Impact of isoniazid resistance on virulence of global and south Indian clinical isolates of Mycobacterium tuberculosis

Tuberculosis

Volumn 94, Issue 6, 2014, Pages 557-563

  Ameeruddin, Nusrath Unissa ^a   Luke Elizabeth, Hanna ^a  

^a NATIONAL INSTITUTE FOR RESEARCH IN TUBERCULOSIS   (India)

Author keywords

Indian isolates; INHresistance; KatG; S315T mutant; South; Virulence

Indexed keywords

AHPC PROTEIN; CATALASE; ISONIAZID; KATG PROTEIN; PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; KATG PROTEIN, MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSTATIC AGENT;

ANTIBIOTIC RESISTANCE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CHRONIC GRANULOMATOUS DISEASE; DISEASE ASSOCIATION; ENZYME ACTIVITY; GENE MUTATION; HUMAN; INDIAN; META ANALYSIS (TOPIC); MOLECULAR BIOLOGY; MONOCYTE; MULTIDRUG RESISTANCE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPIC VARIATION; POINT MUTATION; POPULATION GENETICS; RESPIRATORY BURST; REVIEW; SEQUENCE ANALYSIS; SYSTEMATIC REVIEW (TOPIC); TREATMENT OUTCOME; DRUG EFFECTS; GENETICS; INDIA; MICROBIOLOGY; MULTIDRUG RESISTANT TUBERCULOSIS; MUTATION; PATHOGENICITY; VIRULENCE;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; CATALASE; DRUG RESISTANCE, BACTERIAL; HUMANS; INDIA; ISONIAZID; MUTATION; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS, MULTIDRUG-RESISTANT; VIRULENCE;

EID: 84919467167     PISSN: 14729792     EISSN: 1873281X     Source Type: Journal    
DOI: 10.1016/j.tube.2014.08.011     Document Type: Review

References (81)

1. J.B. Nachega, and R.E. Chaisson Tuberculosis drug resistance: a global threat Clin Infect Dis 36 2003 24 30
2. World Health Organization International Union against tuberculosis and lung disease. Global project on anti- tuberculosis drug resistance surveillance. 2002-2007 Fourth Global Report 2008 WHO Geneva, Switzerland [WHO/HTM/TB/2008.394]
3. C.N. Paramasivan, K. Bhaskaran, Venkataraman, V. Chandrasekhran, and P.R. Narayanan Surveillance of drug resistance in tuberculosis in the state of Tamil Nadu Ind J Tuberc 47 2000 27 33
4. C.N. Paramasivan, P. Venkataraman, V. Chandrasekaran, S. Bhat, and P.R. Narayanan Surveillance of drug resistance tuberculosis in two districts of south India Int J Tuberc Lung Dis 6 2002 479 484
5. A. Cattamanchi, R.B. Dantes, J.Z. Metcalfe, L.G. Jarlsberg, J. Grinsdale, and L. Kawamura Clinical characteristics and treatment outcomes of patients with isoniazid-monoresistant tuberculosis Clin Infect Dis 8 2004 179 185
6. D. Menzies, A. Benedetti, A. Paydar, S. Royce, P. Madhukar, W. Burman, A. Vernon, and C. Lienhard Standardized treatment of active tuberculosis in patients with previous treatment and/or with mono-resistance to isoniazid: a systematic review and meta-analysis PLos Med 6 2009 1 15
7. D. Deepa, S. Achanta, J. Jaju, K. Rao, R. Samyukta, M. Claassens, M.V. Ajay Kumar, and P.H. Vishnu The impact of isoniazid resistance on the treatment outcomes of smear positive re-treatment tuberculosis patients in the state of Andhra Pradesh, India PLoS One 8 2013 10
8. H.E. Jenkins, M. Zignol, and T. Cohen Quantifying the burden and trends of isoniazid resistant tuberculosis, 1994-2009 PLoS One 6 2011 e22927
9. K.R. Jacobson, D. Theron, T.C. Victor, E.M. Streicher, R.M. Warren, and M.B. Murray Treatment outcomes of isoniazid-resistant tuberculosis patients, Western Cape Province, South Africa Clin Infect Dis 53 2011 369 372
10. World Health Organization Guidelines for intensified tuberculosis case-finding and isoniazid preventive therapy for people living with HIV in resource constrained settings 2011 World Health Organization Geneva http://www.who.int/hiv/pub/tb/9789241500708/en/ [accessed 10.10.2013]
11. G. Middlebrook Isoniazid-resistance and catalase activity of tubercle bacilli; a preliminary report Am Rev Tuberc 69 1954 471 472
12. G. Middlebrook, and M.L. Cohn Some observations on the pathogenicity of isoniazid-resistant variants of tubercle bacilli Science 118 1953 297 299
13. F.G. Winder, P. Brennan, and C. Ratledge Synthesis of fatty acids by extracts of mycobacteria and the absence of inhibition by isoniazid Biochem J 93 1964 635 640
14. Y. Zhang, B. Heym, B. Allen, D. Young, and S.T. Cole The catalase-peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis Nature 358 1992 591 593
15. A. Banerjee, E. Dubnau, A. Quemard, V. Balasubramanian, K.S. Um, T. Wilson, D. Collins, G. de Lisle, and W.R. Jacobs Jr. inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis Science 263 1994 227 230
16. K.R. Mdluli, A. Slayden, Y. Zhu, S. Ramaswamy, X. Pan, D. Mead, D.D. Crane, J.M. Musser, and C.E. Barry III Inhibition of a Mycobacterium tuberculosis beta-ketoacyl ACP synthase by isoniazid Science 280 1998 1607 1610
17. S. Sreevatsan, X. Pan, Y. Zhang, V. Deretic, and J.M. Musser Analysis of the oxyR-ahpC region in isoniazid-resistant and -susceptible Mycobacterium tuberculosis complex organisms recovered from diseased humans and animals in diverse localities Antimicrobial Agents Chemother 41 1997 600 606
18. V. Jarlier, and H. Nikaido Permeability barrier to hydrophilic solutes in Mycobacterium chelonei J Bacteriol 172 1990 1418 1423
19. M. Bartos, J.O. Falkinham, and I. Pavlik Mycobacterial catalases, peroxidases, and superoxide dismutases and their effects on virulence and isoniazid-susceptibility in mycobacteria - a review Vet Med 49 2004 161 170
20. C. Manca, S. Paul, C.E.I. Barry, V.H. Freedman, and G. Kaplan Mycobacterium tuberculosis catalase and peroxidase activities and resistance to oxidative killing in human monocytes in vitro Infect Immun 67 1999 74 79
21. J. Chan, Y. Xing, R.S. Magliozzo, and B.R. Bloom Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages J Exp Med 175 1992 1111 1122
22. 2 killing in human monocytes in vitro Infect Immun 65 1997 4850 4857
23. P.C. Loewen, M.G. Klotz, and D.J. Hassett An old enzyme that continues to surprise us ASM News 66 2000 76 82
24. V.H. Ng, J.S. Cox, A.O. Sousa, J.D. MacMicking, and J.D. McKinney Role of KatG catalase-peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst Mol Microbiol 52 2004 1291 1302
25. N.L. Wengenack, M.P. Jensen, F. Rusnak, and M.K. Stern Mycobacterium tuberculosis KatG is a peroxynitritase Biochem Biophys Res Commun 256 1999 485 487
26. B.H. Segal, T.L. Leto, J.I. Gallin, H.L. Malech, and S.M. Holland Genetic, biochemical, and clinical features of chronic granulomatous disease Medicine 9 2000 170 200
27. J.L. Casanova, and L. Abel Genetic dissection of immunity to mycobacteria: the human model Annu Rev Immunol 20 2002 581 620
28. P.J. Cardona, S. Gordillo, I. Amat, J. Diaz, J. Lonca, C. Vilaplana, A. Pallares, R. Llatjos, A. Ariza, and V. Ausina Catalase-peroxidase activity has no influence on virulence in a murine model of tuberculosis Tuberc Edinb 83 2003 351 359
29. D.J. Ordway, M.G. Sonnenberg, S.A. Donahue, J.T. Belisle, and I.M. Orme Drug-resistant strains of Mycobacterium tuberculosis exhibit a range of virulence for mice Infect Immun 63 1995 741 743
30. W.C. Morse, O.L. Weiser, D.M. Kuhns, M. Fusillo, M.C. Dail, and J.R. Evans Study of the virulence of isoniazid-resistant tubercle bacilli in guinea pigs and mice Am Rev Tuberc 69 1954 464 468
31. D.A. Mitchison, J.B. Selkon, and J. Lloyd Virulence in the Guinea-Pig, susceptibility to hydrogen peroxide, and catalase activity of isoniazid-sensitive tubercle bacilli from south Indian and British patients J Pathol Bacteriol 86 1963 377 386
32. Z. Li, C. Kelley, F. Collins, and D. Rouse Expression of katG in Mycobacterium tuberculosis is associated with its growth and persistence in mice and guinea pigs J Infect Dis 177 1998 1030 1035
33. A.S. Pym, P. Domenech, N. Honore, J. Song, V. Deretic, and S.T. Cole Regulation of catalase-peroxidase (KatG) expression, isoniazid sensitivity and virulence by furA of Mycobacterium tuberculosis Mol Microbiol 40 2001 879 889
34. T.M. Wilson, G.W. de Lisle, and D.M. Collins Effect of inhA and katG on isoniazid resistance and virulence of Mycobacterium bovis Mol Microbiol 15 1995 1009 1015
35. P.S. Jackett, V.R. Aber, and D.B. Lowrie Virulence and resistance to superoxide, low pH and hydrogen peroxide among strains of Mycobacterium tuberculosis J Gen Microbiol 104 1978 37 45
36. S. O'Brien, P.S. Jackett, D.B. Lowrie, and P.W. Andrew Guinea-pig alveolar macrophages kill Mycobacterium tuberculosis in vitro, but killing is independent of susceptibility to hydrogen peroxide or triggering of the respiratory burst Microb Pathog 10 1991 199 207
37. D.R. Sherman, K. Mdluli, M.J. Hickey, T.M. Arain, S.L. Morris, C.E. Barry III, and C.K. Stover Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis Science 272 1996 1641 1643
38. A. Nusrath Unissa, N. Selvakumar, Narayanan Sujatha, and P.R. Narayanan Molecular analysis of isoniazid-resistant clinical isolates of Mycobacterium tuberculosis from India Int J Antimicro agents 31 2008 71 75
39. Y. Zhang, S. Dhandayuthapani, and V. Deretic Molecular basis for the exquisite sensitivity of Mycobacterium tuberculosis to isoniazid Proc Natl Acad Sci U S A 93 1996 13212 13216
40. T.M. Wilson, and D.M. Collins ahpC, a gene involved in isoniazid resistance of the Mycobacterium tuberculosis complex Mol Microbiol 19 1996 1025 1034
41. S. Ramaswamy, and J.M. Musser Molecular genetic basis of antimicrobial agent resistance in Mycobacterium tuberculosis: 1998 update Tuber Lung Dis 79 1998 3 29
42. A.S. Pym, B. Saint-Joanis, and S.T. Cole Effect of katG mutations on the virulence of Mycobacterium tuberculosis and the implication for transmission in humans Infect Immun 70 2002 4955 4960
43. S. Borrell, and S. Gagneux Infectiousness, reproductive fitness, and evolution of drug-resistant Mycobactyerium tuberculosis Int J Tuberc Lung Dis 13 2009 1456 1466
44. T. Cohen, B. Sommers, and M. Murray The effect of drug resistance on the fitness of Mycobacterium tuberculosis Lancet Infect Dis 3 2003 13 21
45. D.A. Mitchison Tubercle bacilli resistant to isoniazid: virulence and response to treatment with isoniazid in guinea pigs BMJ 1954 128 130
46. C. Dye, and M.A. Espinal Will tuberculosis become resistant to all antibiotics? Proc Biol Sci 268 2001 45 52
47. T. Cohen, and M. Murray Modeling epidemics of multidrug-resistant Mycobacterium tuberculosis of heterogeneous fitness Nat Med 10 2004 1117 1121
48. D.I. Andersson, and B.R. Levin The biological cost of antibiotic resistance Curr Opin Microbiol 2 1999 489 493
49. M.H. Hazbon, M. Brimacombe, M. Bobadilla del Valle, M. Cavatore, M.I. Guerrero, M. Varma-Basil, H. Billman-Jacobe, C. Lavender, J. Fyfe, L. García-García, C.I. Leon, M. Bose, F. Chaves, M. Murray, K.D. Eisenach, J. Sifuentes-Osornio, M.D. Cave, A. Ponce de Leon, and D. Alland Population genetics study of isoniazid resistance mutations and evolution of multidrug-resistant Mycobacterium tuberculosis Antimicrobial Agents Chemother 50 2006 2640 2649
50. H. Zhang, D. Li, L. Zhao, J. Fleming, N. Lin, T. Wang, Z. Liu, C. Li, N. Galwey, J. Deng, Y. Zhou, Y. Zhu, Y. Gao, T. Wang, S. Wang, Y. Huang, M. Wang, Q. Zhong, L. Zhou, T. Chen, J. Zhou, R. Yang, G. Zhu, H. Hang, J. Zhang, F. Li, K. Wan, J. Wang, X.E. Zhang, and L. Bi Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance Nat Genet 45 2013 1255 1260
51. M.R. Farhat, B.J. Shapiro, K.J. Kieser, R. Sultana, K.R. Jacobson, T.C. Victor, R.M. Warren, E.M. Streicher, A. Calver, and A. Sloutsky Genomic analysis identifies targets of convergent positive selection in drug-resistant Mycobacterium tuberculosis Nat Genet 45 2013 1183 1189
52. H. Safi, S. Lingaraju, A. Amin, S. Kim, M. Jones, M. Holmes, M. McNeil, S.N. Peterson, D. Chatterjee, R. Fleischmann, and D. Alland Evolution of high-level ethambutol-resistant tuberculosis through interacting mutations in decaprenylphosphoryl-β-D-arabinose biosynthetic and utilization pathway genes Nat Genet 45 2013 1190 1197
53. D.F. Warne, and V. Mizrahi Complex genetics of drug resistance in Mycobacterium tuberculosis Nat Genet 45 2013 1107 1108
54. N. Casali, V. Nikolayevskyy, Y. Balabanova, S.R. Harris, O. Ignatyeva, I. Kontsevaya, J. Corander, J. Bryant, J. Parkhill, S. Nejentsev, R.D. Horstmann, T. Brown, and F. Drobniewski Evolution and transmission of drug-resistant tuberculosis in a Russian population Nat Genet 46 2014 279 286
55. S. Gagneux, M.V. Burgos, and K. DeRiemer Impact of bacterial genetics on the transmission of isoniazid-resistant Mycobacterium tuberculosis PLoS Pathog 2 2006 e61
56. D. van Soolingen, P.E. de Haas, H.R. van Doorn, E. Kuijper, H. Rinder, and M.W. Borgdorff Mutations at amino acid position 315 of the katG gene are associated with high-level resistance to isoniazid, other drug resistance, and successful transmission of Mycobacterium tuberculosis in the Netherlands J Infect Dis 182 2000 1788 1790
57. D. van Soolingen, M.W. Borgdorff, P.E. Haas de, M.M. Sebek, J. Veen, M. Dessens, K. Kremer, and J.D. van Embden Molecular epidemiology of tuberculosis in the Netherlands: a nationwide study from 1993 through 1997 J Infect Dis 180 1999 726 736
58. H.J. Marttila, H. Soini, E. Eerola, E. Vyshnevskaya, B.I. Vyshnevskiy, T.F. Otten, A.V. Vasilyef, and M.K. Viljanen A Ser315Thr substitution in KatG is predominant in genetically heterogeneous multidrug-resistant Mycobacterium tuberculosis isolates originating from the St. Petersburg area in Russia Antimicrobial Agents Chemother 42 1998 2443 2445
59. A. Nusrath Unissa, Narayanan Sujatha, C. Suganthi, and N. Selvakumar Detection of isoniazid-resistant clinical isolates of Mycobacterium tuberculosis from India using Ser315Thr marker by comparison of molecular methods Int J Clin Med Microbiol 1 2011 52 59
60. T. Cohen, M.C. Becerra, and M.B. Murray Isoniazid resistance and the future of drug-resistant tuberculosis Microb Drug Resist 10 2004 280 285
61. Y. Hu, S. Hoffner, W. Jiang, W. Wang, and B. Xu Extensive transmission of isoniazid resistant M. tuberculosis and its association with increased multidrug-resistant TB in two rural counties of Eastern China: a molecular epidemiological study BMC Infect Dis 10 2010 43
62. I. Parwati, R. van Crevel, and D. van Soolingen Possible underlying mechanisms for successful emergence of the Mycobacterium tuberculosis Beijing genotype strains Lancet Infect Dis 10 2010 103 111
63. D.A. Mitchison, J.G. Wallace, A.L. Bhatia, J.B. Selkon, Subbaiah, and M.C. Lancaster A comparison of the virulence in guinea pigs of south India and British tubercule bacilli Tubercle 41 1960 1 22
64. A.L. Bhatia, A. csillag, D.A. Mitchison, J.B. Selkon, P.R. Somasundaram, and T.V. Subbaiah The virulence in the guinea-pig of tubercle bacilli isolated before treatment from south Indian patients with pulmonary tuberculosis. 2. Comparison with virulence of tubercle bacilli from British patients Bull World Health Organ 25 1961 313 322
65. T.V. Subbaiah, D.A. Mitchison, and J.B. Selkon The susceptibility of hydrogen peroxide of Indian and British isoniazid-sensitive and isoniazid-resistant tubercle bacilli Tubercle 41 1960 323 333
66. J.B. Selkon, T.V. Subbaiah, A.L. Bhatia, S. Radhakrishna, and D.A. Mitchison A comparison of the sensitivity to p-aminosalicylic acid of tubercle bacilli from south Indian and British patients Bull World Health Organ 23 1960 599 611
67. P. Venkatraman, C.N. Paramasivan, K. Ilampuranam, and R. Prabhakar Intraspecies differentiation of strains of M. tuberculosis obtained from Czechoslovakian, Mongolian and south Indian patients Indian J Med Res 88 1988 211
68. K. Sarita, K. Sujata, R.M. Powar, B. Mangala, V.L. Jahagirdar, and A.M. Saoji Subdivision of M. tuberculosis isolated from pulmonary tuberculosis cases in and around Solapur (south India) into five variants Ind J Tub 38 1991 213 216
69. S. Narayanan, S. Gagneux, L. Hari, A.G. Tsolaki, S. Rajasekhar, P.R. Narayanan, P.M. Small, S. Holmes, and K. Deriemer Genomic interrogation of ancestral Mycobacterium tuberculosis from south India Infect Genet Evol 8 2008 474 483
70. A. Nusrath Unissa, Narayanan Sujatha, and N. Selvakumar Virulence in isoniazid-resistant clinical mutants of Mycobacterium tuberculosis from south India Int J Clin Med Micro 1 2011 87 96
71. N. Siddiqi, M. Shamim, S. Hussain, R.K. Choudhary, N. Ahmed, and Prachee Molecular characterization of multidrug-resistant isolates of Mycobacterium tuberculosis from patients in North India Antimicrobial Agents Chemother 46 2002 443 450
72. N.L. Wengenack, J.R. Uhl, A.L. Stamand, A.J. Tomlinson, L.M. Benson, and S. Naylor Recombinant Mycobacterium tuberculosis KatG (S315T) is a competent catalase-peroxidase with reduced activity toward isoniazid J Infect Dis 176 1997 722 727
73. N.L. Wengenack, and F. Rusnak Evidence for isoniazid-dependent free radical generation catalyzed by Mycobacterium tuberculosis KatG and the isoniazid-resistant mutant KatG (S315T) Biochemistry 40 2001 8990 8996
74. N.L. Wengenack, S. Todorovic, L. Yu, and F. Rusnak Evidence for differential binding of isoniazid byMycobacterium tuberculosis KatG and the isoniazid-resistant mutant KatG(S315T) Biochemistry 37 1998 15825 15834
75. B. Saint-Joanis, H. Souchon, M. Wilming, K. Johnsson, P.M. Alzari, and S.T. Cole Use of site-directed mutagenesis to probe the structure, function and isoniazid activation of the catalase/peroxidase, KatG, from Mycobacterium tuberculosis Biochem J 338 1999 753 760
76. A. Joseph DeVito, and Sheldon Morris Exploring the structure and function of the mycobacterial KatG protein using trans-dominant mutants Antimicrobial Agents Chemother 47 2003 188 195
77. C.J. Wei, B. Lei, J.M. Musser, and S.C. Tu Isoniazid activation defects in recombinant Mycobacterium tuberculosis catalase-peroxidase (KatG) mutants evident in InhA inhibitor production Antimicrobial Agents Chemother 47 2003 670 675
78. J. Suarez, K. Ranguelova, J.P. Schelvis, and R.S. Magliozzo Antibiotic resistance in M. tuberculosis: peroxidase intermediate bypass causes poor isoniazid activation by the Ser315Gly mutant of Mycobacterium tuberculosis catalase-peroxidase (KatG) J Biol Chem 284 2009 16146 16155
79. A. Nusrath Unissa, N. Selvakumar, and Narayanan Sujatha Characterization of isoniazid-resistant mutant (S315R) catalase-peroxidase, KatG, from Mycobacterium tuberculosis Int J Med Sci Technol 4 2011 13 22
80. A. Nusrath Unissa, Sameer Hassan, and Hanna Luke Elizabeth In silico analysis of isoniazid resistance in Mycobacterium tuberculosis Int J Med Pharma Eng 8 2014 389 395
81. A. Nusrath Unissa, Sameer Hassan, and N. Selvakumar Elucidating isoniazid resistance in Mycobacterium tuberculosis using molecular docking approach Int J Pharma Biosci 3 2012 314 326