Transient depletion of B cells in young mice results in activation of regulatory T cells that inhibit development of autoimmune disease in adults

International Immunology

Volumn 24, Issue 4, 2012, Pages 233-242

  Yu, Shiguang ^a,c   Ellis, Jason S ^a   Dunn, Robert ^b   Kehry, Marilyn R ^b   Braley mullen, Helen ^a  

^a University of Missouri   (United States)

^b BIOGEN   (United States)

^c ARKANSAS STATE UNIVERSITY   (United States)

Author keywords

Anti CD20; Autoimmunity; B cells; Treg

Indexed keywords

AUTOANTIBODY; CD20 ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE THYROIDITIS; B CELL DEPLETION; B LYMPHOCYTE; CD25+ T LYMPHOCYTE; CELL SELECTION; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; T LYMPHOCYTE ACTIVATION;

EID: 84859204197     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxs003     Document Type: Article

References (44)

1. Braley-Mullen, H., Sharp, G. C., Medling, B. and Tang, H. 1999. Spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. J. Autoimmun. 12:157.
2. Yu, S., Medling, B., Yagita, H. and Braley-Mullen, H. 2001. Characteristics of inflammatory cells in spontaneous autoimmune thyroiditis of NOD.H-2h4 mice. J. Autoimmun. 16:37.
3. Rasooly, L., Burek, C. L. and Rose, N. R. 1996. Iodine-induced autoimmune thyroiditis in NOD.H-2h4 mice. Clin. Immunol. Immunopathol. 81:287.
4. Verma, S., Hutchings, P., Guo, J., Mclachlan, S., Rapoport, B. and Cooke, A. 2000. Role of MHC class I expression and CD8+ T cells in the evolution of iodine-induced thyroiditis in NOD-H2(h4) and NOD mice. Eur. J. Immunol. 30:1191.
5. Braley-Mullen, H. and Yu, S. 2000. Early requirements for B cells for development of spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. J. Immunol. 165:7262.
6. Yu, S., Maiti, P. K., Dyson, M., Jain, R. and Braley-Mullen, H. 2006. B cell-deficient NOD-H2h4 mice have CD4+CD25+ T regulatory cells that inhibit the development of spontaneous autoimmune thyroiditis. J. Exp. Med. 203:349.
7. Serreze, D. V., Fleming, S. A., Chapman, H. D., Richard, S. D., Leiter, E. H. and Tisch, R. M. 1998. B lymphocytes are critical antigenpresenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J. Immunol. 161:3912.
8. Noorchasm, H., Lieu, Y. K., Noorchasm, N. et al. 1999. I-Ag7-mediated antigen presentation by B lymphocytes is critical in overcoming a checkpoint in T cell tolerance to islet β cells of nonobese diabetic mice. J. Immunol. 163:743.
9. Wong, F. S., Wen, L., Tang, M. et al. 2005. Investigation of the role of B cells in type I diabetes in the NOD mouse. Diabetes 53:2581.
10. Chan, O., Hannum, L. G., Haberman, A. H., Madaio, M. P. and Shlomchik, M. J. 1999. A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J. Exp. Med. 189:1639.
11. Hasegawa, M., Hamaguchi, Y., Yanaba, K. et al. 2006. B-lymphocyte depletion reduces skin fibrosis and autoimmunity in the tight-skin mouse model for systemic sclerosis. Am. J. Pathol. 169:954.
12. Hayakawa, H., Tedder, T. F. and Zhuang, Y. 2007. B-lymphocyte depletion ameliorates Sjogren's syndrome in Id3 knockout mice. Immunology 122:1.
13. Hamel, K., Doodes, P., Cao, Y. et al. 2008. Suppression of proteogycan-induced arthritis by anti-CD20 B cell depletion therapy is mediated by reduction in autoantibodies and CD4+ T cell reactivity. J. Immunol. 180:4994.
14. O'Neill, S. K., Shlomchik, M. K., Giant, T. et al. 2005. Antigenspecific B cells are required as APC's and autoantibodyproducing cells for induction of severe autoimmune arthritis. J. Immunol. 174:3781.
15. Harvey, B., Gee, R., Haberman, A., Shlomchik, M. J. and Mamula, M. 2007. Antigen presentation and transfer between B cells and macrophages. Eur. J. Immunol. 37:1739.
16. Yan, J., Harvey, B., Gee, R., Shlomchik, M. J. and Mamula, M. J. 2006. B cells drive early T cell autoimmunity in vivo prior to autoantigen presentation. J. Immunol. 178:3447.
17. Mauri, C. and Ehrenstein, M. R. 2007. The 'short' history of regulatory B cells. Trends Immunol. 29:34.
18. Mann, M. E., Maresz, K., Shriver, L. P., Tan, Y. and Dittel, B. N. 2007. B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J. Immunol. 178:3447.
19. Matsushita, T., Yanaga, K., Bouaziz, J. D., Fujimoto, M., and Tedder, T. F. 2008. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 118:3420.
20. Thatayatikom, A. and White, A. J. 2006. Rituximab: a promising therapy in systemic lupus erythematosus. Autoimmun. Rev. 5:18.
21. Sanz, I., Anolik, J. and Looney, R. J. 2007. B cell depletion therapy in autoimmune diseases. Front. Biosci. 12:2546.
22. Leandro, M. J. and de la Torre, I. 2009. Translational mini-review series on B cell-directed therapies: the pathogenic role of B cells in autoantibody-associated autoimmune diseases-lessons from B cell-depletion therapy. Clin. Exp. Immunol. 157:191.
23. Hu, C., Rodriguez-Pinto, D., Du, W. et al. 2008. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest. 117:3857.
24. Yu, S., Dunn, R., Kehry, M. R. and Braley-Mullen, H. 2008. B cell depletion inhibits spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. J. Immunol. 180:7706.
25. Yanaba, K., Hamaguchi, Y., Venture, G., Streeter, D., St Clair, E. W. and Tedder, T. F. 2007. B cell depletion delays collagen-induced arthritis in mice: arthritis induction requires synergy between humoral and cell-mediated immunity. J. Immunol. 179:1369.
26. Ahuja, A., Shope, J., Dunn, R., Kashgarian, M., Kehry, M. R. and Shlomchik, M. J. 2007. Depletion of B cells in murine lupus: efficacy and resistance. J. Immunol. 179:3551.
27. Bekar, K. W., Owen, T., Dunn, R. et al. 2010. Prolonged effects of short-term anti-CD20 B cell depletion therapy in murine systemic lupus erythematosus. Arthritis Rheum. 62:2443.
28. Haas, K., Watanabe, M. R., Matsushika, T. et al. 2010. Protective and pathogenic roles for B cells during systemic autoimmunity in NZB/W F1 mice. J. Immunol. 184:4789.
29. Kyaw, T., Tay, C., Khan, A. et al. 2010. Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J. Immunol. 185:4410.
30. Moritoki, Y., Lian, Z. X., Lindor, K. et al. 2009. B-cell depletion with anti-CD20 ameliorates autoimmune cholangitis but exacerbates colitis in transforming growth factor-beta receptor II dominant negative mice. Hepatology 50:1893.
31. Zhang, A.-H., Skupsky, J. and Scott, D. W. 2011. Effect of B cell depletion using anti-CD20 therapy on inhibitory antibody formation to human FVIII in hemophilia A mice. Blood 117:2223.
32. Ueki, I., Abiru, N., Kobayashi, M. et al. 2011. B cell-targeted therapy with anti-CD20 monoclonal antibody in a mouse model of Graves' hyperthyroidism. Clin. Exp. Immunol. 163:309.
33. Dhirapong, A., Lieo, A., Yang, G. X. et al. 2011. B cell depletion therapy exacerbates murine primary biliary cirrhosis. Hepatology 53:527.
34. Podolin, P. L., Pressey, A., DeLarato, N. H., Fischer, P. A., Peterson, L. B. and Wicker, L. S. 1993. I-E+ nonobese diabetic mice develop insulitis and diabetes. J. Exp. Med. 178:793.
35. Pillai, S., Cariappa, A. and Moran, S. T. 2005. Marginal zone B cells. Ann. Rev. Immunol. 23:1161.
36. Marino, E., Batten, M., Groom, J. et al. 2007. Marginal zone B cells of non-obese diabetic mice expand with diabetes onset, invade the pancreatic lymph nodes and present autoantigen to diabetogenic T cells. Diabetes 58:1568.
37. Nagayama, Y., Horie, I., Saitoh, O., Nakahara, M. and Abiru, N. 2007. CD4+CD25+ naturally occurring regulatory T cells and not lymphopenia play a role in the pathogenesis of iodide-induced autoimmune thyroiditis in NOD.H-2h4 mice. J. Autoimmun. 29:195.
38. Attanavanich, K. and Kearney, J. F. 2004. Marginal zone, but not follicular, B cells are potent activators of nai{dotless}̈ve B cells. J. Immunol. 172:803.
39. Marino, E., Villanueva, J., Walters, S., Liuwantara, D., Mackay, F. and Grey, S. T. 2009. CD4+CD25+ T cells control autoimmunity in the absence of B-cells. Diabetes 58:1568.
40. Mellanby, R. J., Thomas, D., Phillips, J. M. and Cooke, A. 2007. Diabetes in non-obese diabetic mice is not associated with quantitative changes in CD4+CD25+ Foxp3+ regulatory T cells. Immunology 121:15.
41. Sfikakis, P. P., Souliotis, V. L., Fragiakaki, K. G., Moutsopoulos, H. M., Boletis, J. N. and Theofilopoulos, A. N. 2007. Increased expression of the Foxp3 functional marker of regulatory T cells following B cell depletion with rituximab in patients with lupus nephritis. Clin. Immunol. 123:66.
42. Vallerskog, T., Gunnarsson, I., Widhe, M. et al. 2007. Treatment with rituximab affects both the cellular arm and the humoral arm of the immune system in patients with SLE. Clin. Immunol. 122:62.
43. Hamel, K., Cao, Y., Ashaye, S. et al. 2011. B cell depletion enhances T regulatory cell activity essential in the suppression of arthritis. J. Immunol. 187:4900.
44. Serreze, D. V., Chapman, H. D., Niens, M. et al. 2011. Loss of intra-islet CD20 expression may complicate efficacy of B celldirected type 1 diabetes therapies. Diabetes 60:2914.