On the mechanism of FtsH-dependent degradation of the σ32 transcriptional regulator of Escherichia coli and the role of the DnaK chaperone machine

Molecular Microbiology

Volumn 31, Issue 1, 1999, Pages 157-166

  Blaszczak, Adam ^a   Georgopoulos, Costa ^b   Liberek, Krzysztof ^a  

^a UNIVERSITY OF GDA SK   (Poland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CHAPERONE; PROTEINASE; RNA POLYMERASE; SIGMA FACTOR;

ARTICLE; AUTOREGULATION; CARBOXY TERMINAL SEQUENCE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN PURIFICATION; TRANSCRIPTION REGULATION;

ATP-DEPENDENT PROTEASES; BACTERIAL PROTEINS; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; SIGMA FACTOR; TRANSCRIPTION FACTORS;

EID: 0032920680     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01155.x     Document Type: Article

References (55)

1. Akiyama, Y., Yoshihisa, T., and Ito, K. (1995) FtsH, a membrane-bound ATPase, forms a complex in the cytoplasmic membrane of Escherichia coli. J Biol Chem 270: 23484-23490.
2. Banecki, B., and Zylicz, M. (1996) Real time kinetics of the DnaK/DnaJ/GrpE molecular chaperone machine. J Biol Chem 271: 6137-6143.
3. Bardwell, J.C.A., and Craig, E.A. (1984) Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous. Proc Natl Acad Sci USA 81: 848-852.
4. 32 factors assembled with RNA polymerase. EMBO J 14: 5085-5093.
5. Bukau, B. (1993) Regulation of the Escherichia coli heat-shock response. Mol Microbiol 9: 671-680.
6. Bukau, B., and Horwich, A.L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92: 351-366.
7. Burgess, R.R., and Jendrisak, J.J. (1975) A procedure for the rapid, large-scale purification of Escherichia coli DNA-dependent RNA polymerase involving polyamin P precipitation and DNA-cellulose chromatography. Biochemistry 14: 4634-4638.
8. Confalonieri, F., and Duguet, M. (1995) A 200-amino-acid ATPase module in search of a basic function. BioEssays 17: 639-650.
9. 32. Cell 69: 833-842.
10. Gamer, J., Multhaup, G., Tomoyasu, T., McCarty, J.S., Rudiger, S., Schonfeld, H.-J., et al. (1996) A cycle of binding and release of DnaK, DnaJ and GrpE chaperones regulates activity of the E. coli heat shock transcription factor sigma 32. EMBO J 15: 607-617.
11. Georgopoulos, C.P. (1971) Bacterial mutants in which the gene N function is blocked have an altered RNA polymerase. Proc Natl Acad Sci USA 68: 2977-2981.
12. Georgopoulos, C., Liberek, K., Zylicz, M., and Ang, D. (1994) Properties of the heat shock proteins of Escherichia coli and the autoregulation of the heat shock response. In The Biology of Heat Shock Proteins and Molecular Chaperones. Morimoto, R.I., Tissieres, A., and Georgopoulos, C. (eds). Cold Spring Harbor NY: Cold Spring Harbor Laboratory Press, pp. 209-249.
13. 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.I., Tissieres, A., and Georgopoulos, C. (eds). Cold Spring Harbor NY: Cold Spring Harbor Laboratory Press, pp. 167-198.
14. 32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc Natl Acad Sci USA 92: 3516-3520.
15. Herman, C., Thevenet, D., Bouloc, P., Walker, G.C., and D'Ari, R. (1998) Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH). Genes Dev 12: 1348-1355.
16. Herman, C., Thevenet, D., D'Ari, R., and Bouloc, P. (1997) The HflB protease of Escherichia coli degrades its inhibitor λclll. J Bacteriol 179: 358-363.
17. 32 mutant with a single amino acid change in the highly conserved region 2.2 exhibits reduced core RNA polymerase affinity. Proc Natl Acad Sci USA 94: 4907-4912.
18. 32 determine core RNA polymerase binding specificity. J Bacteriol 180: 1095-1102.
19. Jubete, Y., Maurizi, M.R., and Gottesman, S. (1996) Role of the heat shock protein DnaJ in the Ion-dependent degradation of naturally unstable proteins. J Biol Chem 271: 30798-30803.
20. 32 and abnormal proteins in Escherichia coli. J Bacteriol 179: 7219-7225.
21. Kihara, A., Akiyama, Y., and Ito, K. (1995) FtsH is required for proteolytic elimination of uncomplexed forms of SecY, an essential protein translocase subunit. Proc Natl Acad Sci USA 92: 4532-4536.
22. Kihara, A., Akiyama, Y., and Ito, K. (1996) A protease complex in the Escherichia coll plasma membrane: HflKC (HflA) forms a complex with FtsH (HflB), regulating its proteolytic activity against SecY. EMBO J 15: 6122-6131.
23. Kumar, A., Mallach, R.A., Fujita, N., Smillie, D., Ishihama, A., and Hayward, R.S. (1993) The minus 35-recognition region of Escherichia coli sigma 70 is inessential for initiation of transcription at an 'extended minus 10' promoter. J Mol Biol 232: 406-418.
24. 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.
25. Liberek, K., and Georgopoulos, C. (1993) Autoregulation of the Escherichia coli heat shock response by the DnaK, DnaJ heat shock proteins. Proc Natl Acad Sci USA 90: 11019-11023.
26. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C., and Zylicz, M. (1991) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA 88: 2874-2878.
27. 32 transcription factor. Proc Natl Acad Sci USA 89: 3516-3520.
28. 70 family: sequence conservation and evolutionary relationship. J Bacteriol 174: 3843-3849.
29. Mensa-Wilmot, K., Seaby, R., Alfano, C., Wold, M.S., Gomes, B., and McMacken, R. (1989) Reconstitution of a nine-protein system that initiates bacteriophage λ DNA replication. J Biol Chem 264: 2853-2861.
30. 32 polypeptide is involved in DnaK-mediated negative control of the heat shock response in Escherichia coli. Proc Natl Acad Sci USA 91: 10280-10284.
31. Pierpaoli, E.V., Sandmeier, E., Baici, A., Schonfeld, H.J., Gisler, S., and Christen, P. (1997) The power stroke of the DnaK/DnaJ/GrpE molecular chaperone system. J Mol Biol 269: 757-768.
32. Prentki, P., and Krisch, H.M. (1984) In vitro insertional mutagenesis with a selectable DNA fragments. Gene 29: 303-313.
33. 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.
34. Sherman, M.Y., and Goldberg, A.L. (1992) Involvement of the chaperonin DnaK in the rapid degradation of a mutant protein in Escherichia coli. EMBO J 11: 71-77.
35. Shetland, Y., Koby, S., Teff, D., Mansur, N., Oren, D.A., Tatematsu, T., et al. (1997) Proteolysis of the phage λ Cll regulatory protein by FtsH (HflB) of Escherichia coli. Mol Microbiol 24: 1303-1310.
36. Silber, K.R., Keiler, K.C., and Sauer, R.T. (1991) Tsp: a tail-specific protease that selectively degrades proteins with nonpolar C termini. Proc Natl Acad Sci USA 89: 295-299.
37. Skowyra, D., Georgopoulos, C., and Zylicz, M. (1990) The Escherichia coli dnaK protein, the hsp70 homologue, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis dependent reaction. Cell 62: 939-944.
38. Straus, D.B., Walter, W.A., and Gross, C.A. (1988) Escherichia coli heat shock gene mutants are defective in proteolysis. Genes Dev 2: 1851-1858.
39. 32 is reduced under conditions of excess heat shock protein production in Escherichia coli. Genes Dev 3: 2003-2010.
40. 32. Genes Dev 4: 2202-2209.
41. Szabo, A., Langer, T., Schroder, 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.
42. 32. J Bacteriol 171: 1585-1589.
43. Tomoyasu, T., Yamanaka, K., Murata, K., Suzuki, T., Bouloc, P., Kato, A., et al. (1993a) Topology and subcellular organization of FtsH protein in Escherichia coli. J Bacteriol 175: 1352-1357.
44. Tomoyasu, T., Yuki, T., Morimura, S., Mori, H., Yamanaka, K., Niki, H., et al. (1993b) The Escherichia coli FtsH protein is a prokaryotic member of a family of putative ATPases involved in membrane function, cell cycle control and gene expression. J Bacteriol 175: 1344-1351.
45. 32. EMBO J 14: 2551-2560.
46. Waghorne, C., and Fuerst, C.R. (1985) Involvement of the htpR gene product of Escherichia coli in phage lambda development. Virology 141: 51-64.
47. Wawrzynów, A., and Zylicz, M. (1995) Divergent effects of ATP on binding of the DnaK and DnaJ chaperones to each other, or to their various native and denatured protein substrates. J Biol Chem 270: 19300-19306.
48. 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.
49. Wickner, S., Hoskins, J., and McKenney, K. (1991) Monomerization of RepA dimers by heat shock proteins activates binding to DNA replication origin. Proc Natl Acad Sci USA 88: 7903-7907.
50. Yura, T., Nagai, H., and Mori, H. (1993) Regulation of the heat-shock response in bacteria. Annu Rev Microbiol 47: 321-350.
51. 32). J Bacteriol 170: 3640-3649.
52. Ziemienowicz, A., Skowyra, D., Zeilstra-Ryalls, J., Fayet, O., Georgopoulos, C., and Zylicz, M. (1993) Either of the Escherichia coli GroEL/GroES and DnaK/DnaJ/GrpE chaperone machines can reactivate heat-treated RNA polymerase: different mechanisms for the same activity. J Biol Chem 268: 25425-25431.
53. Ziemienowicz, A., Zylicz, M., Floth, C., and Hubscher, U. (1995) Calf thymus Hsc70 protein protects and reactivates prokaryotic and eukaryotic enzymes. J Biol Chem 270: 15479-15484.
54. Zubay, G. (1980) The isolation and properties of CAP the catabolite gene activator. Methods Enzymol 65: 856-877.
55. Zylicz, M., Ang, D., Liberek, K., and Georgopoulos, C. (1989) Initiation of λ DNA replication with purified host- and bacteriophage-encoded proteins. EMBO J 8: 1601-1608.