Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro

Journal of Experimental Medicine

Volumn 192, Issue 2, 2000, Pages 227-236

  Vazquez Torres, Andrés ^a   Jones Carson, Jessica ^a   Mastroeni, Pietro ^b   Ischiropoulos, Harry ^c   Fang, Ferric C ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Innate immunity; Nitrosative; Oxidative; Phagocyte; Salmonella

Indexed keywords

HYDROGEN PEROXIDE; NITRIC OXIDE SYNTHASE; OXIDOREDUCTASE; PEROXYNITRITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMICROBIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNITY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NITROSATION; NONHUMAN; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; SALMONELLOSIS;

ANIMALS; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; NADPH OXIDASE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PHAGOCYTOSIS; REACTIVE OXYGEN SPECIES; SALMONELLA TYPHIMURIUM; SUPEROXIDES; TYROSINE;

EID: 0034679577     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.192.2.227     Document Type: Article

References (62)

1. Vazquez-Torres, A., J. Jones-Carson, A.J. Baumler, S. Falkow, R. Valdivia, W. Brown, M. Le, R. Berggren, W.T. Parks, and F.C. Fang. 1999. Extraintestinal dissemination of Salmonella via CD18-expressing phagocytes. Nature. 401: 804-808.
2. Vazquez-Torres, A., and F.C. Fang. 2000. Cellular routes of invasion by enteropathogens. Curr. Opin. Microbiol. 3:54-59.
3. Richter-Dahlfors, A., A.M.J. Buchan, and B.B. Finlay. 1997. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186:569-580.
4. Fields, P.I., R.V. Swanson, C.G. Haidaris, and F. Heffron. 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. USA. 83:5189-5193.
5. Mackaness, G.B. 1962. Cellular resistance to infection. J. Exp. Med. 116:381-406.
6. Miller, R.A., and B.E. Britigan. 1997. Role of oxidants in microbial pathophysiology. Clin. Microbiol. Rev. 10:1-18.
7. Curnutte, J.T., P.J. Scott, and B.M. Babior. 1989. Functional defect in neutrophil cytosols from two patients with autosomal recessive cytochrome-positive chronic granulomatous disease. J. Clin. Invest. 83:1236-1240.
8. Mouy, R., A. Fischer, E. Vilmer, R. Seger, and C. Griscelli. 1989. Incidence, severity, and prevention of infections in chronic granulomatous disease. J. Pediatr. 114:555-560.
9. Shiloh, M.U., J.D. MacMicking, S. Nicholson, J.E. Brause, S. Potter, M. Marino, F. Fang, M. Dinauer, and C. Nathan. 1999. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity. 10:29-38.
10. Mastroeni, P., A. Vazquez-Torres, F.C. Fang, Y. Xu, S. Khan, C.E. Hormaeche, and G. Dougan. 2000. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J. Exp. Med. 192:237-247.
11. Buchmeier, N.A., C.J. Lipps, M.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.
12. MacMicking, J., Q.W. Xie, and C. Nathan. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15:323-350.
13. De Groote, 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.
14. Fang, F.C. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99:2818-2825.
15. Ischiropoulos, H., L. Zhu, and J.S. Beckman. 1992. Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 298:446-451.
16. Pryor, W.A., and G.L. Squadrito. 1995. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am. J. Physiol 268:L699-L722.
17. Zhu, L., C. Gunn, and J.S. Beckman. 1992. Bactericidal activity of peroxynitrite. Arch. Biochem. Biophys. 298:452-457.
18. Vazquez-Torres, A., J. Jones-Carson, E. Balish. 1996. Peroxynitrite contributes to the candidacidal activity of nitric oxide-producing macrophages. Infect. Immun. 64:3127-3133.
19. Pacelli, R., D.A. Wink, J.A. Cook, M.C. Krishna, W. DeGraff, 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.
20. Bogdan, C., M. Röllinghoff, and A. Diefenbach. 1999. Nitric oxide in Leishmaniasis: from antimicrobial activity to immunoregulation. In Nitric Oxide and Infection. F.C. Fang, editor. Kluwer Academic/Plenum Publishers, New York. 361-377.
21. Chan, J., and J. Flynn. 1999. Nitric oxide in Mycobacterium tuberculosis infection. In Nitric Oxide and Infection. F.C. Fang, editor. Kluwer Academic/Plenum Publishers, New York. 281-310.
22. Mastroeni, P., J.A. Harrison, J.H. Robinson, S. Clare, S. Khan, D.J. Maskell, G. Dougan, and C.E. Hormaeche. 1998. Interleukin-12 is required for control of the growth of attenuated aromatic-compound-dependent Salmonellae in BALB/c mice: role of gamma interferon and macrophage activation. Infect. Immun. 66:4767-4776.
23. Mastroeni, P., J.N. Skepper, and C.E. Hormaeche. 1995. Effect of anti-tumor necrosis factor alpha antibodies on histopathology of primary Salmonella infections. Infect. Immun. 63: 3674-3682.
24. 2 and to L-arginine-dependent system in murine macrophages. Microbiol. Immunol. 35: 325-329.
25. De Groote, M.A., U.A. Ochsner, M.U. Shiloh, C. Nathan, J.M. McCord, M.C. Dinauer, S.J. Libby, A. Vazquez-Torres, Y. Xu, and F.C. Fang. 1997. Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc. Natl. Acad. Sci. USA. 94:13997-14001.
26. Chen, L., Q.W. Xie, and C. Nathan. 1998. Alkyl hydroperoxide reductase subunit C (AhpC) protects bacterial and human cells against reactive nitrogen intermediates. Mol. Cell. 1:795-805.
27. Kosaka, H., Y. Oda, and M. Uozumi. 1985. Induction of umuC gene expression by nitrogen dioxide in Salmonella typhimurium. Mutat. Res. 142:99-102.
28. De Groote, M.A., T. Testerman, Y. Xu, G. Stauffer, and F.C. Fang. 1996. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science. 272:414-417.
29. Crawford, M.J., and D.E. Goldberg. 1998. Role for the Salmonella flavohemoglobin in protection from nitric oxide. J. Biol. Chem. 1273:12543-12547.
30. Shiloh, M.U., J. Ruan, and C. Nathan. 1997. Evaluation of bacterial survival and phagocyte function with a fluorescence-based microplate assay. Infect. Immun. 65:3193-3198.
31. Ekman, P., M. Saarinen, Q. He, M. Virtala, M. Salmi, and K. Granfors. 1999. Human monocytic U937 cells kill Salmonella in vitro by NO-independent mechanisms. Infect. Immun. 67: 3670-3673.
32. Mastroeni, P., B. Villarreal-Ramos, and C.E. Hormaeche. 1993. Effect of late administration of anti-TNFα antibodies on a Salmonella infection in the mouse model. Microb. Pathog. 14:473-480.
33. MacMicking, J.D., C. Nathan, G. Hom, N. Chartrain, D.S. Fletcher, M. Trumbauer, K. Stevens, Q.W. Xie, K. Sokol, N. Hutchinson, et al. 1995. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell. 81:641-650.
34. Pollock, J.D., D.A. Williams, M.A. Gifford, L.L. Li, X. Du, J. Fisherman, S.H. Orkin, C.M. Doerschuk, and M.C. Dinauer. 1995. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat. Genet. 9:202-209.
35. Li, Y., H. Zhu, P. Kuppusamy, V. Roubaud, J.L. Zweier, and M.A. Trush. 1998. Validation of lucigenin (bis-N-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J. Biol. Chem. 273:2015-2023.
36. Radi, R., T.P. Cosgrove, J.S. Beckman, and B.A. Freeman. 1993. Peroxynitrite-induced luminol chemiluminescence. Biochem. J. 290:51-57.
37. Hooper, D.C., S. Spitsin, R.B. Kean, J.M. Champion, G.M. Dickson, I. Chaudhry, and H. Koprowski. 1998. Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis. Proc. Natl. Acad. Sci. USA. 95:675-680.
38. Szabo, C., and A.L. Salzman. 1995. Endogenous peroxynitrite is involved in the inhibition of mitochondrial respiration in immuno-stimulated J774.2 macrophages. Biochem. Biophys. Res. Commun. 209:739-743.
39. Pick, E. 1986. Microassays for superoxide and hydrogen peroxide production and nitroblue tetrazolium reduction using an enzyme immunoassay microplate reader. Methods Enzymol. 132:407-421.
40. Gilliam, M.B., M.P. Sherman, J.M. Griscavage, and L.J. Ignarro. 1993. A spectrophotometric assay for nitrate using NADPH oxidation by Aspergillus nitrate reductase. Anal. Biochem. 12:359-365.
41. Verdon, C.P., B.A. Burton, and R.L. Prior. 1995. Sample pretreatment with nitrate reductase and glucose-6-phosphate dehydrogenase quantitatively reduces nitrate while avoiding interference by NADP+ when the Griess reaction is used to assay for nitrite. Anal. Biochem. 224:502-508.
42. Crow, J.P., and H. Ischiropoulos. 1996. Detection and quantitation of nitrotyrosine residues in proteins: in vivo marker of peroxynitrite. Methods Enzymol. 269:185-194.
43. MacFarlane, A.S., M.G. Schwacha, and T.K. Eisenstein. 1999. In vivo blockage of nitric oxide with aminoguanidine inhibits immunosuppression induced by an attenuated strain of Salmonella typhimurium, potentiates Salmonella infection, and inhibits macrophage and polymorphonuclear leukocyte influx into the spleen. Infect. Immun. 67:891-898.
44. al-Ramadi, B.K., J.J. Meissler, Jr., D. Huang, and T.K. Eisenstein. 1992. Immunosuppression induced by nitric oxide and its inhibition by interleukin-4. Eur. J. Immunol. 22: 2249-2254.
45. Gao, J.J., E.G. Zuvanich, Q. Xue, D.L. Horn, R. Silverstein, and D.C. Morrison. 1999. Cutting edge: bacterial DNA and LPS act in synergy in inducing nitric oxide production in RAW 264.7 macrophages. J. Immunol. 163:4095-4099.
46. Clancy, R.M., J. Leszczynska-Piziak, and S.B. Abramson. 1992. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J. Clin. Invest. 90:1116-1121.
47. Iha, S., K. Orita, T. Utsumi, E.F. Sato, M. Inoue, and K. Utsumi. 1996. Oxygen-dependent inhibition of neutrophil respiratory burst by nitric oxide. Free Radic. Res. 25:489-498.
48. Forslund, T., and T. Stundqvist. 1995. Nitric oxide reduces hydrogen peroxide production from human polymorphonuclear neutrophils. Eur. J. Clin. Invest. 25:9-14.
49. Fujii, H., K. Ichmiori, K. Hoshiai, and H. Nakazawa. 1997. Nitric oxide inactivates NADPH oxidase in pig neutrophils by inhibiting its assembling process. J. Biol. Chem. 272: 32773-32778.
50. Wink, D.A., J.A. Cook, S.Y. Kim, Y. Vodovotz, R. Pacelli, M.C. Krishna, A. Russo, J.B. Mitchell, D. Jourd'heuil, A.M. Miles, and M.B. Grisham. 1997. Superoxide modulates the oxidation and nitrosation of thiols by nitric oxide-derived reactive intermediates. Chemical aspects involved in the balance between oxidative and nitrosative stress. J. Biol. Chem. 272:11147-11151.
51. Wink, D.A., Y. Vodovotz, M.B. Grisham, W. DeGraff, J.C. Cook, R. Pacelli, M. Krishna, and J.B. Mitchell. 1999. Antioxidant effects of nitric oxide. Methods Enzymol. 301:413-424.
52. Assreuy, J., F.Q. Cunha, M. Epperlein, A. Noronha-Dutra, C.A. O'Donnell, F.Y. Liew, and S. Moncada. 1994. Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major. Eur. J. Immmuol. 24:672-676.
53. Leenen, P.J., B.P. Canono, D.A. Drevets, J.S. Voerman, and P.A. Campbell. 1994. TNF-alpha and IFN-gamma stimulate a macrophage precursor cell line to kill Listeria monocytogenes in a nitric oxide-independent manner. J. Immunol. 153:5141-5147.
54. Ohya, S., Y. Tanabe, M. Makino, T. Nomura, H. Xiong, M. Arakawa, and M. Mitsuyama. 1998. The contributions of reactive oxygen intermediates and reactive nitrogen intermediates to listericidal mechanisms differ in macrophages activated pre-and postinfection. Infect. Immun. 66:4043-4049.
55. Fang, F.C., M.A. DeGroote, J.W. Foster, A.J. Baumler, U. Ochsner, T. Testernian, S. Bearson, J.C. Giard, Y. Xu, G. Campbell, and T. Laessig. 1999. Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc. Natl. Acad. Sci. USA. 96:7502-7507.
56. Farrant, J.L., A. Sansone, J.R. Canvin, M.J. Pallen, P.R. Langford, T.S. Wallis, G. Dougan, and J.S. Kroll. 1997. Bacterial copper-and zinc-cofactored superoxide dismutase contributes to the pathogenesis of systemic salmonellosis. Mol. Microbiol. 25:785-796.
57. 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.
58. -) in the presence of hydrogen peroxide. J. Biol. Chem. 274: 20909-20915.
59. Hausladen, A., A.J. Gow, and J.S. Stamler. 1998. Nitrosative stress: metabolic pathway involving the flavohemoglobin. Proc. Natl. Acad. Sci. USA. 95:14100-14105.
60. Hickman-Davis, J., J. Gibbs-Erwin, J.R. Lindsey, and S. Matalon. 1999. Surfactant protein A mediates mycoplasmacidal activity of alveolar macrophages by production of peroxynitrite. Proc. Natl. Acad. Sci. USA. 96:4953-4958.
61. Schmidt, H.H., T.D. Warner, M. Nakane, U. Forstermann, and F. Murad. 1992. Regulation and subcellular location of nitrogen oxide synthases in RAW264.7 macrophages. Mol. Pharmacol. 41:615-624.
62. Hecker, M., D.T. Walsh, and J.R. Vane. 1992. Characterization of a microsomal calcium-dependent nitric oxide synthase in activated J774.2 monocyte/macrophages. J. Cardiovasc. Pharmacol. 20(Suppl. 12):S139-S141.