Archives of Oral Biology
Volume 55, Issue 5 , Pages 379-384 , May 2010

The effect of systemic anti-tumor necrosis factor-alpha treatment on Porphyromonas gingivalis infection in type 2 diabetic mice

  • Mayuko Takano

      Affiliations

    • Nihon University Graduate School of Dentistry, Tokyo, Japan
  • ,
  • Rieko Nishihara

      Affiliations

    • Department of Periodontology, Nihon University School of Dentistry, Tokyo, Japan
  • ,
  • Naoyuki Sugano

      Affiliations

    • Department of Periodontology, Nihon University School of Dentistry, Tokyo, Japan
    • Division of Advanced Dental Treatment, Dental Research Center, Nihon University School of Dentistry, Tokyo, Japan
    • Corresponding Author InformationCorresponding author at: Department of Periodontology Nihon University School of Dentistry, 1-8-13, Kanda-Surugadai, Chiyoda-ku, Tokyo 101-8310, Japan. Tel.: +81 3 3219 8107; fax: +81 3 3219 8349.
  • ,
  • Kazuma Matsumoto

      Affiliations

    • Department of Periodontology, Nihon University School of Dentistry, Tokyo, Japan
  • ,
  • Yutaka Yamada

      Affiliations

    • Department of Periodontology, Nihon University School of Dentistry, Tokyo, Japan
    • Division of Advanced Dental Treatment, Dental Research Center, Nihon University School of Dentistry, Tokyo, Japan
  • ,
  • Masatoshi Takane

      Affiliations

    • Department of Periodontology, Nihon University School of Dentistry, Tokyo, Japan
    • Division of Advanced Dental Treatment, Dental Research Center, Nihon University School of Dentistry, Tokyo, Japan
  • ,
  • Yoshiaki Fujisaki

      Affiliations

    • Department of Periodontology, Nihon University School of Dentistry, Tokyo, Japan
  • ,
  • Koichi Ito

      Affiliations

    • Department of Periodontology, Nihon University School of Dentistry, Tokyo, Japan
    • Division of Advanced Dental Treatment, Dental Research Center, Nihon University School of Dentistry, Tokyo, Japan

,Accepted 5 March 2010.

References 

  1. Argilés JM, López-Soriano J, López-Soriano FJ. Cytokines and diabetes: the final step? Involvement of TNF-α in both type I and II diabetes mellitus. Horm Metab Res. 1994;26:447–449
  2. Lang CH, Dobrescu C, Bagby GJ. Tumor necrosis factor impairs insulin action on peripheral glucose disposal and hepatic glucose output. Endocrinology. 1992;130:43–52
  3. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-α- and obesity-induced insulin resistance. Science. 1996;271:665–668
  4. Kroder G, Bossenmaier B, Kellerer M, Capp E, Stoyanov B, Mühlhöfer A, et al. Tumor necrosis factor-α- and hyperglycemia-induced insulin resistance. Evidence for different mechanisms and different effects on insulin signaling. J Clin Invest. 1996;97:1471–1477
  5. Bruun JM, Verdich C, Toubro S, Astrup A, Richelsen B. Association between measures of insulin sensitivity and circulating levels of interleukin-8, interleukin-6 and tumor necrosis factor-α. Effect of weight loss in obese men. Eur J Endocrinol. 2003;148:535–542
  6. Mishima Y, Kuyama A, Tada A, Takahashi K, Ishioka T, Kibata M. Relationship between serum tumor necrosis factor-α and insulin resistance in obese men with Type 2 diabetes mellitus. Diabetes Res Clin Pract. 2001;52:119–123
  7. Fernandez-Real JM, Lainez B, Vendrell J, Rigla M, Castro A, Peñarroja G, et al. Shedding of TNF-α receptors, blood pressure, and insulin sensitivity in type 2 diabetes mellitus. Am J Physiol Endocrinol Metab. 2002;282:E952–E959
  8. Lechleitner M, Herold M, Dzien-Bischinger C, Hoppichler F, Dzien A. Tumour necrosis factor-α plasma levels in elderly patients with type 2 diabetes mellitus-observations over 2 years. Diabetes Med. 2002;19:949–953
  9. Hugoson A, Thorstensson H, Falk H, Kuylenstierna J. Periodontal conditions in insulin-dependent diabetics. J Clin Periodontol. 1989;16:215–223
  10. Nelson RG, Shlossman M, Budding LM, Pettitt DJ, Saad MF, Genco RJ, et al. Periodontal disease and NIDDM in Pima Indians. Diabetes Care. 1990;13:836–840
  11. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in non-insulin-dependent diabetes mellitus. J Periodontol. 1991;62:123–131
  12. Oliver RC, Tervonen T. Periodontitis and tooth loss: comparing diabetics with the general population. J Am Dent Assoc. 1993;124:71–76
  13. Grossi SG, Zambon JJ, Ho AW, Koch G, Dunford RG, Machtei EE, et al. Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol. 1994;65:260–267
  14. Papapanou PN. Periodontal diseases: epidemiology. Ann Periodontol. 1996;1:1–36
  15. Nishimura F, Iwamoto Y, Mineshiba J, Shimizu A, Soga Y, Murayama Y. Periodontal disease and diabetes mellitus: the role of tumor necrosis factor-α in a 2-way relationship. J Periodontol. 2003;74:97–102
  16. Graves DT. The potential role of chemokines and inflammatory cytokines in periodontal disease progression. Clin Infect Dis. 1999;28:482–490
  17. Bretz WA, Weyant RJ, Corby PM, Ren D, Weissfeld L, Kritchevsky SB, et al. Systemic inflammatory markers, periodontal diseases, and periodontal infections in an elderly population. J Am Geriatr Soc. 2005;53:1532–1537
  18. Engebretson1 S, Chertog R, Nichols A, Hey-Hadavi J, Celenti R, Grbic J. Plasma levels of tumour necrosis factor-alpha in patients with chronic periodontitis and type 2 diabetes. J Clin Periodontol. 2007;34:18–24
  19. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance. Science. 1993;259:87–91
  20. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-α in human obesity and insulin resistance. J Clin Invest. 1995;95:2409–2415
  21. Grimble RF. Inflammatory status and insulin resistance. Curr Opin Clin Nutr Metab Care. 2002;5:551–559
  22. Fernández-Real JM, Ricart W. Insulin resistance and chronic cardiovascular inflammatory syndrome. Endocr Rev. 2003;24:278–301
  23. Iwatsuka H, Shino A, Suzuoki Z. General survey of diabetic features of yellow KK mice. Endocrinol Jpn. 1970;17:23–35
  24. Graves DT, Oskoui M, Volejnikova S, Naguib G, Cai S, Desta T, et al. Tumor necrosis factor modulates fibroblast apoptosis. PMN recruitment, and osteoclast formation in response to P. gingivalis infection. J Dent Res. 2001;80:1875–1879
  25. Leone CW, Bokhadhoor H, Kuo D, Desta T, Yang J, Siqueira MF, et al. Immunization enhances inflammation and tissue destruction in response to Porphyromonas gingivalis. Infect Immun. 2006;74:2286–2292
  26. Nishihara R, Sugano N, Takano M, Shimada T, Tanaka H, Oka S, et al. The effect of Porphyromonas gingivalis infection on cytokine levels in type 2 diabetic mice. J Periodontal Res. 2009;44:305–310
  27. Huang X, McClellan SA, Barrett RP, Hazlett LD. IL-18 contributes to host resistance against infection with Pseudomonas aeruginosa through induction of IFN-gamma production. J Immunol. 2002;168:5756–5763
  28. Hotamisligil GS, Budavari A, Murray D, Spiegelman BM. Reduced tyrosine kinase activity of the insulin receptor in obesity-diabetes. Central role of tumor necrosis factor-α. J Clin Invest. 1994;94:1543–1549
  29. Cheung AT, Wang J, Ree D, Kolls JK, Bryer-Ash M. Tumor necrosis factor-α induces hepatic insulin resistance in obese Zucker (fa/fa) rats via interaction of leukocyte antigen-related tyrosine phosphatase with focal adhesion kinase. Diabetes. 2000;49:810–819
  30. Ruan H, Lodish HF. Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor-α. Cytokine Growth Factor Rev. 2003;14:447–455
  31. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-α function. Nature. 1997;389:610–614
  32. Yazdani-Biuki B, Stelzl H, Brezinschek HP, Hermann J, Mueller T, Krippl P, et al. Improvement of insulin sensitivity in insulin resistant subjects during prolonged treatment with the anti-TNF-α antibody infliximab. Eur J Clin Invest. 2004;34:641–642
  33. Gonzalez-Gay MA, De Matias JM, Gonzalez-Juanatey C, Garcia-Porrua C, Sanchez-Andrade A, Martin J, et al. Anti-tumor necrosis factor-α blockade improves insulin resistance in patients with rheumatoid arthritis. Clin Exp Rheumatol. 2006;24:83–86
  34. Scott DL, Kingsley GH. Tumor necrosis factor inhibitors for rheumatoid arthritis. N Engl J Med. 2006;355:704–712
  35. Yazdani-Biuki B, Mueller T, Brezinschek HP, Hermann J, Graninger W, Wascher TC. Relapse of diabetes after interruption of chronic administration of anti-tumor necrosis factor-α antibody infliximab: a case observation. Diabetes Care. 2006;29:1712–1713
  36. Liu R, Bal HS, Desta T, Behl Y, Graves DT. Tumor necrosis factor-α mediates diabetes-enhanced apoptosis of matrix-producing cells and impairs diabetic healing. Am J Pathol. 2006;168:757–764

PII: S0003-9969(10)00055-5

doi: 10.1016/j.archoralbio.2010.03.004

Archives of Oral Biology
Volume 55, Issue 5 , Pages 379-384 , May 2010