acad Sci USA 90: 8648-8652.
42. Skerra, A. (1993) Bacterial expression of immunoglobulin fragments. Curr Op Immunol 5: 256-262.
43. Somerville, C.R., and Somerville, S.C. (1984) Cloning and expression of the Rhodospirillum rubrum ribulosebisphosphate carboxylase gene in E. coli. Mol Gen Genet 193: 214-219.
44. Strandberg, L., and Enfors, S.-O. (1991) Factors influencing inclusion body formation in the production of a fused protein in Escherichia coli. Appl Environ Microbiol 57: 1669-1674.
45. Stempfer, G., Höll-Neugebauer, B., and Rudolph, R. (1996) Improved refolding of an immobilized fusion protein. Nature Biotech 14: 329-334.
46. Studier, F.W., and Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
47. Szabo, A., Langer, T., Schröder, H., Flanagan, J., Bukau, B., and Hartl, F.U. (1994) The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system - DnaK, DnaJ, and GrpE. Proc Natl Acad Sci USA 91: 10345-10349.
48. Thomas, J.G., and Baneyx, F. (1996a) Influence of a global deregulation of the heat-shock response on the expression of heterologous proteins in Escherichia coli. Ann N Y Acad Sci 782: 478-485.
49. Thomas, J.G., and Baneyx, F. (1996b) Protein misfolding and inclusion body formation in recombinant Escherichia coli cells overexpressing heat-shock proteins. J Biol Chem 271: 11141-11147.
50. Tilly, K., Murialdo, H., and Georgopoulos, C. (1981) Identification of a second Escherichia coli groE gene whose product is necessary for bacteriophage morphogenesis. Proc Natl Acad Sci USA 78: 1629-1633.
51. Viitanen, P.V., Gatenby, A.A., and Lorimer, G.H. (1992) Purified chaperonin (GroEL) interacts with the nonnative states of a multitude of Escherichia coli proteins. Protein Sci 1: 363-369.
52. 2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the ATPase activity of DnaK and are sufficient for λ replication. J Biol Chem 269: 5446-5451.
53. Wall, D., Zylicz, M., and Georgopoulos, C. (1995) The conserved G/F motif of the DnaJ chaperone is necessary for the activation of the substrate binding properties of the DnaK chaperone. J Biol Chem 270: 2139-2144.
54. Wawrzynów, A., Banecki, B., Wall., D., Liberek, K., Georgopoulos, C., and Zylicz, M. (1995) ATP hydrolysis is required for the DnaJ-dependent activation of DnaK chaperone for binding to both native and denatured protein substrates. J Biol Chem 270: 19307-19311.
55. Weissman, J.S., Hohl, C.M., Kovalenko, O., Kashi, Y., Chen, S., Braig, K., Saibil, H.R., Fenton, W.A., and Horwich, A.L. (1995) Mechanism of GroEL action: productive release of polypeptide from a sequestered position under GroES. Cell 83: 577-587.
56. 2) of mammalian mitochondrial branched-chain α-keto decarboxylase in Escherichia coli. J Biol Chem 267: 12400-12403.
57. Xiang, J., Qi, Y., Luo, X., and Liu, E. (1993) Recombinant bifunctional molecule FV/IFN-γ possesses the anti-tumor FV as well as the gamma Interferon activities. Cancer Biother 8: 327-337.
58. Xie, Y., and Wetlaufer, D.B. (1996) Control of aggregation in protein refolding: the temperature-leap tactic. Protein Sci 5: 517-523.
59. Yochem, J., Uchida, H., Sunshine, M., Saito, H., Georgopoulos, C.P., and Feiss, M. (1978) Genetic analysis of two genes, dnaJ and dnaK, necessary for Escherichia coli and bacteriophage lambda DNA replication. Mol Gen Genet 164: 9-14.
60. Zeilstra-Ryalls, J., Fayet, O., Baird, L., and Georgopoulos, C. (1993) Sequence analysis and phenotypic characterization of groEL mutations that block λ and T4 bacteriophage growth. J Bacteriol 175: 1134-1143.
61. Zylicz, M., Ang, D., and Georgopoulos, C. (1987) The grpE protein of Escherichia coll. J Biol Chem 262: 17437-17442.