Pathogenic functions of B cells in autoimmune diseases: IFN-γ production joins the criminal gang

European Journal of Immunology

Volumn 45, Issue 4, 2015, Pages 966-970

  Fillatreau, Simon ^a  

^a DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

Author keywords

Arthritis; Autoimmunity; B cells; IFN ; T cells

Indexed keywords

AUTOANTIBODY; GAMMA INTERFERON; CYTOKINE;

ANTIGEN PRESENTATION; ARTHRITIS; AUTOIMMUNE DISEASE; B LYMPHOCYTE; EDITORIAL; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; INNATE IMMUNITY; INTERFERON PRODUCTION; LYMPHOID TISSUE; MACROPHAGE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; TH17 CELL; ANIMAL; ARTHRITIS, RHEUMATOID; AUTOIMMUNE DISEASES; AUTOIMMUNITY; BIOSYNTHESIS; DIABETES MELLITUS, TYPE 1; GENETICS; IMMUNOLOGY; LYMPHOCYTE DEPLETION; MOUSE; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; T LYMPHOCYTE;

ANIMALS; ARTHRITIS, RHEUMATOID; AUTOIMMUNE DISEASES; AUTOIMMUNITY; B-LYMPHOCYTES; CYTOKINES; DIABETES MELLITUS, TYPE 1; HUMANS; INTERFERON-GAMMA; LYMPHOCYTE DEPLETION; MICE; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; T-LYMPHOCYTES;

EID: 84926647980     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545544     Document Type: Editorial

References (40)

1. Edwards, J. C., Szczepanski, L., Szechinski, J., Filipowicz-Sosnowska, A., Emery, P., Close, D. R., Stevens, R. M. et al., Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 2004. 350: 2572-2581.
2. Pescovitz, M. D., Greenbaum, C. J., Krause-Steinrauf, H., Becker, D. J., Gitelman, S. E., Goland, R., Gottlieb, P. A. et al., B-lymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med. 2009. 361: 2143-2152.
3. Bar-Or, A., Calabresi, P. A., Arnold, D., Markowitz, C., Shafer, S., Kasper, L. H., Waubant, E. et al., Rituximab in relapsing-remitting multiple sclerosis: a 72-week, open-label, phase I trial. Ann. Neurol. 2008. 63: 395-400.
4. Dass, S., Vital, E. M. and Emery, P., Development of psoriasis after B cell depletion with rituximab. Arthritis Rheum. 2007. 56: 2715-2718.
5. Fillatreau, S., Sweenie, C. H., McGeachy, M. J., Gray, D. and Anderton, S. M., B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 2002. 3: 944-950.
6. Shen, P., Roch, T., Lampropoulou, V., O'Connor, R. A., Stervbo, U., Hilgenberg, E., Ries, S. et al., IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014. 507: 366-370.
7. Goetz, M., Atreya, R., Ghalibafian, M., Galle, P. R. and Neurath, M. F., Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm. Bowel Dis. 2007. 13: 1365-1368.
8. Cambridge, G., Perry, H. C., Nogueira, L., Serre, G., Parsons, H. M., De La Torre, I., Dickson, M. C. et al., The effect of B-cell depletion therapy on serological evidence of B-cell and plasmablast activation in patients with rheumatoid arthritis over multiple cycles of rituximab treatment. J. Autoimmun. 2014. 50: 67-76.
9. Martin, F. and Chan, A. C., B cell immunobiology in disease: evolving concepts from the clinic. Annu. Rev. Immunol. 2006. 24: 467-496.
10. Tak, P. P., Thurlings, R. M., Rossier, C., Nestorov, I., Dimic, A., Mircetic, V., Rischmueller, M. et al., Atacicept in patients with rheumatoid arthritis: results of a multicenter, phase Ib, double-blind, placebo-controlled, dose-escalating, single- and repeated-dose study. Arthritis Rheum. 2008. 58: 61-72.
11. van Vollenhoven, R. F., Kinnman, N., Vincent, E., Wax, S. and Bathon, J., Atacicept in patients with rheumatoid arthritis and an inadequate response to methotrexate: results of a phase II, randomized, placebo-controlled trial. Arthritis Rheum. 2011. 63: 1782-1792.
12. Olalekan, S.A., Cao, Y., Hamel, K.M. and Finnegan, A., B cells expressing IFN-γ suppress Treg-cell differentiation and promote autoimmune experimental arthritis. Eur. J. Immunol. 2015. 45: 988-998.
13. Glant, T. T., Mikecz, K., Arzoumanian, A. and Poole, A. R., Proteoglycan-induced arthritis in BALB/c mice. Clinical features and histopathology. Arthritis Rheum. 1987. 30: 201-212.
14. Glant, T., Csongor, J. and Szucs, T., Immunopathologic role of proteoglycan antigens in rheumatoid joint disease. Scand. J. Immunol. 1980. 11: 247-252.
15. Witter, J., Roughley, P. J., Webber, C., Roberts, N., Keystone, E. and Poole, A. R., The immunologic detection and characterization of cartilage proteoglycan degradation products in synovial fluids of patients with arthritis. Arthritis Rheum. 1987. 30: 519-529.
16. Hamel, K., Doodes, P., Cao, Y., Wang, Y., Martinson, J., Dunn, R., Kehry, M. R. et al., Suppression of proteoglycan-induced arthritis by anti-CD20 B Cell depletion therapy is mediated by reduction in autoantibodies and CD4+ T cell reactivity. J. Immunol. 2008. 180: 4994-5003.
17. Banerjee, S., Webber, C. and Poole, A. R., The induction of arthritis in mice by the cartilage proteoglycan aggrecan: roles of CD4+ and CD8+ T cells. Cell Immunol. 1992. 144: 347-357.
18. O'Neill, S. K., Shlomchik, M. J., Glant, T. T., Cao, Y., Doodes, P. D. and Finnegan, A., Antigen-specific B cells are required as APCs and autoantibody-producing cells for induction of severe autoimmune arthritis. J. Immunol. 2005. 174: 3781-3788.
19. Mikecz, K., Glant, T. T., Buzas, E. and Poole, A. R., Proteoglycan-induced polyarthritis and spondylitis adoptively transferred to naive (nonimmunized) BALB/c mice. Arthritis Rheum. 1990. 33: 866-876.
20. Kaplan, C. D., O'Neill, S. K., Koreny, T., Czipri, M. and Finnegan, A., Development of inflammation in proteoglycan-induced arthritis is dependent on Fc gamma R regulation of the cytokine/chemokine environment. J. Immunol. 2002. 169: 5851-5859.
21. Hamel, K. M., Cao, Y., Ashaye, S., Wang, Y., Dunn, R., Kehry, M. R., Glant, T. T. et al., B cell depletion enhances T regulatory cell activity essential in the suppression of arthritis. J. Immunol. 2011. 187: 4900-4906.
22. O'Neill, S. K., Cao, Y., Hamel, K. M., Doodes, P. D., Hutas, G. and Finnegan, A., Expression of CD80/86 on B cells is essential for autoreactive T cell activation and the development of arthritis. J. Immunol. 2007. 179: 5109-5116.
23. Hamel, K. M., Cao, Y., Olalekan, S. A. and Finnegan, A., B cell-specific expression of inducible costimulator ligand is necessary for the induction of arthritis in mice. Arthritis Rheumatol. 2014. 66: 60-67.
24. Crotty, S., Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 2011. 29: 621-663.
25. Reinhardt, R. L., Liang, H. E. and Locksley, R. M., Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 2009. 10: 385-393.
26. Luthje, K., Kallies, A., Shimohakamada, Y., Belz, G. T., Light, A., Tarlinton, D. M. and Nutt, S. L., The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat. Immunol. 2012. 13: 491-498.
27. Ma, J., Zhu, C., Ma, B., Tian, J., Baidoo, S. E., Mao, C., Wu, W. et al., Increased frequency of circulating follicular helper T cells in patients with rheumatoid arthritis. Clin. Dev. Immunol. 2012. 2012: 827480.
28. Wang, J., Shan, Y., Jiang, Z., Feng, J., Li, C., Ma, L. and Jiang, Y., High frequencies of activated B cells and T follicular helper cells are correlated with disease activity in patients with new-onset rheumatoid arthritis. Clin. Exp. Immunol. 2013. 174: 212-220.
29. Doodes, P. D., Cao, Y., Hamel, K. M., Wang, Y., Farkas, B., Iwakura, Y. and Finnegan, A., Development of proteoglycan-induced arthritis is independent of IL-17. J. Immunol. 2008. 181: 329-337.
30. Barr, T. A., Brown, S., Mastroeni, P. and Gray, D., TLR and B cell receptor signals to B cells differentially program primary and memory Th1 responses to Salmonella enterica. J. Immunol. 2010. 185: 2783-2789.
31. Bao, Y., Liu, X., Han, C., Xu, S., Xie, B., Zhang, Q., Gu, Y. et al., Identification of IFN-gamma-producing innate B cells. Cell Res. 2014. 24: 161-176.
32. Flaishon, L., Hershkoviz, R., Lantner, F., Lider, O., Alon, R., Levo, Y., Flavell, R. A. et al., Autocrine secretion of interferon gamma negatively regulates homing of immature B cells. J. Exp. Med. 2000. 192: 1381-1388.
33. Hawrylowicz, C. M. and Unanue, E. R., Regulation of antigen-presentation-I. IFN-gamma induces antigen-presenting properties on B cells. J. Immunol. 1988. 141: 4083-4088.
34. Schwarz, G., Boehncke, W. H., Braun, M., Schroter, C. J., Burster, T., Flad, T., Dressel, D. et al., Cathepsin S activity is detectable in human keratinocytes and is selectively upregulated upon stimulation with interferon-gamma. J. Invest. Dermatol. 2002. 119: 44-49.
35. Kendall, P. L., Case, J. B., Sullivan, A. M., Holderness, J. S., Wells, K. S., Liu, E. and Thomas, J. W., Tolerant anti-insulin B cells are effective APCs. J. Immunol. 2013. 190: 2519-2526.
36. Barr, T. A., Shen, P., Brown, S., Lampropoulou, V., Roch, T., Lawrie, S., Fan, B. et al., B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J. Exp. Med. 2012. 209: 1001-1010.
37. Molnarfi, N., Schulze-Topphoff, U., Weber, M. S., Patarroyo, J. C., Prod'homme, T., Varrin-Doyer, M., Shetty, A. et al., MHC class II-dependent B cell APC function is required for induction of CNS autoimmunity independent of myelin-specific antibodies. J. Exp. Med. 2013. 210: 2921-2937.
38. Lampropoulou, V., Hoehlig, K., Roch, T., Neves, P., Calderon Gomez, E., Sweenie, C. H., Hao, Y. et al., TLR-activated B cells suppress T cell-mediated autoimmunity. J. Immunol. 2008. 180: 4763-4773.
39. Wojciechowski, W., Harris, D. P., Sprague, F., Mousseau, B., Makris, M., Kusser, K., Honjo, T. et al., Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity 2009. 30: 421-433.
40. Bruhl, H., Cihak, J., Talke, Y., Gomez, M. R., Hermann, F., Goebel, N., Renner, K. et al., B-cell inhibition by cross-linking CD79b is superior to B-cell depletion with anti-CD20 antibodies in treating murine collagen-induced arthritis. Eur. J. Immunol. 2014. 45: 705-715.