Mice lacking inducible nitric oxide synthase demonstrate impaired killing of Porphyromonas gingivalis

Infection and Immunity

Volumn 71, Issue 9, 2003, Pages 4917-4924

  Gyurko, Robert ^a   Boustany, Gabriel ^a   Huang, Paul L ^b   Kantarci, Alpdogan ^a   Van Dyke, Thomas E ^a   Genco, Caroline A ^a,b   Gibson III, Frank C ^b  

^a BOSTON UNIVERSITY   (United States)

^b BOSTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; INTERLEUKIN 1BETA; INTERLEUKIN 6; NITRIC OXIDE SYNTHASE; NITROGEN; PROSTAGLANDIN E2; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DISEASE MODEL; DISEASE SEVERITY; ENZYME DEFICIENCY; ENZYME INDUCTION; IMMUNE RESPONSE; IMMUNOMODULATION; INOCULATION; LEUKOCYTE COUNT; MOUSE; NONHUMAN; OXIDATIVE STRESS; PERIODONTITIS; POLYMORPHONUCLEAR CELL; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; REGULATORY MECHANISM; SKIN DEFECT; STRAIN DIFFERENCE; SUBCUTANEOUS CHAMBER MODEL; TISSUE INJURY; WILD TYPE;

ANIMALS; ANTIBODIES, BACTERIAL; BACTEROIDACEAE INFECTIONS; COLONY COUNT, MICROBIAL; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; DIFFUSION CHAMBERS, CULTURE; DINOPROSTONE; FEMALE; HUMANS; IMMUNOGLOBULIN G; INFLAMMATION MEDIATORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PORPHYROMONAS GINGIVALIS; SUPEROXIDES;

EID: 0041322821     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.9.4917-4924.2003     Document Type: Article

References (55)

1. Alpagot, T., L. F. Wolff, Q. T. Smith, and S. D. Tran. 1996. Risk indicators for periodontal disease in a racially diverse urban population. J. Clin. Periodontol. 23:982-988.
2. Asai, K., H. Kato, K. Hirose, K. Akaogi, S. Kimura, S. Mukai, M. Inoue, Y. Yamamura, H. Sano, S. Sugino, T. Yoshikawa, and M. Kondo. 2000. PSK and OK-432-induced immunomodulation of inducible nitric oxide (NO) synthase gene expression in mouse peritoneal polymorphonuclear leukocytes and NO-mediated cytotoxicity. Immunopharmacol. Immunotoxicol. 22:221-235.
3. Beckman, J. S., T. W. Beckman, J. Chen, P. A. Marshall, and B. A. Freeman. 1990. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87:1620-1624.
4. Blaylock, M. G., B. H. Cuthbertson, H. F. Galley, N. R. Ferguson, and N. R. Webster. 1998. The effect of nitric oxide and peroxynitrite on apoptosis in human polymorphonuclear leukocytes. Free Radic. Biol. Med. 25:748-752.
5. Carreras, M. C., G. A. Pargament, S. D. Catz, J. J. Poderoso, and A. Boveris. 1994. Kinetics of nitric oxide and hydrogen peroxide production and formation of peroxynitrite during the respiratory burst of human neutrophils. FEBS Lett. 341:65-68.
6. 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. Investig. 90:1116-1121.
7. Coligan, J. E. 1994. Current protocols in immunology. John Wiley & Sons, Inc., New York, N.Y.
8. Cutler, C. W., J. R. Kalmar, and R. R. Arnold. 1991. Phagocytosis of virulent Porphyromonas gingivalis by human polymorphonuclear leukocytes requires specific immunoglobulin G. Infect. Immun. 59:2097-2104.
9. Ebersole, J. L., M. A. Taubman, D. J. Smith, D. E. Frey, A. D. Haffajee, and S. S. Socransky. 1987. Human serum antibody responses to oral microorganisms. IV. Correlation with homologous infection. Oral Microbiol. Immunol. 2:53-59.
10. Fortenberry, J. D., M. L. Owens, and L. A. Brown. 1999. S-Nitrosoglutathione enhances neutrophil DNA fragmentation and cell death. Am. J. Physiol. 276:L435-L442.
11. Fujii, H., K. Ichimori, 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.
12. Genco, C. A., C. W. Cutler, D. Kapezynski, K. Maloney, and R. R. Arnold. 1991. A novel mouse model to study the virulence of and host response to Porphyromonas (Bacteroides) gingivalis. Infect. Immun. 59:1255-1263.
13. Genco, C. A., R. E. Schifferle, T. Njoroge, R. Y. Forng, and C. W. Cutler. 1995. Resistance of a Tn4351-generated polysaccharide mutant of Porphyromonas gingivalis to polymorphonuclear leukocyte killing. Infect. Immun. 63:393-401.
14. Gibson, F. C., III, and C. A. Genco. 2001. Prevention of Porphyromonas gingivalis-induced oral bone loss following immunization with gingipain R1. Infect. Immun. 69:7959-7963.
15. Griffen, A. L., M. R. Becker, S. R. Lyons, M. L. Moeschberger, and E. J. Leys. 1998. Prevalence of Porphyromonas gingivalis and periodontal health status. J. Clin. Microbiol. 36:3239-3242.
16. Gryglewski, R. J., R. M. Palmer, and S. Moncada. 1986. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320:454-456.
17. Haffajee, A. D., M. A. Cugini, A. Tanner, R. P. Pollack, C. Smith, R. L. Kent, Jr., and S. S. Socransky. 1998. Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J. Clin. Periodontol. 25:346-353.
18. Hibbs, J. B., Jr., R. R. Taintor, and Z. Vavrin. 1987. Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science 235:473-476.
19. Holt, S. C., J. Ebersole, J. Felton, M. Brunsvold, and K. S. Kornman. 1988. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 239:55-57.
20. Holt, S. C., L. Kesavalu, S. Walker, and C. A. Genco. 1999. Virulence factors of Porphyromonas gingivalis. Periodontol. 2000 20:168-238.
21. Ialenti, A., A. Ianaro, S. Moncada, and M. Di Rosa. 1992. Modulation of acute inflammation by endogenous nitric oxide. Eur. J. Pharmacol. 211:177-182.
22. Ialenti, A., S. Moncada, and M. Di Rosa. 1993. Modulation of adjuvant arthritis by endogenous nitric oxide. Br. J. Pharmacol. 110:701-706.
23. Jones, K. L., T. W. Bryan, P. A. Jinkins, K. L. Simpson, M. B. Grisham, M. W. Owens, S. A. Milligan, B. A. Markewitz, and R. A. Robbins. 1998. Superoxide released from neutrophils causes a reduction in nitric oxide gas. Am. J. Physiol. 275:L1120-L1126.
24. 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.
25. Kantarci, A., K. Oyaizu, and T. E. Van Dyke. 2003. Neutrophil-mediated tissue injury in periodontal disease pathogenesis: findings from localized aggressive periodontitis. J. Periodontol. 74:66-75.
26. Karupiah, G., J. H. Chen, S. Mahalingam, C. F. Nathan, and J. D. MacMicking. 1998. Rapid interferon gamma-dependent clearance of influenza A virus and protection from consolidating pneumonitis in nitric oxide synthase 2-deficient mice. J. Exp. Med. 188:1541-1546.
27. Kelm, M. 1999. Nitric oxide metabolism and breakdown. Biochim. Biophys. Acta 1411:273-289.
28. Kendall, H. K., H. R. Haase, H. Li, Y. Xiao, and P. M. Bartold. 2000. Nitric oxide synthase type-II is synthesized by human gingival tissue and cultured human gingival fibroblasts. J. Periodontal Res. 35:194-200.
29. Kim, P. K., R. Zamora, P. Petrosko, and T. R. Billiar. 2001. The regulatory role of nitric oxide in apoptosis. Int. Immunopharmacol. 1:1421-1441.
30. Kosonen, O., H. Kankaanranta, J. Uotila, and E. Moilanen. 2000. Inhibition by nitric oxide-releasing compounds of E-selectin expression in and neutrophil adhesion to human endothelial cells. Eur. J. Pharmacol. 394:149-156.
31. Kuwahara, H., Y. Miyamoto, T. Akaike, T. Kubota, T. Sawa, S. Okamoto, and H. Maeda. 2000. Helicobacter pylori urease suppresses bactericidal activity of peroxynitrite via carbon dioxide production. Infect. Immun. 68:4378-4383.
32. Laubach, V. E., E. G. Shesely, O. Smithies, and P. A. Sherman. 1995. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc. Natl. Acad. Sci. USA 92:10688-10692.
33. Lindemann, S., M. Sharafi, M. Spiecker, M. Buerke, A. Fisch, T. Grosser, K. Veit, C. Gierer, W. Ibe, J. Meyer, and H. Darius. 2000. NO reduces PMN adhesion to human vascular endothelial cells due to downregulation of ICAM-1 mRNA and surface expression. Thromb. Res. 97:113-123.
34. Lohinai, Z., P. Benedek, E. Feher, A. Gyorfi, L. Rosivall, A. Fazekas, A. L. Salzman, and C. Szabo. 1998. Protective effects of mercaptoethylguanidine, a selective inhibitor of inducible nitric oxide synthase, in ligature-induced periodontitis in the rat. Br. J. Pharmacol. 123:353-360.
35. 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.
36. MacMicking, J. D., R. J. North, R. LaCourse, J. S. Mudgett, S. K. Shah, and C. F. Nathan. 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 94:5243-5248.
37. Miller, M. J., H. Sadowska-Krowicka, S. Chotinaruemol, J. L. Kakkis, and D. A. Clark. 1993. Amelioration of chronic ileitis by nitric oxide synthase inhibition. J. Pharmacol. Exp. Ther. 264:11-16.
38. Miyata, Y., H. Takeda, S. Kitano, and S. Hanazawa. 1997. Porphyromonas gingivalis lipopolysaccharide-stimulated bone resorption via CD14 is inhibited by broad-spectrum antibiotics. Infect. Immun. 65:3513-3519.
39. Moneada, S., and J. D. Erusalimsky. 2002. Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell. Biol. 3:214-220.
40. Nathan, C. 1997. Inducible nitric oxide synthase: what difference does it make? J. Clin. Investig. 100:2417-2423.
41. Nathan, C., and Q. W. Xie. 1994. Nitric oxide synthases: roles, tolls, and controls. Cell 78:915-918.
42. Ogawa, T., H. Uchida, and K. Amino. 1994. Immunobiological activities of chemically defined lipid A from lipopolysaccharides of Porphyromonas gingivalis. Microbiology 140(Pt. 5):1209-1216.
43. Rodenas, J., M. T. Mitjavila, and T. Carbonell. 1998. Nitric oxide inhibits superoxide production by inflammatory polymorphonuclear leukocytes. Am. J. Physiol. 274:C827-C830.
44. Rubanyi, G. M., E. H. Ho, E. H. Cantor, W. C. Lumma, and L. H. Botelho. 1991. Cytoprotective function of nitric oxide: inactivation of superoxide radicals produced by human leukocytes. Biochem. Biophys. Res. Commun. 181:1392-1397.
45. Sethi, S., and M. Dikshit. 2000. Modulation of polymorphonuclear leukocytes function by nitric oxide. Thromb. Res. 100:223-247.
46. Shapira, L., C. Champagne, T. E. Van Dyke, and S. Amar. 1998. Strain-dependent activation of monocytes and inflammatory macrophages by lipopolysaccharide of Porphyromonas gingivalis. Infect. Immun. 66:2736-2742.
47. Shapira, L., B. Gordon, M. Warbington, and T. E. Van Dyke. 1994. Priming effect of Porphyromonas gingivalis lipopolysaccharide on superoxide production by neutrophils from healthy and rapidly progressive periodontitis subjects. J. Periodontol. 65:129-133.
48. Shibata, K., M. L. Warbington, B. J. Gordon, H. Kurihara, and T. E. Van Dyke. 2001. Nitric oxide synthase activity in neutrophils from patients with localized aggressive periodontitis. J. Periodontol. 72:1052-1058.
49. 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.
50. Stenger, S., N. Donhauser, H. Thuring, M. Rollinghoff, and C. Bogdan. 1996. Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase. J. Exp. Med. 183:1501-1514.
51. Taylor, E. L., I. L. Megson, C. Haslett, and A. G. Rossi. 2001. Dissociation of DNA fragmentation from other hallmarks of apoptosis in nitric oxidetreated neutrophils: differences between individual nitric oxide donor drugs. Biochem. Biophys. Res. Commun. 289:1229-1236.
52. Ward, C., T. H. Wong, J. Murray, I. Rahman, C. Haslett, E. R. Chilvers, and A. G. Rossi. 2000. Induction of human neutrophil apoptosis by nitric oxide donors: evidence for a caspase-dependent, cyclic-GMP-independent, mechanism. Biochem. Pharmacol. 59:305-314.
53. Wei, X. Q., I. G. Charles, A. Smith, J. Ure, 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 375:408-411.
54. Witko-Sarsat, V., P. Rieu, B. Descamps-Latscha, P. Lesavre, and L. Halbwachs-Mecarelli. 2000. Neutrophils: molecules, functions, and pathophysiological aspects. Lab. Investig. 80:617-653.
55. Xie, Q. W., H. J. Cho, J. Calaycay, R. A. Mumford, K. M. Swiderek, T. D. Lee, A. Ding, T. Troso, and C. Nathan. 1992. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256:225-228.