Chronic ingestion of Porphyromonas gingivalis induces systemic nitric oxide response in mice

Oral Microbiology and Immunology

Volumn 24, Issue 3, 2009, Pages 204-210

  Nemec, A ^a   Pavlica, Z ^a   Crossley, D A ^a   Sentjurc M ^b   Jerin, A ^c   Erzen D ^d   Vrecl, M ^a   Majdic G ^a   Zdovc, I ^a   Petelin, M ^a   Skaleric U ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b JO EF STEFAN INSTITUTE   (Slovenia)

^c UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

^d UNIVERSITY CLINIC OF RESPIRATORY AND ALLERGIC DISEASES   (Slovenia)

Author keywords

1400W; Chronic oral challenge; Mice; Porphyromonas gingivalis; Systemic nitric oxide

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; NITRATE; NITRIC OXIDE; NITRITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; AORTA; ARTICLE; BROTH DILUTION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; FEMALE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; KIDNEY; LIVER; LUNG; MOUSE; NONHUMAN; PORPHYROMONAS GINGIVALIS;

AMIDINES; ANIMALS; AORTA; BENZYLAMINES; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; FREE RADICAL SCAVENGERS; GINGIVA; IMMUNOHISTOCHEMISTRY; KIDNEY; LIVER; LUNG; MICE; MICE, INBRED BALB C; MOUTH; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; PORPHYROMONAS GINGIVALIS; RANDOM ALLOCATION; SPECIFIC PATHOGEN-FREE ORGANISMS; SPLEEN; TIME FACTORS; TISSUE DISTRIBUTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 67449118509     PISSN: 09020055     EISSN: 1399302X     Source Type: Journal    
DOI: 10.1111/j.1399-302X.2008.00496.x     Document Type: Article

References (53)

1. Abraham SN, Malaviya R. Mast cells in infection and immunity. Infect Immun 1997 : 65 : 3501 3508. (Pubitemid 27398100)
2. Ahren C, Jungersten L, Sandberg T. Plasma nitrate as an index of nitric oxide formation in patients with acute infectious diseases. Scand J Infect Dis 1999 : 31 : 405 407. (Pubitemid 29454300)
3. Baker PJ, Evans RT, Roopenian DC. Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 1994 : 39 : 1035 1040. (Pubitemid 124034593)
4. Belz GT, Heath TJ. Lymph pathways of the medial retropharyngeal lymph node in dogs. J Anat 1995 : 186 (Pt 3 517 526.
5. Berliner LJ, Fujii H. In vivo spin trapping of nitric oxide. Antioxid Redox Signal 2004 : 6 : 649 656. (Pubitemid 38625385)
6. Choi EY, Hwang YM, Lee JY et al. Lipid A-associated proteins from Porphyromonas gingivalis stimulate release of nitric oxide by inducing expression of inducible nitric oxide synthase. J Periodontal Res 2007 : 42 : 350 360.
7. Eick S, Reissmann A, Rodel J, Schmidt KH, Pfister W. Porphyromonas gingivalis survives within KB cells and modulates inflammatory response. Oral Microbiol Immunol 2006 : 21 : 231 237. (Pubitemid 44336953)
8. Ellis G, Adatia I, Yazdanpanah M, Makela SK. Nitrite and nitrate analyses: a clinical biochemistry perspective. Clin Biochem 1998 : 31 : 195 220. (Pubitemid 28285351)
9. Frolov I, Houri-Hadad Y, Soskolne A, Shapira L. In vivo exposure to Porphyromonas gingivalis up-regulates nitric oxide but suppresses tumour necrosis factor-alpha production by cultured macrophages. Immunology 1998 : 93 : 323 328. (Pubitemid 28133605)
10. Furuta T, Kikuchi T, Akira S, Watanabe N, Yoshikawa Y. Roles of the small intestine for induction of toll-like receptor 4-mediated innate resistance in naturally acquired murine toxoplasmosis. Int Immunol 2006 : 18 : 1655 1662.
11. Garvey EP, Oplinger JA, Furfine ES et al. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 1997 : 272 : 4959 4963. (Pubitemid 27090046)
12. Grenier D, Imbeault S, Plamondon P, Grenier G, Nakayama K, Mayrand D. Role of gingipains in growth of Porphyromonas gingivalis in the presence of human serum albumin. Infect Immun 2001 : 69 : 5166 5172. (Pubitemid 32674505)
13. Han X, Fink MP, Uchiyama T, Yang R, Delude RL. Increased iNOS activity is essential for hepatic epithelial tight junction dysfunction in endotoxemic mice. Am J Physiol Gastrointest Liver Physiol 2004 : 286 : G126 G136. (Pubitemid 38055846)
14. Hardham J, Reed M, Wong J et al. Evaluation of a monovalent companion animal periodontal disease vaccine in an experimental mouse periodontitis model. Vaccine 2005 : 23 : 3148 3156. (Pubitemid 40504057)
15. Hayashi Y, Abe M, Murai A et al. Comparison of effects of nitric oxide synthase (NOS) inhibitors on plasma nitrite/nitrate levels and tissue NOS activity in septic organs. Microbiol Immunol 2005 : 49 : 139 147. (Pubitemid 40372155)
16. Holmqvist B, Olsson CF, Svensson ML, Svanborg C, Forsell J, Alm P. Expression of nitric oxide synthase isoforms in the mouse kidney: cellular localization and influence by lipopolysaccharide and Toll-like receptor 4. J Mol Histol 2005 : 36 : 499 516. (Pubitemid 43829389)
17. Jean-Baptiste E. Cellular mechanisms in sepsis. J Intensive Care Med 2007 : 22 : 63 72.
18. Jungersten L, Edlund A, Hafstrom LO, Karlsson L, Petersson AS, Wennmalm A. Plasma nitrate as an index of immune system activation in animals and man. J Clin Lab Immunol 1993 : 40 : 1 4.
19. Kaiserlian D, Cerf-Bensussan N, Hosmalin A. The mucosal immune system: from control of inflammation to protection against infections. J Leukoc Biol 2005 : 78 : 311 318. (Pubitemid 41061303)
20. Kalyanaraman B. Detection of nitric oxide by electron spin resonance in chemical, photochemical, cellular, physiological, and pathophysiological systems. Methods Enzymol 1996 : 268 : 168 187. (Pubitemid 26286359)
21. Kendall HK, Haase HR, Li H, Xiao Y, Bartold PM. Nitric oxide synthase type-II is synthesized by human gingival tissue and cultured human gingival fibroblasts. J Periodontal Res 2000 : 35 : 194 200.
22. Kim-Shapiro DB, Schechter AN, Gladwin MT. Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler Thromb Vasc Biol 2006 : 26 : 697 705. (Pubitemid 43732141)
23. Klebanoff SJ, Nathan CF. Nitrite production by stimulated human polymorphonuclear leukocytes supplemented with azide and catalase. Biochem Biophys Res Commun 1993 : 197 : 192 196. (Pubitemid 23358895)
24. Kleinert H, Boissel J, Schwarz P, Foerstermann U. Regulation of the expression of nitric oxide synthase isoforms. In : Ignarro LJ, ed. Nitric oxide. Biology and pathobiology. San Diego : Academic Press, 2000 : 105 128.
25. Koornstra PJ, de Jong FI, Vlek LF, Marres EH, van Breda Vriesman PJ. The Waldeyer ring equivalent in the rat. A model for analysis of oronasopharyngeal immune responses. Acta Otolaryngol 1991 : 111 : 591 599.
26. Lamont RJ, Jenkinson HF. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 1998 : 62 : 1244 1263. (Pubitemid 28558298)
27. Malaviya R, Abraham SN. Clinical implications of mast cell-bacteria interaction. J Mol Med 1998 : 76 : 617 623. (Pubitemid 28361880)
28. McCluskie K, Birrell MA, Wong S, Belvisi MG. Nitric oxide as a noninvasive biomarker of lipopolysaccharide-induced airway inflammation: possible role in lung neutrophilia. J Pharmacol Exp Ther 2004 : 311 : 625 633. (Pubitemid 39391548)
29. McNaughton L, Puttagunta L, Martinez-Cuesta MA et al. Distribution of nitric oxide synthase in normal and cirrhotic human liver. Proc Natl Acad Sci USA 2002 : 99 : 17161 17166. (Pubitemid 36034115)
30. Milbourne EA, Bygrave FL. Does nitric oxide play a role in liver function? Cell Signal 1995 : 7 : 313 318.
31. Moroz LL, Norby SW, Cruz L, Sweedler JV, Gillette R, Clarkson RB. Non-enzymatic production of nitric oxide (NO) from NO synthase inhibitors. Biochem Biophys Res Commun 1998 : 253 : 571 576. (Pubitemid 29039184)
32. Muller B, Kleschyov AL, Alencar JL, Vanin A, Stoclet JC. Nitric oxide transport and storage in the cardiovascular system. Ann N Y Acad Sci 2002 : 962 : 131 139. (Pubitemid 34592307)
33. Nemec A, Pavlica Z, Šentjurc M et al. Single gavage with Porphyromonas gingivalis reduces acute systemic nitric oxide response in mice. Oral Microbiol Immunol 2008 : 23 : 435 439.
34. Persichini T, Cantoni O, Suzuki H, Colasanti M. Cross-talk between constitutive and inducible NO synthase: an update. Antioxid Redox Signal 2006 : 8 : 949 954. (Pubitemid 44036511)
35. Poljakovic M, Svensson ML, Svanborg C, Johansson K, Larsson B, Persson K. Escherichia coli-induced inducible nitric oxide synthase and cyclooxygenase expression in the mouse bladder and kidney. Kidney Int 2001 : 59 : 893 904. (Pubitemid 32206852)
36. Scannapieco FA. Role of oral bacteria in respiratory infection. J Periodontol 1999 : 70 : 793 802.
37. Scannapieco FA. Systemic effects of periodontal diseases. Dent Clin North Am 2005 : 49 : 533 550. (Pubitemid 40835772)
38. Shapira L, Ayalon S, Brenner T. Effects of Porphyromonas gingivalis on the central nervous system: activation of glial cells and exacerbation of experimental autoimmune encephalomyelitis. J Periodontol 2002 : 73 : 511 556. (Pubitemid 34546402)
39. Steffen MJ, Holt SC, Ebersole JL. Porphyromonas gingivalis induction of mediator and cytokine secretion by human gingival fibroblasts. Oral Microbiol Immunol 2000 : 15 : 172 180. (Pubitemid 30208579)
40. Suzuki Y, Fujii S, Numagami Y, Tominaga T, Yoshimoto T, Yoshimura T. In vivo nitric oxide detection in the septic rat brain by electron paramagnetic resonance. Free Radic Res 1998 : 28 : 293 299. (Pubitemid 28325576)
41. Swerdlow MP, Kennedy DR, Kennedy JS et al. Expression and function of TLR2, TLR4, and Nod2 in primary canine colonic epithelial cells. Vet Immunol Immunopathol 2006 : 114 : 313 319. (Pubitemid 44634740)
42. Takahashi N, Schachtele CF. Effect of pH on the growth and proteolytic activity of Porphyromonas gingivalis and Bacteroides intermedius. J Dent Res 1990 : 69 : 1266 1269.
43. Takizawa T, Yoshikawa H, Yamada M, Morita H. Expression of nitric oxide synthase isoforms and detection of nitric oxide in rat placenta. Am J Physiol Cell Physiol 2002 : 282 : C762 C767. (Pubitemid 34663138)
44. Tracey WR, Tse J, Carter G. Lipopolysaccharide-induced changes in plasma nitrite and nitrate concentrations in rats and mice: pharmacological evaluation of nitric oxide synthase inhibitors. J Pharmacol Exp Ther 1995 : 272 : 1011 1015.
45. Tsikas D. Methods of quantitative analysis of the nitric oxide metabolites nitrite and nitrate in human biological fluids. Free Radic Res 2005 : 39 : 797 815. (Pubitemid 40975073)
46. Tsutsumi Y, Kihira T, Yamamoto S et al. Chemical modification of natural human tumor necrosis factor-alpha with polyethylene glycol increases its anti-tumor potency. Jpn J Cancer Res 1994 : 85 : 9 12. (Pubitemid 24048284)
47. Vanin AF, Huisman A, van Faassen EE. Iron dithiocarbamate as spin trap for nitric oxide detection: pitfalls and successes. Methods Enzymol 2002 : 359 : 27 42. (Pubitemid 35387007)
48. Venkataraman S, Martin SM, Buettner GR. Electron paramagnetic resonance for quantitation of nitric oxide in aqueous solutions. Methods Enzymol 2002 : 359 : 3 18. (Pubitemid 35387005)
49. Veszelovsky E, Holford NH, Thomsen LL, Knowles RG, Baguley BC. Plasma nitrate clearance in mice: modeling of the systemic production of nitrate following the induction of nitric oxide synthesis. Cancer Chemother Pharmacol 1995 : 36 : 155 159.
50. Walsh LJ. Mast cells and oral inflammation. Crit Rev Oral Biol Med 2003 : 14 : 188 198. (Pubitemid 44560803)
51. Wolf HF, Rateitschak EM, Rateitschak KH, Hassel TM. Color atlas of dental medicine. Periodontology. Stuttgart : Georg Thieme Verlag, 2005.
52. Yakovlev M. Elements of the endotoxin theory of human physiology and pathology. Hum Physiol 2003 : 29 : 476 485. (Pubitemid 36922059)
53. Yoshino S, Sasatomi E, Mori Y, Sagai M. Oral administration of lipopolysaccharide exacerbates collagen-induced arthritis in mice. J Immunol 1999 : 163 : 3417 3422. (Pubitemid 29431845)