The Mycobacterium marinum mel2 locus displays similarity to bacterial bioluminescence systems and plays a role in defense against reactive oxygen and nitrogen species

BMC Microbiology

Volumn 7, Issue , 2007, Pages

  Subbian, Selvakumar ^a   Mehta, Parmod K ^a   Cirillo, Suat L G ^a   Cirillo, Jeffrey D ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BIOLUMINESCENCE; COMPUTER MODEL; CONTROLLED STUDY; GENE LOCUS; GENE SEQUENCE; MACROPHAGE; MOLECULAR MECHANICS; MYCOBACTERIUM MARINUM; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS;

AMINO ACID MOTIFS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; GENE DELETION; GENETIC COMPLEMENTATION TEST; HEAT-SHOCK PROTEINS; LUMINESCENT PROTEINS; MUTAGENESIS, INSERTIONAL; MUTATION; MYCOBACTERIUM MARINUM; OPERON; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM MARINUM;

EID: 33846920861     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-7-4     Document Type: Article

References (63)

1. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. C Nathan MU Shiloh, Proc Natl Acad Sci U S A 2000 97 8841 8848 10922044 10.1073/pnas.97.16.8841
2. Role of KatG catalase-peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst. VH Ng JS Cox AO Sousa JD MacMicking JD McKinney, Mol Microbiol 2004 52 1291 1302 10.1111/j.1365-2958.2004.04078.x 15165233
3. 5'-Adenosinephosphosulphate reductase (CysH) protects Mycobacterium tuberculosis against free radicals during chronic infection phase in mice. RH Senaratne AD De Silva SJ Williams JD Mougous JR Reader T Zhang S Chan B Sidders DH Lee J Chan CR Bertozzi LW Riley, Mol Microbiol 2006 59 1744 1753 10.1111/j.1365-2958.2006.05075.x 16553880
4. Regulation of bacterial gene expression in response to oxidative stress. G Storz MB Toledano, Methods Enzymol 1994 236 196 207 7968610
5. OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. MF Christman G Storz BN Ames, Proc Natl Acad Sci U S A 1989 86 3484 3488 2471187 10.1073/pnas.86.10.3484
6. Pathways of oxidative damage. JA Imlay, Annu Rev Microbiol 2003 57 395 418 10.1146/annurev.micro.57.030502.090938 14527285
7. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. LC Seaver JA Imlay, J Bacteriol 2001 183 7173 7181 11717276 10.1128/JB.183.24.7173-7181.2001
8. Role of Mycobacterium tuberculosis copper-zinc superoxide dismutase. O Dussurget G Stewart O Neyrolles P Pescher D Young G Marchal, Infect Immun 2001 69 529 533 11119546 10.1128/IAI.69.1.529-533.2001
9. Cu,Zn superoxide dismutase of Mycobacterium tuberculosis contributes to survival in activated macrophages that are generating an oxidative burst. DL Piddington FC Fang T Laessig AM Cooper IM Orme NA Buchmeier, Infect Immun 2001 69 4980 4987 11447176 10.1128/IAI.69.8.4980-4987.2001
10. Iron-cofactored superoxide dismutase inhibits host responses to Mycobacterium tuberculosis. KM Edwards MH Cynamon RKR Voladri C Hager MS DeStefano KT Tham DL Lakey MR Bochan DS Kernodle, Am J Respir Crit Care Med 2001 164 2213 2219 11751190
11. Disparate responses to oxidative stress in saprophytic and pathogenic mycobacteria. DR Sherman PJ Sabo MJ Hickey TM Arain GG Mahairas Y Yuan CE Barry 3rd CK Stover, Proc Natl Acad Sci U S A 1995 92 6625 6629 7604044 10.1073/pnas.92.14.6625
12. katG mutations in isoniazid-resistant Mycobacterium tuberculosis isolates recovered from Finnish patients. HJ Marttila H Soini P Huovinen MK Viljanen, Antimicrob Agents Chemother 1996 40 2187 2189 8878604
13. A Ser315Thr substitution in KatG is predominant in genetically heterogeneous multidrug-resistant Mycobacterium tuberculosis isolates originating from the St. Petersburg area in Russia. HJ Marttila H Soini E Eerola E Vyshnevskaya BI Vyshnevskiy TF Otten AV Vasilyef MK Viljanen, Antimicrob Agents Chemother 1998 42 2443 2445 9736581
14. Characterization of the catalase-peroxidase gene (katG) and inhA locus in isoniazid-resistant and -susceptible strains of Mycobacterium tuberculosis by automated DNA sequencing: restricted array of mutations associated with drug resistance. JM Musser V Kapur DL Williams BN Krieswirth D van Soolingen JD van Embden, J Infect Dis 1996 173 196 202 8537659
15. Detection of mutations associated with isoniazid and rifampin resistance in Mycobacterium tuberculosis isolate from Samara Region, Russian Federation. V Nikolayevsky T Brown Y Balabanova M Ruddy I Fedorin F Drobniewski, J Clin Microbiol 2004 42 4498 4502 15472300 10.1128/JCM.42.10.4498-4502.2004
16. Molecular genetic basis of antimicrobial agent resistance in Mycobacterium tuberculosis: 1998 update. S Ramaswamy JM Musser, Tuber Lung Dis 1998 79 3 29 10.1054/tuld.1998.0002 10645439
17. Oxidative stress response and its role in sensitivity to isoniazid in mycobacteria: characterization and inducibility of ahpC by peroxides in Mycobacterium smegmatis and lack of expression in M. aurum and M. tuberculosis. S Dhandayuthapani Y Zhang MH Mudd V Deretic, J Bacteriol 1996 178 3641 3649 8655566
18. Silencing of oxidative stress response in Mycobacterium tuberculosis: expression patterns of ahpC in virulent and avirulent strains and effect of ahpC inactivation. B Springer S Master P Sander T Zahrt M McFalone J Song KG Papavinasasundaram MJ Colston E Boettger V Deretic, Infect Immun 2001 69 5967 5973 11553532 10.1128/IAI.69.10.5967-5973.2001
19. A novel antioxidant gene from Mycobacterium tuberculosis. S Ehrt MU Shiloh J Ruan M Choi S Gunzburg C Nathan Q Xie L Riley, J Exp Med 1997 186 1885 1896 10.1084/jem.186.11.1885 9382887
20. noxR3, a novel gene from Mycobacterium tuberculosis, protects Salmonella typhimurium from nitrosative and oxidative stress. J Ruan G St. Joh S Ehrt L Riley C Nathan, Infect Immun 1999 67 3276 3283 10377101
21. Dihydrolipoamide acyltransferase is critical for Mycobacterium tuberculosis pathogenesis. S Shi S Ehrt, Infect Immun 2006 74 56 63 16368957 10.1128/IAI.74.1.56-63.2006
22. Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. G St John N Brot J Ruan H Erdjument-Bromage P Tempst H Weissbach C Nathan, Proc Natl Acad Sci U S A 2001 98 9901 9906 11481433 10.1073/pnas.161295398
23. Methionine sulfoxide reductase A (MsrA) deficiency affects the survival of Mycobacterium smegmatis within macrophages. T Douglas DS Daniel BK Parida C Jagannath S Dhandayuthapani, J Bacteriol 2004 186 3590 3598 15150247 10.1128/JB.186.11.3590-3598.2004
24. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. KH Darwin S Ehrt JC Gutierrez-Ramos N Weich CF Nathan, Science 2003 302 1963 1966 10.1126/science.1091176 14671303
25. Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages. SS Master B Springer P Sander EC Boettger V Deretic GS Timmins, Microbiology 2002 148 3139 3144 12368447
26. Superoxide dismutase and hydrogen peroxide cause rapid nitric oxide breakdown, peroxynitrite production and subsequent cell death. AG McBride V Borutaite GC Brown, Biochim Biophys Acta 1999 1454 275 288 10452962
27. Toxicity of nitrogen oxides and related oxidants on mycobacteria: M. tuberculosis is resistant to peroxynitrite anion. K Yu C Mitchell Y Xing RS Magliozzo BR Bloom J Chan, Tuber Lung Dis 1999 79 191 198 10.1054/tuld.1998.0203 10692986
28. Experimental evidence for the physiological role of bacterial luciferase in the protection of cells against oxidative stress. H Szpilewska A Czyz G Wegrzyn, Curr Microbiol 2003 47 379 382 10.1007/s00284-002-4024-y 14669913
29. Bioluminescence as a possible auxiliary oxygen detoxifying mechanism in elaterid larvae. MP Barros EJ Bechara, Free Radic Biol Med 1998 24 767 777 10.1016/S0891-5849(97)00335-3 9586807
30. Luciferase and urate may act as antioxidant defenses in larval Pyrearinus termitilluminans (Elateridae: Coleoptera) during natural development and upon 20-hydroxyecdysone treatment. MP Barros EJ Bechara, Photochem Photobiol 2000 71 648 654 10.1562/0031-8655(2000)071<0648:LAUMAA>2.0.CO;2 10818797
31. Daily variations of antioxidant enzyme and luciferase activities in the luminescent click-beetle Pyrearinus termitilluminans: cooperation against oxygen toxicity. MP Barros EJ Bechara, Insect Biochem Mol Biol 2001 31 393 400 10.1016/S0965-1748(00)00132-6 11222948
32. Effects of hydrogen peroxide on light emission by various strains of marine luminescent bacteria. AM Katsev G Wegrzyn H Szpilewska, J Basic Microbiol 2004 44 178 184 10.1002/jobm.200310330 15162391
33. Luminescence of a bacterial luciferase intermediate by reaction with H2O2: the evolutionary origin of luciferase and source of endogenous light emission. H Watanabe T Nagoshi H Inaba, Biochim Biophys Acta 1993 1141 297 302 10.1016/0005-2728(93)90056-L
34. Elicitation of an oxidase activity in bacterial luciferase by site-directed mutation of a noncatalytic residue. X Lei KW Cho ME Herndon SC Tu, J Biol Chem 1990 265 4200 4203 2307667
35. The origins of marine bioluminescence: turning oxygen defence mechanisms into deep-sea communication tools. JF Rees B De Wergifosse O Noiset M Dubuisson B Janssens EM Thompson, J Exp Biol 1998 201 1211 1221 9510532
36. Identification of two Mycobacterium marinum loci that affect interactions with macrophages. SH El-Etr S Subbian SL Cirillo JD Cirillo, Infect Immun 2004 72 6902 6913 15557611 10.1128/IAI.72.12.6902-6913.2004
37. A Mycobacterium marinum mel2 Mutant is Defective for Growth in Macrophages Producing Reactive Oxygen and Nitrogen Species. S Subbian PK Mehta SL Cirillo LE Bermudez JD Cirillo, Infect Immun 2007 17030568
38. The beta subunit polypeptide of Vibrio harveyi luciferase determines light emission at 42 degrees C. A Escher DJ O'Kane AA Szalay, Mol Gen Genet 1991 230 385 393 10.1007/BF00280295 1685011
39. Delineation of the transcriptional boundaries of the lux operon of Vibrio harveyi demonstrates the presence of two new lux genes. E Swartzman C Miyamoto A Graham E Meighen, J Biol Chem 1990 265 3513 3517 2303459
40. The 1.5-A resolution crystal structure of bacterial luciferase in low salt conditions. AJ Fisher TB Thompson JB Thoden TO Baldwin I Rayment, J Biol Chem 1996 271 21956 21968 10.1074/jbc.271.36.21956 8703001
41. Structure of the beta 2 homodimer of bacterial luciferase from Vibrio harveyi: X-ray analysis of a kinetic protein folding trap. JB Thoden HM Holden AJ Fisher JF Sinclair G Wesenberg TO Baldwin I Rayment, Protein Sci 1997 6 13 23 9007973
42. Probing the functionalities of alphaGlu328 and alphaAla74 of Vibrio harveyi luciferase by site-directed mutagenesis and chemical rescue. CH Li SC Tu, Biochemistry 2005 44 13866 13873 10.1021/bi051182i 16229475
43. Active site hydrophobicity is critical to the bioluminescence activity of Vibrio harveyi luciferase. CH Li SC Tu, Biochemistry 2005 44 12970 12977 10.1021/bi050935y 16185065
44. Response of the antioxidant defense system to tert-butyl hydroperoxide and hydrogen peroxide in a human hepatoma cell line (HepG2). M Alia S Ramos R Mateos L Bravo L Goya, J Biochem Mol Toxicol 2005 19 119 128 10.1002/jbt.20061 15849717
45. Generation of oxy radicals in biosystems. MG Simic DS Bergtold LR Karam, Mutat Res 1989 214 3 12 2671698
46. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. WH Koppenol JJ Moreno WA Pryor H Ischiropoulos JS Beckman, Chem Res Toxicol 1992 5 834 842 10.1021/tx00030a017 1336991
47. Peroxynitrite formation from macrophage-derived nitric oxide. H Ischiropoulos L Zhu JS Beckman, Arch Biochem Biophys 1992 298 446 451 10.1016/0003-9861(92)90433-W 1329657
48. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Chan Y Xing RS Magliozzo BR Bloom, J Exp Med 1992 175 1111 1122 10.1084/jem.175.4.1111 1552282
49. Effects of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. J Chan K Tanaka D Carroll J Flynn BR Bloom, Infect Immun 1995 63 736 740 7529749
50. Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. S Ehrt D Schnappinger S Bekiranov J Drenkow S Shi TR Gingeras T Gaasterland G Schoolnik C Nathan, J Exp Med 2001 194 1123 1140 10.1084/jem.194.8.1123 11602641
51. Identification of nitric oxide synthase as a protective locus against tuberculosis. JD MacMicking RJ North R LaCourse JS Mudgett SK Shah CF Nathan, Proc Natl Acad Sci U S A 1997 94 5243 5248 9144222 10.1073/pnas.94.10.5243
52. The role of glutathione in nitric oxide donor toxicity to SN56 cholinergic neuron-like cells. U Fass K Panickar K Williams K Nevels D Personett M McKinney, Brain Res 2004 1005 90 100 10.1016/j.brainres.2004.01.046 15044069
53. Radical releasing properties of nitric oxide donors GEA 3162, SIN-1 and S-nitroso-N-acetylpenicillamine. P Holm H Kankaanranta T Metsa-Ketela E Moilanen, Eur J Pharmacol 1998 346 97 102 10.1016/S0014-2999(98)00009-0 9617758
54. Origin and evolution of bioluminescence. WD McElroy HH Seliger, Horizons in biochemistry New York, Academic Press, Kasha M and Pullman B, 1962 91 101
55. Oxygen-utilizing reactions and symbiotic colonization of the squid light organ by Vibrio fischeri. EG Ruby MJ McFall-Ngai, Trends Microbiol 1999 7 414 420 10.1016/S0966-842X(99)01588-7 10498950
56. Studies on isoniazid and tubercle bacilli. II. The growth requirements, catalase activities, and pathogenic properties of isoniazid-resistant mutants. ML Cohn C Kovitz U Oda G Middlebrook, Am Rev Tuberc 1954 70 641 664 13197742
57. Oxidative stress increases susceptibility of Mycobacterium tuberculosis to isoniazid. VM Bulatovic NL Wengenack JR Uhl L Hall GD Roberts FR Cockerill 3rd F Rusnak, Antimicrob Agents Chemother 2002 46 2765 2771 12183226 10.1128/AAC.46.9.2765-2771.2002
58. Mycobacterium marinum persists in cultured mammalian cells in a temperature-restricted fashion. L Ramakrishnan S Falkow, Infect Immun 1994 62 3222 3229 8039892
59. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. SB Snapper RE Melton S Mustafa T Kieser WR Jacobs Jr., Mol Microbiol 1990 4 1911 1919 10.1111/j.1365-2958.1990.tb02040.x 2082148
60. New use of BCG for recombinant vaccines. CK Stover VF de la Cruz TR Fuerst JE Burlein LA Benson LT Bennet GP Bansal JF Young MH Lee GF Hatfull SB Snapper RG Barletta WR Jacobs Jr. BR Bloom, Nature 1991 351 456 460 10.1038/351456a0 1904554
61. Use of in vivo complementation in Mycobacterium tuberculosis to identify a genomic fragment associated with virulence. L Pascopella FM Collins JM Martin MH Lee GF Hatfull CK Stover BR Bloom WR Jacobs Jr., Infect Immun 1994 62 1313 1319 8132338
62. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman, Nuc Acids Res 1997 25 3389 3402 10.1093/nar/25.17.3389
63. CDD: a curated Entrez database of conserved domain alignments. A Marchler-Bauer JB Anderson C DeWeese-Scott ND Fedorova LY Geer S He DI Hurwitz JD Jackson AR Jacobs CJ Lanczycki CA Liebert C Liu T Madej GH Marchler R Mazumder AN Nikolskaya AR Panchenko BS Rao BA Shoemaker V Simonyan JS Song PA Thiessen S Vasudevan Y Wang RA Yamashita JJ Yin SH Bryant, Nucleic Acids Res 2003 31 383 387 12520028 10.1093/nar/gkg087