Previous Article | Next Article 
Journal of Bacteriology, October 2001, p. 6119-6125, Vol. 183, No. 20
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.20.6119-6125.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
The Alternative Sigma Factor SigH Regulates Major Components
of Oxidative and Heat Stress Responses in
Mycobacterium tuberculosis
Sahadevan
Raman,1
Taeksun
Song,1
Xiaoling
Puyang,1
Stoyan
Bardarov,2
William R.
Jacobs Jr.,2 and
Robert N.
Husson1,*
Division of Infectious Diseases, Children's
Hospital, Harvard Medical School, Boston, Massachusetts
02115,1 and Howard Hughes Medical
Institute, Albert Einstein College of Medicine, Bronx, New York
104612
Received 11 May 2001/Accepted 30 July 2001
Mycobacterium tuberculosis is a specialized
intracellular pathogen that must regulate gene expression to overcome
stresses produced by host defenses during infection. SigH is an
alternative sigma factor that we have previously shown plays a role in
the response to stress of the saprophyte Mycobacterium
smegmatis. In this work we investigated the role of
sigH in the M.
tuberculosis response to heat and oxidative stress. We
determined that a M. tuberculosis sigH
mutant is more susceptible to oxidative stresses and that the inducible
expression of the thioredoxin reductase/thioredoxin genes
trxB2/trxC and a gene of unknown function,
Rv2466c, is regulated by sigH via expression from
promoters directly recognized by SigH. We also determined that the
sigH mutant is more susceptible to heat stress and that
inducible expression of the heat shock genes dnaK and
clpB is positively regulated by sigH. The
induction of these heat shock gene promoters but not of other
SigH-dependent promoters was markedly greater in response to heat
versus oxidative stress, consistent with their additional regulation by
a heat-labile repressor. To further understand the role of
sigH in the M.
tuberculosis stress response, we investigated the
regulation of the stress-responsive sigma factor genes
sigE and sigB. We determined that
inducible expression of sigE is regulated by
sigH and that basal and inducible expression of
sigB is dependent on sigE and
sigH. These data indicate that sigH plays
a central role in a network that regulates heat and oxidative-stress
responses that are likely to be important in M.
tuberculosis pathogenesis.
*
Corresponding author. Mailing address: Children's
Hospital, Enders Rm. 609, 300 Longwood Ave., Boston, MA 02115. Phone:
(617) 355-5151. Fax: (617) 355-8387. E-mail:
robert.husson{at}tch.harvard.edu.
Journal of Bacteriology, October 2001, p. 6119-6125, Vol. 183, No. 20
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.20.6119-6125.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Mehra, S., Kaushal, D.
(2009). Functional Genomics Reveals Extended Roles of the Mycobacterium tuberculosis Stress Response Factor {sigma}H. J. Bacteriol.
191: 3965-3980
[Abstract]
[Full Text]
-
Ehira, S., Teramoto, H., Inui, M., Yukawa, H.
(2009). Regulation of Corynebacterium glutamicum Heat Shock Response by the Extracytoplasmic-Function Sigma Factor SigH and Transcriptional Regulators HspR and HrcA. J. Bacteriol.
191: 2964-2972
[Abstract]
[Full Text]
-
Singh, A. K., Singh, B. N.
(2009). Differential Expression of sigH Paralogs during Growth and under Different Stress Conditions in Mycobacterium smegmatis. J. Bacteriol.
191: 2888-2893
[Abstract]
[Full Text]
-
Park, S. T., Kang, C.-M., Husson, R. N.
(2008). Regulation of the SigH stress response regulon by an essential protein kinase in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA
105: 13105-13110
[Abstract]
[Full Text]
-
Gebhard, S., Humpel, A., McLellan, A. D., Cook, G. M.
(2008). The alternative sigma factor SigF of Mycobacterium smegmatis is required for survival of heat shock, acidic pH and oxidative stress. Microbiology
154: 2786-2795
[Abstract]
[Full Text]
-
Dona, V., Rodrigue, S., Dainese, E., Palu, G., Gaudreau, L., Manganelli, R., Provvedi, R.
(2008). Evidence of Complex Transcriptional, Translational, and Posttranslational Regulation of the Extracytoplasmic Function Sigma Factor {sigma}E in Mycobacterium tuberculosis. J. Bacteriol.
190: 5963-5971
[Abstract]
[Full Text]
-
Li, A. H., Lam, W. L., Stokes, R. W.
(2008). Characterization of genes differentially expressed within macrophages by virulent and attenuated Mycobacterium tuberculosis identifies candidate genes involved in intracellular growth. Microbiology
154: 2291-2303
[Abstract]
[Full Text]
-
Song, T., Song, S.-E., Raman, S., Anaya, M., Husson, R. N.
(2008). Critical Role of a Single Position in the -35 Element for Promoter Recognition by Mycobacterium tuberculosis SigE and SigH. J. Bacteriol.
190: 2227-2230
[Abstract]
[Full Text]
-
Kang, C.-M., Nyayapathy, S., Lee, J.-Y., Suh, J.-W., Husson, R. N.
(2008). Wag31, a homologue of the cell division protein DivIVA, regulates growth, morphology and polar cell wall synthesis in mycobacteria. Microbiology
154: 725-735
[Abstract]
[Full Text]
-
Hett, E. C., Rubin, E. J.
(2008). Bacterial Growth and Cell Division: a Mycobacterial Perspective. Microbiol. Mol. Biol. Rev.
72: 126-156
[Abstract]
[Full Text]
-
Lee, J.-H., Geiman, D. E., Bishai, W. R.
(2008). Role of Stress Response Sigma Factor SigG in Mycobacterium tuberculosis. J. Bacteriol.
190: 1128-1133
[Abstract]
[Full Text]
-
Lee, J.-H., Karakousis, P. C., Bishai, W. R.
(2008). Roles of SigB and SigF in the Mycobacterium tuberculosis Sigma Factor Network. J. Bacteriol.
190: 699-707
[Abstract]
[Full Text]
-
Chowdhury, R. P., Gupta, S., Chatterji, D.
(2007). Identification and Characterization of the dps Promoter of Mycobacterium smegmatis: Promoter Recognition by Stress-Specific Extracytoplasmic Function Sigma Factors {sigma}H and {sigma}F. J. Bacteriol.
189: 8973-8981
[Abstract]
[Full Text]
-
Williams, D. L., Pittman, T. L., Deshotel, M., Oby-Robinson, S., Smith, I., Husson, R.
(2007). Molecular Basis of the Defective Heat Stress Response in Mycobacterium leprae. J. Bacteriol.
189: 8818-8827
[Abstract]
[Full Text]
-
Wu, C.-w., Schmoller, S. K., Shin, S. J., Talaat, A. M.
(2007). Defining the Stressome of Mycobacterium avium subsp. paratuberculosis In Vitro and in Naturally Infected Cows. J. Bacteriol.
189: 7877-7886
[Abstract]
[Full Text]
-
Pang, X., Howard, S. T.
(2007). Regulation of the {alpha}-Crystallin Gene acr2 by the MprAB Two-Component System of Mycobacterium tuberculosis. J. Bacteriol.
189: 6213-6221
[Abstract]
[Full Text]
-
Jakob, K., Satorhelyi, P., Lange, C., Wendisch, V. F., Silakowski, B., Scherer, S., Neuhaus, K.
(2007). Gene Expression Analysis of Corynebacterium glutamicum Subjected to Long-Term Lactic Acid Adaptation. J. Bacteriol.
189: 5582-5590
[Abstract]
[Full Text]
-
Yukawa, H., Omumasaba, C. A., Nonaka, H., Kos, P., Okai, N., Suzuki, N., Suda, M., Tsuge, Y., Watanabe, J., Ikeda, Y., Vertes, A. A., Inui, M.
(2007). Comparative analysis of the Corynebacterium glutamicum group and complete genome sequence of strain R. Microbiology
153: 1042-1058
[Abstract]
[Full Text]
-
Pang, X., Vu, P., Byrd, T. F., Ghanny, S., Soteropoulos, P., Mukamolova, G. V., Wu, S., Samten, B., Howard, S. T.
(2007). Evidence for complex interactions of stress-associated regulons in an mprAB deletion mutant of Mycobacterium tuberculosis. Microbiology
153: 1229-1242
[Abstract]
[Full Text]
-
Rodrigue, S., Brodeur, J., Jacques, P.-E., Gervais, A. L., Brzezinski, R., Gaudreau, L.
(2007). Identification of Mycobacterial {sigma} Factor Binding Sites by Chromatin Immunoprecipitation Assays. J. Bacteriol.
189: 1505-1513
[Abstract]
[Full Text]
-
Agarwal, N., Woolwine, S. C., Tyagi, S., Bishai, W. R.
(2007). Characterization of the Mycobacterium tuberculosis Sigma Factor SigM by Assessment of Virulence and Identification of SigM-Dependent Genes. Infect. Immun.
75: 452-461
[Abstract]
[Full Text]
-
Raman, S., Puyang, X., Cheng, T.-Y., Young, D. C., Moody, D. B., Husson, R. N.
(2006). Mycobacterium tuberculosis SigM Positively Regulates Esx Secreted Protein and Nonribosomal Peptide Synthetase Genes and Down Regulates Virulence-Associated Surface Lipid Synthesis. J. Bacteriol.
188: 8460-8468
[Abstract]
[Full Text]
-
Dainese, E., Rodrigue, S., Delogu, G., Provvedi, R., Laflamme, L., Brzezinski, R., Fadda, G., Smith, I., Gaudreau, L., Palu, G., Manganelli, R.
(2006). Posttranslational Regulation of Mycobacterium tuberculosis Extracytoplasmic-Function Sigma Factor {sigma}L and Roles in Virulence and in Global Regulation of Gene Expression. Infect. Immun.
74: 2457-2461
[Abstract]
[Full Text]
-
He, H., Hovey, R., Kane, J., Singh, V., Zahrt, T. C.
(2006). MprAB Is a Stress-Responsive Two-Component System That Directly Regulates Expression of Sigma Factors SigB and SigE in Mycobacterium tuberculosis. J. Bacteriol.
188: 2134-2143
[Abstract]
[Full Text]
-
Hahn, M.-Y., Raman, S., Anaya, M., Husson, R. N.
(2005). The Mycobacterium tuberculosis Extracytoplasmic-Function Sigma Factor SigL Regulates Polyketide Synthases and Secreted or Membrane Proteins and Is Required for Virulence. J. Bacteriol.
187: 7062-7071
[Abstract]
[Full Text]
-
Schmid, A. K., Howell, H. A., Battista, J. R., Peterson, S. N., Lidstrom, M. E.
(2005). Global Transcriptional and Proteomic Analysis of the Sig1 Heat Shock Regulon of Deinococcus radiodurans. J. Bacteriol.
187: 3339-3351
[Abstract]
[Full Text]
-
Osorio, C. G., Crawford, J. A., Michalski, J., Martinez-Wilson, H., Kaper, J. B., Camilli, A.
(2005). Second-Generation Recombination-Based In Vivo Expression Technology for Large-Scale Screening for Vibrio cholerae Genes Induced during Infection of the Mouse Small Intestine. Infect. Immun.
73: 972-980
[Abstract]
[Full Text]
-
Benachour, A., Muller, C., Dabrowski-Coton, M., Le Breton, Y., Giard, J.-C., Rince, A., Auffray, Y., Hartke, A.
(2005). The Enterococcus faecalis SigV Protein Is an Extracytoplasmic Function Sigma Factor Contributing to Survival following Heat, Acid, and Ethanol Treatments. J. Bacteriol.
187: 1022-1035
[Abstract]
[Full Text]
-
Starck, J., Kallenius, G., Marklund, B.-I., Andersson, D. I., Akerlund, T.
(2004). Comparative proteome analysis of Mycobacterium tuberculosis grown under aerobic and anaerobic conditions. Microbiology
150: 3821-3829
[Abstract]
[Full Text]
-
Raman, S., Hazra, R., Dascher, C. C., Husson, R. N.
(2004). Transcription Regulation by the Mycobacterium tuberculosis Alternative Sigma Factor SigD and Its Role in Virulence. J. Bacteriol.
186: 6605-6616
[Abstract]
[Full Text]
-
Barreiro, C., Gonzalez-Lavado, E., Patek, M., Martin, J.-F.
(2004). Transcriptional Analysis of the groES-groEL1, groEL2, and dnaK genes in Corynebacterium glutamicum: Characterization of Heat Shock-Induced Promoters. J. Bacteriol.
186: 4813-4817
[Abstract]
[Full Text]
-
Bischoff, M., Dunman, P., Kormanec, J., Macapagal, D., Murphy, E., Mounts, W., Berger-Bachi, B., Projan, S.
(2004). Microarray-Based Analysis of the Staphylococcus aureus {sigma}B Regulon. J. Bacteriol.
186: 4085-4099
[Abstract]
[Full Text]
-
Geiman, D. E., Kaushal, D., Ko, C., Tyagi, S., Manabe, Y. C., Schroeder, B. G., Fleischmann, R. D., Morrison, N. E., Converse, P. J., Chen, P., Bishai, W. R.
(2004). Attenuation of Late-Stage Disease in Mice Infected by the Mycobacterium tuberculosis Mutant Lacking the SigF Alternate Sigma Factor and Identification of SigF-Dependent Genes by Microarray Analysis. Infect. Immun.
72: 1733-1745
[Abstract]
[Full Text]
-
Manganelli, R., Proveddi, R., Rodrigue, S., Beaucher, J., Gaudreau, L., Smith, I.
(2004). {sigma} Factors and Global Gene Regulation in Mycobacterium tuberculosis. J. Bacteriol.
186: 895-902
[Full Text]
-
Tyagi, J. S., Saini, D. K.
(2004). Did the loss of two-component systems initiate pseudogene accumulation in Mycobacterium leprae?. Microbiology
150: 4-7
[Full Text]
-
Kumar, A., Bose, M., Brahmachari, V.
(2003). Analysis of Expression Profile of Mammalian Cell Entry (mce) Operons of Mycobacterium tuberculosis. Infect. Immun.
71: 6083-6087
[Abstract]
[Full Text]
-
Recchi, C., Sclavi, B., Rauzier, J., Gicquel, B., Reyrat, J.-M.
(2003). Mycobacterium tuberculosis Rv1395 Is a Class III Transcriptional Regulator of the AraC Family Involved in Cytochrome P450 Regulation. J. Biol. Chem.
278: 33763-33773
[Abstract]
[Full Text]
-
Smith, I.
(2003). Mycobacterium tuberculosis Pathogenesis and Molecular Determinants of Virulence. Clin. Microbiol. Rev.
16: 463-496
[Abstract]
[Full Text]
-
Langlois, P., Bourassa, S., Poirier, G. G., Beaulieu, C.
(2003). Identification of Streptomyces coelicolor Proteins That Are Differentially Expressed in the Presence of Plant Material. Appl. Environ. Microbiol.
69: 1884-1889
[Abstract]
[Full Text]
-
Salazar, L., Guerrero, E., Casart, Y., Turcios, L., Bartoli, F.
(2003). Transcription analysis of the dnaA gene and oriC region of the chromosome of Mycobacterium smegmatis and Mycobacterium bovis BCG, and its regulation by the DnaA protein. Microbiology
149: 773-784
[Abstract]
[Full Text]
-
Schmid, A. K., Lidstrom, M. E.
(2002). Involvement of Two Putative Alternative Sigma Factors in Stress Response of the Radioresistant Bacterium Deinococcus radiodurans. J. Bacteriol.
184: 6182-6189
[Abstract]
[Full Text]
-
Bardarov, S., Bardarov, S. Jr, Pavelka, M. S. Jr, Sambandamurthy, V., Larsen, M., Tufariello, J., Chan, J., Hatfull, G., Jacobs, W. R. Jr
(2002). Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology
148: 3007-3017
[Abstract]
[Full Text]
-
Stewart, G. R., Wernisch, L., Stabler, R., Mangan, J. A., Hinds, J., Laing, K. G., Young, D. B., Butcher, P. D.
(2002). Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology
148: 3129-3138
[Abstract]
[Full Text]
-
Kaushal, D., Schroeder, B. G., Tyagi, S., Yoshimatsu, T., Scott, C., Ko, C., Carpenter, L., Mehrotra, J., Manabe, Y. C., Fleischmann, R. D., Bishai, W. R.
(2002). Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH. Proc. Natl. Acad. Sci. USA
99: 8330-8335
[Abstract]
[Full Text]