Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Apr 11;92(8):3516–3520. doi: 10.1073/pnas.92.8.3516

Degradation of sigma 32, the heat shock regulator in Escherichia coli, is governed by HflB.

C Herman 1, D Thévenet 1, R D'Ari 1, P Bouloc 1
PMCID: PMC42198  PMID: 7724592

Abstract

The heat shock response in Escherichia coli is governed by the concentration of the highly unstable sigma factor sigma 32. The essential protein HflB (FtsH), known to control proteolysis of the phage lambda cII protein, also governs sigma 32 degradation: an HflB-depleted strain accumulated sigma 32 and induced the heat shock response, and the half-life of sigma 32 increased by a factor up to 12 in mutants with reduced HflB function and decreased by a factor of 1.8 in a strain overexpressing HflB. The hflB gene is in the ftsJ-hflB operon, one promoter of which is positively regulated by heat shock and sigma 32. The lambda cIII protein, which stabilizes sigma 32 and lambda cII, appears to inhibit the HflB-governed protease. The E. coli HflB protein controls the stability of two master regulators, lambda cII and sigma 32, responsible for the lysis-lysogeny decision of phage lambda and the heat shock response of the host.

Full text

PDF
3516

Images in this article

3518Fig. 2
on p.3518
3519Fig. 4
on p.3519
3519Fig. 5
on p.3519

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akiyama Y., Ogura T., Ito K. Involvement of FtsH in protein assembly into and through the membrane. I. Mutations that reduce retention efficiency of a cytoplasmic reporter. J Biol Chem. 1994 Feb 18;269(7):5218–5224. [PubMed] [Google Scholar]
  2. Amann E., Brosius J., Ptashne M. Vectors bearing a hybrid trp-lac promoter useful for regulated expression of cloned genes in Escherichia coli. Gene. 1983 Nov;25(2-3):167–178. doi: 10.1016/0378-1119(83)90222-6. [DOI] [PubMed] [Google Scholar]
  3. Bahl H., Echols H., Straus D. B., Court D., Crowl R., Georgopoulos C. P. Induction of the heat shock response of E. coli through stabilization of sigma 32 by the phage lambda cIII protein. Genes Dev. 1987 Mar;1(1):57–64. doi: 10.1101/gad.1.1.57. [DOI] [PubMed] [Google Scholar]
  4. Banuett F., Herskowitz I. Identification of polypeptides encoded by an Escherichia coli locus (hflA) that governs the lysis-lysogeny decision of bacteriophage lambda. J Bacteriol. 1987 Sep;169(9):4076–4085. doi: 10.1128/jb.169.9.4076-4085.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Banuett F., Hoyt M. A., McFarlane L., Echols H., Herskowitz I. hflB, a new Escherichia coli locus regulating lysogeny and the level of bacteriophage lambda cII protein. J Mol Biol. 1986 Jan 20;187(2):213–224. doi: 10.1016/0022-2836(86)90229-9. [DOI] [PubMed] [Google Scholar]
  6. Begg K. J., Tomoyasu T., Donachie W. D., Khattar M., Niki H., Yamanaka K., Hiraga S., Ogura T. Escherichia coli mutant Y16 is a double mutant carrying thermosensitive ftsH and ftsI mutations. J Bacteriol. 1992 Apr;174(7):2416–2417. doi: 10.1128/jb.174.7.2416-2417.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. CAMPBELL A. Sensitive mutants of bacteriophage lambda. Virology. 1961 May;14:22–32. doi: 10.1016/0042-6822(61)90128-3. [DOI] [PubMed] [Google Scholar]
  8. Cheng H. H., Echols H. A class of Escherichia coli proteins controlled by the hflA locus. J Mol Biol. 1987 Aug 5;196(3):737–740. doi: 10.1016/0022-2836(87)90046-5. [DOI] [PubMed] [Google Scholar]
  9. Cheng H. H., Muhlrad P. J., Hoyt M. A., Echols H. Cleavage of the cII protein of phage lambda by purified HflA protease: control of the switch between lysis and lysogeny. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7882–7886. doi: 10.1073/pnas.85.21.7882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chuang S. E., Blattner F. R. Characterization of twenty-six new heat shock genes of Escherichia coli. J Bacteriol. 1993 Aug;175(16):5242–5252. doi: 10.1128/jb.175.16.5242-5252.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cooper S., Ruettinger T. A temperature sensitive nonsense mutation affecting the synthesis of a major protein of Escherichia coli K12. Mol Gen Genet. 1975 Aug 5;139(2):167–176. doi: 10.1007/BF00264696. [DOI] [PubMed] [Google Scholar]
  12. Dubiel W., Ferrell K., Pratt G., Rechsteiner M. Subunit 4 of the 26 S protease is a member of a novel eukaryotic ATPase family. J Biol Chem. 1992 Nov 15;267(32):22699–22702. [PubMed] [Google Scholar]
  13. Erdmann R., Wiebel F. F., Flessau A., Rytka J., Beyer A., Fröhlich K. U., Kunau W. H. PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell. 1991 Feb 8;64(3):499–510. doi: 10.1016/0092-8674(91)90234-p. [DOI] [PubMed] [Google Scholar]
  14. Gamer J., Bujard H., Bukau B. Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor sigma 32. Cell. 1992 May 29;69(5):833–842. doi: 10.1016/0092-8674(92)90294-m. [DOI] [PubMed] [Google Scholar]
  15. Ghislain M., Udvardy A., Mann C. S. cerevisiae 26S protease mutants arrest cell division in G2/metaphase. Nature. 1993 Nov 25;366(6453):358–362. doi: 10.1038/366358a0. [DOI] [PubMed] [Google Scholar]
  16. Gordon C., McGurk G., Dillon P., Rosen C., Hastie N. D. Defective mitosis due to a mutation in the gene for a fission yeast 26S protease subunit. Nature. 1993 Nov 25;366(6453):355–357. doi: 10.1038/366355a0. [DOI] [PubMed] [Google Scholar]
  17. Gottesman S., Maurizi M. R. Regulation by proteolysis: energy-dependent proteases and their targets. Microbiol Rev. 1992 Dec;56(4):592–621. doi: 10.1128/mr.56.4.592-621.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Grossman A. D., Erickson J. W., Gross C. A. The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell. 1984 Sep;38(2):383–390. doi: 10.1016/0092-8674(84)90493-8. [DOI] [PubMed] [Google Scholar]
  19. Herman C., Ogura T., Tomoyasu T., Hiraga S., Akiyama Y., Ito K., Thomas R., D'Ari R., Bouloc P. Cell growth and lambda phage development controlled by the same essential Escherichia coli gene, ftsH/hflB. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10861–10865. doi: 10.1073/pnas.90.22.10861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hoyt M. A., Knight D. M., Das A., Miller H. I., Echols H. Control of phage lambda development by stability and synthesis of cII protein: role of the viral cIII and host hflA, himA and himD genes. Cell. 1982 Dec;31(3 Pt 2):565–573. doi: 10.1016/0092-8674(82)90312-9. [DOI] [PubMed] [Google Scholar]
  21. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  22. Kornitzer D., Altuvia S., Oppenheim A. B. The activity of the CIII regulator of lambdoid bacteriophages resides within a 24-amino acid protein domain. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5217–5221. doi: 10.1073/pnas.88.12.5217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Liberek K., Galitski T. P., Zylicz M., Georgopoulos C. The DnaK chaperone modulates the heat shock response of Escherichia coli by binding to the sigma 32 transcription factor. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3516–3520. doi: 10.1073/pnas.89.8.3516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maurizi M. R. Degradation in vitro of bacteriophage lambda N protein by Lon protease from Escherichia coli. J Biol Chem. 1987 Feb 25;262(6):2696–2703. [PubMed] [Google Scholar]
  25. Mecsas J., Rouviere P. E., Erickson J. W., Donohue T. J., Gross C. A. The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev. 1993 Dec;7(12B):2618–2628. doi: 10.1101/gad.7.12b.2618. [DOI] [PubMed] [Google Scholar]
  26. Nilsson D., Lauridsen A. A., Tomoyasu T., Ogura T. A Lactococcus lactis gene encodes a membrane protein with putative ATPase activity that is homologous to the essential Escherichia coli ftsH gene product. Microbiology. 1994 Oct;140(Pt 10):2601–2610. doi: 10.1099/00221287-140-10-2601. [DOI] [PubMed] [Google Scholar]
  27. Rasmussen L. J., Møller P. L., Atlung T. Carbon metabolism regulates expression of the pfl (pyruvate formate-lyase) gene in Escherichia coli. J Bacteriol. 1991 Oct;173(20):6390–6397. doi: 10.1128/jb.173.20.6390-6397.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rechsteiner M., Hoffman L., Dubiel W. The multicatalytic and 26 S proteases. J Biol Chem. 1993 Mar 25;268(9):6065–6068. [PubMed] [Google Scholar]
  29. Santos D., De Almeida D. F. Isolation and characterization of a new temperature-sensitive cell division mutant of Escherichia coli K-12. J Bacteriol. 1975 Dec;124(3):1502–1507. doi: 10.1128/jb.124.3.1502-1507.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Straus D. B., Walter W. A., Gross C. A. The heat shock response of E. coli is regulated by changes in the concentration of sigma 32. Nature. 1987 Sep 24;329(6137):348–351. doi: 10.1038/329348a0. [DOI] [PubMed] [Google Scholar]
  32. Straus D., Walter W., Gross C. A. DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. Genes Dev. 1990 Dec;4(12A):2202–2209. doi: 10.1101/gad.4.12a.2202. [DOI] [PubMed] [Google Scholar]
  33. Tilly K., McKittrick N., Zylicz M., Georgopoulos C. The dnaK protein modulates the heat-shock response of Escherichia coli. Cell. 1983 Sep;34(2):641–646. doi: 10.1016/0092-8674(83)90396-3. [DOI] [PubMed] [Google Scholar]
  34. Tilly K., Spence J., Georgopoulos C. Modulation of stability of the Escherichia coli heat shock regulatory factor sigma. J Bacteriol. 1989 Mar;171(3):1585–1589. doi: 10.1128/jb.171.3.1585-1589.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tomoyasu T., Yamanaka K., Murata K., Suzaki T., Bouloc P., Kato A., Niki H., Hiraga S., Ogura T. Topology and subcellular localization of FtsH protein in Escherichia coli. J Bacteriol. 1993 Mar;175(5):1352–1357. doi: 10.1128/jb.175.5.1352-1357.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tomoyasu T., Yuki T., Morimura S., Mori H., Yamanaka K., Niki H., Hiraga S., Ogura T. The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J Bacteriol. 1993 Mar;175(5):1344–1351. doi: 10.1128/jb.175.5.1344-1351.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Van Melderen L., Bernard P., Couturier M. Lon-dependent proteolysis of CcdA is the key control for activation of CcdB in plasmid-free segregant bacteria. Mol Microbiol. 1994 Mar;11(6):1151–1157. doi: 10.1111/j.1365-2958.1994.tb00391.x. [DOI] [PubMed] [Google Scholar]
  38. Yano R., Imai M., Yura T. The use of operon fusions in studies of the heat-shock response: effects of altered sigma 32 on heat-shock promoter function in Escherichia coli. Mol Gen Genet. 1987 Apr;207(1):24–28. doi: 10.1007/BF00331486. [DOI] [PubMed] [Google Scholar]
  39. Yura T., Nagai H., Mori H. Regulation of the heat-shock response in bacteria. Annu Rev Microbiol. 1993;47:321–350. doi: 10.1146/annurev.mi.47.100193.001541. [DOI] [PubMed] [Google Scholar]
  40. Zuber U., Schumann W. CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J Bacteriol. 1994 Mar;176(5):1359–1363. doi: 10.1128/jb.176.5.1359-1363.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES