Skip to main content
PMC 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
. 1984 Nov;81(21):6779–6783. doi: 10.1073/pnas.81.21.6779

A gene regulating the heat shock response in Escherichia coli also affects proteolysis.

T A Baker, A D Grossman, C A Gross
PMCID: PMC392015  PMID: 6387713

Abstract

The htpR locus in Escherichia coli encodes a regulator of the heat shock response. Cells containing the htpR165 mutation are defective in the induction of synthesis of heat-shock proteins at high temperature. We show that these cells are also defective in degrading two proteins that are normally unstable in htpR+ cells. The proteolytic defect is manifest at both 30 degrees C and 42 degrees C. We used a marker rescue technique to map this defect to the htpR locus. Although both proteolytic substrates are partially stabilized in lon- strains, we argue that the defect in proteolysis exhibited by the htpR165 strain does not mimic the lon- state. The htpR165 strain synthesizes Lon at the normal rate at 30 degrees C and does not show the phenotypes of mucoidy and radiation sensitivity associated with lon- strains.

Full text

PDF
6783

Images in this article

6781Image
on p.6781

Selected References

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

  1. Ashburner M., Bonner J. J. The induction of gene activity in drosophilia by heat shock. Cell. 1979 Jun;17(2):241–254. doi: 10.1016/0092-8674(79)90150-8. [DOI] [PubMed] [Google Scholar]
  2. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983 Jun;47(2):180–230. doi: 10.1128/mr.47.2.180-230.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bukhari A. I., Zipser D. Mutants of Escherichia coli with a defect in the degradation of nonsense fragments. Nat New Biol. 1973 Jun 20;243(129):238–241. doi: 10.1038/newbio243238a0. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Goldschmidt R. In vivo degradation of nonsense fragments in E. coli. Nature. 1970 Dec 19;228(5277):1151–1154. doi: 10.1038/2281151a0. [DOI] [PubMed] [Google Scholar]
  6. Gottesman S., Gottesman M., Shaw J. E., Pearson M. L. Protein degradation in E. coli: the lon mutation and bacteriophage lambda N and cII protein stability. Cell. 1981 Apr;24(1):225–233. doi: 10.1016/0092-8674(81)90518-3. [DOI] [PubMed] [Google Scholar]
  7. Gottesman S., Zipser D. Deg phenotype of Escherichia coli lon mutants. J Bacteriol. 1978 Feb;133(2):844–851. doi: 10.1128/jb.133.2.844-851.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gross C. A., Grossman A. D., Liebke H., Walter W., Burgess R. R. Effects of the mutant sigma allele rpoD800 on the synthesis of specific macromolecular components of the Escherichia coli K12 cell. J Mol Biol. 1984 Jan 25;172(3):283–300. doi: 10.1016/s0022-2836(84)80027-3. [DOI] [PubMed] [Google Scholar]
  9. Grossman A. D., Burgess R. R., Walter W., Gross C. A. Mutations in the Ion gene of E. coli K12 phenotypically suppress a mutation in the sigma subunit of RNA polymerase. Cell. 1983 Jan;32(1):151–159. doi: 10.1016/0092-8674(83)90505-6. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Herendeen S. L., VanBogelen R. A., Neidhardt F. C. Levels of major proteins of Escherichia coli during growth at different temperatures. J Bacteriol. 1979 Jul;139(1):185–194. doi: 10.1128/jb.139.1.185-194.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Johnson R. C., Yin J. C., Reznikoff W. S. Control of Tn5 transposition in Escherichia coli is mediated by protein from the right repeat. Cell. 1982 Oct;30(3):873–882. doi: 10.1016/0092-8674(82)90292-6. [DOI] [PubMed] [Google Scholar]
  14. Kowit J. D., Goldberg A. L. Intermediate steps in the degradation of a specific abnormal protein in Escherichia coli. J Biol Chem. 1977 Dec 10;252(23):8350–8357. [PubMed] [Google Scholar]
  15. Krueger J. H., Walker G. C. groEL and dnaK genes of Escherichia coli are induced by UV irradiation and nalidixic acid in an htpR+-dependent fashion. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1499–1503. doi: 10.1073/pnas.81.5.1499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  17. Landick R., Vaughn V., Lau E. T., VanBogelen R. A., Erickson J. W., Neidhardt F. C. Nucleotide sequence of the heat shock regulatory gene of E. coli suggests its protein product may be a transcription factor. Cell. 1984 Aug;38(1):175–182. doi: 10.1016/0092-8674(84)90538-5. [DOI] [PubMed] [Google Scholar]
  18. Larimore F. S., Waxman L., Goldberg A. L. Studies of the ATP-dependent proteolytic enzyme, protease La, from Escherichia coli. J Biol Chem. 1982 Apr 25;257(8):4187–4195. [PubMed] [Google Scholar]
  19. Lemaux P. G., Herendeen S. L., Bloch P. L., Neidhardt F. C. Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell. 1978 Mar;13(3):427–434. doi: 10.1016/0092-8674(78)90317-3. [DOI] [PubMed] [Google Scholar]
  20. Little J. W., Mount D. W. The SOS regulatory system of Escherichia coli. Cell. 1982 May;29(1):11–22. doi: 10.1016/0092-8674(82)90085-x. [DOI] [PubMed] [Google Scholar]
  21. McKnight J. L., Fried V. A. A novel proteolytic activity apparently initiating degradation of beta-galactosidase nonsense fragments in in vitro extracts of Escherichia coli. J Biol Chem. 1983 Jun 25;258(12):7550–7555. [PubMed] [Google Scholar]
  22. McKnight J. L., Fried V. A. Limited proteolysis. Early steps in the processing of large premature termination fragments of beta-galactosidase in Escherichia coli. J Biol Chem. 1981 Sep 25;256(18):9652–9661. [PubMed] [Google Scholar]
  23. Mizusawa S., Gottesman S. Protein degradation in Escherichia coli: the lon gene controls the stability of sulA protein. Proc Natl Acad Sci U S A. 1983 Jan;80(2):358–362. doi: 10.1073/pnas.80.2.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mount D. W. The genetics of protein degradation in bacteria. Annu Rev Genet. 1980;14:279–319. doi: 10.1146/annurev.ge.14.120180.001431. [DOI] [PubMed] [Google Scholar]
  25. Neidhardt F. C., Phillips T. A., VanBogelen R. A., Smith M. W., Georgalis Y., Subramanian A. R. Identity of the B56.5 protein, the A-protein, and the groE gene product of Escherichia coli. J Bacteriol. 1981 Jan;145(1):513–520. doi: 10.1128/jb.145.1.513-520.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Neidhardt F. C., VanBogelen R. A., Lau E. T. Molecular cloning and expression of a gene that controls the high-temperature regulon of Escherichia coli. J Bacteriol. 1983 Feb;153(2):597–603. doi: 10.1128/jb.153.2.597-603.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Neidhardt F. C., VanBogelen R. A. Positive regulatory gene for temperature-controlled proteins in Escherichia coli. Biochem Biophys Res Commun. 1981 May 29;100(2):894–900. doi: 10.1016/s0006-291x(81)80257-4. [DOI] [PubMed] [Google Scholar]
  28. Neidhardt F. C., VanBogelen R. A., Vaughn V. The genetics and regulation of heat-shock proteins. Annu Rev Genet. 1984;18:295–329. doi: 10.1146/annurev.ge.18.120184.001455. [DOI] [PubMed] [Google Scholar]
  29. Phillips T. A., VanBogelen R. A., Neidhardt F. C. lon gene product of Escherichia coli is a heat-shock protein. J Bacteriol. 1984 Jul;159(1):283–287. doi: 10.1128/jb.159.1.283-287.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Plesset J., Palm C., McLaughlin C. S. Induction of heat shock proteins and thermotolerance by ethanol in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1982 Oct 15;108(3):1340–1345. doi: 10.1016/0006-291x(82)92147-7. [DOI] [PubMed] [Google Scholar]
  31. Schoemaker J. M., Gayda R. C., Markovitz A. Regulation of cell division in Escherichia coli: SOS induction and cellular location of the sulA protein, a key to lon-associated filamentation and death. J Bacteriol. 1984 May;158(2):551–561. doi: 10.1128/jb.158.2.551-561.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Taylor W. E., Straus D. B., Grossman A. D., Burton Z. F., Gross C. A., Burgess R. R. Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell. 1984 Sep;38(2):371–381. doi: 10.1016/0092-8674(84)90492-6. [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., Murialdo H., Georgopoulos C. Identification of a second Escherichia coli groE gene whose product is necessary for bacteriophage morphogenesis. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1629–1633. doi: 10.1073/pnas.78.3.1629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Welply J. K., Mandecki W., Fowler A. V., Zabin I. beta-galactosidase omega-complementation with a small cyanogen bromide peptide. Biochem Biophys Res Commun. 1980 Mar 13;93(1):223–227. doi: 10.1016/s0006-291x(80)80269-5. [DOI] [PubMed] [Google Scholar]
  36. Yamamori T., Ito K., Nakamura Y., Yura T. Transient regulation of protein synthesis in Escherichia coli upon shift-up of growth temperature. J Bacteriol. 1978 Jun;134(3):1133–1140. doi: 10.1128/jb.134.3.1133-1140.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yamamori T., Yura T. Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1982 Feb;79(3):860–864. doi: 10.1073/pnas.79.3.860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Yamamori T., Yura T. Temperature-induced synthesis of specific proteins in Escherichia coli: evidence for transcriptional control. J Bacteriol. 1980 Jun;142(3):843–851. doi: 10.1128/jb.142.3.843-851.1980. [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