G(-) anaerobes-reactive CD4+ T-cells trigger RANKL-mediated enhanced alveolar bone loss in diabetic NOD mice

Diabetes

Volumn 54, Issue 5, 2005, Pages 1477-1486

  Mahamed, Deeqa A ^a,b   Marleau, Annette ^b   Alnaeeli, Mawadda ^a   Singh, Bhagirath ^b   Zhang, Xiaoxia ^a   Penninger, Joseph M ^c   Teng, Yen Tung Andy ^a,b,d  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^d UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GLUCOSE; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELLULAR IMMUNITY; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE SEVERITY; EXPERIMENTAL MOUSE; FEMALE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GRAM NEGATIVE ANAEROBIC BACTERIA; HIGH RISK POPULATION; INCIDENCE; INOCULATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; ONSET AGE; OSTEOLYSIS; PERIODONTITIS; PRIORITY JOURNAL; T LYMPHOCYTE;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ACTINOBACILLUS INFECTIONS; ALVEOLAR BONE LOSS; ANIMALS; BACTERIA, ANAEROBIC; CARRIER PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; GLYCOPROTEINS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED NOD; OSTEOPROTEGERIN; PREDIABETIC STATE; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, TUMOR NECROSIS FACTOR;

EID: 17844376542     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.54.5.1477     Document Type: Article

References (47)

1. Brown LJ, Loe H: Prevalence, extent, severity and progression of periodontal disease. Periodontol 2:57-71, 1993
2. Teng Y-T: The role of acquired immunity and periodontal disease progression. Crit Rev Oral Biol Med 14:237-252, 2003
3. Dzink JL, Tanner AC, Haffajee AD, Socransky SS: Gram negative species associated with active destructive periodontal lesions. J Clin Periodontol 12:648-659, 1985
4. Fives-Taylor PM, Meyer DH, Mintz KP, Brissette C: Virulence factors of Actinobacillus actinomycetemcomitans (Review). Periodontol 2000:136-167, 1999
5. Henderson B, Wilson M, Sharp L, Ward JM: Actinobacillus actinomycetemcomitans. J Med Microbiol 51:1013-1020, 2002
6. Teng YT, Hu W: Expression cloning of a periodontitis-associated apoptotic effector, cagE homologue, in Actinobacillus actinomycetemcomitans. Biochem Biophys Res Communs 303:1086-1094, 2003
7. Baker PJ: The role of immune responses in bone loss during periodontal disease (Review). Microbes Infect 2:1181-1192, 2000
8. Teng YT, Nguyen H, Gao X, Kong YY, Gorczynski RM, Singh B, Ellen RP, Penninger JM: Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. J Clin Invest 106:R59-R67, 2000.
9. Teng YT: Mixed periodontal Th1-Th2 cytokine profile in Actinobacillus actinomycetemcomitans-specific osteoprotegerin ligand (or RANK-L)-mediated alveolar bone destruction in vivo. Infect Immun 70:5269-5273, 2002
10. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ: Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176, 1998
11. Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R. McCabe S, Wong T, Campagnuolo G, Moran E, Bogoch ER, Van G, Nguyen LT, Ohashi PS, Lacey DL, Fish E, Boyle WJ, Penninger JM: Activated T-cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402:304-309, 1999
12. Theill LE, Boyle WJ, Penninger JM: RANK-L and RANK: T-cells, bone loss, and mammalian evolution. Annu Rev Immunol 20:795-823, 2002
13. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G, DeRose M, Elliott R, Colombero A, Tan HL, Trail G, Sullivan J, Davy E, Bucay N, Renshaw-Gegg L, Hughes TM, Hill D, Pattison W, Campbell P, Sander S, Van G, Tarpley J, Derby P, Lee R, Boyle WJ: Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89:309-319, 1997
14. Yun TJ, Tallquist MD, Aicher A, Rafferty KL, Marshall AJ, Moon JJ, Ewings ME, Mohaupt M, Herring SW, Clark EA: Osteoprotegerin, a crucial regulator of bone metabolism, also regulates B cell development and function. J Immunol 166:1482-1491, 2001
15. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, Morony S, Oliveira-dos-Santos AJ, Van G, Itie A, Khoo W, Wakeham A, Dunstan CR, Lacey DL, Mak TW, Boyle WJ, Penninger JM: OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397:315-323, 1999
16. Ogasawara T, Yoshimine Y, Kiyoshima T, Kobayashi I, Matsuo K, Akamine A, Sakai H: In situ expression of RANKL, RANK, osteoprotegerin and cytokines in osteoclasts of rat periodontal tissue. J Periodontal Res 39: 42-49, 2004
17. Wong FS, Janeway CA Jr: The role of CD4 and CD8 T-cells in type I diabetes in the NOD mouse. Res Immunol 28:327-332, 1997
18. Mottram PL, Murray-Segal LJ, Han W, Maguire J, Stein-Oakley A, Mandel TE: Long-term survival of segmental pancreas isografts in NOD/Lt mice treated with anti-CD4 and anti-CD8 monoclonal antibodies. Diabetes 47:1399-1405, 1998
19. Rabinovitch A: An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus. Diabetes Metab Rev 14:129-151, 1998
20. American Academy of Periodontology: Diabetes and periodontal diseases. J Periodontol 71:664-678, 2000
21. Grossi SG, Genco RJ: Periodontal disease and diabetes mellitus: a two-way relationship (Review). Ann Periodontol 3:51-61, 1998
22. Tervonen T, Karjalainen K, Knuuttila M, Huumonen S: Alveolar bone loss in type 1 diabetes subjects. J Clin Periodontol 27:567-571, 2000
23. Lalla E, Lamster IB, Feit M, Huang L, Spessot A, Qu W, Kislinger T, Lu Y, Stern DM, Schmidt AM: Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. J Clin Invest 105:1117-1124, 2000
24. Teng YT, Nguyen H, Hassanloo A, Ellen RP, Hozumi N, Gorczynski RM: Periodontal immune responses of human lymphocytes in Actinobacillus actinomycetemcomitans-inoculated NOD/SCID mice engrafted with peripheral blood leukocytes of periodontitis patients. J Periodontal Res 34:54-61, 1999
25. Cooke A, Tonks P, Jones FM, O'Shea H, Hutchings P, Fulford AJ, Dunne DW: Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol 21:169-176, 1999
26. Sadelain MW, Qin HY, Lauzon J, Singh B: Prevention of type I diabetes in NOD mice by adjuvant immunotherapy. Diabetes 39:583-589, 1990
27. Oldstone MB: Viruses as therapeutic agents. I. Treatment of nonobese insulin-dependent diabetes mice with virus prevents insulin-dependent diabetes mellitus while maintaining general immune competence. J Exp Med 171:2077-2089, 1990
28. Serreze DV, Hamaguchi K Leiter EH: Immunostimulation circumvents diabetes in NOD/Lt mice. J Autoimmun 2:759-776, 1989
29. Singh B, Prange S, Jevnikar AM: Protective and destructive effects of microbial infection in insulin-dependent diabetes mellitus. Semi Immunol 10:79-86, 1998
30. Sims TJ, Lernmark A, Mancl LA, Schifferle RE, Page RC, Persson GR: Serum IgG to heat shock proteins and Porphyromonas gingivalis antigens in diabetic patients with periodontitis. J Clin Periodontol 29:551-562, 2002
31. Lagervall M, Jansson L, Bergstrom J: Systemic disorders in patients with periodontal disease. J Clin Periodontol 30:293-299, 2003
32. Klausen B; Microbiological and immunological aspects of experimental periodontal disease in rats: a review article (Review). J Periodontol 62:59-73, 1991
33. Lin D, Smith MA, Elter J, Champagne C, Downey CL, Beck J, Offenbacher S: Porphyromonas gingivalis infection in pregnant mice is associated with placental dissemination, an increase in the placental Th1/Th2 cytokine ratio, and fetal growth restriction. Infect Immun 71:5163-5168, 2003
34. Firatli E: The relationship between clinical periodontal status and insulin-dependent diabetes mellitus: results after 5 years. J Periodontol 68:136-140, 1997
35. Tuominen R, Reunanen A, Paunio M, Paunio I, Aromaa A: Oral health indicators poorly predict coronary heart disease deaths. J Dent Res 82: 713-718, 2003
36. Horwood NJ, Kartsogiannis V, Quinn, JM, Romas E, Martin TJ, Gillespie MT: Activated T lymphocytes support osteoclast formation in vitro. Biochem Biophys Res Commun 265:144-150, 1999
37. Assuma R, Oates T, Cochran D, Amar S, Graves DT: IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immunol 160:403-409, 1998
38. Kobayashi K, Takahashi N, Jimi E, Udagawa N, Takami M, Kotake S, Nakagawa N, Kinosaki M, Yamaguchi K, Shima N, Yasuda H, Morinaga T, Higashio K, Martin TJ, Suda T: Tumor necrosis factor alpha stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL-RANK interaction. J Exp Med 191:275-286, 2000
39. Alonzi T, Fattori E, Lazzaro D, Costa P, Probert L, Kollias G, De Benedetti F, Poli V, Ciliberto G: Interleukin-6 is required for the development of collagen-induced arthritis. J Exp Med 187:461-468, 1998
40. Cameron MJ, Arreaza GA, Zucker P, Chensue SW, Strieter RM, Chakrabarti S, Delovitch TL: IL-4 prevents insulitis and insulin-dependent diabetes mellitus in nonobese diabetic mice by potentiation of regulatory T helper-2 cell function. J Immunol 159:4686-4692, 1997
41. + T-cells in Actinobacillus actinomycetemcomitans-infected LJP patients and LJP-derived, HuPBL-reconstituted NOD/SCID mice. J Periodontol Res 37:399-404, 2002
42. Yoshida K, Kikutani H: Genetic and immunological basis of autoimmunity in the NOD mouse. Rev Immunogenet 2:140-146, 2000
43. Zipris D, Lazarus AH, Crow AR, Hadzija M, Delovitch TL: Defective thymic T cell activation by concanavalin A and anti-CD3 in autoimmune nonobese diabetic mice. J Immunol 146:3763-3771, 1991
44. + immunregulatory T cells that control autoimmune diabetes. Immunity 12:431-440, 2000
45. Sharif S, Arreaza GA, Zucker P, Mi QS, Delovitch TL: Regulation of autoimmune disease by natural killer T cells. J Mol Med 80:290-300, 2002
46. Kishimoto H, Sprent J: A defect in central tolerance in NOD mice. Nat Immunol 2:1025-1031, 2001
47. Decallonne B, van Etten E, Giulietti A, Casteels K, Overbergh L, Bouillon R, Mathieu C: Defect in activation-induced cell death in non-obese diabetic (NOD) T lymphocytes. J Autoimmun 20:219-226, 2003