Comprehensive definition of the SigH regulon of mycobacterium tuberculosis reveals transcriptional control of diverse stress responses

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Sharp, Jared D ^a,d   Singh, Atul K ^a   Park, Sang Tae ^b,e   Lyubetskaya, Anna ^b,f   Peterson, Matthew W ^b   Gomes, Antonio L C ^b,g   Potluri, Lakshmi Prasad ^a   Raman, Sahadevan ^b,h   Galagan, James E ^b,c   Husson, Robert N ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BOSTON UNIVERSITY   (United States)

^c Boston University   (United States)

^d Affinivax   (United States)

^e Macrogen Inc   (South Korea)

^f BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^g Och Spine at New York Presbyterian Hospitals   (United States)

^h BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SIGMA FACTOR; SIGMA FACTOR SIGH; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; SIGH PROTEIN, BACTERIA;

AMINO ACID SEQUENCE; AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; DNA REPAIR; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC REGULATION; HEAT STRESS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; PROMOTER REGION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REGULON; RNA TRANSLATION; TRANSCRIPTION REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; PHYSIOLOGICAL STRESS; PROCEDURES;

BACTERIAL PROTEINS; BINDING SITES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MYCOBACTERIUM TUBERCULOSIS; OPERON; PROMOTER REGIONS, GENETIC; REGULON; SIGMA FACTOR; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 84962167769     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0152145     Document Type: Article

References (38)

1. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS, Eum SY, et al. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun. 2008; 76(6): 2333-40. PMID: 18347040. doi: 10.1128/IAI.01515-07
2. Nathan C, Shiloh MU. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA. 2000; 97(16): 8841-8. PMID: 10922044.
3. Camus JC, Pryor MJ, Medigue C, Cole ST. Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology. 2002; 148(Pt 10): 2967-73. PMID: 12368430.
4. Rodrigue S, Provvedi R, Jacques P-E, Gaudreau L, Manganelli R. The sigma factors of Mycobacterium tuberculosis. FEMS Microbiology Reviews. 2006; 30(6): 926-41. doi: 10.1111/j.1574-6976.2006.00040.x PMID: 17064287.
5. Manganelli R. Sigma factors: Key Molecules in Mycobacterium tuberculosis Physiology and Virulence. Microbiol Spectr. 2014; 2(1). doi: 10.1128/microbiolspec.MGM2-0007-2013
6. Lonetto MA, Brown KL, Rudd KE, Buttner MJ. 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 USA. 1994; 91(16): 7573-7. PMID: 8052622; PubMed Central PMCID: PMC44444.
7. Paget MSB, Helmann JD. The sigma70 family of sigma factors. Genome Biol. 2003; 4(1): 203. PMID: 12540296; PubMed Central PMCID: PMC151288.
8. Helmann JD Anti-sigma factors. Curr Opin Microbiol. 1999; 2(2): 135-41. doi: 10.1016/S1369-5274(99)80024-1 PMID: 10322161.
9. Paget MS, Bae JB, Hahn MY, Li W, Kleanthous C, Roe JH, et al. Mutational analysis of RsrA, a zinc-binding anti-sigma factor with athiol-disulphide redox switch. Mol Microbiol. 2001; 39(4): 1036-47. PMID: 11251822
10. Song T, Dove SL, Lee KH, Husson RN. RshA, an anti-sigma factor that regulates the activity of the mycobacterial stress response sigma factor SigH. Mol Microbiol. 2003; 50(3): 949-59. PMID: 14617153.
11. Raman S, Song T, Puyang X, Bardarov S, Jacobs Jr. W, Husson R. The alternative sigma factor SigH regulates major components of the oxidative and heat stress responses in Mycobacterium tuberculosis. J Bacteriol. 2001; 183(20): 6119-25. PMID: 11567012
12. Manganelli R, Voskuil MI, Schoolnik GK, Dubnau E, Gomez M, Smith I. Role of the extracytoplasmic-function sigma Factor sigmaH in Mycobacterium tuberculosis global gene expression. Mol Microbiol. 2002; 45(2): 365-74. PMID: 12123450
13. Park ST, Kang CM, Husson RN. Regulation of the SigH stress response regulon by an essential protein kinase in Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2008; 105(35): 13105-10. PMID: 18728196. doi: 10.1073/pnas.0801143105
14. Kaushal D, Schroeder BG, Tyagi S, Yoshimatsu T, Scott C, Ko C, et al. Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH. Proc Natl Acad Sci USA. 2002; 99(12): 8330-5. doi: 10.1073/pnas.102055799 PMID: 12060776; PubMed Central PMCID: PMC123067.
15. Mehra S, Golden NA, Stuckey K, Didier PJ, Doyle LA, Russell-Lodrigue KE, et al. The Mycobacterium tuberculosis Stress Response Factor SigH Is Required for Bacterial Burden as Well as Immunopathology in Primate Lungs. J Infect Dis. 2012. doi: 10.1093/infdis/jis102 PMID: 22402035.
16. Dutta NK, Mehra S, Martinez AN, Alvarez X, Renner NA, Morici LA, et al. The stress-response factor SigH modulates the interaction between Mycobacterium tuberculosis and host phagocytes. PLoS ONE. 2012; 7(1): e28958. doi: 10.1371/journal.pone.0028958 PMID: 22235255; PubMed Central PMCID: PMC3250399.
17. Kaushal D, Foreman TW, Gautam US, Alvarez X, Adekambi T, Rangel-Moreno J, et al. Mucosal vaccination with attenuated Mycobacterium tuberculosis induces strong central memory responses and protects against tuberculosis. Nature Communications. 2015; 6: 8533. doi: 10.1038/ncomms9533 PMID: 26460802; PubMed Central PMCID: PMCPMC4608260.
18. Ghosh P, Wu C-w, Talaat AM. Key role forthe alternative sigma factor, SigH, in the intracellular life of Mycobacterium avium subsp. paratuberculosis during macrophage stress. Infect Immun. 2013; 81 (6): 2242-57. doi: 10.1128/IAI.01273-12 PMID: 23569115; PubMed Central PMCID: PMC3676012.
19. Song T, Song SE, Raman S, Anaya M, Husson RN. Critical role of a single position in the-35 element for promoter recognition by Mycobacterium tuberculosis SigE and SigH. J Bacteriol. 2008; 190 (6): 2227-30. PMID: 18192397. doi: 10.1128/JB.01642-07
20. Galagan JE, Minch K, Peterson M, Lyubetskaya A, Azizi E, Sweet L, et al. The Mycobacterium tuberculosis regulatory network and hypoxia. Nature. 2013; 499(7457): 178-83. doi: 10.1038/nature12337 PMID: 23823726; PubMed Central PMCID: PMC4087036.
21. Klotzsche M, Ehrt S, Schnappinger D. Improved tetracycline repressors for gene silencing in mycobacteria. Nucleic Acids Research. 2009; 37(6): 1778-88. doi: 10.1093/nar/gkp015 PMID: 19174563
22. Galagan J, Lyubetskaya A, Gomes A. ChIP-Seq and the Complexity of Bacterial Transcriptional Regulation. Current topics in microbiology and immunology. 2013; 363: 43-68. Epub 2012/09/18. doi: 10.1007/822012257 PMID: 22983621.
23. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie2. Nat Meth. 2012; 9(4): 357-9. doi: 10.1038/nmeth.1923 PMID: 22388286; PubMed Central PMCID: PMC3322381.
24. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25(16): 2078-9. doi: 10.1093/bioinformatics/btp352 PMID: 19505943
25. Gomes ALC, Abeel T, Peterson M, Azizi E, Lyubetskaya A, Carvalho L, et al. Decoding ChIP-seq with a double-binding signal refines binding peaks to single-nucleotides and predicts cooperative interaction. Genome Research. 2014. doi: 10.1101/gr.161711.113 PMID: 25024162.
26. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEMESUITE: tools for motif discovery and searching. Nucleic Acids Research. 2009; 37(Web Server issue): W202-8. doi: 10.1093/nar/gkp335 PMID: 19458158; PubMed Central PMCID: PMC2703892.
27. Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol. 1994; 2: 28-36. PMID: 7584402.
28. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011; 29(1): 24-6. doi: 10.1038/nbt.1754 PMID: 21221095; PubMed Central PMCID: PMC3346182.
29. Arany Z. High-Throughput Quantitative Real-Time PCR in Current Protocols in Human Genetics. Hoboken, NJ, USA: John Wiley & Sons, Inc.; 2001.
30. Stewart GR, Wernisch L, Stabler R, Mangan JA, Hinds J, Laing KG, et al. Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology (Reading, Engl). 2002; 148(Pt 10): 3129-38. PMID: 12368446.
31. Hartkoorn RC, Sala C, Uplekar S, Busso P, Rougemont J, Cole ST. Genome-wide definition of the SigF regulon in Mycobacterium tuberculosis. J Bacteriol. 2012; 194(8): 2001-9. doi: 10.1128/JB.06692-11 PMID: 22307756; PubMed Central PMCID: PMC3318452.
32. Minch KJ, Rustad TR, Peterson EJR, Winkler J, Reiss DJ, Ma S, et al. The DNA-binding network of Mycobacterium tuberculosis. Nature Communications. 2015; 6: 5829. doi: 10.1038/ncomms6829 PMID: 25581030.
33. Kahramanoglou C, Cortes T, Matange N, Hunt DM, Visweswariah SS, Young DB, et al. Genomic mapping of cAMP receptor protein (CRP Mt) in Mycobacterium tuberculosis: relation to transcriptional start sites and the role of CRPMt as a transcription factor. Nucleic Acids Research. 2014; 42(13): 8320-9. doi: 10.1093/nar/gku548 PMID: 24957601; PubMed Central PMCID: PMC4117774.
34. Fitzgerald DM, Bonocora RP, Wade JT. Comprehensive mapping of the Escherichia coli flagellar regulatory network. PLoS Genet. 2014; 10(10): e1004649. doi: 10.1371/journal.pgen.1004649 PMID: 25275371; PubMed Central PMCID: PMC4183435.
35. Paget MS, Molle V, Cohen G, Aharonowitz Y, Buttner MJ. Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the sigmaR regulon. Mol Microbiol. 2001; 42(4): 1007-20. PMID: 11737643
36. Burns KE, Baumgart S, Dorrestein PC, Zhai H, McLafferty FW, Begley TP. Reconstitution of a new cysteine biosynthetic pathway in Mycobacterium tuberculosis. J Am Chem Soc. 2005; 127(33): 11602-3. doi: 10.1021/ja053476x PMID: 16104727; PubMed Central PMCID: PMC2536522.
37. Hsu LM Promoter clearance and escape in prokaryotes. Biochim Biophys Acta. 2002; 1577(2): 191-207. PMID: 12213652.
38. Revyakin A, Liu C, Ebright RH, Strick TR. Abortive initiation and productive initiation by RNA polymerase involve DNA scrunching. Science. 2006; 314(5802): 1139-43. doi: 10.1126/science.1131398 PMID: 17110577; PubMed Central PMCID: PMC2754787.