B-cell inhibition by cross-linking CD79b is superior to B-cell depletion with anti-CD20 antibodies in treating murine collagen-induced arthritis

European Journal of Immunology

Volumn 45, Issue 3, 2015, Pages 705-715

  Brühl, Hilke ^a   Cihak, Josef ^b   Talke, Yvonne ^a   Gomez, Manuel Rodriguez ^a   Hermann, Fabian ^a   Goebel, Nicole ^a   Renner, Kerstin ^a   Plachý, Jiří ^c   Stangassinger, Manfred ^b   Aschermann, Susanne ^d   Nimmerjahn, Falk ^d   Mack, Matthias ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Arthritis; B cells; B cell depletion; B cell inhibition; CD79b; Humoral immune response

Indexed keywords

ANTIINFLAMMATORY AGENT; B LYMPHOCYTE RECEPTOR; CD20 ANTIBODY; CD40 ANTIGEN; CD79B ANTIBODY; CD79B ANTIGEN; CD810 ANTIGEN; CHONDROITIN SULFATE; FC RECEPTOR; IMMUNOSUPPRESSIVE AGENT; LYMPHOCYTE ANTIGEN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; ANTIRHEUMATIC AGENT; CD79 ANTIGEN; CD79B PROTEIN, MOUSE; LEUKOCYTE ANTIGEN; LY78 PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; RITUXIMAB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMORAL IMMUNE DEFICIENCY; HUMORAL IMMUNITY; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; SYNOVIUM; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTHRITIS, EXPERIMENTAL; CAPPING PHENOMENON; CELL PROLIFERATION; DBA MOUSE; DRUG EFFECTS; IMMUNOLOGY; LYMPHOCYTE DEPLETION; PATHOLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIGENS, CD; ANTIGENS, CD40; ANTIGENS, CD79; ANTIRHEUMATIC AGENTS; ARTHRITIS, EXPERIMENTAL; B-LYMPHOCYTES; CELL PROLIFERATION; IMMUNITY, HUMORAL; IMMUNOLOGIC CAPPING; LYMPHOCYTE DEPLETION; MALE; MICE; MICE, INBRED DBA; RECEPTORS, ANTIGEN, B-CELL;

EID: 84924530951     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444971     Document Type: Article

References (34)

1. Cohen, S. B., Emery, P., Greenwald, M. W., Dougados, M., Furie, R. A., Genovese, M. C., Keystone, E. C. et al., Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum. 2006. 54: 2793-2806.
2. Edwards, J. C., Szczepanski, L., Szechinski, J., Filipowicz-Sosnowska, A., Emery, P., Close, D. R., Stevens, R. M. and Shaw, T., Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 2004. 350: 2572-2581.
3. Jones, R. B., Tervaert, J. W., Hauser, T., Luqmani, R., Morgan, M. D., Peh, C. A., Savage, C. O. et al., Rituximab versus cyclophosphamide in ANCA-associated renal vasculitis. N. Engl. J. Med. 2010. 363: 211-220.
4. Stone, J. H., Merkel, P. A., Spiera, R., Seo, P., Langford, C. A., Hoffman, G. S., Kallenberg, C. G. et al., Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N. Engl. J. Med. 2010. 363: 221-232.
5. Emery, P., Deodhar, A., Rigby, W. F., Isaacs, J. D., Combe, B., Racewicz, A. J., Latinis, K. et al., Efficacy and safety of different doses and retreatment of rituximab: a randomised, placebo-controlled trial in patients who are biological naive with active rheumatoid arthritis and an inadequate response to methotrexate (Study Evaluating Rituximab's Efficacy in MTX iNadequate rEsponders (SERENE)). Ann. Rheum. Dis. 2010. 69: 1629-1635.
6. Tak, P. P., Rigby, W. F., Rubbert-Roth, A., Peterfy, C. G., van Vollenhoven, R. F., Stohl, W., Hessey, E. et al., Inhibition of joint damage and improved clinical outcomes with rituximab plus methotrexate in early active rheumatoid arthritis: the IMAGE trial. Ann. Rheum. Dis. 2011. 70: 39-46.
7. Rovin, B. H., Furie, R., Latinis, K., Looney, R. J., Fervenza, F. C., Sanchez-Guerrero, J., Maciuca, R. et al., Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum. 2012. 64: 1215-1226.
8. Mysler, E. F., Spindler, A. J., Guzman, R., Bijl, M., Jayne, D., Furie, R. A., Houssiau, F. A. et al., Efficacy and safety of ocrelizumab in active proliferative lupus nephritis: results from a randomized, double-blind, phase III study. Arthritis Rheum. 2013. 65: 2368-2379.
9. Yanaba, K., Hamaguchi, Y., Venturi, G. M., Steeber, D. A., St Clair, E. W. and Tedder, T. F., B cell depletion delays collagen-induced arthritis in mice: arthritis induction requires synergy between humoral and cell-mediated immunity. J. Immunol. 2007. 179: 1369-1380.
10. Dunussi-Joannopoulos, K., Hancock, G. E., Kunz, A., Hegen, M., Zhou, X. X., Sheppard, B. J., Lamothe, J. et al., B-cell depletion inhibits arthritis in a collagen-induced arthritis (CIA) model, but does not adversely affect humoral responses in a respiratory syncytial virus (RSV) vaccination model. Blood 2005. 106: 2235-2243.
11. Yarkoni, Y., Getahun, A. and Cambier, J. C., Molecular underpinning of B-cell anergy. Immunol. Rev. 2010. 237: 249-263.
12. Gazumyan, A., Reichlin, A. and Nussenzweig, M. C., Ig beta tyrosine residues contribute to the control of B cell receptor signaling by regulating receptor internalization. J. Exp. Med. 2006. 203: 1785-1794.
13. O'Neill, S. K., Getahun, A., Gauld, S. B., Merrell, K. T., Tamir, I., Smith, M. J., Dal Porto, J. M. et al., Monophosphorylation of CD79a and CD79b ITAM motifs initiates a SHIP-1 phosphatase-mediated inhibitory signaling cascade required for B cell anergy. Immunity 2011. 35: 746-756.
14. Vilen, B. J., Nakamura, T. and Cambier, J. C., Antigen-stimulated dissociation of BCR mIg from Ig-alpha/Ig-beta: implications for receptor desensitization. Immunity 1999. 10: 239-248.
15. Kraus, M., Alimzhanov, M. B., Rajewsky, N. and Rajewsky, K., Survival of resting mature B lymphocytes depends on BCR signaling via the Igalpha/beta heterodimer. Cell 2004. 117: 787-800.
16. Tseng, J., Eisfelder, B. J. and Clark, M. R., B-cell antigen receptor-induced apoptosis requires both Ig alpha and Ig beta. Blood 1997. 89: 1513-1520.
17. Li, Y., Chen, F., Putt, M., Koo, Y. K., Madaio, M., Cambier, J. C., Cohen, P. L. and Eisenberg, R. A., B cell depletion with anti-CD79 mAbs ameliorates autoimmune disease in MRL/lpr mice. J. Immunol. 2008. 181: 2961-2972.
18. Ahuja, A., Shupe, J., Dunn, R., Kashgarian, M., Kehry, M. R. and Shlomchik, M. J., Depletion of B cells in murine lupus: efficacy and resistance. J. Immunol. 2007. 179: 3351-3361.
19. Bekar, K. W., Owen, T., Dunn, R., Ichikawa, T., Wang, W., Wang, R., Barnard, J. et al., Prolonged effects of short-term anti-CD20 B cell depletion therapy in murine systemic lupus erythematosus. Arthritis Rheum. 2010. 62: 2443-2457.
20. Haas, K. M., Watanabe, R., Matsushita, T., Nakashima, H., Ishiura, N., Okochi, H., Fujimoto, M. and Tedder, T. F., Protective and pathogenic roles for B cells during systemic autoimmunity in NZB/W F1 mice. J. Immunol. 2010. 184: 4789-4800.
21. Hardy, I. R., Anceriz, N., Rousseau, F., Seefeldt, M. B., Hatterer, E., Irla, M., Buatois, V. et al., Anti-CD79 antibody induces B cell anergy that protects against autoimmunity. J. Immunol. 2014. 192: 1641-1650.
22. Nose, M. and Wigzell, H., Biological significance of carbohydrate chains on monoclonal antibodies. Proc. Natl. Acad. Sci. USA 1983. 80: 6632-6636.
23. Arnold, J. N., Wormald, M. R., Sim, R. B., Rudd, P. M. and Dwek, R. A., The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 2007. 25: 21-50.
24. Van Kooten, C., Galibert, L., Seon, B. K., Garrone, P., Liu, Y. J. and Banchereau, J., Cross-linking of antigen receptor via Ig-beta (B29, CD79b) can induce both positive and negative signals in CD40-activated human B cells. Clin. Exp. Immunol. 1997. 110: 509-515.
25. Nakamura, T., Koyama, M., Koike, Y., Miyazaki, K., Yoneyema, A., Higashihara, M., Azuma, M. and Kurokawa, K., Suppression of humoral immunity by monoclonal antibody to CD79b, an invariant component of antigen receptors on B lymphocytes. Int. J. Hematol. 1996. 64: 39-46.
26. Nakamura, T., Kubagawa, H. and Cooper, M. D., Heterogeneity of immunoglobulin-associated molecules on human B cells identified by monoclonal antibodies. Proc. Natl. Acad. Sci. USA 1992. 89: 8522-8526.
27. Nakamura, T., Sekar, M. C., Kubagawa, H. and Cooper, M. D., Signal transduction in human B cells initiated via Ig beta ligation. Int. Immunol. 1993. 5: 1309-1315.
28. Shlomchik, M. J. and Weisel, F., Germinal center selection and the development of memory B and plasma cells. Immunol. Rev. 2012. 247: 52-63.
29. Nguyen, T. G., Little, C. B., Yenson, V. M., Jackson, C. J., McCracken, S. A., Warning, J., Stevens, V. et al., Anti-IgD antibody attenuates collagen-induced arthritis by selectively depleting mature B-cells and promoting immune tolerance. J. Autoimmun. 2010. 35: 86-97.
30. Koyama, M., Ishihara, K., Karasuyama, H., Cordell, J. L., Iwamoto, A. and Nakamura, T., CD79 alpha/CD79 beta heterodimers are expressed on pro-B cell surfaces without associated mu heavy chain. Int. Immunol. 1997. 9: 1767-1772.
31. Biburger, M., Aschermann, S., Schwab, I., Lux, A., Albert, H., Danzer, H., Woigk, M. et al., Monocyte subsets responsible for immunoglobulin G-dependent effector functions in vivo. Immunity 2011. 35: 932-944.
32. Uchida, J., Hamaguchi, Y., Oliver, J. A., Ravetch, J. V., Poe, J. C., Haas, K. M. and Tedder, T. F., The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J. Exp. Med. 2004. 199: 1659-1669.
33. Bruhl, H., Cihak, J., Niedermeier, M., Denzel, A., Rodriguez Gomez, M., Talke, Y., Goebel, N. et al., Important role of interleukin-3 in the early phase of collagen-induced arthritis. Arthritis Rheum. 2009. 60: 1352-1361.
34. Bruhl, H., Cihak, J., Goebel, N., Talke, Y., Renner, K., Hermann, F., Rodriguez-Gomez, M. et al., Chondroitin sulfate activates B cells in vitro, expands CD138+ cells in vivo, and interferes with established humoral immune responses. J. Leukoc. Biol. 2014. 96: 65-72.