WhiB7, a transcriptional activator that coordinates physiology with intrinsic drug resistance in Mycobacterium tuberculosis

Expert Review of Anti-Infective Therapy

Volumn 10, Issue 9, 2012, Pages 1037-1047

  Burian, Ján ^a   Ramón García, Santiago ^a   Howes, Charles G ^a   Thompson, Charles J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

antibiotic resistance; combinational therapy; Mycobacterium tuberculosis; redox; tuberculosis; WhiB

Indexed keywords

CLARITHROMYCIN; CLINDAMYCIN; ETHAMBUTOL; ISONIAZID; PROTEIN WHIB7; PYRAZINAMIDE; REGULATOR PROTEIN; RIFAMPICIN; SPECTINOMYCIN; STREPTOMYCIN; TETRACYCLINE; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CHEMICAL MODIFICATION; DRUG EFFICACY; DRUG POTENCY; DRUG STRUCTURE; DRUG TARGETING; GENE EXPRESSION; GENE FUNCTION; HIGH THROUGHPUT SCREENING; HUMAN; MICROBIAL MORPHOLOGY; MOLECULAR PATHOLOGY; MULTIDRUG RESISTANCE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REDOX STRESS; REGULON; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TREATMENT DURATION; TUBERCULOSIS; WHIB7 GENE;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MYCOBACTERIUM TUBERCULOSIS; OXIDATION-REDUCTION; REGULON; TRANSCRIPTION FACTORS;

EID: 84868146046     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/eri.12.90     Document Type: Review

References (76)

1. WHO. Global Tuberculosis Control: WHO Report 2011. WHO, Geneva, Switzerland (2011).
2. Nguyen L, Thompson CJ. Foundations of antibiotic resistance in bacterial physiology: the mycobacterial paradigm. Trends Microbiol. 14(7), 304-312 (2006).
3. Cole ST, Brosch R, Parkhill J et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393(6685), 537-544 (1998).
4. Girgis HS, Hottes AK, Tavazoie S. Genetic architecture of intrinsic antibiotic susceptibility. PLoS One 4(5), e5629 (2009).
5. Fajardo A, Martínez-Martín N, Mercadillo M et al. The neglected intrinsic resistome of bacterial pathogens. PLoS ONE 3(2), e1619 (2008).
6. Gallagher LA, Shendure J, Manoil C. Genome-scale identification of resistance functions in Pseudomonas aeruginosa using Tn-seq. MBio 2(1), e00315Ye00310 (2011).
7. Gomez MJ, Neyfakh AA. Genes involved in intrinsic antibiotic resistance of Acinetobacter baylyi. Antimicrob. Agents Chemother. 50(11), 3562-3567 (2006).
8. Nguyen L, Chinnapapagari S, Thompson CJ. FbpA-Dependent biosynthesis of trehalose dimycolate is required for the intrinsic multidrug resistance, cell wall structure, and colonial morphology of Mycobacterium smegmatis. J. Bacteriol. 187(19), 6603-6611 (2005).
9. Philalay JS, Palermo CO, Hauge KA, Rustad TR, Cangelosi GA. Genes required for intrinsic multidrug resistance in Mycobacterium avium. Antimicrob. Agents Chemother. 48(9), 3412-3418 (2004).
10. Goh EB, Yim G, Tsui W, McClure J, Surette MG, Davies J. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc. Natl Acad. Sci. USA 99(26), 17025-17030 (2002).
11. Holmes DJ, Caso JL, Thompson CJ. Autogenous transcriptional activation of a thiostrepton-induced gene in Streptomyces lividans. EMBO J. 12(8), 3183-3191 (1993).
12. Novotna J, Vohradsky J, Berndt P et al. Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol. Microbiol. 48(5), 1289-1303 (2003).
13. Ren H, Liu J. AsnB is involved in natural resistance of Mycobacterium smegmatis to multiple drugs. Antimicrob. Agents Chemother. 50(1), 250-255 (2006).
14. Vohradsky J, Li XM, Dale G et al. Developmental control of stress stimulons in Streptomyces coelicolor revealed by statistical analyses of global gene expression patterns. J. Bacteriol. 182(17), 4979-4986 (2000).
15. VanBogelen RA, Neidhardt FC. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc. Natl Acad. Sci. USA 87(15), 5589-5593 (1990).
16. Bizzini A, Zhao C, Auffray Y, Hartke A. The Enterococcus faecalis superoxide dismutase is essential for its tolerance to vancomycin and penicillin. J. Antimicrob. Chemother. 64(6), 1196-1202 (2009).
17. Feld L, Knudsen GM, Gram L. Bactericidal antibiotics do not appear to cause oxidative stress in Listeria monocytogenes. Appl. Environ. Microbiol. 78(12), 4353-4357 (2012).
18. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130(5), 797-810 (2007).
19. Shatalin K, Shatalina E, Mironov A, Nudler E. H2S: a universal defense against antibiotics in bacteria. Science 334(6058), 986-990 (2011).
20. Chater KF. A morphological and genetic mapping study of white colony mutants of Streptomyces coelicolor. J. Gen. Microbiol. 72(1), 9-28 (1972).
21. Hopwood DA, Wildermuth H, Palmer HM. Mutants of Streptomyces coelicolor defective in sporulation. J. Gen. Microbiol. 61(3), 397-408 (1970).
22. Davis NK, Chater KF. The Streptomyces coelicolor whiB gene encodes a small transcription factor-like protein dispensable for growth but essential for sporulation. Mol. Gen. Genet. 232(3), 351-358 (1992).
23. Soliveri J, Vijgenboom E, Granozzi C, Plaskitt KA, Chater KF. Functional and evolutionary implications of a survey of various actinomycetes for homologues of two Streptomyces coelicolor sporulation genes. J. Gen. Microbiol. 139(11), 2569-2578 (1993).
24. Soliveri JA, Gomez J, Bishai WR, Chater KF. Multiple paralogous genes related to the Streptomyces coelicolor developmental regulatory gene whiB are present in Streptomyces and other actinomycetes. Microbiology (Reading, Engl.) 146 (Pt 2), 333-343 (2000).
25. Smith LJ, Stapleton MR, Fullstone GJ et al. Mycobacterium tuberculosis WhiB1 is an essential DNA-binding protein with a nitric oxide-sensitive iron-sulfur cluster. Biochem. J. 432(3), 417-427 (2010).
26. Stapleton MR, Smith LJ, Hunt DM, Buxton RS, Green J. Mycobacterium tuberculosis WhiB1 represses transcription of the essential chaperonin GroEL2. Tuberculosis (Edinb.) 92(4), 328-332 (2012).
27. Agarwal N, Lamichhane G, Gupta R, Nolan S, Bishai WR. Cyclic AMP intoxication of macrophages by a Mycobacterium tuberculosis adenylate cyclase. Nature 460(7251), 98-102 (2009).
28. Rickman L, Scott C, Hunt DM et al. A member of the cAMP receptor protein family of transcription regulators in Mycobacterium tuberculosis is required for virulence in mice and controls transcription of the rpfA gene coding for a resuscitation promoting factor. Mol. Microbiol. 56(5), 1274-1286 (2005).
29. Stapleton M, Haq I, Hunt DM et al. Mycobacterium tuberculosis cAMP receptor protein (Rv3676) differs from the Escherichia coli paradigm in its cAMP binding and DNA binding properties and transcription activation properties. J. Biol. Chem. 285(10), 7016-7027 (2010).
30. Mukamolova GV, Turapov OA, Young DI, Kaprelyants AS, Kell DB, Young M. A family of autocrine growth factors in Mycobacterium tuberculosis. Mol. Microbiol. 46(3), 623-635 (2002).
31. Gomez JE, Bishai WR. whmD is an essential mycobacterial gene required for proper septation and cell division. Proc. Natl Acad. Sci. U.S.A. 97(15), 8554-8559 (2000).
32. Raghunand TR, Bishai WR. Mapping essential domains of Mycobacterium smegmatis WhmD: insights into WhiB structure and function. J. Bacteriol. 188(19), 6966-6976 (2006).
33. Rybniker J, Nowag A, van Gumpel E et al. Insights into the function of the WhiB-like protein of mycobacteriophage TM4 Y a transcriptional inhibitor of WhiB2. Mol. Microbiol. 77(3), 642-657 (2010).
34. Geiman DE, Raghunand TR, Agarwal N, Bishai WR. Differential gene expression in response to exposure to antimycobacterial agents and other stress conditions among seven Mycobacterium tuberculosis whiB-like genes. Antimicrob. Agents Chemother. 50(8), 2836-2841 (2006).
35. Steyn AJ, Collins DM, Hondalus MK, Jacobs WR Jr, Kawakami RP, Bloom BR. Mycobacterium tuberculosis WhiB3 interacts with RpoV to affect host survival but is dispensable for in vivo growth. Proc. Natl Acad. Sci. USA 99(5), 3147-3152 (2002).
36. Singh A, Crossman DK, Mai D et al. Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog. 5(8), e1000545 (2009).
37. Singh A, Guidry L, Narasimhulu KV et al. Mycobacterium tuberculosis WhiB3 responds to O2 and nitric oxide via its [4Fe-4S] cluster and is essential for nutrient starvation survival. Proc. Natl Acad. Sci. USA 104(28), 11562-11567 (2007).
38. Guo M, Feng H, Zhang J et al. Dissecting transcription regulatory pathways through a new bacterial one-hybrid reporter system. Genome Res. 19(7), 1301-1308 (2009).
39. Hümpel A, Gebhard S, Cook GM, Berney M. The SigF regulon in Mycobacterium smegmatis reveals roles in adaptation to stationary phase, heat, and oxidative stress. J. Bacteriol. 192(10), 2491-2502 (2010).
40. Casonato S, Cervantes Sánchez A, Haruki H et al. WhiB5: a transcriptional regulator contributing to Mycobacterium tuberculosis virulence and reactivation. Infect. Immun. 80(9), 3132-3144(2012).
41. Das C, Ghosh TS, Mande SS. Computational analysis of the ESX-1 region of Mycobacterium tuberculosis: insights into the mechanism of type VII secretion system. PLoS One 6(11), e27980 (2011).
42. Homolka S, Niemann S, Russell DG, Rohde KH. Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog. 6(7), e1000988 (2010).
43. Morris RP, Nguyen L, Gatfield J et al. Ancestral antibiotic resistance in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 102(34), 12200-12205 (2005).
44. Boshoff HI, Myers TG, Copp BR, McNeil MR, Wilson MA, Barry CE 3rd. The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J. Biol. Chem. 279(38), 40174-40184 (2004).
45. Burian J, Ramón-García S, Sweet G, Gómez-Velasco A, Av-Gay Y, Thompson CJ. The mycobacterial transcriptional regulator whiB7 gene links redox homeostasis and intrinsic antibiotic resistance. J. Biol. Chem. 287(1), 299-310 (2012).
46. Ramón-García S, Mick V, Dainese E et al. Functional and genetic characterization of the tap efflux pump in Mycobacterium bovis BCG. Antimicrob. Agents Chemother. 56(4), 2074-2083 (2012).
47. Smulski DR, Huang LL, McCluskey MP et al. Combined, functional genomicbiochemical approach to intermediary metabolism: interaction of acivicin, a glutamine amidotransferase inhibitor, with Escherichia coli K-12. J. Bacteriol. 183(11), 3353-3364 (2001).
48. Imlay JA. Pathways of oxidative damage. Annu. Rev. Microbiol. 57, 395-418 (2003).
49. Rawat M, Newton GL, Ko M, Martinez GJ, Fahey RC, Av-Gay Y. Mycothioldeficient Mycobacterium smegmatis mutants are hypersensitive to alkylating agents, free radicals, and antibiotics. Antimicrob. Agents Chemother. 46(11), 3348-3355 (2002).
50. Boshoff HI, Xu X, Tahlan K et al. Biosynthesis and recycling of nicotinamide cofactors in Mycobacterium tuberculosis. An essential role for NAD in nonreplicating bacilli. J. Biol. Chem. 283(28), 19329-19341 (2008).
51. Venketaraman V, Dayaram YK, Talaue MT, Connell ND. Glutathione and nitrosoglutathione in macrophage defense against Mycobacterium tuberculosis. Infect. Immun. 73(3), 1886-1889 (2005).
52. Murphy MP. How mitochondria produce reactive oxygen species. Biochem. J. 417(1), 1-13 (2009).
53. Votyakova TV, Reynolds IJ. Detection of hydrogen peroxide with Amplex Red: interference by NADH and reduced glutathione auto-oxidation. Arch. Biochem. Biophys. 431(1), 138-144 (2004).
54. Kelkar DS, Kumar D, Kumar P et al. Proteogenomic analysis of Mycobacterium tuberculosis by high resolution mass spectrometry. Mol. Cell Proteomics 10(12), M111.011627 (2011).
55. Wei J, Dahl JL, Moulder JW et al. Identification of a Mycobacterium tuberculosis gene that enhances mycobacterial survival in macrophages. J. Bacteriol. 182(2), 377-384 (2000).
56. Kim KH, An DR, Song J et al. Mycobacterium tuberculosis Eis protein initiates suppression of host immune responses by acetylation of DUSP16/MKP-7. Proc. Natl Acad. Sci. USA 109(20), 7729-7734 (2012).
57. Chen W, Biswas T, Porter VR, Tsodikov OV, Garneau-Tsodikova S. Unusual regioversatility of acetyltransferase Eis, a cause of drug resistance in XDR-TB. Proc. Natl Acad. Sci. USA 108(24), 9804-9808 (2011).
58. Zaunbrecher MA, Sikes RD Jr, Metchock B, Shinnick TM, Posey JE. Overexpression of the chromosomally encoded aminoglycoside acetyltransferase eis confers kanamycin resistance in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 106(47), 20004-20009 (2009).
59. Wu S, Barnes PF, Samten B et al. Activation of the eis gene in a W-Beijing strain of Mycobacterium tuberculosis correlates with increased SigA levels and enhanced intracellular growth. Microbiology (Reading, Engl.) 155(Pt 4), 1272-1281 (2009).
60. Aínsa JA, Blokpoel MC, Otal I, Young DB, De Smet KA, Martín C. Molecular cloning and characterization of Tap, a putative multidrug efflux pump present in Mycobacterium fortuitum and Mycobacterium tuberculosis. J. Bacteriol. 180(22), 5836-5843 (1998).
61. Ramón-García S, Martín C, Aínsa JA, De Rossi E. Characterization of tetracycline resistance mediated by the efflux pump Tap from Mycobacterium fortuitum. J. Antimicrob. Chemother. 57(2), 252-259 (2006).
62. da Silva PE, Von Groll A, Martin A, Palomino JC. Efflux as a mechanism for drug resistance in Mycobacterium tuberculosis. FEMS Immunol. Med. Microbiol. 63(1), 1-9 (2011).
63. Nishino K, Nikaido E, Yamaguchi A. Regulation and physiological function of multidrug efflux pumps in Escherichia coli and Salmonella. Biochim. Biophys. Acta 1794(5), 834-843 (2009).
64. Louw GE, Warren RM, Gey van Pittius NC et al. Rifampicin reduces susceptibility to ofloxacin in rifampicin-resistant Mycobacterium tuberculosis through efflux. Am. J. Respir. Crit. Care Med. 184(2), 269-276 (2011).
65. Buriánková K, Doucet-Populaire F, Dorson O et al. Molecular basis of intrinsic macrolide resistance in the Mycobacterium tuberculosis complex. Antimicrob. Agent. Chemother. 48(1), 143-150 (2004).
66. Nash KA. Intrinsic macrolide resistance in Mycobacterium smegmatis is conferred by a novel erm gene, erm(38). Antimicrob. Agents Chemother. 47(10), 3053-3060 (2003).
67. Alam MS, Garg SK, Agrawal P. Studies on structural and functional divergence among seven WhiB proteins of Mycobacterium tuberculosis H37Rv. FEBS J. 276(1), 76-93 (2009).
68. Reeves R, Nissen MS. The A.T-DNAbinding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure. J. Biol. Chem. 265(15), 8573-8582 (1990).
69. Johnson DC, Dean DR, Smith AD, Johnson MK. Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 74, 247-281 (2005).
70. Cleynen I, Van de Ven WJ. The HMGA proteins: a myriad of functions (Review). Int. J. Oncol. 32(2), 289-305 (2008).
71. Dove SL, Darst SA, Hochschild A. Region 4 of sigma as a target for transcription regulation. Mol. Microbiol. 48(4), 863-874 (2003).
72. Collins DM, Kawakami RP, de Lisle GW, Pascopella L, Bloom BR, Jacobs WR Jr. Mutation of the principal sigma factor causes loss of virulence in a strain of the Mycobacterium tuberculosis complex. Proc. Natl Acad. Sci. USA 92(17), 8036-8040 (1995).
73. Garg S, Alam MS, Bajpai R, Kishan KR, Agrawal P. Redox biology of Mycobacterium tuberculosis H37Rv: protein-protein interaction between GlgB and WhiB1 involves exchange of thiol-disulfide. BMC Biochem. 10, 1 (2009).
74. Ramón-García S, Ng C, Anderson H et al. Synergistic drug combinations for tuberculosis therapy identified by a novel high-throughput screen. Antimicrob. Agents Chemother. 55(8), 3861-3869 (2011).
75. Nguyen D, Joshi-Datar A, Lepine F et al. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334(6058), 982-986 (2011).
76. Larkin MA, Blackshields G, Brown NP et al. Clustal W and Clustal X version 2.0. Bioinformatics 23(21), 2947-2948 (2007).