1887

Abstract

encodes a number of important genes that aid in survival during times of oxidative stress. The same immune cells capable of oxygen-dependent killing mechanisms also have the capacity to generate reactive nitrogen species (RNS) that may function antimicrobially. F62 and eight additional gonococcal strains displayed a high level of resistance to peroxynitrite, while and showed a four- to seven-log and a four-log decrease in viability, respectively. Mutation of gonococcal orthologues that are known or suspected to be involved in RNS defence in other bacteria ( and ) resulted in no loss of viability, suggesting that has a novel mechanism of resistance to peroxynitrite. Whole-cell extracts of F62 prevented the oxidation of dihydrorhodamine, and decomposition of peroxynitrite was not dependent on or . F62 grown in co-culture with strain DH10B was shown to protect viability 10-fold. Also, peroxynitrite treatment of F62 did not result in accumulation of nitrated proteins, suggesting that an active peroxynitrite reductase is responsible for peroxynitrite decomposition rather than a protein sink for amino acid modification.

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2009-08-01
2020-07-07
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References

  1. Aktan F.. 2004; iNOS-mediated nitric oxide production and its regulation. Life Sci75:639–653
    [Google Scholar]
  2. Alam M. S., Akaike T., Okamoto S., Kubota T., Yoshitake J., Sawa T., Miyamoto Y., Tamura F., Maeda H.. 2002; Role of nitric oxide in host defense in murine salmonellosis as a function of its antibacterial and antiapoptotic activities. Infect Immun70:3130–3142
    [Google Scholar]
  3. Alam M. S., Zaki M. H., Yoshitake J., Akuta T., Ezaki T., Akaike T.. 2006; Involvement of Salmonella enterica serovar Typhi RpoS in resistance to NO-mediated host defense against serovar Typhi infection. Microb Pathog40:116–125
    [Google Scholar]
  4. Alcorn T. M., Zheng H. Y., Gunther M. R., Hassett D. J., Cohen M. S.. 1994; Variation in hydrogen peroxide sensitivity between different strains of Neisseria gonorrhoeae is dependent on factors in addition to catalase activity. Infect Immun62:2138–2140
    [Google Scholar]
  5. Alvarez B., Radi R.. 2003; Peroxynitrite reactivity with amino acids and proteins. Amino Acids25:295–311
    [Google Scholar]
  6. Archibald F. S., Duong M. N.. 1986; Superoxide dismutase and oxygen toxicity defenses in the genus Neisseria. Infect Immun51:631–641
    [Google Scholar]
  7. Barth K., Clark V. L.. 2008; Differences in nitric oxide steady states between arginine, hypoxanthine, uracil auxotrophs (AHU) and non-AHU strains of Neisseria gonorrhoeae during anaerobic respiration in the presence of nitrite. Can J Microbiol54:639–646
    [Google Scholar]
  8. Beckman J. S., Koppenol W. H.. 1996; Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol271:C1424–C1437
    [Google Scholar]
  9. Bogdan C.. 2001; Nitric oxide and the immune response. Nat Immunol2:907–916
    [Google Scholar]
  10. Bogdan C., Rollinghoff M., Diefenbach A.. 2000; Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol12:64–76
    [Google Scholar]
  11. Braun C., Zumft W. G.. 1991; Marker exchange of the structural genes for nitric oxide reductase blocks the denitrification pathway of Pseudomonas stutzeri at nitric oxide. J Biol Chem266:22785–22788
    [Google Scholar]
  12. Bryk R., Griffin P., Nathan C.. 2000; Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature407:211–215
    [Google Scholar]
  13. Burney S., Caulfield J. L., Niles J. C., Wishnok J. S., Tannenbaum S. R.. 1999; The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat Res424:37–49
    [Google Scholar]
  14. Cardinale J. A., Clark V. L.. 2005; Determinants of nitric oxide steady-state levels during anaerobic respiration by Neisseria gonorrhoeae. Mol Microbiol58:177–188
    [Google Scholar]
  15. Carreras M. C., Pargament G. A., Catz S. D., Poderoso J. J., Boveris A.. 1994; Kinetics of nitric oxide and hydrogen peroxide production and formation of peroxynitrite during the respiratory burst of human neutrophils. FEBS Lett341:65–68
    [Google Scholar]
  16. Casey S. G., Veale D. R., Smith H.. 1979; Demonstration of intracellular growth of gonococci in human phagocytes using spectinomycin to kill extracellular organisms. J Gen Microbiol113:395–398
    [Google Scholar]
  17. Casey S. G., Shafer W. M., Spitznagel J. K.. 1986; Neisseria gonorrhoeae survive intraleukocytic oxygen-independent antimicrobial capacities of anaerobic and aerobic granulocytes in the presence of pyocin lethal for extracellular gonococci. Infect Immun52:384–389
    [Google Scholar]
  18. Chakravortty D., Hensel M.. 2003; Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microbes Infect5:621–627
    [Google Scholar]
  19. Chakravortty D., Hansen-Wester I., Hensel M.. 2002; Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med195:1155–1166
    [Google Scholar]
  20. Chan E. D., Chan J., Schluger N. W.. 2001; What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge. Am J Respir Cell Mol Biol25:606–612
    [Google Scholar]
  21. Cowley S. C., Myltseva S. V., Nano F. E.. 1996; Phase variation in Francisella tularensis affecting intracellular growth, lipopolysaccharide antigenicity and nitric oxide production. Mol Microbiol20:867–874
    [Google Scholar]
  22. Cramm R., Siddiqui R. A., Friedrich B.. 1997; Two isofunctional nitric oxide reductases in Alcaligenes eutrophus H16. J Bacteriol179:6769–6777
    [Google Scholar]
  23. De Groote M. A., Granger D., Xu Y., Campbell G., Prince R., Fang F. C.. 1995; Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model. Proc Natl Acad Sci U S A92:6399–6403
    [Google Scholar]
  24. De Groote M. A., Ochsner U. A., Shiloh M. U., Nathan C., McCord J. M., Dinauer M. C., Libby S. J., Vazquez-Torres A., Xu Y., Fang F. C.. 1997; Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci U S A94:13997–14001
    [Google Scholar]
  25. Dyet K., Moir J.. 2006; Effect of combined oxidative and nitrosative stress on Neisseria meningitidis. Biochem Soc Trans34:197–199
    [Google Scholar]
  26. Edwards J. L., Apicella M. A.. 2004; The molecular mechanisms used by Neisseria gonorrhoeae to initiate infection differ between men and women. Clin Microbiol Rev17:965–981
    [Google Scholar]
  27. Ehrt S., Shiloh M. U., Ruan J., Choi M., Gunzburg S., Nathan C., Xie Q., Riley L. W.. 1997; A novel antioxidant gene from Mycobacterium tuberculosis. J Exp Med186:1885–1896
    [Google Scholar]
  28. Ezraty B., Aussel L., Barras F.. 2005; Methionine sulfoxide reductases in prokaryotes. Biochim Biophys Acta1703:221–229
    [Google Scholar]
  29. Fang F. C.. 2004; Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol2:820–832
    [Google Scholar]
  30. Fu H. S., Hassett D. J., Cohen M. S.. 1989; Oxidant stress in Neisseria gonorrhoeae: adaptation and effects on l-(+)-lactate dehydrogenase activity. Infect Immun57:2173–2178
    [Google Scholar]
  31. Gobert A. P., McGee D. J., Akhtar M., Mendz G. L., Newton J. C., Cheng Y., Mobley H. L., Wilson K. T.. 2001; Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc Natl Acad Sci U S A98:13844–13849
    [Google Scholar]
  32. Goldstein S., Merenyi G.. 2008; The chemistry of peroxynitrite: implications for biological activity. Methods Enzymol436:49–61
    [Google Scholar]
  33. Green S. J., Meltzer M. S., Hibbs J. B. Jr, Nacy C. A.. 1990; Activated macrophages destroy intracellular Leishmania major amastigotes by an l-arginine-dependent killing mechanism. J Immunol144:278–283
    [Google Scholar]
  34. Hampton M. B., Kettle A. J., Winterbourn C. C.. 1998; Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood92:3007–3017
    [Google Scholar]
  35. Hassett D. J., Charniga L., Cohen M. S.. 1990; recA and catalase in H2O2-mediated toxicity in Neisseria gonorrhoeae. J Bacteriol172:7293–7296
    [Google Scholar]
  36. Hedges S. R., Sibley D. A., Mayo M. S., Hook E. W. III, Russell M. W.. 1998; Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections. J Infect Dis178:742–751
    [Google Scholar]
  37. Hillis S. D., Nakashima A., Marchbanks P. A., Addiss D. G., Davis J. P.. 1994; Risk factors for recurrent Chlamydia trachomatis infections in women. Am J Obstet Gynecol170:801–806
    [Google Scholar]
  38. Householder T. C., Belli W. A., Lissenden S., Cole J. A., Clark V. L.. 1999; cis- and trans-acting elements involved in regulation of aniA, the gene encoding the major anaerobically induced outer membrane protein in Neisseria gonorrhoeae. J Bacteriol181:541–551
    [Google Scholar]
  39. Householder T. C., Fozo E. M., Cardinale J. A., Clark V. L.. 2000; Gonococcal nitric oxide reductase is encoded by a single gene, norB, which is required for anaerobic growth and is induced by nitric oxide. Infect Immun68:5241–5246
    [Google Scholar]
  40. Igietseme J. U., Uriri I. M., Chow M., Abe E., Rank R. G.. 1997; Inhibition of intracellular multiplication of human strains of Chlamydia trachomatis by nitric oxide. Biochem Biophys Res Commun232:595–601
    [Google Scholar]
  41. Ischiropoulos H., Gow A., Thom S. R., Kooy N. W., Royall J. A., Crow J. P.. 1999; Detection of reactive nitrogen species using 2,7-dichlorodihydrofluorescein and dihydrorhodamine 123. Methods Enzymol301:367–373
    [Google Scholar]
  42. Jeong W., Cha M. K., Kim I. H.. 2000; Thioredoxin-dependent hydroperoxide peroxidase activity of bacterioferritin comigratory protein (BCP) as a new member of the thiol-specific antioxidant protein (TSA)/alkyl hydroperoxide peroxidase C (AhpC) family. J Biol Chem275:2924–2930
    [Google Scholar]
  43. Kellogg D. S. Jr, Peacock W. L. Jr, Deacon W. E., Brown L., Pirkle D. I.. 1963; Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J Bacteriol85:1274–1279
    [Google Scholar]
  44. Kooy N. W., Royall J. A., Ischiropoulos H., Beckman J. S.. 1994; Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Radic Biol Med16:149–156
    [Google Scholar]
  45. Kuwahara H., Miyamoto Y., Akaike T., Kubota T., Sawa T., Okamoto S., Maeda H.. 2000; Helicobacter pylori urease suppresses bactericidal activity of peroxynitrite via carbon dioxide production. Infect Immun68:4378–4383
    [Google Scholar]
  46. Liaudet L., Soriano F. G., Szabo C.. 2000; Biology of nitric oxide signaling. Crit Care Med28:N37–N52
    [Google Scholar]
  47. MacMicking J. D., Nathan C., Hom G., Chartrain N., Fletcher D. S., Trumbauer M., Stevens K., Xie Q. W., Sokol K.. other authors 1995; Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell81:641–650
    [Google Scholar]
  48. MacMicking J., Xie Q. W., Nathan C.. 1997; Nitric oxide and macrophage function. Annu Rev Immunol15:323–350
    [Google Scholar]
  49. Mayer J., Woods M. L., Vavrin Z., Hibbs J. B. Jr. 1993; Gamma interferon-induced nitric oxide production reduces Chlamydia trachomatis infectivity in McCoy cells. Infect Immun61:491–497
    [Google Scholar]
  50. Moskovitz J.. 2005; Methionine sulfoxide reductases: ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases. Biochim Biophys Acta 1703;213–219
    [Google Scholar]
  51. Overton T. W., Whitehead R., Li Y., Snyder L. A., Saunders N. J., Smith H., Cole J. A.. 2006; Coordinated regulation of the Neisseria gonorrhoeae-truncated denitrification pathway by the nitric oxide-sensitive repressor, NsrR, and nitrite-insensitive NarQ–NarP. J Biol Chem281:33115–33126
    [Google Scholar]
  52. Overton T. W., Justino M. C., Li Y., Baptista J. M., Melo A. M., Cole J. A., Saraiva L. M.. 2008; Widespread distribution in pathogenic bacteria of di-iron proteins that repair oxidative and nitrosative damage to iron-sulfur centers. J Bacteriol190:2004–2013
    [Google Scholar]
  53. Pacher P., Beckman J. S., Liaudet L.. 2007; Nitric oxide and peroxynitrite in health and disease. Physiol Rev87:315–424
    [Google Scholar]
  54. Poole L. B.. 2005; Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch Biochem Biophys433:240–254
    [Google Scholar]
  55. Poole R. K., Hughes M. N.. 2000; New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol Microbiol36:775–783
    [Google Scholar]
  56. Radi R., Beckman J. S., Bush K. M., Freeman B. A.. 1991a; Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem266:4244–4250
    [Google Scholar]
  57. Radi R., Beckman J. S., Bush K. M., Freeman B. A.. 1991b; Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys288:481–487
    [Google Scholar]
  58. Reiter C. D., Teng R. J., Beckman J. S.. 2000; Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite. J Biol Chem275:32460–32466
    [Google Scholar]
  59. Rest R. F., Fischer S. H., Ingham Z. Z., Jones J. F.. 1982; Interactions of Neisseria gonorrhoeae with human neutrophils: effects of serum and gonococcal opacity on phagocyte killing and chemiluminescence. Infect Immun36:737–744
    [Google Scholar]
  60. Roos D., de Boer M., Kuribayashi F., Meischl C., Weening R. S., Segal A. W., Ahlin A., Nemet K., Hossle J. P.. other authors 1996; Mutations in the X-linked and autosomal recessive forms of chronic granulomatous disease. Blood87:1663–1681
    [Google Scholar]
  61. Rouhier N., Jacquot J. P.. 2003; Molecular and catalytic properties of a peroxiredoxin–glutaredoxin hybrid from Neisseria meningitidis. FEBS Lett554:149–153
    [Google Scholar]
  62. Ruan J., St John G., Ehrt S., Riley L., Nathan C.. 1999; noxR3, a novel gene from Mycobacterium tuberculosis, protects Salmonella typhimurium from nitrosative and oxidative stress. Infect Immun67:3276–3283
    [Google Scholar]
  63. Seib K. L., Jennings M. P., McEwan A. G.. 2003; A Sco homologue plays a role in defence against oxidative stress in pathogenic Neisseria. FEBS Lett546:411–415
    [Google Scholar]
  64. Seib K. L., Tseng H. J., McEwan A. G., Apicella M. A., Jennings M. P.. 2004; Defenses against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis: distinctive systems for different lifestyles. J Infect Dis190:136–147
    [Google Scholar]
  65. Seib K. L., Wu H. J., Kidd S. P., Apicella M. A., Jennings M. P., McEwan A. G.. 2006; Defenses against oxidative stress in Neisseria gonorrhoeae: a system tailored for a challenging environment. Microbiol Mol Biol Rev70:344–361
    [Google Scholar]
  66. Seib K. L., Wu H. J., Srikhanta Y. N., Edwards J. L., Falsetta M. L., Hamilton A. J., Maguire T. L., Grimmond S. M., Apicella M. A.. other authors 2007; Characterization of the OxyR regulon of Neisseria gonorrhoeae. Mol Microbiol63:54–68
    [Google Scholar]
  67. Senaratne R. H., De Silva A. D., Williams S. J., Mougous J. D., Reader J. R., Zhang T., Chan S., Sidders B., Lee D. H.. other authors 2006; 5′-Adenosinephosphosulphate reductase (CysH) protects Mycobacterium tuberculosis against free radicals during chronic infection phase in mice. Mol Microbiol59:1744–1753
    [Google Scholar]
  68. Shiloh M. U., MacMicking J. D., Nicholson S., Brause J. E., Potter S., Marino M., Fang F., Dinauer M., Nathan C.. 1999; Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity10:29–38
    [Google Scholar]
  69. Simons M. P., Nauseef W. M., Apicella M. A.. 2005; Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes. Infect Immun73:1971–1977
    [Google Scholar]
  70. Skaar E. P., Tobiason D. M., Quick J., Judd R. C., Weissbach H., Etienne F., Brot N., Seifert H. S.. 2002; The outer membrane localization of the Neisseria gonorrhoeae MsrA/B is involved in survival against reactive oxygen species. Proc Natl Acad Sci U S A99:10108–10113
    [Google Scholar]
  71. Stevanin T. M., Moir J. W., Read R. C.. 2005; Nitric oxide detoxification systems enhance survival of Neisseria meningitidis in human macrophages and in nasopharyngeal mucosa. Infect Immun73:3322–3329
    [Google Scholar]
  72. Stohl E. A., Criss A. K., Seifert H. S.. 2005; The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection. Mol Microbiol58:520–532
    [Google Scholar]
  73. Subbian S., Mehta P. K., Cirillo S. L., Cirillo J. D.. 2007; The Mycobacterium marinum mel2 locus displays similarity to bacterial bioluminescence systems and plays a role in defense against reactive oxygen and nitrogen species. BMC Microbiol7:4
    [Google Scholar]
  74. Szabo C., Ischiropoulos H., Radi R.. 2007; Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov6:662–680
    [Google Scholar]
  75. Turner S., Reid E., Smith H., Cole J.. 2003; A novel cytochrome c peroxidase from Neisseria gonorrhoeae: a lipoprotein from a Gram-negative bacterium. Biochem J373:865–873
    [Google Scholar]
  76. Turner S. M., Moir J. W., Griffiths L., Overton T. W., Smith H., Cole J. A.. 2005; Mutational and biochemical analysis of cytochrome c′, a nitric oxide-binding lipoprotein important for adaptation of Neisseria gonorrhoeae to oxygen-limited growth. Biochem J388:545–553
    [Google Scholar]
  77. Umezawa K., Akaike T., Fujii S., Suga M., Setoguchi K., Ozawa A., Maeda H.. 1997; Induction of nitric oxide synthesis and xanthine oxidase and their roles in the antimicrobial mechanism against Salmonella typhimurium infection in mice. Infect Immun65:2932–2940
    [Google Scholar]
  78. Yu K., Mitchell C., Xing Y., Magliozzo R. S., Bloom B. R., Chan J.. 1999; Toxicity of nitrogen oxides and related oxidants on mycobacteria: M. tuberculosis is resistant to peroxynitrite anion. Tuber Lung Dis79:191–198
    [Google Scholar]
  79. Zhu L., Gunn C., Beckman J. S.. 1992; Bactericidal activity of peroxynitrite. Arch Biochem Biophys298:452–457
    [Google Scholar]
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