Tuberculosis and Respiratory Diseases

The Korean Academy of Tuberculosis and Respiratory Diseases (대한결핵및호흡기학회)
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An Overview of Genetic Information of Latent Mycobacterium tuberculosis

  • Hamidieh, Faezeh (Departement of Microbiology, Faculty of Biological Sciences, North Tehran Branch, Islamic Azad University) ;
  • Farnia, Parissa (Mycobacteriology Research (MRC), National Research Institute of Tuberculosis and Lung Disease (NRITLD), Shahid Beheshti University of Medical Sciences) ;
  • Nowroozi, Jamileh (Departement of Microbiology, Faculty of Biological Sciences, North Tehran Branch, Islamic Azad University) ;
  • Farnia, Poopak (Mycobacteriology Research (MRC), National Research Institute of Tuberculosis and Lung Disease (NRITLD), Shahid Beheshti University of Medical Sciences) ;
  • Velayati, Ali Akbar (Mycobacteriology Research (MRC), National Research Institute of Tuberculosis and Lung Disease (NRITLD), Shahid Beheshti University of Medical Sciences)
  • Received : 2020.09.18
  • Accepted : 2020.10.30
  • Published : 2021.01.31
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Abstract

Mycobacterium tuberculosis has infected more than two billion individuals worldwide, of whom 5%-10% have clinically active disease and 90%-95% remain in the latent stage with a reservoir of viable bacteria in the macrophages for extended periods of time. The tubercle bacilli at this stage are usually called dormant, non-viable, and/or non-culturable microorganisms. The patients with latent bacilli will not have clinical pictures and are not infectious. The infections in about 2%-23% of the patients with latent status become reactivated for various reasons such as cancer, human immunodeficiency virus infection, diabetes, and/or aging. Many studies have examined the mechanisms involved in the latent state of Mycobacterium and showed that latency modified the expression of many genes. Therefore, several mechanisms will change in this bacterium. Hence, this study aimed to briefly examine the genes involved in the latent state as well as the changes that are caused by Mycobacterium tuberculosis. The study also evaluated the relationship between the functions of these genes.

Keywords

Acknowledgement

This article is sponsored by Dr. Masih Daneshvari Hospital, Mycobacteriology Research Center (MRC), National Research Institute of Tuberculosis and Lung Disease (NRITLD) and they are thanked.

References

  1. Velayati AA, Farnia P, Masjedi MR. Latent tuberculosis (TB) bacilli: yes or no to preventive chemotherapy. Int J Mycobacteriol 2012;1:1-2. https://doi.org/10.1016/j.ijmyco.2012.01.002
  2. Hibah NA, Hasan HE. Prevalence of latent tuberculosis infection among multinational healthcare workers in Muhayil Saudi Arabia. Egypt J Bronchol 2015;9:183-7. https://doi.org/10.4103/1687-8426.158078
  3. Houben RM, Dodd PJ. The global burden of latent tuberculosis infection: a re-estimation using mathematical modelling. PLoS Med 2016;13:e1002152. https://doi.org/10.1371/journal.pmed.1002152
  4. World Health Organization. Latent TB infection: updated and consolidated guidelines for programmatic management. Geneva: World Health Organization; 2018.
  5. Balkhy HH, El Beltagy K, El-Saed A, Aljasir B, Althaqafi A, Alothman AF, et al. Comparison of QuantiFERON-TB gold in tube test versus tuberculin skin test for screening of latent tuberculosis infection in Saudi Arabia: a population-based study. Ann Thorac Med 2016;11:197-201. https://doi.org/10.4103/1817-1737.185759
  6. Daniel TM. The history of tuberculosis. Respir Med 2006;100:1862-70. https://doi.org/10.1016/j.rmed.2006.08.006
  7. Grosset J. The sterilizing value of rifampicin and pyrazinamide in experimental short-course chemotherapy. Bull Int Union Tuberc 1978;53:5-12.
  8. Wayne LG. Dormancy of Mycobacterium tuberculosis and latency of disease. Eur J Clin Microbiol Infect Dis 1994;13:908-14. https://doi.org/10.1007/BF02111491
  9. Agarwal R. Treatment of latent tuberculous infection in India: is it worth the salt? Lung India 2005;22:105-6.
  10. Huaman MA, Ticona E, Miranda G, Kryscio RJ, Mugruza R, Aranda E, et al. The relationship between latent tuberculosis infection and acute myocardial infarction. Clin Infect Dis 2018;66:886-92. https://doi.org/10.1093/cid/cix910
  11. Velayati AA, Abeel T, Shea T, Konstantinovich Zhavnerko G, Birren B, Cassell GH, et al. Populations of latent Mycobacterium tuberculosis lack a cell wall: Isolation, visualization, and whole-genome characterization. Int J Mycobacteriol 2016;5:66-73. https://doi.org/10.1016/j.ijmyco.2015.12.001
  12. McDermott W. Inapparent infection: relation of latent and dormant infections to microbial persistence. Public Health Rep 1959;74:485-99. https://doi.org/10.2307/4590490
  13. Adeiza MA. Diagnosis of latent tuberculosis infection: the tuberculin skin test and interferon gamma release assays. Ann Niger Med 2011;5:35-7. https://doi.org/10.4103/0331-3131.92946
  14. Zondervan NA, van Dam JC, Schaap PJ, Martins Dos Santos VA, Suarez-Diez M. Regulation of three virulence strategies of Mycobacterium tuberculosis: a success story. Int J Mol Sci 2018;19:347. https://doi.org/10.3390/ijms19020347
  15. Welin A. Survival strategies of Mycobacterium tuberculosis inside the human macrophage. Linkoping: Linkoping University; 2011.
  16. Curcic R, Dhandayuthapani S, Deretic V. Gene expression in mycobacteria: transcriptional fusions based on xylE and analysis of the promoter region of the response regulator mtrA from Mycobacterium tuberculosis. Mol Microbiol 1994;13:1057-64. https://doi.org/10.1111/j.1365-2958.1994.tb00496.x
  17. O'Neill MB, Mortimer TD, Pepperell CS. Diversity of Mycobacterium tuberculosis across Evolutionary Scales. PLoS Pathog 2015;11:e1005257. https://doi.org/10.1371/journal.ppat.1005257
  18. Beste DJ, Laing E, Bonde B, Avignone-Rossa C, Bushell ME, McFadden JJ. Transcriptomic analysis identifies growth rate modulation as a component of the adaptation of mycobacteria to survival inside the macrophage. J Bacteriol 2007;189:3969-76. https://doi.org/10.1128/JB.01787-06
  19. Voskuil MI, Visconti KC, Schoolnik GK. Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 2004;84:218-27. https://doi.org/10.1016/j.tube.2004.02.003
  20. Lancaster CR, Kroger A. Succinate: quinone oxidoreductases: new insights from X-ray crystal structures. Biochim Biophys Acta 2000;1459:422-31. https://doi.org/10.1016/S0005-2728(00)00180-8
  21. Kana BD, Weinstein EA, Avarbock D, Dawes SS, Rubin H, Mizrahi V. Characterization of the cydAB-encoded cytochrome bd oxidase from Mycobacterium smegmatis. J Bacteriol 2001;183:7076-86. https://doi.org/10.1128/JB.183.24.7076-7086.2001
  22. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998;393:537-44. https://doi.org/10.1038/31159
  23. Pham TV, Murkin AS, Moynihan MM, Harris L, Tyler PC, Shetty N, et al. Mechanism-based inactivator of isocitrate lyases 1 and 2 from Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 2017;114:7617-22. https://doi.org/10.1073/pnas.1706134114
  24. Neidhardt FC, Curtiss R. Escherichia coli and Salmonella: cellular and molecular biology. Washington, DC: ASM Press; 1996. p. 1227-31.
  25. Kumar R, Bhakuni V. Mycobacterium tuberculosis isocitrate lyase (MtbIcl): role of divalent cations in modulation of functional and structural properties. Proteins 2008;72:892-900. https://doi.org/10.1002/prot.21984
  26. Smith CV, Huang CC, Miczak A, Russell DG, Sacchettini JC, Honer zu Bentrup K. Biochemical and structural studies of malate synthase from Mycobacterium tuberculosis. J Biol Chem 2003;278:1735-43. https://doi.org/10.1074/jbc.M209248200
  27. Gengenbacher M, Kaufmann SH. Mycobacterium tuberculosis : success through dormancy. FEMS Microbiol Rev 2012;36:514-32. https://doi.org/10.1111/j.1574-6976.2012.00331.x
  28. Ellenbarger JF, Krieger IV, Huang HL, Gomez-Coca S, Ioerger TR, Sacchettini JC, et al. Anion-pi interactions in computer-aided drug design: modeling the inhibition of malate synthase by phenyl-diketo acids. J Chem Inf Model 2018;58:2085-91. https://doi.org/10.1021/acs.jcim.8b00417
  29. Wayne LG, Sohaskey CD. Nonreplicating persistence of mycobacterium tuberculosis. Annu Rev Microbiol 2001;55:139-63. https://doi.org/10.1146/annurev.micro.55.1.139
  30. Huang HL, Krieger IV, Parai MK, Gawandi VB, Sacchettini JC. Mycobacterium tuberculosis malate synthase structures with fragments reveal a portal for substrate/product exchange. J Biol Chem 2016;291:27421-32. https://doi.org/10.1074/jbc.M116.750877
  31. Kelkar DS, Kumar D, Kumar P, Balakrishnan L, Muthusamy B, Yadav AK, et al. Proteogenomic analysis of Mycobacterium tuberculosis by high resolution mass spectrometry. Mol Cell Proteomics 2011;10:M111.011627.
  32. Berney M, Cook GM. Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One 2010;5:e8614. https://doi.org/10.1371/journal.pone.0008614
  33. Parrish NM, Dick JD, Bishai WR. Mechanisms of latency in Mycobacterium tuberculosis. Trends Microbiol 1998;6:107-12. https://doi.org/10.1016/S0966-842X(98)01216-5
  34. Wayne LG, Hayes LG. Nitrate reduction as a marker for hypoxic shiftdown of Mycobacterium tuberculosis. Tuber Lung Dis 1998;79:127-32. https://doi.org/10.1054/tuld.1998.0015
  35. Sohaskey CD, Wayne LG. Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J Bacteriol 2003;185:7247-56. https://doi.org/10.1128/JB.185.24.7247-7256.2003
  36. Sohaskey CD. Nitrate enhances the survival of Mycobacterium tuberculosis during inhibition of respiration. J Bacteriol 2008;190:2981-6. https://doi.org/10.1128/JB.01857-07
  37. Sohaskey CD. Regulation of nitrate reductase activity in Mycobacterium tuberculosis by oxygen and nitric oxide. Microbiology (Reading) 2005;151:3803-10. https://doi.org/10.1099/mic.0.28263-0
  38. Black GF, Thiel BA, Ota MO, Parida SK, Adegbola R, Boom WH, et al. Immunogenicity of novel DosR regulon-encoded candidate antigens of Mycobacterium tuberculosis in three high-burden populations in Africa. Clin Vaccine Immunol 2009;16:1203-12. https://doi.org/10.1128/CVI.00111-09
  39. Hutter B, Dick T. Analysis of the dormancy-inducible narK2 promoter in Mycobacterium bovis BCG. FEMS Microbiol Lett 2000;188:141-6. https://doi.org/10.1111/j.1574-6968.2000.tb09185.x
  40. Sohaskey CD, Modesti L. Differences in nitrate reduction between Mycobacterium tuberculosis and Mycobacterium bovis are due to differential expression of both narGHJI and narK2. FEMS Microbiol Lett 2009;290:129-34. https://doi.org/10.1111/j.1574-6968.2008.01424.x
  41. Honaker RW, Stewart A, Schittone S, Izzo A, Klein MR, Voskuil MI. Mycobacterium bovis BCG vaccine strains lack narK2 and narX induction and exhibit altered phenotypes during dormancy. Infect Immun 2008;76:2587-93. https://doi.org/10.1128/IAI.01235-07
  42. Giffin MM, Raab RW, Morganstern M, Sohaskey CD. Mutational analysis of the respiratory nitrate transporter NarK2 of Mycobacterium tuberculosis. PLoS One 2012;7:e45459. https://doi.org/10.1371/journal.pone.0045459
  43. Kendall SL, Movahedzadeh F, Rison SC, Wernisch L, Parish T, Duncan K, et al. The Mycobacterium tuberculosis dosRS two-component system is induced by multiple stresses. Tuberculosis (Edinb) 2004;84:247-55. https://doi.org/10.1016/j.tube.2003.12.007
  44. Hutter B, Dick T. Up-regulation of narX, encoding a putative 'fused nitrate reductase' in anaerobic dormant Mycobacterium bovis BCG. FEMS Microbiol Lett 1999;178:63-9. https://doi.org/10.1111/j.1574-6968.1999.tb13760.x
  45. Fenhalls G, Stevens L, Moses L, Bezuidenhout J, Betts JC, van Helden P, et al. In situ detection of Mycobacterium tuberculosis transcripts in human lung granulomas reveals differential gene expression in necrotic lesions. Infect Immun 2002;70:6330-8. https://doi.org/10.1128/IAI.70.11.6330-6338.2002
  46. Queiroz A, Riley LW. Bacterial immunostat: Mycobacterium tuberculosis lipids and their role in the host immune response. Rev Soc Bras Med Trop 2017;50:9-18. https://doi.org/10.1590/0037-8682-0230-2016
  47. Bekierkunst A. Acute granulomatous response produced in mice by trehalose-6,6-dimycolate. J Bacteriol 1968;96:958-61. https://doi.org/10.1128/jb.96.4.958-961.1968
  48. Ishikawa E, Ishikawa T, Morita YS, Toyonaga K, Yamada H, Takeuchi O, et al. Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med 2009;206:2879-88. https://doi.org/10.1084/jem.20091750
  49. Rao V, Fujiwara N, Porcelli SA, Glickman MS. Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J Exp Med 2005;201:535-43. https://doi.org/10.1084/jem.20041668
  50. Huang CC, Smith CV, Glickman MS, Jacobs WR Jr, Sacchettini JC. Crystal structures of mycolic acid cyclopropane synthases from Mycobacterium tuberculosis. J Biol Chem 2002;277:11559-69. https://doi.org/10.1074/jbc.M111698200
  51. PupMed. pcaA: cyclopropane mycolic acid synthase (Mycobacterium tuberculosis H37Rv). Bethesda: National Library of Medicine; 2018.
  52. Corrales RM, Molle V, Leiba J, Mourey L, de Chastellier C, Kremer L. Phosphorylation of mycobacterial PcaA inhibits mycolic acid cyclopropanation: consequences for intracellular survival and for phagosome maturation block. J Biol Chem 2012;287:26187-99. https://doi.org/10.1074/jbc.M112.373209
  53. Nishimoto T, Nakano M, Nakada T, Chaen H, Fukuda S, Sugimoto T, et al. Purification and properties of a novel enzyme, trehalose synthase, from Pimelobacter sp. R48. Biosci Biotechnol Biochem 1996;60:640-4. https://doi.org/10.1271/bbb.60.640
  54. Caner S, Nguyen N, Aguda A, Zhang R, Pan YT, Withers SG, et al. The structure of the Mycobacterium smegmatis trehalose synthase reveals an unusual active site configuration and acarbose-binding mode. Glycobiology 2013;23:1075-83. https://doi.org/10.1093/glycob/cwt044
  55. Umesiri FE, Sanki AK, Boucau J, Ronning DR, Sucheck SJ. Recent advances toward the inhibition of mAG and LAM synthesis in Mycobacterium tuberculosis. Med Res Rev 2010;30:290-326. https://doi.org/10.1002/med.20190
  56. Thanna S, Sucheck SJ. Targeting the trehalose utilization pathways of Mycobacterium tuberculosis. Medchemcomm 2016;7:69-85. https://doi.org/10.1039/C5MD00376H
  57. Zahrt TC, Deretic V. Mycobacterium tuberculosis signal transduction system required for persistent infections. Proc Natl Acad Sci U S A 2001;98:12706-11. https://doi.org/10.1073/pnas.221272198
  58. Marszalek M, Planas A, Pellicer T. Two-component systems of Mycobacterium tuberculosis as potential targets for drug development. Afinidad 2014;71:172-8.
  59. Banerjee SK, Kumar M, Alokam R, Sharma AK, Chatterjee A, Kumar R, et al. Targeting multiple response regulators of Mycobacterium tuberculosis augments the host immune response to infection. Sci Rep 2016;6:25851. https://doi.org/10.1038/srep25851
  60. Jordan S, Hutchings MI, Mascher T. Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol Rev 2008;32:107-46. https://doi.org/10.1111/j.1574-6976.2007.00091.x
  61. Zhou P, Long Q, Zhou Y, Wang H, Xie J. Mycobacterium tuberculosis two-component systems and implications in novel vaccines and drugs. Crit Rev Eukaryot Gene Expr 2012;22:37-52. https://doi.org/10.1615/CritRevEukarGeneExpr.v22.i1.30
  62. Tyagi JS, Sharma D. Signal transduction systems of mycobacteria with special reference to M. tuberculosis. Curr Sci 2004;86:93-102.
  63. Wisedchaisri G, Wu M, Sherman DR, Hol WG. Crystal structures of the response regulator DosR from Mycobacterium tuberculosis suggest a helix rearrangement mechanism for phosphorylation activation. J Mol Biol 2008;378:227-42. https://doi.org/10.1016/j.jmb.2008.02.029
  64. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, et al. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 2003;48:833-43. https://doi.org/10.1046/j.1365-2958.2003.03474.x
  65. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystallin. Proc Natl Acad Sci U S A 2001;98:7534-9. https://doi.org/10.1073/pnas.121172498
  66. Magombedze G, Dowdy D, Mulder N. Latent tuberculosis: models, computational efforts and the pathogen's regulatory mechanisms during dormancy. Front Bioeng Biotechnol 2013;1:4. https://doi.org/10.3389/fbioe.2013.00004
  67. Kalscheuer R. Genetics of wax ester and triacylglycerol biosynthesis in bacteria. In: Timmis KN, editor. Handbook of hydrocarbon and lipid microbiology. Berlin: Springer; 2010. p. 527-35.
  68. Kwon KW, Kim WS, Kim H, Han SJ, Hahn MY, Lee JS, et al. Novel vaccine potential of Rv3131, a DosR regulon-encoded putative nitroreductase, against hyper-virulent Mycobacterium tuberculosis strain K. Sci Rep 2017;7:44151. https://doi.org/10.1038/srep44151
  69. Sharma S, Tyagi JS. Mycobacterium tuberculosis DevR/DosR dormancy regulator activation mechanism: dispensability of phosphorylation, cooperativity and essentiality of alpha10 helix. PLoS One 2016;11:e0160723. https://doi.org/10.1371/journal.pone.0160723
  70. Dasgupta N, Kapur V, Singh KK, Das TK, Sachdeva S, Jyothisri K, et al. Characterization of a two-component system, devR-devS, of Mycobacterium tuberculosis. Tuber Lung Dis 2000;80:141-59. https://doi.org/10.1054/tuld.2000.0240
  71. Saini DK, Malhotra V, Dey D, Pant N, Das TK, Tyagi JS. DevR-DevS is a bona fide two-component system of Mycobacterium tuberculosis that is hypoxia-responsive in the absence of the DNA-binding domain of DevR. Microbiology (Reading) 2004;150:865-75. https://doi.org/10.1099/mic.0.26218-0
  72. Perez E, Samper S, Bordas Y, Guilhot C, Gicquel B, Martin C. An essential role for phoP in Mycobacterium tuberculosis virulence. Mol Microbiol 2001;41:179-87. https://doi.org/10.1046/j.1365-2958.2001.02500.x
  73. Hutter B, Dick T. Increased alanine dehydrogenase activity during dormancy in Mycobacterium smegmatis. FEMS Microbiol Lett 1998;167:7-11. https://doi.org/10.1111/j.1574-6968.1998.tb13200.x
  74. Gonzalo-Asensio J, Mostowy S, Harders-Westerveen J, Huygen K, Hernandez-Pando R, Thole J, et al. PhoP: a missing piece in the intricate puzzle of Mycobacterium tuberculosis virulence. PLoS One 2008;3:e3496. https://doi.org/10.1371/journal.pone.0003496
  75. Bretl DJ, He H, Demetriadou C, White MJ, Penoske RM, Salzman NH, et al. MprA and DosR coregulate a Mycobacterium tuberculosis virulence operon encoding Rv1813c and Rv1812c. Infect Immun 2012;80:3018-33. https://doi.org/10.1128/IAI.00520-12
  76. Pang X, Samten B, Cao G, Wang X, Tvinnereim AR, Chen XL, et al. MprAB regulates the espA operon in Mycobacterium tuberculosis and modulates ESX-1 function and host cytokine response. J Bacteriol 2013;195:66-75. https://doi.org/10.1128/JB.01067-12
  77. Sachdeva P, Misra R, Tyagi AK, Singh Y. The sigma factors of Mycobacterium tuberculosis: regulation of the regulators. FEBS J 2010;277:605-26. https://doi.org/10.1111/j.1742-4658.2009.07479.x
  78. He H, Hovey R, Kane J, Singh V, Zahrt TC. MprAB is a stress-responsive two-component system that directly regulates expression of sigma factors SigB and SigE in Mycobacterium tuberculosis. J Bacteriol 2006;188:2134-43. https://doi.org/10.1128/JB.188.6.2134-2143.2006
  79. Agrawal R, Saini DK. Rv1027c-Rv1028c encode functional KdpDE two-component system in Mycobacterium tuberculosis. Biochem Biophys Res Commun 2014;446:1172-8. https://doi.org/10.1016/j.bbrc.2014.03.066
  80. Heermann R, Jung K. K+ supply, osmotic stress and the KdpD/KdpE two-component system. In: Gross R, Beier D, editors. Two-component systems in bacteria. Poole: Caister Academic Press; 2012. p. 181-99.
  81. Haydel SE, Clark-Curtiss JE. Global expression analysis of two-component system regulator genes during Mycobacterium tuberculosis growth in human macrophages. FEMS Microbiol Lett 2004;236:341-7. https://doi.org/10.1111/j.1574-6968.2004.tb09667.x
  82. Folkvardsen DB, Norman A, Andersen AB, Rasmussen EM, Lillebaek T, Jelsbak L. A major Mycobacterium tuberculosis outbreak caused by one specific genotype in a low-incidence country: exploring gene profile virulence explanations. Sci Rep 2018;8:11869. https://doi.org/10.1038/s41598-018-30363-3
  83. Parish T, Smith DA, Kendall S, Casali N, Bancroft GJ, Stoker NG. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect Immun 2003;71:1134-40. https://doi.org/10.1128/IAI.71.3.1134-1140.2003
  84. Bhattacharya M, Biswas A, Das AK. Interaction analysis of TcrX/Y two component system from Mycobacterium tuberculosis. Biochimie 2010;92:263-72. https://doi.org/10.1016/j.biochi.2009.11.009
  85. Haydel SE, Benjamin WH, Jr., Dunlap NE, Clark-Curtiss JE. Expression, autoregulation, and DNA binding properties of the Mycobacterium tuberculosis TrcR response regulator. J Bacteriol 2002;184:2192-203. https://doi.org/10.1128/JB.184.8.2192-2203.2002
  86. Haydel SE, Dunlap NE, Benjamin WH, Jr. In vitro evidence of two-component system phosphorylation between the Mycobacterium tuberculosis TrcR/TrcS proteins. Microb Pathog 1999;26:195-206. https://doi.org/10.1006/mpat.1998.0265
  87. Feklistov A, Sharon BD, Darst SA, Gross CA. Bacterial sigma factors: a historical, structural, and genomic perspective. Annu Rev Microbiol 2014;68:357-76. https://doi.org/10.1146/annurev-micro-092412-155737
  88. Gruber TM, Gross CA. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 2003;57:441-66. https://doi.org/10.1146/annurev.micro.57.030502.090913
  89. Rodrigue S, Provvedi R, Jacques PE, Gaudreau L, Manganelli R. The sigma factors of Mycobacterium tuberculosis. FEMS Microbiol Rev 2006;30:926-41. https://doi.org/10.1111/j.1574-6976.2006.00040.x
  90. Lonetto M, Gribskov M, Gross CA. The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol 1992;174:3843-9. https://doi.org/10.1128/jb.174.12.3843-3849.1992
  91. Beaucher J, Rodrigue S, Jacques PE, Smith I, Brzezinski R, Gaudreau L. Novel Mycobacterium tuberculosis anti-sigma factor antagonists control sigmaF activity by distinct mechanisms. Mol Microbiol 2002;45:1527-40. https://doi.org/10.1046/j.1365-2958.2002.03135.x
  92. Geiman DE, Kaushal D, Ko C, Tyagi S, Manabe YC, Schroeder BG, et al. Attenuation of late-stage disease in mice infected by the Mycobacterium tuberculosis mutant lacking the SigF alternate sigma factor and identification of SigFdependent genes by microarray analysis. Infect Immun 2004;72:1733-45. https://doi.org/10.1128/IAI.72.3.1733-1745.2004
  93. Jeong EH, Son YM, Hah YS, Choi YJ, Lee KH, Song T, et al. RshA mimetic peptides inhibiting the transcription driven by a Mycobacterium tuberculosis sigma factor SigH. Biochem Biophys Res Commun 2006;339:392-8. https://doi.org/10.1016/j.bbrc.2005.11.032
  94. Li L, Fang C, Zhuang N, Wang T, Zhang Y. Structural basis for transcription initiation by bacterial ECF sigma factors. Nat Commun 2019;10:1153. https://doi.org/10.1038/s41467-019-09096-y
  95. Fang C, Li L, Shen L, Shi J, Wang S, Feng Y, et al. Structures and mechanism of transcription initiation by bacterial ECF factors. Nucleic Acids Res 2019;47:7094-104. https://doi.org/10.1093/nar/gkz470
  96. 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 U S A 2002;99:8330-5. https://doi.org/10.1073/pnas.102055799
  97. Graham JE, Clark-Curtiss JE. Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proc Natl Acad Sci U S A 1999;96:11554-9. https://doi.org/10.1073/pnas.96.20.11554
  98. Hernandez Pando R, Aguilar LD, Smith I, Manganelli R. Immunogenicity and protection induced by a Mycobacterium tuberculosis sigE mutant in a BALB/c mouse model of progressive pulmonary tuberculosis. Infect Immun 2010;78:3168-76. https://doi.org/10.1128/IAI.00023-10
  99. Banaiee N, Jacobs WR Jr, Ernst JD. Regulation of Mycobacterium tuberculosis whiB3 in the mouse lung and macrophages. Infect Immun 2006;74:6449-57. https://doi.org/10.1128/IAI.00190-06
  100. Singh A, Crossman DK, Mai D, Guidry L, Voskuil MI, Renfrow MB, et al. Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog 2009;5:e1000545. https://doi.org/10.1371/journal.ppat.1000545