The emerging roles of B cells as partners and targets in periodontitis

References

• Irfan, U. M., D. V. Dawson, and N. F. Bissada. 2001. Epidemiology of periodontal disease: a review and clinical perspectives. J. Int. Acad. Periodontol. 3: 14–21
   PubMedGoogle Scholar
• Jonsson, R., A. Pitts, C. Lue, et al. 1991. Immunoglobulin isotype distribution of locally produced autoantibodies to collagen type I in adult periodontitis. Relationship to periodontal treatment. J. Clin. Periodontol. 18: 703–707
   PubMed Web of Science ®Google Scholar
• Kayal, R. A. 2013. The role of osteoimmunology in periodontal disease. Biomed. Res. Int. 2013: 639368
   PubMed Web of Science ®Google Scholar
• Seymour, G. J., R. N. Powell, K. L. Cole, et al. 1983. Experimental gingivitis in humans. A histochemical and immunological characterization of the lymphoid cell subpopulations. J. Periodont. Res. 18: 375–385
   PubMed Web of Science ®Google Scholar
• Zhu, M., A. C. Belkina, J. DeFuria, et al. 2014. B cells promote obesity-associated periodontitis and oral pathogen-associated inflammation. J. Leukoc. Biol. 96: 349–357
   PubMed Web of Science ®Google Scholar
• Mackler, B. F., K. B. Frostad, P. B. Robertson, and B. M. Levy. 1977. Immunoglobulin bearing lymphocytes and plasma cells in human periodontal disease. J. Periodont. Res. 12: 37–45
   PubMed Web of Science ®Google Scholar
• Sugawara, M., K. Yamashita, H. Yoshie, and K. Hara. 1992. Detection of, and anti-collagen antibody produced by, CD5-positive B cells in inflamed gingival tissues. J. Periodont. Res. 27: 489–498
   PubMed Web of Science ®Google Scholar
• Seymour, G. J., and J. S. Greenspan. 1979. The phenotypic characterization of lymphocyte subpopulations in established human periodontal disease. J. Periodont. Res. 14: 39–46
   PubMed Web of Science ®Google Scholar
• Berglundh, T., M. Donati, and N. Zitzmann. 2007. B cells in periodontitis: friends or enemies? Periodontology. 2000. 45: 51–66
   PubMed Web of Science ®Google Scholar
• Hirsch, H. Z., A. Tarkowski, E. J. Miller, et al. 1988. Autoimmunity to collagen in adult periodontal disease. J. Oral Pathol. 17: 456–459
   PubMedGoogle Scholar
• Stoufi, E. D., M. A. Taubman, J. L. Ebersole, et al. 1987. Phenotypic analyses of mononuclear cells recovered from healthy and diseased human periodontal tissues. J. Clin. Immunol. 7: 235–245
   PubMed Web of Science ®Google Scholar
• McArthur, W. P., and W. B. Clark. 1993. Specific antibodies and their potential role in periodontal diseases. J. Periodontol. 64: 807–818
   PubMed Web of Science ®Google Scholar
• Apatzidou, D. A., M. P. Riggio, and D. F. Kinane. 2005. Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J. Clin. Periodontol. 32: 973–983
   PubMed Web of Science ®Google Scholar
• Murray, P. A., D. A. Burstein, and J. R. Winkler. 1989. Antibodies to Bacteroides gingivalis in patients with treated and untreated periodontal disease. J. Periodontol. 60: 96–103
   PubMed Web of Science ®Google Scholar
• Harada, Y., X. Han, K. Yamashita, et al. 2006. Effect of adoptive transfer of antigen-specific B cells on periodontal bone resorption. J. Periodont. Res. 41: 101–107
   PubMed Web of Science ®Google Scholar
• Meghji, S., B. Henderson, and M. Wilson. 1993. Higher-titer antisera from patients with periodontal disease inhibit bacterial capsule-induced bone breakdown. J. Periodont. Res. 28: 115–121
   PubMed Web of Science ®Google Scholar
• Wheeler, T. T., W. P. McArthur, I. Magnusson, et al. 1994. Modeling the relationship between clinical, microbiologic, and immunologic parameters and alveolar bone levels in an elderly population. J. Periodontol. 65: 68–78
   PubMed Web of Science ®Google Scholar
• Klausen, B., H. P. Hougen, and N. E. Fiehn. 1989. Increased periodontal bone loss in temporarily B lymphocyte-deficient rats. J. Periodont. Res. 24: 384–390
   PubMed Web of Science ®Google Scholar
• Kaur, S., S. White, and P. M. Bartold. 2013. Periodontal disease and rheumatoid arthritis: a systematic review. J. Dent. Res. 92: 399–408
   PubMed Web of Science ®Google Scholar
• Harvey, G. P., T. R. Fitzsimmons, A. A. Dhamarpatni, et al. 2013. Expression of peptidylarginine deiminase-2 and -4, citrullinated proteins and anti-citrullinated protein antibodies in human gingiva. J. Periodont. Res. 48: 252–261
   PubMed Web of Science ®Google Scholar
• Lappin, D. F., D. Apatzidou, A. M. Quirke, 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
   PubMed Web of Science ®Google Scholar
• de Pablo, P., T. Dietrich, I. L. Chapple, 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
   PubMed Web of Science ®Google Scholar
• Reinhardt, R. A., R. W. Bolton, T. L. McDonald, et al. 1988. In situ lymphocyte subpopulations from active versus stable periodontal sites. J. Periodontol. 59: 656–670
   PubMed Web of Science ®Google Scholar
• Han, X., T. Kawai, J. W. Eastcott, and M. A. Taubman. 2006. Bacterial-responsive B lymphocytes induce periodontal bone resorption. J. Immunol. 176: 625–631
   PubMed Web of Science ®Google Scholar
• Baker, P. J., N. R. Boutaugh, M. Tiffany, and D. C. Roopenian. 2009. B cell IgD deletion prevents alveolar bone loss following murine oral infection. Interdiscip. Perspect. Infect. Dis. 2009: 864359
   PubMedGoogle Scholar
• Oliver-Bell, J., J. P. Butcher, J. Malcolm, et al. 2015. Periodontitis in the absence of B cells and specific anti-bacterial antibody. Mol. Oral. Microbiol. 30: 160–169
   PubMed Web of Science ®Google Scholar
• Kitamura, D., J. Roes, R. Kuhn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature. 350: 423–426
   PubMed Web of Science ®Google Scholar
• Hajishengallis, G., and J. M. Korostoff. 2015. Response to comment on “The B cell-stimulatory cytokines BLyS and APRIL are elevated in human periodontitis and are required for B cell-dependent bone loss in experimental murine periodontitis”. J. Immunol. 195: 5099–5100
   PubMed Web of Science ®Google Scholar
• Johansson, N., M. Ahonen, and V. M. Kahari. 2000. Matrix metalloproteinases in tumor invasion. Cell. Mol. Life Sci. 57: 5–15
   PubMed Web of Science ®Google Scholar
• Lopez-Otin, C., and C. M. Overall. 2002. Protease degradomics: a new challenge for proteomics. Nat. Rev. Mol. Cell Biol. 3: 509–519
   PubMed Web of Science ®Google Scholar
• Kowashi, Y., F. Jaccard, and G. Cimasoni. 1979. Increase of free collagenase and neutral protease activities in the gingival crevice during experimental gingivitis in man. Arch. Oral Biol. 24: 645–650
   PubMed Web of Science ®Google Scholar
• Ohlsson, K., I. Olsson, and G. Tynelius-Bratthall. 1974. Neutrophil leukocyte collagenase, elastase and serum protease inhibitors in human gingival crevicles. Acta Odontol. Scand. 32: 51–59
   PubMed Web of Science ®Google Scholar
• Haerian, A., E. Adonogianaki, J. Mooney, et al. 1996. Effects of treatment on gingival crevicular collagenase, stromelysin and tissue inhibitor of metalloproteinases and their ability to predict response to treatment. J. Clin. Periodontol. 23: 83–91
   PubMed Web of Science ®Google Scholar
• Di Girolamo, N., N. Tedla, A. Lloyd, and D. Wakefield. 1998. Expression of matrix metalloproteinases by human plasma cells and B lymphocytes. Eur. J. Immunol. 28: 1773–1784
   PubMed Web of Science ®Google Scholar
• Wahlgren, J., P. Maisi, T. Sorsa, et al. 2001. Expression and induction of collagenases (MMP-8 and -13) in plasma cells associated with bone-destructive lesions. J. Pathol. 194: 217–224
   PubMed Web of Science ®Google Scholar
• Gupta, N., N. D. Gupta, A. Gupta, et al. 2015. Role of salivary matrix metalloproteinase-8 (MMP-8) in chronic periodontitis diagnosis. Front. Med. 9: 72–76
   PubMed Web of Science ®Google Scholar
• Johnson, N., J. L. Ebersole, R. J. Kryscio, et al. 2016. Rapid assessment of salivary MMP-8 and periodontal disease using lateral flow immunoassay. Oral Dis. 22: 681–687
   PubMed Web of Science ®Google Scholar
• Manilay, J. O., and M. Zouali. 2014. Tight relationships between B lymphocytes and the skeletal system. Trends Mol. Med. 20: 405–412
   PubMed Web of Science ®Google Scholar
• Choi, Y., K. M. Woo, S. H. Ko, et al. 2001. Osteoclastogenesis is enhanced by activated B cells but suppressed by activated CD8(+) T cells. Eur. J. Immunol. 31: 2179–2188
   PubMed Web of Science ®Google Scholar
• Karsenty, G. 2003. The complexities of skeletal biology. Nature. 423: 316–318
   PubMed Web of Science ®Google Scholar
• Kong, Y. Y., U. Feige, I. Sarosi, et al. 1999. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature. 402: 304–309
   PubMed Web of Science ®Google Scholar
• Lacey, D. L., E. Timms, H. L. Tan, et al. 1998. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 93: 165–176
   PubMed Web of Science ®Google Scholar
• Garlet, G. P., C. R. Cardoso, T. A. Silva, et al. 2006. Cytokine pattern determines the progression of experimental periodontal disease induced by Actinobacillus actinomycetemcomitans through the modulation of MMPs, RANKL, and their physiological inhibitors. Oral Microbiol. Immunol. 21: 12–20
   PubMedGoogle Scholar
• Jin, Q., J. A. Cirelli, C. H. Park, et al. 2007. RANKL inhibition through osteoprotegerin blocks bone loss in experimental periodontitis. J. Periodontol. 78: 1300–1308
   PubMed Web of Science ®Google Scholar
• Crotti, T., M. D. Smith, R. Hirsch, et al. 2003. Receptor activator NF kappaB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. J. Periodont. Res. 38: 380–387
   PubMed Web of Science ®Google Scholar
• Kawai, T., T. Matsuyama, Y. Hosokawa, 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
   PubMed Web of Science ®Google Scholar
• Wara-aswapati, N., R. Surarit, A. Chayasadom, et al. 2007. RANKL upregulation associated with periodontitis and Porphyromonas gingivalis. J. Periodontol. 78: 1062–1069
   PubMed Web of Science ®Google Scholar
• Belibasakis, G. N., and N. Bostanci. 2012. The RANKL-OPG system in clinical periodontology. J. Clin. Periodontol. 39: 239–248
   PubMed Web of Science ®Google Scholar
• Zouali, M. 2002. B cell diversity and longevity in systemic autoimmunity. Mol. Immunol. 38: 895–901
   PubMed Web of Science ®Google Scholar
• Abe, T., M. AlSarhan, M. R. Benakanakere, et al. 2015. The B cell-stimulatory cytokines BLyS and APRIL are elevated in human periodontitis and are required for B cell-dependent bone loss in experimental murine periodontitis. J. Immunol. 195: 1427–1435
   PubMed Web of Science ®Google Scholar
• Ftis, A., G. Singh, and A. E. Dolby. 1986. Antibody to collagen type I in periodontal disease. J. Periodontol. 57: 693–698
   PubMed Web of Science ®Google Scholar
• Anusaksathien, O., G. Singh, N. Matthews, and A. E. Dolby. 1992. Autoimmunity to collagen in adult periodontal disease: immunoglobulin classes in sera and tissue. J. Periodont. Res. 27: 55–61
   PubMed Web of Science ®Google Scholar
• Tabeta, K., K. Yamazaki, H. Hotokezaka, et al. 2000. Elevated humoral immune response to heat shock protein 60 (hsp60) family in periodontitis patients. Clin. Exp. Immunol. 120: 285–293
   PubMed Web of Science ®Google Scholar
• Rajapakse, P. S., and A. E. Dolby. 2004. Evidence for local production of antibodies to auto and non-self antigens in periodontal disease. Oral Dis. 10: 99–105
   PubMed Web of Science ®Google Scholar
• Govze, Y., and M. C. Herzberg. 1993. Serum and gingival crevicular fluid anti-desmosomal antibodies in periodontitis. J. Periodontol. 64: 603–608
   PubMed Web of Science ®Google Scholar
• Novo, E., E. Garcia-MacGregor, N. Viera, et al. 1999. Periodontitis and anti-neutrophil cytoplasmic antibodies in systemic lupus erythematosus and rheumatoid arthritis: a comparative study. J. Periodontol. 70: 185–188
   PubMed Web of Science ®Google Scholar
• Schenkein, H. A., C. R. Berry, J. A. Burmeister, et al. 2003. Anti-cardiolipin antibodies in sera from patients with periodontitis. J. Dent. Res. 82: 919–922
   PubMed Web of Science ®Google Scholar
• Koutouzis, T., D. Haber, L. Shaddox, et al. 2009. Autoreactivity of serum immunoglobulin to periodontal tissue components: a pilot study. J. Periodontol. 80: 625–633
   PubMed Web of Science ®Google Scholar
• Serreze, D. V., S. A. Fleming, H. D. Chapman, et al. 1998. B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J. Immunol. 161: 3912–3918
   PubMed Web of Science ®Google Scholar
• Jagannathan, M., H. Hasturk, Y. Liang, et al. 2009. TLR cross-talk specifically regulates cytokine production by B cells from chronic inflammatory disease patients. J. Immunol. 183: 7461–7470
   PubMed Web of Science ®Google Scholar
• Wara-aswapati, N., A. Chayasadom, R. Surarit, et al. 2013. Induction of toll-like receptor expression by Porphyromonas gingivalis. J. Periodontol. 84: 1010–1018
   PubMed Web of Science ®Google Scholar
• Zouali, M. 1995. Human pathogenic autoantibodies and their escape from deletion. Ann. N. Y. Acad. Sci. 764: 436–439
   PubMed Web of Science ®Google Scholar
• Kurien, B. T., and R. H. Scofield. 2008. Autoimmunity and oxidatively modified autoantigens. Autoimmun. Rev. 7: 567–573
   PubMed Web of Science ®Google Scholar
• Vanderlugt, C. L., and S. D. Miller. 2002. Epitope spreading in immune-mediated diseases: implications for immunotherapy. Nat. Rev. Immunol. 2: 85–95
   PubMed Web of Science ®Google Scholar
• Jeong, E., J. Y. Lee, S. J. Kim, and J. Choi. 2012. Predominant immunoreactivity of Porphyromonas gingivalis heat shock protein in autoimmune diseases. J. Periodont. Res. 47: 811–816
   PubMed Web of Science ®Google Scholar
• Kwon, E. Y., G. S. Cha, E. Jeong, et al. 2016. Pep19 drives epitope spreading in periodontitis and periodontitis-associated autoimmune diseases. J. Periodont. Res. 51: 381–394
   PubMed Web of Science ®Google Scholar
• Hendler, A., T. K. Mulli, F. J. Hughes, et al. 2010. Involvement of autoimmunity in the pathogenesis of aggressive periodontitis. J. Dent. Res. 89: 1389–1394
   PubMed Web of Science ®Google Scholar
• Klareskog, L., J. Ronnelid, K. Lundberg, et al. 2008. Immunity to citrullinated proteins in rheumatoid arthritis. Annu. Rev. Immunol. 26: 651–675
   PubMed Web of Science ®Google Scholar
• Viau, M., and M. Zouali. 2005. B-lymphocytes, innate immunity, and autoimmunity. Clin. Immunol. 114: 17–26
   PubMed Web of Science ®Google Scholar
• Hikada, M., and M. Zouali. 2010. Multistoried roles for B lymphocytes in autoimmunity. Nat. Immunol. 11: 1065–1068
   PubMedGoogle Scholar
• Zouali, M. 2014. Tweaking the B lymphocyte compartment in autoimmune diseases. Nat. Immunol. 15: 209–212
   PubMed Web of Science ®Google Scholar
• Zouali, M., and Y. Richard. 2011. Marginal zone B-cells, a gatekeeper of innate immunity. Front. Immun. 2: 63
   PubMed Web of Science ®Google Scholar
• Afar, B., D. Engel, and E. A. Clark. 1992. Activated lymphocyte subsets in adult periodontitis. J. Periodont. Res. 27: 126–133
   PubMed Web of Science ®Google Scholar
• Albandar, J. M., C. F. Streckfus, M. R. Adesanya, and D. M. Winn. 2000. Cigar, pipe, and cigarette smoking as risk factors for periodontal disease and tooth loss. J. Periodontol. 71: 1874–1881
   PubMed Web of Science ®Google Scholar
• Berglundh, T., B. Liljenberg, A. Tarkowski, and J. Lindhe. 2002. The presence of local and circulating autoreactive B cells in patients with advanced periodontitis. J. Clin. Periodontol. 29: 281–286
   PubMed Web of Science ®Google Scholar
• Aramaki, M., T. Nagasawa, T. Koseki, and I. Ishikawa. 1998. Presence of activated B-1 cells in chronic inflamed gingival tissue. J. Clin. Immunol. 18: 421–429
   PubMed Web of Science ®Google Scholar
• O'Garra, A., R. Chang, N. Go, et al. 1992. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur. J. Immunol. 22: 711–717
   PubMed Web of Science ®Google Scholar
• Slots, J., I. Saygun, M. Sabeti, and A. Kubar. 2006. Epstein-Barr virus in oral diseases. J. Periodont. Res. 41: 235–244
   PubMed Web of Science ®Google Scholar
• Berglundh, T., B. Liljenberg, and J. Lindhe. 1999. Some effects of periodontal therapy on local and systemic immunological parameters. J. Clin. Periodontol. 26: 91–98
   PubMed Web of Science ®Google Scholar
• Donati, M., B. Liljenberg, N. U. Zitzmann, and T. Berglundh. 2009. B-1a cells in experimental gingivitis in humans. J. Periodontol. 80: 1141–1145
   PubMed Web of Science ®Google Scholar
• Yasuda, H., N. Shima, N. Nakagawa, et al. 1999. A novel molecular mechanism modulating osteoclast differentiation and function. Bone. 25: 109–113
   PubMed Web of Science ®Google Scholar
• Li, Y., G. Toraldo, A. Li, 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
   PubMed Web of Science ®Google Scholar