Periodontitis in the absence of B cells and specific anti-bacterial antibody

Molecular Oral Microbiology

Volumn 30, Issue 2, 2015, Pages 160-169

  Oliver Bell, J ^a   Butcher, J P ^b   Malcolm, J ^a   Macleod, M K L ^a   Adrados Planell, A ^a   Campbell, L ^a   Nibbs, R J B ^a   Garside, P ^a   Mcinnes, I B ^a   Culshaw, S ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF THE WEST OF SCOTLAND   (United Kingdom)

Author keywords

B cells; Murine models; Periodontitis

Indexed keywords

BACTERIUM ANTIBODY; IMMUNOGLOBULIN G; OSTEOCLAST DIFFERENTIATION FACTOR; TNFSF11 PROTEIN, MOUSE;

ALVEOLAR BONE; ALVEOLAR BONE LOSS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CERVICAL LYMPH NODE; COMPARATIVE STUDY; CONTROLLED STUDY; EFFECTOR CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GINGIVA; LYMPHOCYTE SUBPOPULATION; MEMORY CELL; MOUSE; NONHUMAN; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PROTEIN EXPRESSION; T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY;

ALVEOLAR BONE LOSS; ANIMALS; ANTIBODIES, BACTERIAL; B-LYMPHOCYTES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GINGIVA; IMMUNOGLOBULIN G; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PORPHYROMONAS GINGIVALIS; RANK LIGAND;

EID: 84924420947     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/omi.12082     Document Type: Article

References (44)

1. Apatzidou, D.A., Riggio, M.P. and Kinane, D.F. (2005) Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J Clin Periodontol 32: 973-983.
2. Baker, P.J., Evans, R.T. and Roopenian, D.C. (1994) Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 39: 1035-1040.
3. + T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 67: 2804-2809.
4. Baker, P.J., Howe, L., Garneau, J. and Roopenian, D.C. (2002) T cell knockout mice have diminished alveolar bone loss after oral infection with Porphyromonas gingivalis. FEMS Immunol Med Microbiol 34: 45-50.
5. Baker, P.J., Boutaugh, N.R., Tiffany, M. and Roopenian, D.C. (2009) B Cell IgD deletion prevents alveolar bone loss following murine oral infection. Interdisc Persp Infect Dis 2009: 1-6.
6. Belibasakis, G.N., Reddi, D. and Bostanci, N. (2011) Porphyromonas gingivalis induces RANKL in T-cells. Inflammation 34: 133-138.
7. Berglundh, T. and Donati, M. (2005) Aspects of adaptive host response in periodontitis. J Clin Periodontol 32(Suppl 6): 87-107.
8. Berglundh, T., Liljenberg, B., Tarkowski, A. and Lindhe, J. (2002) The presence of local and circulating autoreactive B cells in patients with advanced periodontitis. J Clin Periodontol 29: 281-286.
9. Brandtzaeg, P. (2013) Secretory immunity with special reference to the oral cavity. J Oral Microbiol 5: 20401.
10. Cao, D., Khmaladze, I., JIA, H. et al. (2011) Pathogenic autoreactive B cells are not negatively selected toward matrix protein collagen II. J Immunol 187: 4451-4458.
11. Crawford, A., Macleod, M., Schumacher, T., Corlett, L., Gray, D. (2006) Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells. J Immunol 176: 3498-3506.
12. Dal Porto, J.M., Haberman, A.M., Shlomchik, M.J. and Kelsoe, G. (1998) Antigen drives very low affinity B cells to become plasmacytes and enter germinal centers. J Immunol 161: 5373-5381.
13. Donati, M., Liljenberg, B., Zitzmann, N.U. and Berglundh, T. (2009) B-1a cells in experimental gingivitis in humans. J Periodontol 80: 1141-1145.
14. Fagarasan, S., Watanabe, N. and Honjo, T. (2000) Generation, expansion, migration and activation of mouse B1 cells. Immunol Rev 176: 205-215.
15. Gemmell, E., Carter, C.L., Hart, D.N., Drysdale, K.E. and Seymour, G.J. (2002) Antigen-presenting cells in human periodontal disease tissues. Oral Microbiol Immunol 17: 388-393.
16. Gmur, R., Hrodek, K., Saxer, U.P. and Guggenheim, B. (1986) Double-blind analysis of the relation between adult periodontitis and systemic host response to suspected periodontal pathogens. Infect Immun 52: 768-776.
17. Gumus, P., Nizam, N., Lappin, D.F. and Buduneli, N. (2014) Saliva and serum levels of B-cell activating factors and tumor necrosis factor-alpha in patients with periodontitis. J Periodontol 85: 270-280.
18. Han, X., Kawai, T., Eastcott, J.W. and Taubman, M.A. (2006) Bacterial-responsive B lymphocytes induce periodontal bone resorption. J Immunol 176: 625-631.
19. Han, X., Lin, X., Seliger, A.R., Eastcott, J., Kawai, T. and Taubman, M.A. (2009) Expression of receptor activator of nuclear factor-κB ligand by B cells in response to oral bacteria. Oral Microbiol Immunol 24: 190-196.
20. Han, X., Lin, X., Yu, X. et al. (2013) Porphyromonas gingivalis infection-associated periodontal bone resorption is dependent on receptor activator of NF-kappaB ligand. Infect Immun, 81: 1502-1509.
21. Harvey, G.P., Fitzsimmons, T.R., Dhamarpatni, A.A., Marchant, C., Haynes, D.R. and Bartold, P.M. (2013) Expression of peptidylarginine deiminase-2 and -4, citrullinated proteins and anti-citrullinated protein antibodies in human gingiva. J Periodontal Res 48: 252-261.
22. Hirsch, H.Z., Tarkowski, A., Miller, E.J., Gay, S., Koopman, W.J. and Mestecky, J. (1988) Autoimmunity to collagen in adult periodontal disease. J Oral Pathol 17: 456-459.
23. Kaur, S., White, S. and Bartold, P.M. (2013) Periodontal disease and rheumatoid arthritis: a systematic review. J Dent Res 92: 399-408.
24. Kawai, T., Matsuyama, T., Hosokawa, Y. et al. (2006) B and T Lymphocytes Are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 169: 987-998.
25. Kinane, D.F., Preshaw, P.M. and Loos, B.G. (2011) Host-response: understanding the cellular and molecular mechanisms of host-microbial interactions - Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol 38: 44-48.
26. Kitamura, D., Roes, J., Kuhn, R. and Rajewsky, K. (1991) A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350: 423-426.
27. Klareskog, L., Ronnelid, J., Lundberg, K., Padyukov, L. and Alfredsson, L. (2008) Immunity to citrullinated proteins in rheumatoid arthritis. Annu Rev Immunol 26: 651-675.
28. Lappin, D.F., Apatzidou, D., Quirke, A.M. et al. (2013) Influence of periodontal disease, Porphyromonas gingivalis and cigarette smoking on systemic anti-citrullinated peptide antibody titres. J Clin Periodontol, 40: 907-915.
29. Li, Y., Toraldo, G., Li, A. et al. (2007) B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood, 109: 3839-3848.
30. Mackler, B.F., Frostad, K.B., Robertson, P.B. and Levy, B.M. (1977) Immunoglobulin bearing lymphocytes and plasma cells in human periodontal disease. J Periodontal Res, 12: 37-45.
31. Macaulay, A.E., DeKruyff, R.H., Goodnow, C.C., Umetsu, D.T. (1997) Antigen-specific B cells preferentially induce CD4+ T cells to produce IL-4. J Immunol 158: 4171-4179.
32. Manilay, J.O. and Zouali, M. (2014) Tight relationships between B lymphocytes and the skeletal system. Trends Mol Med 20: 405-412.
33. Mollo, S.B., Zajac, A.J. and Harrington, L.E. (2013) Temporal requirements for B cells in the establishment of CD4 T cell memory. J Immunol 191: 6052-6059.
34. Mooney, J., Adonogianaki, E. and Kinane, D.F. (1993) Relative avidity of serum antibodies to putative periodontopathogens in periodontal disease. J Periodontal Res 28: 444-450.
35. Moutsopoulos, N.M. and Madianos, P.N. (2006) Low-grade inflammation in chronic infectious diseases: paradigm of periodontal infections. Ann N Y Acad Sci 1088: 251-264.
36. Naito, Y., Takematsu, H., Koyama, S. et al. (2007) Germinal center marker GL7 probes activation-dependent repression of N-glycolylneuraminic acid, a sialic acid species involved in the negative modulation of B-cell activation. Mol Cell Biol, 27: 3008-3022.
37. Okada, M., Kobayashi, T., Ito, S. et al. (2013) Periodontal treatment decreases levels of antibodies to Porphyromonas Gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol 84: e74-e84.
38. de Pablo, P., Dietrich, T., Chapple, I.L. et al. (2014) The autoantibody repertoire in periodontitis: a role in the induction of autoimmunity to citrullinated proteins in rheumatoid arthritis? Ann Rheum Dis 73: 580-586.
39. Seymour, G.J. and Greenspan, J.S. (1979) The phenotypic characterization of lymphocyte subpopulations in established human periodontal disease. J Periodontal Res 14: 39-46.
40. Takahashi, Y., Ohta, H. and Takemori, T. (2001) Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 14: 181-192.
41. Takeuchi, Y., Aramaki, M., Nagasawa, T., Umeda, M., Oda, S. and Ishikawa, I. (2006) Immunoglobulin G subclass antibody profiles in Porphyromonas gingivalis-associated aggressive and chronic periodontitis patients. Oral Microbiol Immunol 21: 314-318.
42. Wara-Aswapati, N., Surarit, R., Chayasadom, A., Boch, J.A. and Pitiphat, W. (2007) RANKL upregulation associated with periodontitis and Porphyromonas gingivalis. J Periodontol 78: 1062-1069.
43. Yasuda, H., Shima, N., Nakagawa, N. et al. (1999) A novel molecular mechanism modulating osteoclast differentiation and function. Bone 25: 109-113.
44. Yuan, H., Gupte, R., Zelkha, S. and Amar, S. (2011) Receptor activator of nuclear factor kappa B ligand antagonists inhibit tissue inflammation and bone loss in experimental periodontitis. J Clin Periodontol 38: 1029-1036.