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. 1991 Sep;59(9):3086–3093. doi: 10.1128/iai.59.9.3086-3093.1991

Heat shock proteins and antigens of Mycobacterium tuberculosis.

D B Young 1, T R Garbe 1
PMCID: PMC258138  PMID: 1679042

Abstract

The heat shock response of Mycobacterium tuberculosis has been characterized in detail by one- and two-dimensional polyacrylamide gel electrophoresis after metabolic labeling with [35S]methionine and 14C-amino acids. A temperature increase from 37 to 42 degrees C induced elevated synthesis of three major proteins corresponding to the DnaK, GroEL, and GroES proteins of M. tuberculosis previously identified as prominent antigens. At higher temperatures (45 to 48 degrees C), synthesis of GroEL decreased and novel heat shock proteins with molecular masses of 90, 28, 20, and 15 kDa were observed. These new proteins did not comigrate with known antigens during two-dimensional gel electrophoresis. The heat shock response is discussed with regard to the possible importance of transcriptional regulation of mycobacterial genes in vivo.

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Selected References

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

  1. Andersen A. B., Yuan Z. L., Hasløv K., Vergmann B., Bennedsen J. Interspecies reactivity of five monoclonal antibodies to Mycobacterium tuberculosis as examined by immunoblotting and enzyme-linked immunosorbent assay. J Clin Microbiol. 1986 Mar;23(3):446–451. doi: 10.1128/jcm.23.3.446-451.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baird P. N., Hall L. M., Coates A. R. A major antigen from Mycobacterium tuberculosis which is homologous to the heat shock proteins groES from E. coli and the htpA gene product of Coxiella burneti. Nucleic Acids Res. 1988 Sep 26;16(18):9047–9047. doi: 10.1093/nar/16.18.9047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buchmeier N. A., Heffron F. Induction of Salmonella stress proteins upon infection of macrophages. Science. 1990 May 11;248(4956):730–732. doi: 10.1126/science.1970672. [DOI] [PubMed] [Google Scholar]
  4. Coates A. R., Hewitt J., Allen B. W., Ivanyi J., Mitchison D. A. Antigenic diversity of Mycobacterium tuberculosis and Mycobacterium bovis detected by means of monoclonal antibodies. Lancet. 1981 Jul 25;2(8239):167–169. doi: 10.1016/s0140-6736(81)90355-x. [DOI] [PubMed] [Google Scholar]
  5. Damiani G., Biano A., Beltrame A., Vismara D., Mezzopreti M. F., Colizzi V., Young D. B., Bloom B. R. Generation and characterization of monoclonal antibodies to 28-, 35-, and 65-kilodalton proteins of Mycobacterium tuberculosis. Infect Immun. 1988 May;56(5):1281–1287. doi: 10.1128/iai.56.5.1281-1287.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ellis R. J. The molecular chaperone concept. Semin Cell Biol. 1990 Feb;1(1):1–9. [PubMed] [Google Scholar]
  7. Erickson J. W., Gross C. A. Identification of the sigma E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression. Genes Dev. 1989 Sep;3(9):1462–1471. doi: 10.1101/gad.3.9.1462. [DOI] [PubMed] [Google Scholar]
  8. Goff S. A., Goldberg A. L. Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes. Cell. 1985 Jun;41(2):587–595. doi: 10.1016/s0092-8674(85)80031-3. [DOI] [PubMed] [Google Scholar]
  9. Hulton C. S., Seirafi A., Hinton J. C., Sidebotham J. M., Waddell L., Pavitt G. D., Owen-Hughes T., Spassky A., Buc H., Higgins C. F. Histone-like protein H1 (H-NS), DNA supercoiling, and gene expression in bacteria. Cell. 1990 Nov 2;63(3):631–642. doi: 10.1016/0092-8674(90)90458-q. [DOI] [PubMed] [Google Scholar]
  10. Johnson K., Charles I., Dougan G., Pickard D., O'Gaora P., Costa G., Ali T., Miller I., Hormaeche C. The role of a stress-response protein in Salmonella typhimurium virulence. Mol Microbiol. 1991 Feb;5(2):401–407. doi: 10.1111/j.1365-2958.1991.tb02122.x. [DOI] [PubMed] [Google Scholar]
  11. Kaufmann S. H. Heat shock proteins and the immune response. Immunol Today. 1990 Apr;11(4):129–136. doi: 10.1016/0167-5699(90)90050-j. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Lamb F. I., Singh N. B., Colston M. J. The specific 18-kilodalton antigen of Mycobacterium leprae is present in Mycobacterium habana and functions as a heat-shock protein. J Immunol. 1990 Mar 1;144(5):1922–1925. [PubMed] [Google Scholar]
  14. Lathigra R. B., Young D. B., Sweetser D., Young R. A. A gene from Mycobacterium tuberculosis which is homologous to the DnaJ heat shock protein of E. coli. Nucleic Acids Res. 1988 Feb 25;16(4):1636–1636. doi: 10.1093/nar/16.4.1636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lindquist S. The heat-shock response. Annu Rev Biochem. 1986;55:1151–1191. doi: 10.1146/annurev.bi.55.070186.005443. [DOI] [PubMed] [Google Scholar]
  16. Lipinska B., Sharma S., Georgopoulos C. Sequence analysis and regulation of the htrA gene of Escherichia coli: a sigma 32-independent mechanism of heat-inducible transcription. Nucleic Acids Res. 1988 Nov 11;16(21):10053–10067. doi: 10.1093/nar/16.21.10053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mehlert A., Young D. B. Biochemical and antigenic characterization of the Mycobacterium tuberculosis 71kD antigen, a member of the 70kD heat-shock protein family. Mol Microbiol. 1989 Feb;3(2):125–130. doi: 10.1111/j.1365-2958.1989.tb01801.x. [DOI] [PubMed] [Google Scholar]
  18. Miller J. F., Mekalanos J. J., Falkow S. Coordinate regulation and sensory transduction in the control of bacterial virulence. Science. 1989 Feb 17;243(4893):916–922. doi: 10.1126/science.2537530. [DOI] [PubMed] [Google Scholar]
  19. Minden P., Kelleher P. J., Freed J. H., Nielsen L. D., Brennan P. J., McPheron L., McClatchy J. K. Immunological evaluation of a component isolated from Mycobacterium bovis BCG with a monoclonal antibody to M. bovis BCG. Infect Immun. 1984 Nov;46(2):519–525. doi: 10.1128/iai.46.2.519-525.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Morgan R. W., Christman M. F., Jacobson F. S., Storz G., Ames B. N. Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8059–8063. doi: 10.1073/pnas.83.21.8059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Murray C. J., Styblo K., Rouillon A. Tuberculosis in developing countries: burden, intervention and cost. Bull Int Union Tuberc Lung Dis. 1990 Mar;65(1):6–24. [PubMed] [Google Scholar]
  22. Nerland A. H., Mustafa A. S., Sweetser D., Godal T., Young R. A. A protein antigen of Mycobacterium leprae is related to a family of small heat shock proteins. J Bacteriol. 1988 Dec;170(12):5919–5921. doi: 10.1128/jb.170.12.5919-5921.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Parsot C., Mekalanos J. J. Expression of ToxR, the transcriptional activator of the virulence factors in Vibrio cholerae, is modulated by the heat shock response. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9898–9902. doi: 10.1073/pnas.87.24.9898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rothman J. E. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell. 1989 Nov 17;59(4):591–601. doi: 10.1016/0092-8674(89)90005-6. [DOI] [PubMed] [Google Scholar]
  26. Shinnick T. M., Plikaytis B. B., Hyche A. D., Van Landingham R. M., Walker L. L. The Mycobacterium tuberculosis BCG-a protein has homology with the Escherichia coli GroES protein. Nucleic Acids Res. 1989 Feb 11;17(3):1254–1254. doi: 10.1093/nar/17.3.1254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shinnick T. M., Vodkin M. H., Williams J. C. The Mycobacterium tuberculosis 65-kilodalton antigen is a heat shock protein which corresponds to common antigen and to the Escherichia coli GroEL protein. Infect Immun. 1988 Feb;56(2):446–451. doi: 10.1128/iai.56.2.446-451.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sokolovic Z., Fuchs A., Goebel W. Synthesis of species-specific stress proteins by virulent strains of Listeria monocytogenes. Infect Immun. 1990 Nov;58(11):3582–3587. doi: 10.1128/iai.58.11.3582-3587.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. VanBogelen R. A., Kelley P. M., Neidhardt F. C. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J Bacteriol. 1987 Jan;169(1):26–32. doi: 10.1128/jb.169.1.26-32.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. VanBogelen R. A., Neidhardt F. C. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5589–5593. doi: 10.1073/pnas.87.15.5589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. WALLACE J. G. The heat resistance of tubercle bacilli in the lungs of infected mice. Am Rev Respir Dis. 1961 Jun;83:866–871. doi: 10.1164/arrd.1961.83.6.866. [DOI] [PubMed] [Google Scholar]
  33. Yamaguchi R., Matsuo K., Yamazaki A., Nagai S., Terasaka K., Yamada T. Immunogenic protein MPB57 from Mycobacterium bovis BCG: molecular cloning, nucleotide sequence and expression. FEBS Lett. 1988 Nov 21;240(1-2):115–117. doi: 10.1016/0014-5793(88)80350-8. [DOI] [PubMed] [Google Scholar]
  34. Young D. B., Fohn M. J., Khanolkar S. R., Buchanan T. M. Monoclonal antibodies to a 28,000 mol. wt protein antigen of Mycobacterium leprae. Clin Exp Immunol. 1985 Jun;60(3):546–552. [PMC free article] [PubMed] [Google Scholar]
  35. Young D., Lathigra R., Hendrix R., Sweetser D., Young R. A. Stress proteins are immune targets in leprosy and tuberculosis. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4267–4270. doi: 10.1073/pnas.85.12.4267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Young R. A. Stress proteins and immunology. Annu Rev Immunol. 1990;8:401–420. doi: 10.1146/annurev.iy.08.040190.002153. [DOI] [PubMed] [Google Scholar]

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