Mechanisms of nitric oxide-related antimicrobial activity

Journal of Clinical Investigation

Volumn 99, Issue 12, 1997, Pages 2818-2825

  Fang, Ferric C ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE; ANTIINFECTIVE AGENT; BACTERIAL DNA;

ANTIMICROBIAL ACTIVITY; DEFENSE MECHANISM; DRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; BACTERIUM; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; DNA, BACTERIAL; HUMANS; NITRIC OXIDE; REACTIVE OXYGEN SPECIES;

EID: 0031570501     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/jci119473     Document Type: Review

References (73)

1. Gorham, F.P., and C.L. Scamman, editors. 1934. Papers of Charles V. Chapin, M.D. New York. Commonwealth Fund.
2. Fang, F.C. 1997. NO contest: understanding the complex roles of nitric oxide in infection. ASM News. In press.
3. Anstey, N.M., J.B. Weinberg, M.Y. Hassanali, E.D. Mwaikamho, D. Manyenga, M.A. Misukonis, D.R. Arnelle, D. Hollis, M.I. McDonald, and D.L. Granger. 1996. Nitric oxide in Tanzanian children with malaria. Inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression. J. Exp. Med. 184:557-567.
4. Evans, T.G., L. Thai, D.L. Granger, and J.B. Hibbs, Jr. 1993. Effect of in vivo inhibition of nitric oxide production in murine leishmaniasis. J. Immunol. 151:907-915.
5. Ochoa, J.B., A.O. Udekwu, T.R. Billiar, R.D. Curran, F.B. Cerra, R.L. Simmons, and A.B. Peitzman. 1991. Nitrogen oxide levels in patients after trauma and during sepsis. Ann. Surg. 214:621-626.
6. Stenger, S., N. Donhauser, H. Thüring, M. Röllinghoff, and C. Bogdan. 1996. Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase. J. Exp. Med. 183:1501-1514.
7. Nicholson, S., M.D.G. Bonecini-Almeida, J.R. Lapa e Silva, C. Nathan, Q.-W. Xie, R. Mumford, J.R. Weidner, J. Calaycay, J. Geng, N. Boechat, et al. 1996. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J. Exp. Med. 183:2293-2302.
8. MacMicking, J.D., R.J. North, R. LaCourse, J.S. Mudgett, S.K. Shah, and C.F. Nathan. 1997. Identification of NOS2 as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA. 94:5243-5248.
9. Adams, L.B., J.B.J. Hibbs, R.R. Taintor, and J.L. Krahenbuhl. 1990. Microbiostatic effect of murine-activated macrophages for Toxoplasma gondii. J. Immunol. 144:2725-2729.
10. DeGroote, M.A., and F.C. Fang. 1995. NO inhibitions: antimicrobial properties of nitric oxide. Clin. Infect. Dis. 21(Suppl. 2):S162-S165.
11. Sternberg, J., N. Mabbott, I. Sutherland, and F.Y. Liew. 1994. Inhibition of nitric oxide synthesis leads to reduced parasitemia in murine Trypanosoma brucei infection. Infect. Immun. 62:2135-2137.
12. Mannick, J.B., K. Asano, K. Izumi, E. Kieff, and J.S. Stamler. 1994. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell. 79:1137-1146.
13. Hibbs, J.B.J., C. Westenfelder, R. Taintor, Z. Vavrin, C. Kablitz, R.L. Baranowski, J.H. Ward, R.L. Menlove, M.P. McMurray, J.P. Kushner, and W. Samlowski. 1992. Evidence for cytokine-inducible nitric oxide synthesis from L-arginine in patients receiving interleukin-2 therapy. J. Clin. Invest. 89:867-877.
14. Vouldokis, I., V. Riveros-Moreno, B. Dugas, F. Ouaaz, P. Becherel, P. Debre, S. Moncada, and M.D. Mossalayi. 1995. The killing of Leishmania major by human macrophages is mediated by nitric oxide induced after ligation of the Fc∈RII/CD23 surface antigen. Proc. Natl. Acad. Sci. USA. 92:7804-7808.
15. DeMaria, R., M.G. Cifone, R. Trotta, M.R. Rippo, C. Festuccia, A. Santoni, and R. Testi. 1994. Triggering of human monocyte activation through CD69, a member of the natural killer cell gene complex family of signal transducing receptors. J. Exp. Med. 180:1999-2004.
16. Bukrinsky, M.I., H.S.L.M. Nottet, H. Schmidtmayerova, L. Dubrovsky, C.R. Flanagan, M.E. Mullins, S.A. Lipton, and H.R. Gendelman. 1995. Regulation of nitric oxide synthase activity in human immunodeficiency virus type 1 (HIV-1)-infected monocytes. Implications for HIV-associated neurological disease. J. Exp. Med. 181:735-745.
17. Evans, T.J., L.D.K. Buttery, A. Carpenter, D.R. Springall, J.M. Polak, and J. Cohen. 1996. Cytokine-treated human neutrophils contain inducible nitric oxide synthase that produces nitration of ingested bacteria. Proc. Natl. Acad. Sci. USA. 93:9553-9558.
18. Wheeler, M.A., S.D. Smith, G. García-Cardeña, C.F. Nathan, R.M. Weiss, and W.C. Sessa. 1997. Bacterial infection induces nitric oxide synthase in human neutrophils. J. Clin. Invest. 99:110-116.
19. St. Clair, E.W., W.E. Wilkinson, T. Lang, L. Sanders, M.A. Misukonis, G.S. Gilkeson, D.S. Pisetsky, D.L. Granger, and J.B. Weinberg. 1996. Increased expression of blood mononuclear cell nitric oxide synthase type 2 in rheumatoid arthritis patients. J. Exp. Med. 184:1173-1178.
20. Condino-Neto, A., M.N. Muscará, A.S. Grumach, M.M.S. Carneiro-Sampaio, and G. De Nucci. 1993. Neutrophils and mononuclear cells from patients with chronic granulomatous disease release nitric oxide. Br. J. Clin. Pharmacol. 35:485-490.
21. Kumar, V., S.K. Jindal, and N.K. Ganguly. 1995. Release of reactive oxygen and nitrogen intermediates from monocytes of patients with pulmonary tuberculosis. Scand. J. Clin. Lab. Invest. 55:163-169.
22. Gow, A.J., D.G. Buerk, and H. Ischiropoulos. 1997. A novel reaction mechanism for the formation of S-nitrosothiols in vivo. J. Biol. Chem. 272: 2841-2845.
23. Eiserich, J.P., C.E. Cross, A.D. Jones, B. Halliwell, and A. Van der Vliet. 1996. Formation of nitrating and chlorinating species by reaction of nitrite with hypochlorous acid. A novel mechanism for nitric oxide-mediated protein modification. J. Biol. Chem. 271:19199-19208.
24. Vazquez-Torres, A., J. Jones-Carson, and E. Balish. 1996. Peroxynitrite contributes to the candidacidal activity of nitric oxide-producing macrophages. Infect. Immun. 64:3127-3133.
25. Pacelli, R., D.A. Wink, J.A. Cook, M.C. Krishna, W. De Graft, N. Friedman, M. Tsokos, A. Samuni, and J.B. Mitchell. 1995. Nitric oxide potentiates hydrogen peroxide-induced killing of Escherichia coli. J. Exp. Med. 182:1469-1479.
26. Noronha-Dutra, A.A., M.M. Epperlein, and N. Woolf. 1993. Reaction of nitric oxide with hydrogen peroxide to produce potentially cytotoxic singlet oxygen as a model for nitric oxide-mediated killing. FEBS Lett. 321:59-62.
27. Freeman, B.A., C.R. White, H. Gutierrez, A. Paler-Martínez, M.M. Tarpey, and H. Rubbo. 1995. Oxygen radical-nitric oxide reactions in vascular diseases. Adv. Pharmacol. 34:45-69.
28. Kim, Y.-M., H.A. Bergonia, C. Müller, B.R. Pitt, W.D. Watkins, and J.R. Lancaster, Jr. 1995. Nitric oxide and intracellular heme. Adv. Pharmacol. 34:277-291.
29. Park, J.W. 1996. Attenuation of P47(phox) and P67(phox) membrane translocation as the inhibitory mechanism of S-nitrosothiol on the respiratory burst oxidase in human neutrophils. Biochem. Biophys. Res. Commun. 220:31-35.
30. Kanner, J., S. Harel, and R. Granit. 1991. Nitric oxide as an antioxidant. Arch. Biochem. Biophys. 289:130-136.
31. Wink, D.A., J.A. Cook, R. Pacelli, J. Liebmann, M.C. Krishna, and J.B. Mitchell. 1995. Nitric oxide (NO) protects against cellular damage by reactive oxygen species. Toxicol. Lett. 82-83:221-226.
32. Kim, Y.M., H. Bergonia, and J.R. Lancaster, Jr. 1995. Nitrogen oxide-induced autoprotection in isolated rat hepatocytes. FEBS Lett. 374:228-232.
33. Wink, D.A., M.B. Grisham, J.C. Cook, R. Pacelli, J. Liebman, M. Krishna, and J.B. Mitchell. 1996. Chemical biology of nitric oxide. Direct and indirect effects. In Proceedings of the 2nd International Conference on Biochemistry and Molecular Biology of Nitric Oxide. UCLA, Los Angeles, CA.
34. Assreuy, J., F.Q. Cunha, M. Epperlein, A. Noronha-Dutra, C.A. O'Donell, F.Y. Liew, and S. Moncada. 1994. Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major. Eur. J. Immunol. 24:672-676.
35. Fernandes, P.D., and J. Assreuy. 1997. Role of nitric oxide and superoxide in Giardia lamblia killing. Braz. J. Med. Biol. Res. 30:93-99.
36. Denicola, A., J.M. Souza, R. Radi, and E. Lissi. 1996. Nitric oxide diffusion in membranes determined by fluorescence quenching. Arch. Biochem. Biophys. 328:208-212.
37. Nunoshiba, T., T. deRojas-Walker, J.S. Wishnok, S.R. Tannenbaum, and B. Demple. 1993. Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophages. Proc. Natl. Acad. Sci. USA. 90:9993-9997.
38. Abouhamad, W.N., M. Manson, M.M. Gibson, and C.F. Higgins. 1991. Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol. Microbiol. 5:1035-1047.
39. DeGroote, M.A., D. Granger, Y. Xu, G. Campbell, R. Prince, and F.C. Fang. 1995. Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model. Proc. Natl. Acad. Sci. USA. 92:6399-6403.
40. Kaplan, S.S., J.R. Lancaster, R.E. Basford, and R.L. Simmons. 1996. Effect of nitric oxide on staphylococcal killing and interactive effect with Superoxide. Infect. Immun. 64:69-76.
41. Wink, D.A., K.S. Kasprzak, C.M. Maragos, R.K. Elespuru, M. Misra, T.M. Dunams, T.A. Cebula, W.H. Koch, A.W. Andrews, J.S. Allen, and L.K. Keefer. 1991. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science (Wash. DC). 254:1001-1003.
42. Juedes, M.J., and G.N. Wogan. 1996. Peroxynitrite-induced mutation spectra of pSP189 following replication in bacteria and in human cells. Mutat. Res. 349:51-61.
43. Maragos, C.M., A.W. Andrews, L.K. Keefer, and R.K. Elespuru. 1993. Mutagenicity of glyceryl trinitrate (nitroglycerin) in Salmonella typhimurium. Mutat. Res. 298:187-195.
44. Deleted in proof.
45. Ischiropoulos, H., and A.B. Al-Mehdi. 1995. Peroxynitrite-mediated oxidative protein modifications. FEBS Lett. 364:279-282.
46. Drapier, J.C., C. Pellat, and Y. Henry. 1991. Generation of EPR-detectable nitrosyl-iron complexes in tumor target cells co-cultured with activated macrophages. J. Biol. Chem. 266:10162-10167.
47. Hausladen, A., and I. Fridovich. 1994. Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not. J. Biol. Chem. 269:29405-29408.
48. Hentze, M.W., and L.C. Kühn. 1996. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA. 93:8175-8182.
49. Ahmed, S.F., I.P. Oswald, P. Caspar, S. Hieny, L. Keefer, A. Sher, and S.L. James. 1997. Developmental differences determine larval susceptibility to nitric oxide-mediated killing in a murine model of vaccination against Schistosoma mansoni. Infect. Immun. 65:219-226.
50. Murad, F. 1994. Regulation of cytosolic guanylyl cyclase by nitric oxide: the NO-cyclic GMP signal transduction system. Adv. Pharmacol. 26:19-33.
51. Lepoivre, M., B. Chenais, A. Yapo, G. Lemaire, L. Thelander, and J.-P. Tenu. 1990. Alterations of ribonucleotide reductase activity following induction of the nitrite-generating pathway in adenocarcinoma cells. J. Biol. Chem. 265: 14143-14149.
52. Melkova, Z., and M. Esteban. 1995. Inhibition of vaccinia virus DNA replication by inducible expression of nitric oxide synthase. J. Immunol. 155: 5711-5718.
53. Karupiah, G., and N. Harris. 1995. Inhibition of viral replication by nitric oxide and its reversal by ferrous sulfate and tricarboxylic acid cycle metabolites. J. Exp. Med. 181:2171-2179.
54. Stamler, J.S. 1995. S-nitrosothiols and the bioregulatory actions of nitrogen oxides through reactions with thiol groups. Curr. Top. Microbiol. 196:19-36.
55. Morris, S.L., and J.N. Hansen. 1981. Inhibition of Bacillus cereus spore outgrowth by covalent modification of a sulfhydryl group by nitrosothiol and iodoacetate. J. Bacteriol. 148:465-471.
56. Crow, J.P., and J.S. Beckman. 1995. Reactions between nitric oxide, superoxide, and peroxynitrite: footprints of peroxynitrite. Adv. Pharmacol. 34:17-43.
57. DeGroote, M.A., U.A. Ochsner. M. Shiloh, C. Nathan, J. McCord, M.C. Dinauer, and F.C. Fang. 1997. The role of Cu,Zn Superoxide dismutase (SodC) in Salmonella typhimurium pathogenesis. In Proceedings of the 97th General Meeting of the American Society for Microbiology. ASM Press, Washington, DC, No. B279.
58. Rubbo, H., R. Radi, M. Trujillo, R. Telleri, B. Kalyanaraman, S. Barnes, M. Kirk, and B.A. Freeman. 1994. Nitric oxide regulation of Superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 269:26066-26075.
59. Halliwell, B., M.L. Hu, S. Louie, T.R. Duvall, B.K. Tarkington, P. Motchnik, and C.E. Cross. 1992. Interaction of nitrogen dioxide with human plasma. Antioxidant depletion and oxidative damage. FEBS Lett. 313:62-66.
60. Wei, X.Q., I.G. Charles, A. Smith, J. Lire, G.J. Feng, F.P. Huang, D. Xu, W. Muller, S. Moncada, and F.Y. Liew. 1995. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature (Lond.). 375:408-411.
61. Newton, G.L., K. Arnold, M.S. Price, C. Sherrill, S.B. Delcardayre, Y. Aharonowitz, G. Cohen, J. Davies, R.C. Fahey, and C. Davis. 1996. Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes. J. Bacteriol. 178:1990-1995.
62. Fairlamb, A.H., and A. Cerami. 1992. Metabolism and functions of trypanothione in the kinetoplastida. Ann. Rev. Microbiol. 46:695-729.
63. Singh, S.P., J.S. Wishnok, M. Keshive, W.M. Deen, and S.R. Tannenbaum. 1996. The chemistry of the S-nitrosoglutathione/glutathione system. Proc. Natl. Acad. Sci. USA. 93:14428-14433.
64. DeGroote, M.A., T. Testerman, Y. Xu, G. Stauffer, and F.C. Fang. 1996. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science (Wash. DC). 272:414-417.
65. Loscalzo, J. 1996. The oxidant stress of hyperhomocyst(e)inemia. J. Clin. Invest. 98:5-7.
66. Buchmeier, N., C.J. Lipps, M.H.Y. So, and F. Heffron. 1993. Recombination-deficient mutants of Salmonella typhimurium are avirulent and sensitive to the oxidative burst of macrophages. Mol. Microbiol. 7:933-936.
67. Nunoshiba, T., T. DeRojas-Walker, S.R. Tannenbaum, and B. Demple. 1995. Roles of nitric oxide in inducible resistance of Escherichia coli to activated murine macrophages. Infect. Immun. 63:794-798.
68. Tsaneva, I.R., and B. Weiss. 1990. soxR. a locus governing a Superoxide response regulon in Escherichia coli K-12. J. Bacteriol. 172:4197-4205.
69. Christman, M.F., R.W. Morgan, F.S. Jacobson, and B.N. Ames. 1985. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell. 41:753-762.
70. Hausladen, A., C.T. Privalle, T. Keng, J. De Angelo, and J.S. Stamler. 1996. Nitrosative stress: activation of the transcription factor OxyR. Cell. 86: 719-729.
71. Warren, J.B., R. Loi, N.B. Rendell, and G.W. Taylor. 1990. Nitric oxide is inactivated by the bacterial pigment pyocyanin. Biochem. J. 266:921-923.
72. Cowley, S.C., S.V. Myltseva, and F.E. Nano. 1996. Phase variation in Francisella tularensis affecting intracellular growth, lipopolysaccharide antigenicity and nitric oxide production. Mol. Microbiol. 20:867-874.
73. Prada, J., J. Malinowski, S. Muller, U. Bienzle, and P.G. Kremsner. 1996. Effects of Plasmodium vinckei hemozoin on the production of oxygen radicals and nitrogen oxides in murine macrophages. Am. J. Trop. Med. Hyg. 54:620-62.