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. 1990 Apr;58(4):1038–1042. doi: 10.1128/iai.58.4.1038-1042.1990

Thermoregulation of protein synthesis in Borrelia burgdorferi.

R G Cluss 1, J T Boothby 1
PMCID: PMC258579  PMID: 2318529

Abstract

Borrelia burgdorferi, the etiological agent of Lyme disease, infects humans via the bite of a tick. The microbe survives in at least two vastly different environments: an arthropod vector and a warm-blooded host. We examined protein synthesis in B. burgdorferi B31 in response to sudden heat stress, which is similar to that which occurs during the transmission from vector to host. Proteins synthesized after shifts from 28 degrees C to higher temperatures and in pulse-chase experiments were labeled with 3H-labeled amino acids for 4 h and characterized by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and fluorography. The synthesis of four proteins we designated as heat stress proteins (HSPs) was increased by shifts to higher temperatures (HSP-1, 75 kilodaltons [kDa]; HSP-2, 42 kDa; HSP-3, 39 kDa; and HSP-4, 27 kDa); and the amount of one protein we designated as heat-labile protein 1 (29.5 kDa) was decreased at higher temperatures. At 37 to 40 degrees C, the major heat stress protein, HSP-1, represented 14 to 18% of the total cell protein compared with 1 to 2% of the total cell protein at 28 degrees C. HSP-1 was stable during a 4-h chase at either 40 or 28 degrees C. Demonstration of similar HSPs in low-passage, pathogenic strains of B. burgdorferi suggests that the heat stress response may be common among B. burgdorferi strains and may play a role in Lyme disease.

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Selected References

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  1. Barbour A. G. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med. 1984 Jul-Aug;57(4):521–525. [PMC free article] [PubMed] [Google Scholar]
  2. Barthold S. W., Moody K. D., Terwilliger G. A., Duray P. H., Jacoby R. O., Steere A. C. Experimental Lyme arthritis in rats infected with Borrelia burgdorferi. J Infect Dis. 1988 Apr;157(4):842–846. doi: 10.1093/infdis/157.4.842. [DOI] [PubMed] [Google Scholar]
  3. Bortolussi R., Ferrieri P., Quie P. G. Influence of growth temperature of Escherichia coli on K1 capsular antigen production and resistance to opsonization. Infect Immun. 1983 Mar;39(3):1136–1141. doi: 10.1128/iai.39.3.1136-1141.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buchanan T. M., Nomaguchi H., Anderson D. C., Young R. A., Gillis T. P., Britton W. J., Ivanyi J., Kolk A. H., Closs O., Bloom B. R. Characterization of antibody-reactive epitopes on the 65-kilodalton protein of Mycobacterium leprae. Infect Immun. 1987 Apr;55(4):1000–1003. doi: 10.1128/iai.55.4.1000-1003.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Craig E. A. The heat shock response. CRC Crit Rev Biochem. 1985;18(3):239–280. doi: 10.3109/10409238509085135. [DOI] [PubMed] [Google Scholar]
  6. Evans D. G., Silver R. P., Evans D. J., Jr, Chase D. G., Gorbach S. L. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans. Infect Immun. 1975 Sep;12(3):656–667. doi: 10.1128/iai.12.3.656-667.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Göransson M., Uhlin B. E. Environmental temperature regulates transcription of a virulence pili operon in E. coli. EMBO J. 1984 Dec 1;3(12):2885–2888. doi: 10.1002/j.1460-2075.1984.tb02225.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Habicht G. S., Beck G., Benach J. L., Coleman J. L. Borrelia burgdorferi lipopolysaccharide and its role in the pathogenesis of Lyme disease. Zentralbl Bakteriol Mikrobiol Hyg A. 1986 Dec;263(1-2):137–141. doi: 10.1016/s0176-6724(86)80115-8. [DOI] [PubMed] [Google Scholar]
  9. Hansen K., Bangsborg J. M., Fjordvang H., Pedersen N. S., Hindersson P. Immunochemical characterization of and isolation of the gene for a Borrelia burgdorferi immunodominant 60-kilodalton antigen common to a wide range of bacteria. Infect Immun. 1988 Aug;56(8):2047–2053. doi: 10.1128/iai.56.8.2047-2053.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Howe T. R., Mayer L. W., Barbour A. G. A single recombinant plasmid expressing two major outer surface proteins of the Lyme disease spirochete. Science. 1985 Feb 8;227(4687):645–646. doi: 10.1126/science.3969554. [DOI] [PubMed] [Google Scholar]
  11. Isberg R. R., Swain A., Falkow S. Analysis of expression and thermoregulation of the Yersinia pseudotuberculosis inv gene with hybrid proteins. Infect Immun. 1988 Aug;56(8):2133–2138. doi: 10.1128/iai.56.8.2133-2138.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jones G. W., Richardson L. A. The attachment to, and invasion of HeLa cells by Salmonella typhimurium: the contribution of mannose-sensitive and mannose-resistant haemagglutinating activities. J Gen Microbiol. 1981 Dec;127(2):361–370. doi: 10.1099/00221287-127-2-361. [DOI] [PubMed] [Google Scholar]
  13. Källenius G., Möllby R., Winberg J. In vitro adhesion of uropathogenic Escherichia coli to human periurethral cells. Infect Immun. 1980 Jun;28(3):972–980. doi: 10.1128/iai.28.3.972-980.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  15. Laemmli U. K., Favre M. Maturation of the head of bacteriophage T4. I. DNA packaging events. J Mol Biol. 1973 Nov 15;80(4):575–599. doi: 10.1016/0022-2836(73)90198-8. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Maurelli A. T., Blackmon B., Curtiss R., 3rd Temperature-dependent expression of virulence genes in Shigella species. Infect Immun. 1984 Jan;43(1):195–201. doi: 10.1128/iai.43.1.195-201.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Sokolovic Z., Goebel W. Synthesis of listeriolysin in Listeria monocytogenes under heat shock conditions. Infect Immun. 1989 Jan;57(1):295–298. doi: 10.1128/iai.57.1.295-298.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Steere A. C., Bartenhagen N. H., Craft J. E., Hutchinson G. J., Newman J. H., Rahn D. W., Sigal L. H., Spieler P. N., Stenn K. S., Malawista S. E. The early clinical manifestations of Lyme disease. Ann Intern Med. 1983 Jul;99(1):76–82. doi: 10.7326/0003-4819-99-1-76. [DOI] [PubMed] [Google Scholar]
  22. Steere A. C., Batsford W. P., Weinberg M., Alexander J., Berger H. J., Wolfson S., Malawista S. E. Lyme carditis: cardiac abnormalities of Lyme disease. Ann Intern Med. 1980 Jul;93(1):8–16. doi: 10.7326/0003-4819-93-1-8. [DOI] [PubMed] [Google Scholar]
  23. Steere A. C., Malawista S. E., Hardin J. A., Ruddy S., Askenase W., Andiman W. A. Erythema chronicum migrans and Lyme arthritis. The enlarging clinical spectrum. Ann Intern Med. 1977 Jun;86(6):685–698. doi: 10.7326/0003-4819-86-6-685. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Vodkin M. H., Williams J. C. A heat shock operon in Coxiella burnetti produces a major antigen homologous to a protein in both mycobacteria and Escherichia coli. J Bacteriol. 1988 Mar;170(3):1227–1234. doi: 10.1128/jb.170.3.1227-1234.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Williams P. H., Hinson G. Temperature-dependent transcriptional regulation of expression of fimbriae in an Escherichia coli strain isolated from a child with severe enteritis. Infect Immun. 1987 Jul;55(7):1734–1736. doi: 10.1128/iai.55.7.1734-1736.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. de Graaf F. K., Wientjes F. B., Klaasen-Boor P. Production of K99 antigen by enterotoxigenic Escherichia coli strains of antigen groups o8, o9, o20, and o101 grown at different conditions. Infect Immun. 1980 Jan;27(1):216–221. doi: 10.1128/iai.27.1.216-221.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]

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