B cells promote obesity-associated periodontitis and oral pathogen-associated inflammation

Journal of Leukocyte Biology

Volumn 96, Issue 2, 2014, Pages 349-357

  Zhu, Min ^a   Belkina, Anna C ^a   DeFuria, Jason ^a   Carr, Jordan D ^a   Van Dyke, Thomas E ^b   Gyurko, Robert ^c   Nikolajczyk, Barbara S ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FORSYTH INSTITUTE   (United States)

^c BOSTON UNIVERSITY   (United States)

Author keywords

B lymphocyte; Cytokine; Mouse model; Porphyromonas gingivalis; Type 2 diabetes

Indexed keywords

CXCL3 CHEMOKINE; GLUCOSE; INSULIN; TUMOR NECROSIS FACTOR ALPHA;

ALVEOLAR BONE LOSS; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; GLUCOSE INTOLERANCE; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; MORPHOMETRICS; MOUSE; MOUTH INFECTION; MOUTH INFLAMMATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OSTEOCLASTOGENESIS; PATHOGENESIS; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL;

B LYMPHOCYTE; CYTOKINE; MOUSE MODEL; PORPHYROMONAS GINGIVALIS; TYPE 2 DIABETES;

ANIMALS; B-LYMPHOCYTES; CHEMOKINE CXCL2; DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; MALE; MICE; MICE, MUTANT STRAINS; OBESITY; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84904984618     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.4A0214-095R     Document Type: Article

References (45)

1. Vos, T., Flaxman, A. D., Naghavi, M., Lozano, R., Michaud, C., Ezzati, M., Shibuya, K., Salomon, J. A., Abdalla, S., Aboyans, V., et al. (2012) Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380, 2163-2196.
2. Lockhart, P. B., Bolger, A. F., Papapanou, P. N., Osinbowale, O., Trevisan, M., Levison, M. E., Taubert, K. A., Newburger, J. W., Gornik, H. L., Gewitz, M. H., et al. (2012) Periodontal disease and atherosclerotic vascular disease: does the evidence support an independent association? A scientific statement from the American Heart Association. Circulation 125, 2520-2544.
3. Preshaw, P. M., Alba, A. L., Herrera, D., Jepsen, S., Konstantinidis, A., Makrilakis, K., Taylor, R. (2012) Periodontitis and diabetes: a two-way relationship. Diabetologia 55, 21-31.
4. Nikolajczyk, B. S. (2010) B cells as under-appreciated mediators of nonauto-immune inflammatory disease. Cytokine 50, 234-242.
5. Seymour, G. J., Powell, R. N., Davies, W. I. (1979) The immunopathogenesis of progressive chronic inflammatory periodontal disease. J. Oral Pathol. 8, 249-265.
6. Reinhardt, R. A., Bolton, R. W., McDonald, T. L., DuBois, L. M., Kaldahl, W. B. (1988) In situ lymphocyte subpopulations from active versus stable periodontal sites. J. Periodontol. 59, 656-670.
7. Harada, Y., Han, X., Yamashita, K., Kawai, T., Eastcott, J. W., Smith, D. J., Taubman, M. A. (2006) Effect of adoptive transfer of antigen-specific B cells on periodontal bone resorption. J. Periodontal. Res. 41, 101-107.
8. Teng, Y. T. (2006) Protective and destructive immunity in the periodontium: part 1-innate and humoral immunity and the periodontium. J. Dent. Res. 85, 198-208.
9. Hall, L. M., Dunford, R. G., Genco, R. J., Sharma, A. (2012) Levels of serum immunoglobulin G specific to bacterial surface protein A of Tannerella forsythia are related to periodontal status. J. Periodontol. 83, 228-234.
10. Albandar, J. M., DeNardin, A. M., Adesanya, M. R., Diehl, S. R., Winn, D. M. (2001) Associations between serum antibody levels to periodontal pathogens and early-onset periodontitis. J. Periodontol. 72, 1463-1469.
11. Jagannathan, M., Hasturk, H., Liang, Y., Shin, H., Hetzel, J. T., Kantarci, A., Rubin, D., McDonnell, M. E., Van Dyke, T. E., Ganley-Leal, L. M., Nikolajczyk, B. S. (2009) TLR cross-talk specifically regulates cytokine production by B cells from chronic inflammatory disease patients. J. Immunol. 183, 7461-7470.
12. Kawai, T., Matsuyama, T., Hosokawa, Y., Makihira, S., Seki, M., Karimbux, N. Y., Goncalves, R. B., Valverde, P., Dibart, S., Li, Y. P., Miranda, L. A., Ernst, C. W., Izumi, Y., Taubman, M. A. (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.
13. Winer, D. A., Winer, S., Shen, L., Wadia, P. P., Yantha, J., Paltser, G., Tsui, H., Wu, P., Davidson, M. G., Alonso, M. N., et al. (2011) B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 17, 610-617.
14. DeFuria, J., Belkina, A. C., Jagannathan-Bogdan, M., Snyder-Cappione, J., Carr, J. D., Nersesova, Y. R., Markham, D., Strissel, K. J., Watkins, A. A., Zhu, M., et al. (2013) B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc. Natl. Acad. Sci. USA 110, 5133-5138.
15. Jagannathan, M., McDonnell, M., Liang, Y., Hasturk, H., Hetzel, J., Rubin, D., Kantarci, A., Van Dyke, T. E., Ganley-Leal, L. M., Nikolajczyk, B. S. (2010) Toll-like receptors regulate B cell cytokine production in patients with diabetes. Diabetologia 53, 1461-1471.
16. Kitamura, D., Roes, J., Kuhn, R., Rajewsky, K. (1991) A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature 350, 423-426.
17. Baker, P. J., Evans, R. T., 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.
18. Kawai, T., Eisen-Lev, R., Seki, M., Eastcott, J. W., Wilson, M. E., Taubman, M. A. (2000) Requirement of B7 costimulation for Th1-mediated inflammatory bone resorption in experimental periodontal disease. J. Immunol. 164, 2102-2109.
19. Cinti, S., Mitchell, G., Barbatelli, G., Murano, I., Ceresi, E., Faloia, E., Wang, S., Fortier, M., Greenberg, A. S., Obin, M. S. (2005) Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 46, 2347-2355.
20. Negishi-Koga, T., Takayanagi, H. (2009) Ca2+-NFATc1 signaling is an essential axis of osteoclast differentiation. Immunol. Rev. 231, 241-256.
21. Jain, S., Coats, S. R., Chang, A. M., Darveau, R. P. (2013) A novel class of lipoprotein lipase-sensitive molecules mediates Toll-like receptor 2 activation by Porphyromonas gingivalis. Infect. Immun. 81, 1277-1286.
22. Tonetti, M. S., Imboden, M. A., Lang, N. P. (1998) Neutrophil migration into the gingival sulcus is associated with transepithelial gradients of interleukin-8 and ICAM-1. J. Periodontol. 69, 1139-1147.
23. Cipolletta, D., Feuerer, M., Li, A., Kamei, N., Lee, J., Shoelson, S. E., Benoist, C., Mathis, D. (2012) PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue T-reg cells. Nature 486, 549-553.
24. Zhu, M., Nikolajczyk, B. S. (2014) Immune cells link obesity-associated type 2 diabetes and periodontitis. J. Dent. Res. 93, 346-352.
25. Lalla, E., Lamster, I. B., Feit, M., Huang, L., Spessot, A., Qu, W., Kislinger, T., Lu, Y., Stern, D. M., Schmidt, A. M. (2000) Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. J. Clin. Invest. 105, 1117-1124.
26. Taylor, J. J., Preshaw, P. M., Lalla, E. (2013) A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J. Clin. Periodontol. 40, S113-S134.
27. Amar, S., Zhou, Q., Shaik-Dasthagirisaheb, Y., Leeman, S. (2007) Dietinduced obesity in mice causes changes in immune responses and bone loss manifested by bacterial challenge. Proc. Natl. Acad. Sci. USA 104, 20466-20471.
28. Ley, R. E., Turnbaugh, P. J., Klein, S., Gordon, J. I. (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022-1023.
29. Shulzhenko, N., Morgun, A., Hsiao, W., Battle, M., Yao, M., Gavrilova, O., Orandle, M., Mayer, L., Macpherson, A. J., McCoy, K. D., Fraser-Liggett, C., Matzinger, P. (2011) Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat. Med. 17, 1585-1593.
30. Berglundh, T., Donati, M., Zitzmann, N. (2007) B cells in periodontitis-friends or enemies? Periodontol. 2000 45, 51-66.
31. Ebersole, J. L. (2003) Humoral immune responses in gingival crevice fluid: local and systemic implications. Periodontol. 2000 31, 135-166.
32. Tew, J., Engel, D., Mangan, D. (1989) Polyclonal B-cell activation in periodontitis. J. Periodontal Res. 24, 225-241.
33. De-Gennaro, L. A., Lopes, J. D., Mariano, M. (2006) Autoantibodies directed to extracellular matrix components in patients with different clinical forms of periodontitis. J. Periodontol. 77, 2025-2030.
34. Teng, Y. T. (2003) The role of acquired immunity and periodontal disease progression. Crit. Rev. Oral Biol. Med. 14, 237-252.
35. Hamze, M., Desmetz, C., Guglielmi, P. (2013) B cell-derived cytokines in disease. Eur. Cytokine Netw. 24, 20-26.
36. Hu, W., Pasare, C. (2013) Location, location, location: tissue-specific regulation of immune responses. J. Leukoc. Biol. 94, 409-421.
37. Duffaut, C., Galitzky, J., Lafontan, M., Bouloumie, A. (2009) Unexpected trafficking of immune cells within the adipose tissue during the onset of obesity. Biochem. Biophys. Res. Commun. 384, 482-485.
38. Graves, D. T., Cochran, D. (2003) The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. J. Periodontol. 74, 391-401.
39. Papadopoulos, G., Weinberg, E. O., Massari, P., Gibson III, F. C., Wetzler, L. M., Morgan, E. F., Genco, C. A. (2013) Macrophage-specific TLR2 signaling mediates pathogen-induced TNF-dependent inflammatory oral bone loss. J. Immunol. 190, 1148-1157.
40. Di Paola, R., Mazzon, E., Muia, C., Crisafulli, C., Terrana, D., Greco, S., Britti, D., Santori, D., Oteri, G., Cordasco, G., Cuzzocrea, S. (2007) Effects of etanercept, a tumour necrosis factor-β antagonist, in an experimental model of periodontitis in rats. Br. J. Pharmacol. 150, 286-297.
41. Kim, N., Kadono, Y., Takami, M., Lee, J., Lee, S. H., Okada, F., Kim, J. H., Kobayashi, T., Odgren, P. R., Nakano, H., Yeh, W. C., Lee, S. K., Lorenzo, J. A., Choi, Y. (2005) Osteoclast differentiation independent of the TRANCE-RANK-TRAF6 axis. J. Exp. Med. 202, 589-595.
42. Azuma, Y., Kaji, K., Katogi, R., Takeshita, S., Kudo, A. (2000) Tumor necrosis factor-β induces differentiation of and bone resorption by osteoclasts. J. Biol. Chem. 275, 4858-4864.
43. Graves, D. T., Oskoui, M., Volejnikova, S., Naguib, G., Cai, S., Desta, T., Kakouras, A., Jiang, Y. (2001) Tumor necrosis factor modulates fibroblast apoptosis, PMN recruitment, and osteoclast formation in response to P. gingivalis infection. J. Dent. Res. 80, 1875-1879.
44. Uysal, K. T., Wiesbrock, S. M., Marino, M. W., Hotamisligil, G. S. (1997) Protection from obesity-induced insulin resistance in mice lacking TNF-α function. Nature 389, 610-614.
45. Javed, F., Al-Askar, M., Al-Hezaimi, K. (2012) Cytokine profile in the gingival crevicular fluid of periodontitis patients with and without type 2 diabetes: a literature review. J. Periodontol. 83, 156-161.