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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
. 1982 Feb;79(3):860–864. doi: 10.1073/pnas.79.3.860

Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12.

T Yamamori, T Yura
PMCID: PMC345852  PMID: 7038687

Abstract

When Escherichia coli cells grown at 30 degrees C are transferred to 42 degrees C, synthesis of several polypeptides is markedly and transiently induced. A temperature-sensitive nonsense mutant (tsn-K165) of E. coli K-12 is found to be defective in the induction of these proteins. mRNA for one major heat-shock polypeptide (groE protein) tested is induced in the wild type but not in the mutant upon temperature shift. Hence, the mutation defines a (regulatory) gene, designated hin (heat shock induction), whose product is required for active transcription of a set of heat-inducible operons in E. coli. The results reported herein suggest that the heat-shock polypeptides controlled by the hin gene play an important role in cell growth at high temperature. The possible involvement of the hin gene product in protection against thermal killing is also discussed.

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Selected References

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  1. Anderson K. W., Smith J. D. Still more mutant tyrosine transfer ribonucleic acids. J Mol Biol. 1972 Aug 28;69(3):349–356. doi: 10.1016/0022-2836(72)90249-5. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Bachmann B. J., Low K. B. Linkage map of Escherichia coli K-12, edition 6. Microbiol Rev. 1980 Mar;44(1):1–56. doi: 10.1128/mr.44.1.1-56.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Dennis P. P., Nomura M. Regulation of the expression of ribosomal protein genes in Escherichia coli. J Mol Biol. 1975 Sep 5;97(1):61–76. doi: 10.1016/s0022-2836(75)80022-2. [DOI] [PubMed] [Google Scholar]
  7. Georgopoulos C. P., Hohn B. Identification of a host protein necessary for bacteriophage morphogenesis (the groE gene product). Proc Natl Acad Sci U S A. 1978 Jan;75(1):131–135. doi: 10.1073/pnas.75.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Guttman S. D., Glover C. V., Allis C. D., Gorovsky M. A. Heat shock, deciliation and release from anoxia induce the synthesis of the same set of polypeptides in starved T. pyriformis. Cell. 1980 Nov;22(1 Pt 1):299–307. doi: 10.1016/0092-8674(80)90177-4. [DOI] [PubMed] [Google Scholar]
  9. Hendrix R. W. Purification and properties of groE, a host protein involved in bacteriophage assembly. J Mol Biol. 1979 Apr 15;129(3):375–392. doi: 10.1016/0022-2836(79)90502-3. [DOI] [PubMed] [Google Scholar]
  10. Hohn T., Hohn B., Engel A., Wurtz M., Smith P. R. Isolation and characterization of the host protein groE involved in bacteriophage lambda assembly. J Mol Biol. 1979 Apr 15;129(3):359–373. doi: 10.1016/0022-2836(79)90501-1. [DOI] [PubMed] [Google Scholar]
  11. Ishihama A., Ikeuchi T., Yura T. A novel adenosine triphosphatase isolated from RNA polymerase preparations of Escherichia coli. I. Copurification and separation. J Biochem. 1976 May;79(5):917–925. doi: 10.1093/oxfordjournals.jbchem.a131159. [DOI] [PubMed] [Google Scholar]
  12. Kelley P. M., Schlesinger M. J. The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell. 1978 Dec;15(4):1277–1286. doi: 10.1016/0092-8674(78)90053-3. [DOI] [PubMed] [Google Scholar]
  13. Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. McAlister L., Finkelstein D. B. Heat shock proteins and thermal resistance in yeast. Biochem Biophys Res Commun. 1980 Apr 14;93(3):819–824. doi: 10.1016/0006-291x(80)91150-x. [DOI] [PubMed] [Google Scholar]
  17. Miller M. J., Xuong N. H., Geiduschek E. P. A response of protein synthesis to temperature shift in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5222–5225. doi: 10.1073/pnas.76.10.5222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nakamura Y., Yura T. Evidence for a positive regulation of RNA polymerase synthesis in Escherichia coli. J Mol Biol. 1975 Oct 5;97(4):621–642. doi: 10.1016/s0022-2836(75)80063-5. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  22. Russell R. L., Abelson J. N., Landy A., Gefter M. L., Brenner S., Smith J. D. Duplicate genes for tyrosine transfer RNA in Escherichia coli. J Mol Biol. 1970 Jan 14;47(1):1–13. doi: 10.1016/0022-2836(70)90397-9. [DOI] [PubMed] [Google Scholar]
  23. Sato T., Ito K., Yura T. Membrane proteins of Escherichia coli K-12: two-dimensional polyacrylamide gel electrophoresis of inner and outer membranes. Eur J Biochem. 1977 Sep;78(2):557–567. doi: 10.1111/j.1432-1033.1977.tb11769.x. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Tissières A., Mitchell H. K., Tracy U. M. Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol. 1974 Apr 15;84(3):389–398. doi: 10.1016/0022-2836(74)90447-1. [DOI] [PubMed] [Google Scholar]
  26. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  27. 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]
  28. 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]

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