Determinants of nitric oxide steady-state levels during anaerobic respiration by Neisseria gonorrhoeae

Molecular Microbiology

Volumn 58, Issue 1, 2005, Pages 177-188

  Cardinale, Jean A ^a   Clark, Virginia L ^b  

^a ALFRED UNIVERSITY   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRATE REDUCTASE; NITRIC OXIDE; NITRITE;

ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL METABOLISM; INFLAMMATION; MICROBIAL RESPIRATION; NEISSERIA GONORRHOEAE; NONHUMAN; PH; PRIORITY JOURNAL; STEADY STATE;

ANAEROBIOSIS; FEMALE; GONORRHEA; HUMANS; HYDROGEN-ION CONCENTRATION; NEISSERIA GONORRHOEAE; NITRIC OXIDE; NITRITE REDUCTASES; NITRITES; NITROUS OXIDE; OXIDOREDUCTASES; TRIAZENES;

BACTERIA (MICROORGANISMS); NEISSERIA GONORRHOEAE;

EID: 26244449967     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04807.x     Document Type: Article

References (55)

1. Anjum, M.F., Stevanin, T.M., Read, R.C., and Moir, J.W. (2002) Nitric oxide metabolism in Neisseria meningitidis. J Bacteriol 184: 2987-2993.
2. Boulanger, M.J., and Murphy, M.E. (2002) Crystal structure of the soluble domain of the major anaerobically induced outer membrane protein (AniA) from pathogenic Neisseria: a new class of copper-containing nitrite reductases. J Mol Biol 315: 1111-1127.
3. Cameron, I.T., and Campbell, S. (1998) Nitric oxide in the endometrium. Hum Reprod Update 4: 565-569.
4. Cardinale, J.A. (2000) Structural and functional analysis of AniA, the major anaerobically induced outer membrane protein of Neisseria gonorrhoeae. PhD Thesis. Rochester, NY: University of Rochester.
5. Clark, V.L., Campbell, L.A., Palermo, D.A., Evans, T.M., and Kumpel, K.W. (1987) Induction and repression of outer membrane proteins by anaerobic growth of Neisseria gonorrhoeae. Infect Immun 55: 1359-1364.
6. Clark, V.L., Knapp, U.S., Thompson, S., and Kumpel, K.W. (1988) Presence of antibodies to the major anaerobically induced gonococcal outer membrane protein in sera from patients with gonococcal infections. Microb Pathog 5: 381-390.
7. Cohen, M.S., and Britigan, B.E. (1987) Metabolic responses of Neisseria gonorrhoeae to human serum and myeloid cells. Adaptation to host defenses? Antonie Van Leeuwenhoek 53: 545-550.
8. Colasanti, M., Persichini, T., Venturini, G., and Ascenzi, P. (1999) S-nitrosylation of viral proteins: molecular bases for antiviral effect of nitric oxide. IUBMB Life 48: 25-31.
9. Connelly, L., Palacios-Callender, M., Ameixa, C., Moncada, S., and Hobbs, A.J. (2001) Biphasic regulation of NF-kappa B activity underlies the pro- and anti-inflammatory actions of nitric oxide. J Immunol 166: 3873-3881.
10. Davis, K.L., Martin, E., Turko, I.V., and Murad, F. (2001) Novel effects of nitric oxide. Annu Rev Pharmacol Toxicol 41: 203-236.
11. Deora, A.A., and Lander, H.M. (2000) Regulation of signal transduction and gene expression by reactive nitrogen species. In Antioxidant and Redox Regulation of Genes. Sen, C.K., Sies, H., and Baeurle, P.A. (eds). San Diego, CA: Academic Press, pp. 147-178.
12. Dermastia, M., Turk, T., and Hollocher, T.C. (1991) Nitric oxide reductase. Purification from Paracoccus denitrificans with use of a single column and some characteristics. J Biol Chem 266: 10899-10905.
13. Fichorova, R.N., Desai, P.J., Gibson, F.C., 3rd, and Genco, C.A. (2001) Distinct proinflammatory host responses to Neisseria gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect Immun 69: 5840-5848.
14. Garnett, G.P., Mertz, K.J., Finelli, L., Levine, W.C., and St. Louis, M.E. (1999) The transmission dynamics of gonorrhea: modeling the reported behavior of infected patients from Newark, New Jersey. Philos Trans R Soc Lond B Biol Sci 354: 787-797.
15. Gobert, A.P., McGee, D.J., Akhtar, M., Mendz, G.L., Newton, J.C., Cheng, Y., et al. (2001) Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc Natl Acad Sci USA 98: 13844-13849.
16. Goretski, J., Zafiriou, O.C., and Hollocher, T.C. (1990) Steady-state nitric oxide concentrations during denitrification. J Biol Chem 265: 11535-11538.
17. Harvey, H.A., Post, D.M., and Apicella, M.A. (2002) Immortalization of human urethral epithelial cells: a model for the study of the pathogenesis of and the inflammatory cytokine response to Neisseria gonorrhoeae infection. Infect Immun 70: 5808-5815.
18. Hauck, C.R., and Meyer, T.F. (2003) 'Small' talk: Opa proteins as mediators of Neisseria-host-cell communication. Curr Opin Microbiol 6: 43-49.
19. Hedges, S.R., Sibley, D.A., Mayo, M.S., Hook, E.W., III, and Russell, M.W. (1998) Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections. J Infect Dis 178: 742-751.
20. Hedges, S.R., Mayo, M.S., Mestecky, J., Hook, E.W., III, and Russell, M.W. (1999) Limited local and systemic antibody responses to Neisseria gonorrhoeae during uncomplicated genital infections. Infect Immun 67: 3937-3946.
21. Heiss, B., Frunzke, K., and Zumft, W.G. (1989) Formation of the N-N bond from nitric oxide by a membrane-bound cytochrome be complex of nitrate-respiring (denitrifying) Pseudomonas stutzeri. J. Bacteriol 171: 3288-3297.
22. Householder, T.C., Belli, W.A., Lissenden, S., Cole, J.A., and 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 Bacteriol 181: 541-551.
23. Householder, T.C., Fozo, E.M., Cardinale, J.A., and 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 Immun 68: 5241-5246.
24. Igietseme, J.U., Uriri, I.M., Chow, M., Abe, E., and Rank, R.G. (1997) Inhibition of intracellular multiplication of human strains of Chlamydia trachomatis by nitric oxide. Biochem Biophys Res Commun 232: 595-601.
25. Ignarro, L.J., Wood, K.S., and Wolin, M.S. (1984) Regulation of purified soluble guanylate cyclase by porphyrins and metalloporphyrins: a unifying concept. Adv Cyclic Nucleotide Protein Phosphorylation Res 17: 267-274.
26. Isbey, S.F., Alcorn, T.M., Davis, R.H., Haizlip, J., Leone, P.A., and Cohen, M.S. (1997) Characterisation of Neisseria gonorrhoeae in semen during urethral infection in men. Genitourin Med 73: 378-382.
27. Katsuyama, K., Shichiri, M., Marumo, F., and Hirata, Y. (1998) NO inhibits cytokine-induced iNOS expression and NF-kappaB activation by interfering with phosphorylation and degradation of IkappaB-alpha. Arterioscler Thromb Vasc Biol 18: 1796-1802.
28. Kellogg, D.S., Jr, Peacock, W.L., Jr, Deacon, W.E., Brown, L., and Pirkle, C.I. (1963) Neisseria gonorrhoeae I. Virulence genetically linked to clonal variation. J Bacteriol 85: 1274-1279.
29. Khorram, O., Garthwaite, M., and Magness, R.R. (1999) Endometrial and myometrial expression of nitric oxide synthase isoforms in pre- and postmenopausal women. J Clin Endocrinol Metab 84: 2226-2232.
30. Knapp, J.S., and Clark, V.L. (1984) Anaerobic growth of Neisseria gonorrhoeae coupled to nitrite reduction. Infect Immun 46: 176-181.
31. Liaudat, L., Soriano, F.G., and Szabo, C. (2000) Biology of nitric oxide signaling. Crit Care Med 28: N37-N52.
32. Lissenden, S., Mohan, S., Overton Regan, T.T., Crooke, H., Cardinale, J.A., Householder, T.C., et al. (2000) Identification of transcription activators that regulate gonococcal adaptation from aerobic to anaerobic or oxygen-limited growth. Mol Microbiol 37: 839-855.
33. Lowe, T.L., and Kraus, S.J. (1976) Quantitation of Neisseria gonorrhoeae from women with gonorrhea. J Infect Dis 133: 621-626.
34. Mannick, J.B., Stamler, J.S., Teng, E., Simpson, N., Lawrence, J., Jordan, J., and Finberg, R.W. (1999) Nitric oxide modulates HIV-1 replication. J Acquir Immune Defic Syndr 22: 1-9.
35. Mateo, A.O., and de Artinano, M.A.A. (2000) Nitric oxide reactivity and mechanisms involved in it biological effects. Pharm Res 42: 421-427.
36. Miranda, K.M., Espey, M.G., and Wink, D.A. (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5: 62-71.
37. Naumann, M., Rudel, T., Wieland, B., Bartsch, C., and Meyer, T.F. (1997) Coordinate activation of activator protein and inflammatory cytokines in response to Neisseria gonorrhoeae epithelial cell contact involves stress response kinases. J Exp Med 188: 1277-1286.
38. Peng, H.B., Libby, P., and Liao, J.K. (1995) Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J Biol Chem 270: 14214-14219.
39. Poole, R.K. (2005) Nitric oxide and nitrosative stress tolerance in bacteria. Biochem Soc Trans 33: 176-180.
40. Prudencio, M., Eady, R.R., and Sawers, G. (1999) The blue copper-containing nitrite reductase from Alcaligenes xylosoxidans: cloning of the nirA gene and characterization of the recombinant enzyme. J Bacteriol 181: 2323-2329.
41. Ram, S., Mackinnon, F.G., Gulati, S., McQuillen, D.P., Vogel, U., Frosch, M., et al. (1999) The contrasting mechanisms of serum resistance of Neisseria gonorrhoeae and group B Neisseria meningitidis. Mol Immunol 36: 915-928.
42. Reynaert, N.L., Ckless, K., Korn, S.H., Vos, N., Guala, A.S., Wouters, E.F., et al. (2004) Nitric oxide represses inhibitory kappaB kinase through Snitrosylation. Proc Natl Acad Sci USA 101: 8945-8950.
43. Richardson, D.J. (2000) Bacterial respiration: a flexible process for a changing environment. Microbiology 146: 551-571.
44. Russell, M.W., Hedges, S.R., Wu, H.-Y., Hook, E.W., III, and Mestecky, J. (1999) Mucosal Immunity in the genital tract: prospects for vaccines against sexually transmitted diseases - a review. Am J Reprod Immunol 42: 58-63.
45. Seifert, H.S. (1996) Questions about gonococcal pilus phase- and antigenic variation. Mol Microbiol 21: 433-440.
46. Stefano, G.B., Goumon, Y., Bilfinger, T.V., Welters, I.D., and Cadet, P. (2000) Basal nitric oxide limits immune, nervous and cardiovascular excitation: human endothelia express a mu opiate receptor. Prog Neurobiol 60: 513-530.
47. Taguchi, M., Alfer, J., Chwalisz, K., Beier, H.M., and Classen-Linke, I. (2000) Endothelial nitric oxide synthase is differently expressed in human endometrial vessels during the menstrual cycle. Mol Hum Reprod 6: 185-190.
48. Torre, D., Pugliese, A., and Speranza, F. (2002) Role of nitric oxide in HIV-1 infection: friend or foe? Lancet Infect Dis 2: 273-280.
49. Tschugguel, W., Schneeberger, C., Lass, H., Stonek, F., Zaghlula, M.B., Czerwenka, K., et al. (1999a) Human cervical ripening is associated with an increase in cervical inducible nitric oxide synthase expression. Biol Reprod 60: 1367-1372.
50. Tschugguel, W., Schneeberger, C., Untried, G., Brautigam, G., Stonek, F., Wieser, F., et al. (1999b) Elevation of inducible nitric oxide synthase activity in human endometrium during menstruation. Biol Reprod 60: 297-304.
51. Vaisanen-Tommiska, M., Nuutila, M., Aittomaki, K., Hiilesmaa, V., and Ylikorkala, O. (2003) Nitric oxide metabolites in cervical fluid during pregnancy: further evidence for the role of cervical nitric oxide in cervical ripening. Am J Obstet Gynecol 188: 779-785.
52. Vaisanen-Tommiska, M., Mikkola, T.S., and Ylikorkala, O. (2004) Increased release of cervical nitric oxide in spontaneous abortion before clinical symptoms: a possible mechanism for preabortal cervical ripening. J Clin Endocrinol Metab 89: 5622-5626.
53. Yoshiki, N., Kubota, T., and Aso, T. (2000) Expression and localization of inducible nitric oxide synthase in human non-pregnant and early pregnant endometrium. Mol Hum Reprod 6: 283-287.
54. Young, H., Sarafian, S.K., Harris, A.B., and McMillan, A. (1983) Non-cultural detection of Neisseria gonorrhoeae in cervical and vaginal washings. J Med Microbiol 16: 183-191.
55. Zumft, W.G. (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 533-616.