Regulatory B cells mediate tolerance to apoptotic self in health: Implications for disease

International Immunology

Volumn 27, Issue 10, 2015, Pages 505-511

  Gray, Mohini ^a   Gray, David ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Apoptosis; Autoimmunity; B cell; Immune regulation; Innate like B cell

Indexed keywords

AUTOANTIGEN; CELL ANTIGEN; COLLAGEN ANTIBODY; DNA; GAMMA INTERFERON; INTERLEUKIN 10; RITUXIMAB; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; IL10 PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; TLR9 PROTEIN, HUMAN;

ANTIGEN RECOGNITION; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; CELL COMPARTMENTALIZATION; CYTOKINE PRODUCTION; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOGENESIS; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; ANIMAL; CELL LINEAGE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MOUSE; PATHOLOGY; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; APOPTOSIS; ARTHRITIS, RHEUMATOID; AUTOANTIGENS; B-LYMPHOCYTES, REGULATORY; CELL LINEAGE; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-10; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 9;

EID: 84946743922     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxv045     Document Type: Article

References (100)

1. Kerr, J. F., Wyllie, A. H. and Currie, A. R. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26:239.
2. Reed, J. C. 2006. Drug insight: cancer therapy strategies based on restoration of endogenous cell death mechanisms. Nat. Clin. Pract. Oncol. 3:388.
3. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y. and Henson, P. M. 1998. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101:890.
4. Serhan, C. N., Chiang, N. and Dalli, J. 2015. The resolution code of acute inflammation: Novel pro-resolving lipid mediators in resolution. Semin. Immunol. 27:200.
5. Miles, K., Clarke, D. J., Lu, W. et al. 2009. Dying and necrotic neutrophils are anti-inflammatory secondary to the release of alphadefensins. J. Immunol. 183:2122.
6. Albert, M. L., Jegathesan, M. and Darnell, R. B. 2001. Dendritic cell maturation is required for the cross-tolerization of CD8+ T cells. Nat. Immunol. 2:1010.
7. Belz, G. T., Behrens, G. M., Smith, C. M. et al. 2002. The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J. Exp. Med. 196:1099.
8. Ferguson, T. A., Herndon, J., Elzey, B., Griffith, T. S., Schoenberger, S. and Green, D. R. 2002. Uptake of apoptotic antigen-coupled cells by lymphoid dendritic cells and cross-priming of CD8(+) T cells produce active immune unresponsiveness. J. Immunol. 168:5589.
9. Seong, S. Y. and Matzinger, P. 2004. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 4:469.
10. Bendelac, A., Bonneville, M. and Kearney, J. F. 2001. Autoreactivity by design: innate B and T lymphocytes. Nat. Rev. Immunol. 1:177.
11. Oliver, A. M., Martin, F., Gartland, G. L., Carter, R. H. and Kearney, J. F. 1997. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 27:2366.
12. Oliver, A. M., Martin, F. and Kearney, J. F. 1999. IgMhighCD21high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J. Immunol. 162:7198.
13. Attanavanich, K. and Kearney, J. F. 2004. Marginal zone, but not follicular B cells, are potent activators of naive CD4 T cells. J. Immunol. 172:803.
14. Crawford, A., Macleod, M., Schumacher, T., Corlett, L. and Gray, D. 2006. Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells. J. Immunol. 176:3498.
15. Matzinger, P. 2002. The danger model: a renewed sense of self. Science 296:301.
16. Green, D. R., Ferguson, T., Zitvogel, L. and Kroemer, G. 2009. Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 9:353.
17. Arbuckle, M. R., McClain, M. T., Rubertone, M. V. et al. 2003. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 349:1526.
18. Gray, M., Miles, K., Salter, D., Gray, D. and Savill, J. 2007. Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc. Natl Acad. Sci. USA 104:14080.
19. Miles, K., Heaney, J., Sibinska, Z. et al. 2012. A tolerogenic role for Toll-like receptor 9 is revealed by B-cell interaction with DNA complexes expressed on apoptotic cells. Proc. Natl Acad. Sci. USA 109:887.
20. Burdin, N., Rousset, F. and Banchereau, J. 1997. B-cell-derived IL-10: production and function. Methods 11:98.
21. Moore, K. W., Vieira, P., Fiorentino, D. F., Trounstine, M. L., Khan, T. A. and Mosmann, T. R. 1990. Homology of cytokine synthesis inhibitory factor (IL-10) to the Epstein-Barr virus gene BCRFI. Science 248:1230.
22. Vieira, P., de Waal-Malefyt, R., Dang, M. N. et al. 1991. Isolation and expression of human cytokine synthesis inhibitory factor cDNA clones: homology to Epstein-Barr virus open reading frame BCRFI. Proc. Natl Acad. Sci. USA 88:1172.
23. O'Garra, A. and Howard, M. 1992. Cytokines and Ly-1 (B1) B cells. Int. Rev. Immunol. 8:219.
24. Wolf, S. D., Dittel, B. N., Hardardottir, F. and Janeway, C. A. Jr. 1996. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J. Exp. Med. 184:2271.
25. 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.
26. Mizoguchi, A., Mizoguchi, E., Smith, R. N., Preffer, F. I. and Bhan, A. K. 1997. Suppressive role of B cells in chronic colitis of T cell receptor alpha mutant mice. J. Exp. Med. 186:1749.
27. Mauri, C., Gray, D., Mushtaq, N. and Londei, M. 2003. Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. 197:489.
28. Bouaziz, J. D., Yanaba, K. and Tedder, T. F. 2008. Regulatory B cells as inhibitors of immune responses and inflammation. Immunol. Rev. 224:201.
29. Mauri, C., Mars, L. T. and Londei, M. 2000. Therapeutic activity of agonistic monoclonal antibodies against CD40 in a chronic autoimmune inflammatory process. Nat. Med. 6:673.
30. Vences-Catalán, F. and Santos-Argumedo, L. 2011. CD38 through the life of a murine B lymphocyte. IUBMB Life 63:840.
31. Blair, P. A., Noreña, L. Y., Flores-Borja, F. et al. 2010. CD19(+) CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 32:129.
32. Lampropoulou, V., Hoehlig, K., Roch, T. et al. 2008. TLR-activated B cells suppress T cell-mediated autoimmunity. J. Immunol. 180:4763.
33. Yanaba, K., Bouaziz, J. D., Matsushita, T., Tsubata, T. and Tedder, T. F. 2009. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J. Immunol. 182:7459.
34. Yanaba, K., Bouaziz, J. D., Haas, K. M., Poe, J. C., Fujimoto, M. and Tedder, T. F. 2008. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28:639.
35. Maseda, D., Candando, K. M., Smith, S. H. et al. 2013. Peritoneal cavity regulatory B cells (B10 cells) modulate IFN-α+CD4+ T cell numbers during colitis development in mice. J. Immunol. 191:2780.
36. Shen, P., Roch, T., Lampropoulou, V. et al. 2014. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 507:366.
37. Savage, H. P. and Baumgarth, N. Characteristics of natural antibody-secreting cells. Ann. N. Y. Acad. Sci. June 23, 2015. doi:10.1111/nyas.12799.
38. Baumgarth, N. 2011. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11:34.
39. Baumgarth, N. 2013. Innate-like B cells and their rules of engagement. Adv. Exp. Med. Biol. 785:57.
40. Choi, Y. S., Dieter, J. A., Rothaeusler, K., Luo, Z. and Baumgarth, N. 2012. B-1 cells in the bone marrow are a significant source of natural IgM. Eur. J. Immunol. 42:120.
41. Griffin, D. O., Holodick, N. E. and Rothstein, T. L. 2011. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD70-. J. Exp. Med. 208:67.
42. Rothstein, T. L., Griffin, D. O., Holodick, N. E., Quach, T. D. and Kaku, H. 2013. Human B-1 cells take the stage. Ann. N. Y. Acad. Sci. 1285:97.
43. Cerutti, A., Cols, M. and Puga, I. 2013. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat. Rev. Immunol. 13:118.
44. Ichikawa, D., Asano, M., Shinton, S. A. et al. 2015. Natural antiintestinal goblet cell autoantibody production from marginal zone B cells. J. Immunol. 194:606.
45. Spencer, J., Finn, T., Pulford, K. A., Mason, D. Y. and Isaacson, P. G. 1985. The human gut contains a novel population of B lymphocytes which resemble marginal zone cells. Clin. Exp. Immunol. 62:607.
46. Chen, Y., Khanna, S., Goodyear, C. S. et al. 2009. Regulation of dendritic cells and macrophages by an anti-apoptotic cell natural antibody that suppresses TLR responses and inhibits inflammatory arthritis. J. Immunol. 183:1346.
47. Kouskoff, V., Lacaud, G., Pape, K., Retter, M. and Nemazee, D. 2000. B cell receptor expression level determines the fate of developing B lymphocytes: receptor editing versus selection. Proc. Natl Acad. Sci. USA 97:7435.
48. Watanabe, N., Nisitani, S., Ikuta, K., Suzuki, M., Chiba, T. and Honjo, T. 1999. Expression levels of B cell surface immunoglobulin regulate efficiency of allelic exclusion and size of autoreactive B-1 cell compartment. J. Exp. Med. 190:461.
49. Lau, C. M., Broughton, C., Tabor, A. S. et al. 2005. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202:1171.
50. Marshak-Rothstein, A. 2006. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 6:823.
51. Barr, T. A., Brown, S., Ryan, G., Zhao, J. and Gray, D. 2007. TLRmediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells. Eur. J. Immunol. 37:3040.
52. Savill, J., Dransfield, I., Gregory, C. and Haslett, C. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2:965.
53. Casciola-Rosen, L. A., Anhalt, G. and Rosen, A. 1994. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179:1317.
54. Radic, M., Marion, T. and Monestier, M. 2004. Nucleosomes are exposed at the cell surface in apoptosis. J. Immunol. 172:6692.
55. Chang, M. K., Binder, C. J., Torzewski, M. and Witztum, J. L. 2002. C-reactive protein binds to both oxidized LDL and apoptotic cells through recognition of a common ligand: Phosphorylcholine of oxidized phospholipids. Proc. Natl Acad. Sci. USA 99:13043.
56. Chang, M. K., Bergmark, C., Laurila, A. et al. 1999. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc. Natl Acad. Sci. USA 96:6353.
57. Chang, M. K., Binder, C. J., Miller, Y. I. et al. 2004. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J. Exp. Med. 200:1359.
58. Binder, C. J., Shaw, P. X., Chang, M. K. et al. 2005. The role of natural antibodies in atherogenesis. J. Lipid Res. 46:1353.
59. Binder, C. J. and Silverman, G. J. 2005. Natural antibodies and the autoimmunity of atherosclerosis. Springer Semin. Immunopathol. 26:385.
60. Notley, C. A., Brown, M. A., Wright, G. P. and Ehrenstein, M. R. 2011. Natural IgM is required for suppression of inflammatory arthritis by apoptotic cells. J. Immunol. 186:4967.
61. Ehrenstein, M. R. and Notley, C. A. 2010. The importance of natural IgM: scavenger, protector and regulator. Nat. Rev. Immunol. 10:778.
62. Weller, S., Braun, M. C., Tan, B. K. et al. 2004. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104:3647.
63. Iwata, Y., Matsushita, T., Horikawa, M. et al. 2011. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117:530.
64. Hemmi, H., Takeuchi, O., Kawai, T. et al. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740.
65. Bernasconi, N. L., Onai, N. and Lanzavecchia, A. 2003. A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101:4500.
66. Tsokos, G. C. 2011. Systemic lupus erythematosus. N. Engl. J. Med. 365:2110.
67. Perry, D., Sang, A., Yin, Y., Zheng, Y. Y. and Morel, L. 2011. Murine models of systemic lupus erythematosus. J. Biomed. Biotechnol. 2011:271694.
68. Yurasov, S., Wardemann, H., Hammersen, J. et al. 2005. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 201:703.
69. Levy, E., Ambrus, J., Kahl, L., Molina, H., Tung, K. and Holers, V. M. 1992. T lymphocyte expression of complement receptor 2 (CR2/CD21): a role in adhesive cell-cell interactions and dysregulation in a patient with systemic lupus erythematosus (SLE). Clin. Exp. Immunol. 90:235.
70. Willcocks, L. C., Carr, E. J., Niederer, H. A. et al. 2010. A defunctioning polymorphism in FCGR2B is associated with protection against malaria but susceptibility to systemic lupus erythematosus. Proc. Natl Acad. Sci. USA 107:7881.
71. Christensen, S. R., Kashgarian, M., Alexopoulou, L., Flavell, R. A., Akira, S. and Shlomchik, M. J. 2005. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J. Exp. Med. 202:321.
72. Wu, X. and Peng, S. L. 2006. Toll-like receptor 9 signaling protects against murine lupus. Arthritis Rheum. 54:336.
73. Christensen, S. R. and Shlomchik, M. J. 2007. Regulation of lupusrelated autoantibody production and clinical disease by Toll-like receptors. Semin. Immunol. 19:11.
74. Christensen, S. R., Shupe, J., Nickerson, K., Kashgarian, M., Flavell, R. A. and Shlomchik, M. J. 2006. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity 25:417.
75. Haas, K. M., Watanabe, R., Matsushita, T. et al. 2010. Protective and pathogenic roles for B cells during systemic autoimmunity in NZB/W F1 mice. J. Immunol. 184:4789.
76. Watanabe, R., Ishiura, N., Nakashima, H. et al. 2010. Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J. Immunol. 184:4801.
77. Teichmann, L. L., Kashgarian, M., Weaver, C. T., Roers, A., Müller, W. and Shlomchik, M. J. 2012. B cell-derived IL-10 does not regulate spontaneous systemic autoimmunity in MRL.Fas(lpr) mice. J. Immunol. 188:678.
78. Gong, Q., Ou, Q., Ye, S. et al. 2005. Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J. Immunol. 174:817.
79. Edwards, J. C., Szczepanski, L., Szechinski, J. et al. 2004. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350:2572.
80. Hauser, S. L., Waubant, E., Arnold, D. L. et al.; HERMES Trial Group. 2008. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. 358:676.
81. Díaz-Lagares, C., Croca, S., Sangle, S. et al.; UK-BIOGEAS Registry. 2012. Efficacy of rituximab in 164 patients with biopsy-proven lupus nephritis: pooled data from European cohorts. Autoimmun. Rev. 11:357.
82. Leandro, M. J., Cambridge, G., Ehrenstein, M. R. and Edwards, J. C. 2006. Reconstitution of peripheral blood B cells after depletion with rituximab in patients with rheumatoid arthritis. Arthritis Rheum. 54:613.
83. Anolik, J. H., Barnard, J., Cappione, A. et al. 2004. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum. 50:3580.
84. Rodríguez-Bayona, B., Ramos-Amaya, A., Pérez-Venegas, J. J., Rodríguez, C. and Brieva, J. A. 2010. Decreased frequency and activated phenotype of blood CD27 IgD IgM B lymphocytes is a permanent abnormality in systemic lupus erythematosus patients. Arthritis Res. Ther. 12:R108.
85. Flores-Borja, F., Bosma, A., Ng, D. et al. 2013. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci. Transl. Med. 5:173.
86. Sfikakis, P. P., Boletis, J. N., Lionaki, S. et al. 2005. Remission of proliferative lupus nephritis following B cell depletion therapy is preceded by down-regulation of the T cell costimulatory molecule CD40 ligand: an open-label trial. Arthritis Rheum. 52:501.
87. Lund, F. E. and Randall, T. D. 2010. Effector and regulatory B cells: modulators of CD4+ T cell immunity. Nat. Rev. Immunol. 10:236.
88. Vallerskog, T., Gunnarsson, I., Widhe, M. et al. 2007. Treatment with rituximab affects both the cellular and the humoral arm of the immune system in patients with SLE. Clin. Immunol. 122:62.
89. Vigna-Perez, M., Hernández-Castro, B., Paredes-Saharopulos, O. et al. 2006. Clinical and immunological effects of Rituximab in patients with lupus nephritis refractory to conventional therapy: a pilot study. Arthritis Res. Ther. 8:R83.
90. Hu, C. Y., Rodriguez-Pinto, D., Du, W. et al. 2007. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest. 117:3857.
91. Lanzavecchia, A. and Sallusto, F. 2007. Toll-like receptors and innate immunity in B-cell activation and antibody responses. Curr. Opin. Immunol. 19:268.
92. Dass, S., Vital, E. M. and Emery, P. 2007. Development of psoriasis after B cell depletion with rituximab. Arthritis Rheum. 56:2715.
93. El Fassi, D., Nielsen, C. H., Kjeldsen, J., Clemmensen, O. and Hegedüs, L. 2008. Ulcerative colitis following B lymphocyte depletion with rituximab in a patient with Graves' disease. Gut 57:714.
94. Goetz, M., Atreya, R., Ghalibafian, M., Galle, P. R. and Neurath, M. F. 2007. Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm. Bowel Dis. 13:1365.
95. Yanaba, K., Kamata, M., Ishiura, N. et al. 2013. Regulatory B cells suppress imiquimod-induced, psoriasis-like skin inflammation. J. Leukoc. Biol. 94:563.
96. Clatworthy, M. R., Watson, C. J., Plotnek, G. et al. 2009. B-celldepleting induction therapy and acute cellular rejection. N. Engl. J. Med. 360:2683.
97. Matsushita, T., Yanaba, 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.
98. Duddy, M., Niino, M., Adatia, F. et al. 2007. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. 178:6092.
99. Correale, J., Farez, M. and Razzitte, G. 2008. Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann. Neurol. 64:187.
100. Yoshizaki, A., Miyagaki, T., DiLillo, D. J. et al. 2012. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 491:264.