Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice

Journal of Clinical Investigation

Volumn 117, Issue 12, 2007, Pages 3857-3867

  Hu, Chang Yun ^a   Rodriguez Pinto, Daniel ^a,c   Du, Wei ^a   Ahuja, Anupama ^a   Henegariu, Octavian ^a   Wong, F Susan ^b   Shlomchik, Mark J ^a   Wen, Li ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIBODY; CD22 ANTIGEN; GLUCOSE; IMMUNOGLOBULIN G;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CELL FUNCTION; CELL INFILTRATION; CLINICAL FEATURE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE COURSE; DRUG EFFICACY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN PRESENTATION; ANTIGENS, CD20; AUTOANTIBODIES; B-LYMPHOCYTES; CYTOKINES; DIABETES MELLITUS, TYPE 1; HUMANS; HYPERGLYCEMIA; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; T-LYMPHOCYTES, REGULATORY;

EID: 36849027817     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI32405     Document Type: Article

References (48)

1. Serreze, D.V., et al. 1996. B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD.Ig mu null mice. J. Exp. Med. 184:2049-2053.
2. Wong, F.S., et al. 1998. The role of lymphocyte subsets in accelerated diabetes in nonobese diabetic-rat insulin promoter-B7-1 (NOD-RIP-B7-1) mice. J. Exp. Med. 187:1985-1993.
3. Noorchashm, H., et al. 1997. B-cells are required for the initiation of insulitis and sialitis in nonobese diabetic mice. Diabetes. 46:941-946.
4. Wong, F.S., and Wen, L. 2005. B cells in autoimmune diabetes. Rev. Diabet. Stud. 2:121-135.
5. Yu, L., et al. 2000. Early expression of antiinsulin autoantibodies of humans and the NOD mouse: evidence for early determination of subsequent diabetes. Proc. Natl. Acad. Sci. U. S. A. 97:1701-1706.
6. Baekkeskov, S., et al. 1990. Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature. 347:151-156.
7. Hawkes, C.J., Wasmeier, C., Christie, M.R., and Hutton, J.C. 1996. Identification of the 37-kDa antigen in IDDM as a tyrosine phosphatase-like protein (phogrin) related to IA-2. Diabetes. 45:1187-1192.
8. Solimena, M., et al. 1996. ICA 512, an autoantigen of type I diabetes, is an intrinsic membrane protein of neurosecretory granules. EMBO J. 15:2102-2114.
9. Beyan, H., Ola, T., David, R., and Leslie, G. 2006. Progression of autoimmune diabetes: slowly progressive insulin-dependent diabetes mellitus or latent autoimmune diabetes of adult. Ann. N. Y. Acad. Sci. 1079:81-89.
10. Wasserfall, C.H., and Atkinson, M.A. 2006. Autoantibody markers for the diagnosis and prediction of type 1 diabetes. Autoimmun. Rev. 5:424-428.
11. Miao, D., Yu, L., and Eisenbarth, G.S. 2007. Role of autoantibodies in type 1 diabetes. Front. Biosci. 12:1889-1898.
12. Gardner, S.G., et al. 1999. Progression to diabetes in relatives with islet autoantibodies. Is it inevitable? Diabetes Care. 22:2049-2054.
13. Akashi, T., et al. 1997. Direct evidence for the contribution of B cells to the progression of insulitis and the development of diabetes in non-obese diabetic mice. Int. Immunol. 9:1159-1164.
14. Falcone, M., Lee, J., Patstone, G., Yeung, B., and Sarvetnick, N. 1998. B lymphocytes are crucial antigen-presenting cells in the pathogenic autoimmune response to GAD65 antigen in nonobese diabetic mice. J. Immunol. 161:1163-1168.
15. Serreze, D.V., 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.
16. Hulbert, C., Riseili, B., Rojas, M., and Thomas, J.W. 2001. B cell specificity contributes to the outcome of diabetes in nonobese diabetic mice. J. Immunol. 167:5535-5538.
17. Serreze, D.V., and Silveira, P.A. 2003. The role of B lymphocytes as key antigen-presenting cells in the development of T cell-mediated autoimmune type 1 diabetes. Curr. Dir. Autoimmun. 6:212-227.
18. Wong, F.S., et al. 2004. Investigation of the role of B-cells in type 1 diabetes in the NOD mouse. Diabetes. 53:2581-2587.
19. Tian, J., Zekzer, D., Lu, Y., Dang, H., and Kaufman, D.L. 2006. B cells are crucial for determinant spreading of T cell autoimmunity among beta cell antigens in diabetes-prone nonobese diabetic mice. J. Immunol. 176:2654-2661.
20. Greeley, S.A., et al. 2002. Elimination of maternally transmitted autoantibodies prevents diabetes in nonobese diabetic mice. Nat. Med. 8:399-402.
21. Rastetter, W., Molina, A., and White, C.A. 2004. Rituximab: expanding role in therapy for lymphomas and autoimmune diseases. Annu. Rev. Med. 55:477-503.
22. Martin, F., and Chan, A.C. 2004. Pathogenic roles of B cells in human autoimmunity; insights from the clinic. Immunity. 20:517-527.
23. Martin, F., and Chan, A.C. 2006. B cell immunobiology in disease: evolving concepts from the clinic. Annu. Rev. Immunol. 24:467-496.
24. Johnson, P., and Glennie, M. 2003. The mechanisms of action of rituximab in the elimination of tumor cells. Semin. Oncol. 30:3-8.
25. Edwards, J.C., Leandro, M.J., and Cambridge, G. 2005. B lymphocyte depletion in rheumatoid arthritis: targeting of CD20. Curr. Dir. Autoimmun. 8:175-192.
26. Edwards, J.C., et al. 2004. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350:2572-2581.
27. Kneitz, C., Wilhelm, M., and Tony, H.P. 2002. Effective B cell depletion with rituximab in the treatment of autoimmune diseases. Immunobiology. 206:519-527.
28. Uchida, J., et al. 2004. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J. Exp. Med. 199:1659-1669.
29. Hamaguchi, Y., Xiu, Y., Komura, K., Nimmerjahn, F., and Tedder, T.F. 2006. Antibody isotype-specific engagement of Fcgamma receptors regulates B lymphocyte depletion during CD20 immunotherapy. J. Exp. Med. 203:743-753.
30. Ahuja, A., Shupe, J., Dunn, R., Kashgarian, M., Kehry, M., and Shlomchik, M. 2007. Depletion of B cells in murine lupus: efficacy and resistance. J. Immunol. 179:3351-3361.
31. Hamaguchi, Y., et al. 2005. The peritoneal cavity provides a protective niche for B1 and conventional B lymphocytes during anti-CD20 immunotherapy in mice. J. Immunol. 174:4389-4399.
32. Du, W., et al. 2006. TGF-beta signaling is required for the function of insulin-reactive T regulatory cells. J. Clin. Invest. 116:1360-1370.
33. Hori, S., Nomura, T., and Sakaguchi, S. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science. 299:1057-1061.
34. Fontenot, J.D., Gavin, M.A., and Rudensky, A.Y. 2003. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4:330-336.
35. Khattri, R., Cox, T., Yasayko, S.A., and Ramsdell, F. 2003. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol. 4:337-342.
36. Shlomchik, M.J., Craft, J.E., and Mamula, M.J. 2001. From T to B and back again: positive feedback in systemic autoimmune disease. Nat. Rev. Immunol. 1:147-153.
37. Tuscano, J.M., Harris, G.S., and Tedder, T.F. 2003. B lymphocytes contribute to autoimmune disease pathogenesis: current trends and clinical implications. Autoimmun. Rev. 2:101-108.
38. Dorner, T. 2006. Crossroads of B cell activation in autoimmunity: rationale of targeting B cells. J. Rheumatol. Suppl. 77:3-11.
39. Sherry, N.A., et al. 2006. Effects of autoimmunity and immune therapy on beta-cell turnover in type 1 diabetes. Diabetes. 55:3238-3245.
40. Sherry, N.A., et al. 2007. Exendin-4 improves reversal of diabetes in NOD mice treated with anti-CD3 mAb by enhancing recovery of {beta} cells. Endocrinology. 148:5136-5144.
41. Fillatreau, S., Sweenie, C.H., McGeachy, M.J., Gray, D., and Anderton, S.M. 2002. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 3:944-950.
42. Mauri, C., Gray, D., Mushtaq, N., and Londei, M. 2003. Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. 197:489-501.
43. Mizoguchi, A., and Bhan, A.K. 2006. A case for regulatory B cells. J. Immunol. 176:705-710.
44. Mann, M.K., 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. 178:3447-3456.
45. Mathis, D., Vence, L., and Benoist, C. 2001. beta-Cell death during progression to diabetes. Nature. 414:792-798.
46. Evans, J.G., et al. 2007. Novel suppressive function of transitional 2 B cells in experimental arthritis. J. Immunol. 178:7868-7878.
47. Anolik, J.H., et al. 2007. Delayed memory B cell recovery in peripheral blood and lymphoid tissue in systemic lupus erythematosus after B cell depletion therapy. Arthritis Rheum. 56:3044-3056.
48. Peng, J., et al. 2007. Converting antigen-specific diabetogenic CD4 and CD8 T cells to TGF-beta producing non-pathogenic regulatory cells following FoxP3 transduction. J. Autoimmun. 28:188-200.