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. 1996 Apr 2;93(7):2790–2794. doi: 10.1073/pnas.93.7.2790

A stationary-phase stress-response sigma factor from Mycobacterium tuberculosis.

J DeMaio 1, Y Zhang 1, C Ko 1, D B Young 1, W R Bishai 1
PMCID: PMC39711  PMID: 8610119

Abstract

Alternative RNA polymerase sigma factors are a common means of coordinating gene regulation in bacteria. Using PCR amplification with degenerate primers, we identified and cloned a sigma factor gene, sigF, from Mycobacterium tuberculosis. The deduced protein encoded by sigF shows significant similarity to SigF sporulation sigma factors from Streptomyces coelicolor and Bacillus subtilis and to SigB, a stress-response sigma factor, from B. subtilis. Southern blot surveys with a sigF-specific probe identified cross-hybridizing bands in other slow-growing mycobacteria, Mycobacterium bovis bacille Calmette-Guérin (BCG) and Mycobacterium avium, but not in the rapid-growers Mycobacterium smegmatis or Mycobacterium abscessus. RNase protection assays revealed that M. tuberculosis sigF mRNA is not present during exponential-phase growth in M. bovis BCG cultures but is strongly induced during stationary phase, nitrogen depletion, and cold shock. Weak expression of M. tuberculosis sigF was also detected during late-exponential phase, oxidative stress, anaerobiasis, and alcohol shock. The specific expression of M. tuberculosis sigF during stress or stationary phase suggests that it may play a role in the ability of tubercle bacilli to adapt to host defenses and persist during human infection.

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Selected References

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

  1. Alland D., Kalkut G. E., Moss A. R., McAdam R. A., Hahn J. A., Bosworth W., Drucker E., Bloom B. R. Transmission of tuberculosis in New York City. An analysis by DNA fingerprinting and conventional epidemiologic methods. N Engl J Med. 1994 Jun 16;330(24):1710–1716. doi: 10.1056/NEJM199406163302403. [DOI] [PubMed] [Google Scholar]
  2. Alper S., Duncan L., Losick R. An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in B. subtilis. Cell. 1994 Apr 22;77(2):195–205. doi: 10.1016/0092-8674(94)90312-3. [DOI] [PubMed] [Google Scholar]
  3. Benson A. K., Haldenwang W. G. Bacillus subtilis sigma B is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2330–2334. doi: 10.1073/pnas.90.6.2330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benson A. K., Haldenwang W. G. Regulation of sigma B levels and activity in Bacillus subtilis. J Bacteriol. 1993 Apr;175(8):2347–2356. doi: 10.1128/jb.175.8.2347-2356.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boylan S. A., Redfield A. R., Brody M. S., Price C. W. Stress-induced activation of the sigma B transcription factor of Bacillus subtilis. J Bacteriol. 1993 Dec;175(24):7931–7937. doi: 10.1128/jb.175.24.7931-7937.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Doukhan L., Predich M., Nair G., Dussurget O., Mandic-Mulec I., Cole S. T., Smith D. R., Smith I. Genomic organization of the mycobacterial sigma gene cluster. Gene. 1995 Nov 7;165(1):67–70. doi: 10.1016/0378-1119(95)00427-8. [DOI] [PubMed] [Google Scholar]
  7. Firestein G. S., Gardner S. M., Roeder W. D. Quantitative molecular hybridization with unfractionated, solubilized cells using RNA probes and polyacrylamide gel electrophoresis. Anal Biochem. 1987 Dec;167(2):381–386. doi: 10.1016/0003-2697(87)90180-1. [DOI] [PubMed] [Google Scholar]
  8. GEDDE-DAHL T. Tuberculous infection in the light of tuberculin matriculation. Am J Hyg. 1952 Sep;56(2):139–214. doi: 10.1093/oxfordjournals.aje.a119547. [DOI] [PubMed] [Google Scholar]
  9. Gholamhoseinian A., Piggot P. J. Timing of spoII gene expression relative to septum formation during sporulation of Bacillus subtilis. J Bacteriol. 1989 Oct;171(10):5747–5749. doi: 10.1128/jb.171.10.5747-5749.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Haines D. S., Gillespie D. H. RNA abundance measured by a lysate RNase protection assay. Biotechniques. 1992 May;12(5):736–741. [PubMed] [Google Scholar]
  11. Haldenwang W. G. The sigma factors of Bacillus subtilis. Microbiol Rev. 1995 Mar;59(1):1–30. doi: 10.1128/mr.59.1.1-30.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hein J. Unified approach to alignment and phylogenies. Methods Enzymol. 1990;183:626–645. doi: 10.1016/0076-6879(90)83041-7. [DOI] [PubMed] [Google Scholar]
  13. Honoré N., Bergh S., Chanteau S., Doucet-Populaire F., Eiglmeier K., Garnier T., Georges C., Launois P., Limpaiboon T., Newton S. Nucleotide sequence of the first cosmid from the Mycobacterium leprae genome project: structure and function of the Rif-Str regions. Mol Microbiol. 1993 Jan;7(2):207–214. doi: 10.1111/j.1365-2958.1993.tb01112.x. [DOI] [PubMed] [Google Scholar]
  14. Jacobs W. R., Jr, Kalpana G. V., Cirillo J. D., Pascopella L., Snapper S. B., Udani R. A., Jones W., Barletta R. G., Bloom B. R. Genetic systems for mycobacteria. Methods Enzymol. 1991;204:537–555. doi: 10.1016/0076-6879(91)04027-l. [DOI] [PubMed] [Google Scholar]
  15. Kalman S., Duncan M. L., Thomas S. M., Price C. W. Similar organization of the sigB and spoIIA operons encoding alternate sigma factors of Bacillus subtilis RNA polymerase. J Bacteriol. 1990 Oct;172(10):5575–5585. doi: 10.1128/jb.172.10.5575-5585.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kempsell K. E., Ji Y. E., Estrada I. C., Colston M. J., Cox R. A. The nucleotide sequence of the promoter, 16S rRNA and spacer region of the ribosomal RNA operon of Mycobacterium tuberculosis and comparison with Mycobacterium leprae precursor rRNA. J Gen Microbiol. 1992 Aug;138(Pt 8):1717–1727. doi: 10.1099/00221287-138-8-1717. [DOI] [PubMed] [Google Scholar]
  17. Khomenko A. G. The variability of Mycobacterium tuberculosis in patients with cavitary pulmonary tuberculosis in the course of chemotherapy. Tubercle. 1987 Dec;68(4):243–253. doi: 10.1016/0041-3879(87)90064-x. [DOI] [PubMed] [Google Scholar]
  18. Khomenko A. G. The variability of Mycobacterium tuberculosis in patients with cavitary pulmonary tuberculosis in the course of chemotherapy. Tubercle. 1987 Dec;68(4):243–253. doi: 10.1016/0041-3879(87)90064-x. [DOI] [PubMed] [Google Scholar]
  19. Lonetto M. A., Brown K. L., Rudd K. E., Buttner M. J. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7573–7577. doi: 10.1073/pnas.91.16.7573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lonetto M., Gribskov M., Gross C. A. The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol. 1992 Jun;174(12):3843–3849. doi: 10.1128/jb.174.12.3843-3849.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Margolis P., Driks A., Losick R. Establishment of cell type by compartmentalized activation of a transcription factor. Science. 1991 Oct 25;254(5031):562–565. doi: 10.1126/science.1948031. [DOI] [PubMed] [Google Scholar]
  22. Min K. T., Hilditch C. M., Diederich B., Errington J., Yudkin M. D. Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase. Cell. 1993 Aug 27;74(4):735–742. doi: 10.1016/0092-8674(93)90520-z. [DOI] [PubMed] [Google Scholar]
  23. Potúcková L., Kelemen G. H., Findlay K. C., Lonetto M. A., Buttner M. J., Kormanec J. A new RNA polymerase sigma factor, sigma F, is required for the late stages of morphological differentiation in Streptomyces spp. Mol Microbiol. 1995 Jul;17(1):37–48. doi: 10.1111/j.1365-2958.1995.mmi_17010037.x. [DOI] [PubMed] [Google Scholar]
  24. Schmidt R., Margolis P., Duncan L., Coppolecchia R., Moran C. P., Jr, Losick R. Control of developmental transcription factor sigma F by sporulation regulatory proteins SpoIIAA and SpoIIAB in Bacillus subtilis. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9221–9225. doi: 10.1073/pnas.87.23.9221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Siegele D. A., Kolter R. Life after log. J Bacteriol. 1992 Jan;174(2):345–348. doi: 10.1128/jb.174.2.345-348.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Small P. M., Hopewell P. C., Singh S. P., Paz A., Parsonnet J., Ruston D. C., Schecter G. F., Daley C. L., Schoolnik G. K. The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N Engl J Med. 1994 Jun 16;330(24):1703–1709. doi: 10.1056/NEJM199406163302402. [DOI] [PubMed] [Google Scholar]
  27. Sudre P., ten Dam G., Kochi A. Tuberculosis: a global overview of the situation today. Bull World Health Organ. 1992;70(2):149–159. [PMC free article] [PubMed] [Google Scholar]
  28. Tanaka K., Shiina T., Takahashi H. Multiple principal sigma factor homologs in eubacteria: identification of the "rpoD box". Science. 1988 Nov 18;242(4881):1040–1042. doi: 10.1126/science.3194753. [DOI] [PubMed] [Google Scholar]
  29. Wayne L. G. Dynamics of submerged growth of Mycobacterium tuberculosis under aerobic and microaerophilic conditions. Am Rev Respir Dis. 1976 Oct;114(4):807–811. doi: 10.1164/arrd.1976.114.4.807. [DOI] [PubMed] [Google Scholar]

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