Skip to main page content

• HOME
• Current Issue
• Archive
• Alerts
• About ASM
• Contact us
• Tech Support
• Journals.ASM.org

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Dainese, E. Articles by Manganelli, R. Search for Related Content PubMed PubMed Citation Articles by Dainese, E. Articles by Manganelli, R.

 Previous Article  |  Next Article 

Infection and Immunity, April 2006, p. 2457-2461, Vol. 74, No. 4
0019-9567/06/$08.00+0     doi:10.1128/IAI.74.4.2457-2461.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Posttranslational Regulation of Mycobacterium tuberculosis Extracytoplasmic-Function Sigma Factor ^L and Roles in Virulence and in Global Regulation of Gene Expression

Elisa Dainese,^1, Sébastien Rodrigue,^2, Giovanni Delogu,³ Roberta Provvedi,¹ Liette Laflamme,² Ryszard Brzezinski,⁴ Giovanni Fadda,³ Issar Smith,⁵ Luc Gaudreau,² Giorgio Palù,¹ and Riccardo Manganelli^1*

Department of Histology, Microbiology and Medical Biotechnologies, University of Padova, Padova, Italy,¹ Centre de Recherche sur les Mécanismes du Fonctionnement Cellulaire, Université de Sherbrooke, Sherbrooke, Québec, Canada,² Institute of Microbiology, Catholic University of the Sacred Hearth, Rome, Italy,³ Centre de Valorisation de la Diversité Microbienne, Département de Biologie, Université de Sherbrooke, Sherbrooke, Québec, Canada;,⁴ TB Center, The Public Health Research Institute, Newark, New Jersey⁵

Received 9 November 2005/ Returned for modification 12 December 2005/ Accepted 23 January 2006

Top Abstract Text References

 
In this report, we demonstrate that SigL is posttranslationally regulated by a specific anti-sigma factor, RslA, and contributes to the expression of at least 28 genes. Several of these genes could mediate important cell envelope-related processes. Importantly, a sigL-rslA mutant strain was significantly attenuated in a mouse model of infection.

Top Abstract Text References

 
Sigma factors are interchangeable subunits that provide the promoter recognition function to bacterial RNA polymerase (RNAP) holoenzymes (10). Thirteen sigma factor genes were predicted from the genome sequence of Mycobacterium tuberculosis. Several of these were shown to be important for appropriate stress responses and virulence (9, 15-18, 20, 27, 29). Interestingly, the expression of the ^B-encoding gene (sigB) is induced in response to several stimuli (4, 14, 17, 18), suggesting a potential general role in stress responses (16, 24). Previous studies have shown that transcription of sigB can be initiated at the same nucleotide by RNAP holoenzymes that contain extracytoplasmic-function sigma factor ^E or ^H (17, 18, 21). It was also recently reported that the extracytoplasmic-function sigma factor ^L may also have a role in the expression of sigB (11, 16).

Using an in vitro transcription assay, we have tested each M. tuberculosis sigma factor to determine whether additional sigma factors could elicit transcription of sigB. Reactions were performed as previously described (3) using purified Mycobacterium smegmatis RNAP, 150 fmol of sigB DNA template (encompassing base pairs –361 to +329 relative to the first translated nucleotide), and 3 pmol of recombinant sigma factors (13). As expected, primer extension products were detected for the ^E- and ^H-containing holoenzymes (Fig. 1A). Interestingly, the ^L-dependent transcription signal also originated from the same nucleotide (Fig. 1A). Importantly, the ^E-, ^H-, and ^L-dependent signals matched the sigB transcriptional start site identified in vivo (17, 21). In addition, an upstream ^F-dependent promoter with striking homology to the proposed ^F consensus was identified (Fig. 1A) (3, 9, 16). No signal was observed with the nine remaining M. tuberculosis sigma factors (data not shown). Primer extension assays were performed according to standard procedures using the following oligonucleotide: Mtb sigB-EXT (5'-ATCCAGATCGCTGTCAACCCGG-3'). A putative promoter closely resembling the ^E-^H-^L-dependent sigB promoter was also found upstream of sigL. In vitro transcription was thus performed as in Fig. 1A using a sigL DNA template (base pairs –345 to +138 relative to the translation start site) and oligonucleotide Mtb sigL-EXT (5'-CTCTTGGACGACGTCTTC-3'). Interestingly, ^L was the only sigma factor that allowed transcription from this promoter, suggesting that minor divergences in DNA sequences may account for promoter discrimination by ^E, ^H, and ^L (Fig. 1B).

View larger version (66K): [in this window] [in a new window]

FIG. 1. Identification of M. tuberculosis (Mtb) sigma factors involved in the transcription of selected genes. (A) High-resolution mapping of transcription signals observed using an in vitro transcription screening of the sigB upstream region. E, H, and L initiate transcription at the same nucleotide, while F use an upstream promoter. (B) sigL is expressed from an autoregulated promoter. In vitro transcription with the corresponding sigma factors was followed by a primer extension procedure. Proposed promoter boxes are underlined. Arrows indicate transcriptional start sites.

Hahn and colleagues recently proposed that RslA could be a ^L anti-sigma factor and detected an interaction between these proteins in a bacterial two-hybrid assay (11). Since RslA is a predicted transmembrane protein, we have fused its cytoplasmic moiety (amino acids 1 to 114) to glutathione S-transferase (GST) and performed direct interaction assays with hexahistidine-tagged ^E, ^F, ^H, and ^L. Assays were performed as previously described (3) and analyzed by immunoblotting using anti-His antibody. Figure 2A shows a direct interaction between ^L and GST-RslA. No interaction was detected between GST-RslA and ^E, ^F, and ^H or between GST and any sigma factor (Fig. 2A and data not shown). In vitro transcription assays next demonstrated that RslA inhibits ^L-dependent transcription of the sigB gene in a dose-dependent manner (Fig. 2B). In this latter experiment, increasing concentrations (1.5, 3.0, 6.0, and 12 pmol) of the N-terminally hexahistidine-tagged RslA cytoplasmic moiety were added to a fixed amount of ^L-containing holoenzyme and sigB promoter template as described above for Fig. 1. Importantly, the ^L-dependent signal was not affected by the addition of RshA or Rv1222, a ^H (26) and a ^E anti-sigma factor, respectively (data not shown). Taken together, these results demonstrate that RslA is a ^L-specific anti-sigma factor.

View larger version (46K): [in this window] [in a new window]

FIG. 2. RslA is a L-specific anti-sigma factor. (A) GST-RslA interacts with L. Results of GST pull-down assays between GST-RslA and hexahistidine-tagged H or L revealed by immunoblotting using an anti-His antibody are shown. L, loading control; S, supernatant; P, pellet. (B) RslA inhibits L activity in a dose-dependent manner. In vitro transcription inhibition assays at the sigB promoter were carried out in the absence (–) or presence (+) of L and increasing amounts (triangle) of hexahistidine-tagged RslA cytoplasmic moiety.

The DNA region including sigL and rslA was next replaced in the genome of M. tuberculosis H37Rv by an hygromycin resistance gene using specialized transduction (2). The growth curve and colony morphology of the resulting strain (TB1) was indistinguishable from the wild-type (wt) strain (data not shown). In agreement with the results obtained by Hahn et al. using a similar sigL mutant (11), we have not observed any difference in the sensitivity of the TB1 and wt strains to diamide, cumene hydroperoxide, H₂O₂, and sodium nitroprusside (data not shown) using a previously described disk diffusion assay methodology (18). Moreover, the TB1 and wt strains were not differentially affected by EDTA, vancomycin, tetracycline, heat shock (45°C), acidic pH, hyperosmolarity, and dithiothreitol. However, in contrast to the findings of Hahn and colleagues, we have noticed a small but reproducible sensitivity of TB1 to the superoxide generator plumbagine and to the detergent sodium dodecyl sulfate relative to the wt strain in disk diffusion assays performed as previously described (18); these phenotypes were fully complemented by the introduction of the sigL-rslA locus (or by the sigL gene alone, see TB3 strain described below) at the L5 integration site (data not shown). However, no significant increase in sigL expression was monitored by quantitative reverse transcription-PCR (qRT-PCR) after exposure to plumbagine or sodium dodecyl sulfate (data not shown).

Hahn and colleagues have shown that a sigL mutant of M. tuberculosis is attenuated in BALB/c mice in a high-dose intravenous infection model. We have performed a similar analysis using a low-dose aerosol infection model for two different mouse strains with different natural resistances to infection. C57BL/6 and DBA/2 mice were challenged, with 100 and 200 CFU/mouse of the TB1 or H37Rv strain (6). No major differences were observed in the abilities of the two strains to colonize lung and spleen tissues or in the size and extent of lesions as assessed by histopathology analysis at 28 and 60 days postinfection (Table 1 and data not shown). DBA/2 mice were also held for observation and determination of the time to death. A significant extension of the median survival time was observed for mice infected with the TB1 mutant compared to the parental strain, thus indicating that sigL is important for virulence (Fig. 3).

View this table: [in this window] [in a new window]

TABLE 1. Bacterial counts in organs of C57BL/6 mice after aerosol infection

View larger version (11K): [in this window] [in a new window]

FIG. 3. Time-to-death analysis in DBA/2 mice after aerosol infection with M. tuberculosis H37Rv (squares) and with the sigL mutant strain (circles).

Using qRT-PCR and primer extension assays, Hahn and colleagues have concluded that sigL is constitutively expressed through mid-exponential and stationary phase by a ^L-independent promoter located 130 bases upstream of sigL (11). However, by using a plasmid containing a fusion of the first 564 nucleotides upstream of sigL to lacZ, ß-galactosidase activity in the TB1 and wt strains (measured by the method of Miller [19]) tended to increase with culture density, especially in the transition from lag to exponential phase (Fig. 4).

View larger version (25K): [in this window] [in a new window]

FIG. 4. Measurement of sigL expression. M. tuberculosis H37Rv harboring a reporter plasmid carrying the sigL upstream region fused to lacZ was grown in Middlebrook 7H9 medium, and ß-galactosidase activity was measured at different points of the growth curve. The bars show ß-galactosidase activity (in Miller units), and the line shows the optical density at 540 nm (OD 540).

In order to study the role of ^L by mimicking naturally inducing conditions (release of ^L by RslA), we have complemented the TB1 mutant strain by the introduction of sigL and its upstream region at the L5 integration site (12). The resulting "partially complemented" strain (TB3) thus contains sigL but not rslA, which should allow a constitutive activity of ^L. A 25-fold induction of sigL was indeed measured by qRT-PCR in this strain with respect to the H37Rv strain (data not shown). The TB1 and TB3 strains were grown to mid-exponential phase, and the RNA expression profiles were compared using oligonucleotide microarrays as previously described (18). The resulting data were analyzed using the significance analysis of microarray method (28). A total of 27 genes from 12 putative transcription units were up-regulated in TB3 relative to TB1 (Table 2). No repressed genes were identified. Six induced genes were chosen, and their induction levels were confirmed by qRT-PCR (Table 2). The mRNA levels of the selected genes in H37Rv and TB1 mutant strains were also compared. All genes were expressed at similar levels in both strains, suggesting that inhibition of ^L activity by RslA is virtually complete under these conditions (Table 2).

View this table: [in this window] [in a new window]

TABLE 2. Genes under L controla

Hahn and colleagues have recently identified 19 genes induced by the overexpression of ^L from an acetamide-inducible promoter (11). Some genes (pks10, pks7, Rv1138c, mpt53, and Rv2877c) were identified by both approaches. However, the remaining four genes from the pks10 operon, three genes from the putative mmpL13 operon, four genes from the putative operon starting with Rv3166c, mce2F and its upstream gene, sigB, and others, were identified only in this work. Putative promoter boxes similar to those of in vitro-identified ^L-dependent promoters (Fig. 1) and compatible with the proposed ^L consensus sequence (11) were found upstream of eight of these genes (Table 2). Rapid amplification of cDNA end (5'-RACE) experiments, performed as previously described (17), confirmed that the transcriptional start sites of sigL, mmpL13A, and mpt53 were suitably located to allow ^L to recognize these promoter elements (data not shown). Interestingly, although ^E, ^H, and ^L all recognize the same promoter upstream of sigB, no other genes seem to be regulated by any combination of these sigma factors (17, 18). This suggests that although the consensus sequences recognized by these sigma factors are similar, few differences are sufficient for promoter discrimination.

Many of the genes regulated by ^L could be involved in processes related to the cell envelope (Table 2). For example, the pks10 operon and ppsA gene products are likely to be involved in the biosynthesis of dimycocerosyl phthiocerol, an important component of the mycobacterial cell wall (1, 5, 8, 22, 23). Moreover, the mmpL13a and mmpL13b gene products belong to a family of proteins involved in lipid transport (5), sulfolipid biosynthesis (7), and peptidoglycolipid biogenesis (25). From this perspective, it is noteworthy that RslA is a predicted transmembrane protein that could possibly sense the condition of the cell envelope or an external signal. The absence of ^L could thus result in a weakening the cell surface or in an inappropriate modulation of the host immune response by the bacterium, which could at least partially explain the attenuation of the sigL mutant reported in this paper and by others (11).

 
This work was supported by grants from ISS (PN-AIDS 50F.24 [R.M.] and 50F.13 [G.F.]), MIUR (PRIN 2003 grant no. 2003059340 [R.M.]), and NIH (grant no. AI-44856 [I.S.]) and from the NSERC "Genomics projects" (R.B. and L.G.). L.G. holds a Canada Research Chair on mechanisms of gene transcription. S.R. is the recipient of fellowships from NSERC and FRSQ.

 
* Corresponding author. Mailing address: Department of Histology, Microbiology and Medical Biotechnologies, University of Padova, Via Gabelli 63, 35100 Padova, Italy. Phone: 39 49 827 2366. Fax: 39 49 827 2355. E-mail: riccardo.manganelli{at}unipd.it.

Editor: F. C. Fang

E.D. and S.R. contributed equally to this work.

Top Abstract Text References

 

1
1. Azad, A. K., T. D. Sirakova, N. D. Fernandes, and P. E. Kolattukudy. 1997. Gene knockout reveals a novel gene cluster for the synthesis of a class of cell wall lipids unique to pathogenic mycobacteria. J. Biol. Chem. 272:16741-16745.[Abstract/Free Full Text]
2
2. Bardarov, S., S. Bardarov, Jr., M. S. Pavelka, Jr., V. Sambandamurthy, M. Larsen, J. Tufariello, J. Chan, G. Hatfull, and W. R. Jacobs, 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/Free Full Text]
3
3. Beaucher, J., S. Rodrigue, P. E. Jacques, I. Smith, R. Brzezinski, and L. Gaudreau. 2002. Novel Mycobacterium tuberculosis anti-sigma factor antagonists control SigF activity by distinct mechanisms. Mol. Microbiol. 45:1527-1540.[CrossRef][Medline]
4
4. Betts, J. C., P. T. Lukey, L. C. Robb, R. A. McAdam, and K. Duncan. 2002. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43:717-731.[CrossRef][Medline]
5
5. Camacho, L. R., P. Constant, C. Raynaud, M. A. Laneelle, J. A. Triccas, B. Gicquel, M. Daffe, and C. Guilhot. 2001. Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Evidence that this lipid is involved in the cell wall permeability barrier. J. Biol. Chem. 276:19845-19854.[Abstract/Free Full Text]
6
6. Collins, F. M. 1985. Protection to mice afforded by BCG vaccines against an aerogenic challenge by three mycobacteria of decreasing virulence. Tubercle 66:267-276.[CrossRef][Medline]
7
7. Converse, S. E., and J. S. Cox. 2005. A protein secretion pathway critical for Mycobacterium tuberculosis virulence is conserved and functional in Mycobacterium smegmatis. J. Bacteriol. 187:1238-1245.[Abstract/Free Full Text]
8
8. Dubey, V. S., T. D. Sirakova, M. H. Cynamon, and P. E. Kolattukudy. 2003. Biochemical function of msl5 (pks8 plus pks17) in Mycobacterium tuberculosis H37Rv: biosynthesis of monomethyl branched unsaturated fatty acids. J. Bacteriol. 185:4620-4625.[Abstract/Free Full Text]
9
9. Geiman, D. E., D. Kaushal, C. Ko, S. Tyagi, Y. C. Manabe, B. G. Schroeder, R. D. Fleischmann, N. E. Morrison, P. J. Converse, P. Chen, and W. R. Bishai. 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/Free Full Text]
10
10. Gruber, T. M., and C. A. Gross. 2003. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57:441-466.[CrossRef][Medline]
11
11. Hahn, M. Y., S. Raman, M. Anaya, and R. N. Husson. 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/Free Full Text]
12
12. Hatfull, G. F., and G. J. Sarkis. 1993. DNA sequence, structure and gene expression of mycobacteriophage L5: a phage system for mycobacterial genetics. Mol. Microbiol. 7:395-405.[Medline]
13
13. Jacques, J.-F., S. Rodrigue, R. Brzezinski, and L. Gaudreau. 2006. A recombinant Mycobacterium tuberculosis in vitro transcription system. FEMS Microbiol. Lett. 255:140-147.[CrossRef][Medline]
14
14. Manganelli, R., E. Dubnau, S. Tyagi, F. R. Kramer, and I. Smith. 1999. Differential expression of 10 sigma factor genes in Mycobacterium tuberculosis. Mol. Microbiol. 31:715-724.[CrossRef][Medline]
15
15. Manganelli, R., L. Fattorini, D. Tan, E. Iona, G. Orefici, G. Altavilla, P. Cusatelli, and I. Smith. 2004. The extra cytoplasmic function sigma factor SigE is essential for Mycobacterium tuberculosis virulence in mice. Infect. Immun. 72:3038-3041.[Abstract/Free Full Text]
16
16. Manganelli, R., R. Provvedi, S. Rodrigue, J. Beaucher, L. Gaudreau, and I. Smith. 2004. Sigma factors and global gene regulation in Mycobacterium tuberculosis. J. Bacteriol. 186:895-902.[Free Full Text]
17
17. Manganelli, R., M. I. Voskuil, G. K. Schoolnik, E. Dubnau, M. Gomez, and I. Smith. 2002. Role of the extracytoplasmic-function sigma factor SigH in Mycobacterium tuberculosis global gene expression. Mol. Microbiol. 45:365-374.[CrossRef][Medline]
18
18. Manganelli, R., M. I. Voskuil, G. K. Schoolnik, and I. Smith. 2001. The Mycobacterium tuberculosis ECF sigma factor SigE: role in global gene expression and survival in macrophages. Mol. Microbiol. 41:423-437.[CrossRef][Medline]
19
19. Miller, J. H. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
20
20. Raman, S., R. Hazra, C. C. Dascher, and R. N. Husson. 2004. Transcription regulation by the Mycobacterium tuberculosis alternative sigma factor SigD and its role in virulence. J. Bacteriol. 186:6605-6616.[Abstract/Free Full Text]
21
21. Raman, S., T. Song, X. Puyang, S. Bardarov, W. R. Jacobs, Jr., and R. N. Husson. 2001. The alternative sigma factor SigH regulates major components of oxidative and heat stress responses in Mycobacterium tuberculosis. J. Bacteriol. 183:6119-6125.[Abstract/Free Full Text]
22
22. Rousseau, C., T. D. Sirakova, V. S. Dubey, Y. Bordat, P. E. Kolattukudy, B. Gicquel, and M. Jackson. 2003. Virulence attenuation of two Mas-like polyketide synthase mutants of Mycobacterium tuberculosis. Microbiology 149:1837-1847.[Abstract/Free Full Text]
23
23. Sirakova, T. D., V. S. Dubey, M. H. Cynamon, and P. E. Kolattukudy. 2003. Attenuation of Mycobacterium tuberculosis by disruption of a mas-like gene or a chalcone synthase-like gene, which causes deficiency in dimycocerosyl phthiocerol synthesis. J. Bacteriol. 185:2999-3008.[Abstract/Free Full Text]
24
24. Smith, I. 2003. Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin. Microbiol. Rev. 16:463-496.[Abstract/Free Full Text]
25
25. Sonden, B., D. Kocincova, C. Deshayes, D. Euphrasie, L. Rhayat, F. Laval, C. Frehel, M. Daffe, G. Etienne, and J. M. Reyrat. 2005. Gap, a mycobacterial specific integral membrane protein, is required for glycolipid transport to the cell surface. Mol. Microbiol. 58:426-440.[CrossRef][Medline]
26
26. Song, T., S. L. Dove, K. H. Lee, and R. N. Husson. 2003. RshA, an anti-sigma factor that regulates the activity of the mycobacterial stress response sigma factor SigH. Mol. Microbiol. 50:949-959.[CrossRef][Medline]
27
27. Sun, R., P. J. Converse, C. Ko, S. Tyagi, N. E. Morrison, and W. R. Bishai. 2004. Mycobacterium tuberculosis ECF sigma factor sigC is required for lethality in mice and for the conditional expression of a defined gene set. Mol. Microbiol. 52:25-38.[CrossRef][Medline]
28
28. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98:5116-5121.[Abstract/Free Full Text]
29
29. Wu, S., S. T. Howard, D. L. Lakey, A. Kipnis, B. Samten, H. Safi, V. Gruppo, B. Wizel, H. Shams, R. J. Basaraba, I. M. Orme, and P. F. Barnes. 2004. The principal sigma factor sigA mediates enhanced growth of Mycobacterium tuberculosis in vivo. Mol. Microbiol. 51:1551-1562.[CrossRef][Medline]

---

Infection and Immunity, April 2006, p. 2457-2461, Vol. 74, No. 4
0019-9567/06/$08.00+0     doi:10.1128/IAI.74.4.2457-2461.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

This article has been cited by other articles:

• Fontan, P. A., Voskuil, M. I., Gomez, M., Tan, D., Pardini, M., Manganelli, R., Fattorini, L., Schoolnik, G. K., Smith, I. (2009). The Mycobacterium tuberculosis Sigma Factor {sigma}B Is Required for Full Response to Cell Envelope Stress and Hypoxia In Vitro, but It Is Dispensable for In Vivo Growth. J. Bacteriol. 191: 5628-5633 [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]  
• Gordon, N. D., Ottaviano, G. L., Connell, S. E., Tobkin, G. V., Son, C. H., Shterental, S., Gehring, A. M. (2008). Secreted-Protein Response to {sigma}U Activity in Streptomyces coelicolor. J. Bacteriol. 190: 894-904 [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, E. P., Lee, J.-H., Bishai, W. R., Colantuoni, C., Karakousis, P. C. (2007). Mycobacterium tuberculosis SigF Regulates Genes Encoding Cell Wall-Associated Proteins and Directly Regulates the Transcriptional Regulatory Gene phoY1. J. Bacteriol. 189: 4234-4242 [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]  

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Dainese, E. Articles by Manganelli, R. Search for Related Content PubMed PubMed Citation Articles by Dainese, E. Articles by Manganelli, R.