Deletion of IgG-switched autoreactive B cells and defects in Fas lpr lupus mice

Journal of Immunology

Volumn 185, Issue 2, 2010, Pages 1015-1027

  Aït Azzouzene, Djemel ^a   Kono, Dwight H ^a   Gonzalez Quintial, Rosana ^a   McHeyzer Williams, Louise J ^a   Lim, Min ^a   Wickramarachchi, Dilki ^a   Gerdes, Tobias ^a   Gavin, Amanda L ^a   Skog, Patrick ^a   McHeyzer Williams, Michael G ^a   Nemazee, David ^a   Theofilopoulos, Argyrios N ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; FAS ANTIGEN; IMMUNOGLOBULIN G2A; PROTEIN BCL 2; BCL2 PROTEIN, MOUSE; IMMUNOGLOBULIN G; ONCOPROTEIN; SUPERANTIGEN;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CELL MATURATION; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CELL LINE; CYTOLOGY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENE REARRANGEMENT; GENETICS; HUMAN; IMMUNOLOGY; MALE; METABOLISM; MOUSE STRAIN; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD95; B-LYMPHOCYTES; CELL LINE; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN G; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; MICE, INBRED STRAINS; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN; SUPERANTIGENS;

EID: 77955488972     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000698     Document Type: Article

References (71)

1. McHeyzer-Williams, L. J., D. J. Driver, and M. G. McHeyzer-Williams. 2001. Germinal center reaction. Curr. Opin. Hematol. 8: 52-59.
2. Diamond, B., J. B. Katz, E. Paul, C. Aranow, D. Lustgarten, and M. D. Scharff. 1992. The role of somatic mutation in the pathogenic anti-DNA response. Annu. Rev. Immunol. 10: 731-757.
3. Shlomchik, M., M. Mascelli, H. Shan, M. Z. Radic, D. Pisetsky, A. Marshak-Rothstein, and M. Weigert. 1990. Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation. J. Exp. Med. 171: 265-292.
4. Shlomchik, M. J., A. Marshak-Rothstein, C. B. Wolfowicz, T. L. Rothstein, and M. G. Weigert. 1987. The role of clonal selection and somatic mutation in autoimmunity. Nature 328: 805-811.
5. Nemazee, D. A., and K. Bürki. 1989. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature 337: 562-566.
6. Goodnow, C. C., J. Crosbie, H. Jorgensen, R. A. Brink, and A. Basten. 1989. Induction of self-tolerance in mature peripheral B lymphocytes. Nature 342: 385-391.
7. Hartley, S. B., J. Crosbie, R. Brink, A. B. Kantor, A. Basten, and C. C. Goodnow. 1991. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353: 765-769.
8. Russell, D. M., Z. Dembić, G. Morahan, J. F. Miller, K. Bürki, and D. Nemazee. 1991. Peripheral deletion of self-reactive B cells. Nature 354: 308-311.
9. Tiegs, S. L., D. M. Russell, and D. Nemazee. 1993. Receptor editing in self-reactive bone marrow B cells. J. Exp. Med. 177: 1009-1020.
10. Linton, P. J., A. Rudie, and N. R. Klinman. 1991. Tolerance susceptibility of newly generating memory B cells. J. Immunol. 146: 4099-4104.
11. Pulendran, B., M. Karvelas, and G. J. Nossal. 1994. A form of immunologic tolerance through impairment of germinal center development. Proc. Natl. Acad. Sci. USA 91: 2639-2643.
12. Han, S., B. Zheng, J. Dal Porto, and G. Kelsoe. 1995. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. IV. Affinity-dependent, antigen-driven B cell apoptosis in germinal centers as a mechanism for maintaining self-tolerance. J. Exp. Med. 182: 1635-1644.
13. Pulendran, B., G. Kannourakis, S. Nouri, K. G. Smith, and G. J. Nossal. 1995. Soluble antigen can cause enhanced apoptosis of germinal-centre B cells. Nature 375: 331-334.
14. Shokat, K. M., and C. C. Goodnow. 1995. Antigen-induced B-cell death and elimination during germinal-centre immune responses. Nature 375: 334-338.
15. Cornall, R. J., C. C. Goodnow, and J. G. Cyster. 1995. The regulation of self-reactive B cells. Curr. Opin. Immunol. 7: 804-811.
16. Hämmerling, G. J., J. W. Chamberlain, O. Dill, S. Y. Yang, B. Dupont, R. Khan, R. Chua, S. M. Weissman, and U. Hämmerling. 1990. Self-tolerance to HLA focuses the response of immunized HLA-transgenic mice on production of antibody to precise polymorphic HLA alloantigens. Proc. Natl. Acad. Sci. USA 87: 235-239.
17. Minnerath, J. M., C. M. Mueller, S. Buron, and R. Jemmerson. 1995. B lymphocyte recognition of cytochrome c: higher frequency of cells specific for self versus foreign antigen early in the immune response and V gene usage in the response to self antigen. Eur. J. Immunol. 25: 784-791.
18. Hande, S., E. Notidis, and T. Manser. 1998. Bcl-2 obstructs negative selection of autoreactive, hypermutated antibody V regions during memory B cell development. Immunity 8: 189-198. (Pubitemid 28123746)
19. Notidis, E., L. Heltemes, and T. Manser. 2002. Dominant, hierarchical induction of peripheral tolerance during foreign antigen-driven B cell development. Immunity 17: 317-327. (Pubitemid 35279552)
20. Guay, H. M., L. Panarey, A. J. Reed, and A. J. Caton. 2004. Specificity-based negative selection of autoreactive B cells during memory formation. J. Immunol. 173: 5485-5494.
21. Ait-Azzouzene, D., L. Verkoczy, J. Peters, A. Gavin, P. Skog, J. L. Vela, and D. Nemazee. 2005. An immunoglobulin C kappa-reactive single chain antibody fusion protein induces tolerance through receptor editing in a normal polyclonal immune system. J. Exp. Med. 201: 817-828.
22. Aït-Azzouzene, D., L. Verkoczy, B. Duong, P. Skog, A. L. Gavin, and D. Nemazee. 2006. Split tolerance in peripheral B cell subsets in mice expressing a low level of Igkappa-reactive ligand. J. Immunol. 176: 939-948. (Pubitemid 43099692)
23. Allen, D., A. Cumano, R. Dildrop, C. Kocks, K. Rajewsky, N. Rajewsky, J. Roes, F. Sablitzky, and M. Siekevitz. 1987. Timing, genetic requirements and functional consequences of somatic hypermutation during B-cell development. Immunol. Rev. 96: 5-22.
24. Strasser, A., S. Whittingham, D. L. Vaux, M. L. Bath, J. M. Adams, S. Cory, and A. W. Harris. 1991. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl. Acad. Sci. USA 88: 8661-8665.
25. Huang, C. M., M. Parsons, V. T. Oi, H. J. Huang, and L. A. Herzenberg. 1983. Genetic characterization of mouse immunoglobulin allotypic determinants (allotopes) defined by monoclonal antibodies. Immunogenetics 18: 311-321.
26. Collins, C. E., A. L. Gavin, T. S. Migone, D. M. Hilbert, D. Nemazee, and W. Stohl. 2006. B lymphocyte stimulator (BLyS) isoforms in systemic lupus erythematosus: disease activity correlates better with blood leukocyte BLyS mRNA levels than with plasma BLyS protein levels. Arthritis Res. Ther. 8: R6.
27. McHeyzer-Williams, L. J., M. Cool, and M. G. McHeyzer-Williams. 2000. Antigen-specific B cell memory: expression and replenishment of a novel b220(-) memory b cell compartment. J. Exp. Med. 191: 1149-1166.
28. Stavnezer, J. 1996. Immunoglobulin class switching. Curr. Opin. Immunol. 8: 199-205.
29. William, J., C. Euler, and M. J. Shlomchik. 2005. Short-lived plasmablasts dominate the early spontaneous rheumatoid factor response: differentiation pathways, hypermutating cell types, and affinity maturation outside the germinal center. J. Immunol. 174: 6879-6887.
30. Bergqvist, P., E. Gärdby, A. Stensson, M. Bemark, and N. Y. Lycke. 2006. Gut IgA class switch recombination in the absence of CD40 does not occur in the lamina propria and is independent of germinal centers. J. Immunol. 177: 7772-7783.
31. Han, J. H., S. Akira, K. Calame, B. Beutler, E. Selsing, and T. Imanishi-Kari. 2007. Class switch recombination and somatic hypermutation in early mouse B cells are mediated by B cell and Toll-like receptors. Immunity 27: 64-75.
32. Castigli, E., S. A. Wilson, S. Scott, F. Dedeoglu, S. Xu, K. P. Lam, R. J. Bram, H. Jabara, and R. S. Geha. 2005. TACI and BAFF-R mediate isotype switching in B cells. J. Exp. Med. 201: 35-39.
33. Litinskiy, M. B., B. Nardelli, D. M. Hilbert, B. He, A. Schaffer, P. Casali, and A. Cerutti. 2002. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3: 822-829.
34. Benner, R., W. Hijmans, and J. J. Haaijman. 1981. The bone marrow: the major source of serum immunoglobulins, but still a neglected site of antibody formation. Clin. Exp. Immunol. 46: 1-8.
35. Slifka, M. K., M. Matloubian, and R. Ahmed. 1995. Bone marrow is a major site of long-term antibody production after acute viral infection. J. Virol. 69: 1895-1902.
36. Reed, A. J., M. P. Riley, and A. J. Caton. 2000. Virus-induced maturation and activation of autoreactive memory B cells. J. Exp. Med. 192: 1763-1774.
37. Galibert, L., N. Burdin, C. Barthélémy, G. Meffre, I. Durand, E. Garcia, P. Garrone, F. Rousset, J. Banchereau, and Y. J. Liu. 1996. Negative selection of human germinal center B cells by prolonged BCR cross-linking. J. Exp. Med. 183: 2075-2085.
38. Finkelman, F. D., J. M. Holmes, O. I. Dukhanina, and S. C. Morris. 1995. Cross-linking of membrane immunoglobulin D, in the absence of T cell help, kills mature B cells in vivo. J. Exp. Med. 181: 515-525.
39. Kench, J. A., D. M. Russell, and D. Nemazee. 1998. Efficient peripheral clonal elimination of B lymphocytes in MRL/lpr mice bearing autoantibody transgenes. J. Exp. Med. 188: 909-917.
40. Klinman, N. R. 1997. The cellular origins of memory B cells. Semin. Immunol. 9: 241-247.
41. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science 267: 1449-1456.
42. Izui, S., V. E. Kelley, K. Masuda, H. Yoshida, J. B. Roths, and E. D. Murphy. 1984. Induction of various autoantibodies by mutant gene lpr in several strains of mice. J. Immunol. 133: 227-233.
43. Giese, T., and W. F. Davidson. 1994. Chronic treatment of C3H-lpr/lpr and C3H-gld/gld mice with anti-CD8 monoclonal antibody prevents the accumulation of double negative T cells but not autoantibody production. J. Immunol. 152: 2000-2010.
44. Drappa, J., A. K. Vaishnaw, K. E. Sullivan, J. L. Chu, and K. B. Elkon. 1996. Fas gene mutations in the Canale-Smith syndrome, an inherited lymphoproliferative disorder associated with autoimmunity. N. Engl. J. Med. 335: 1643-1649.
45. Fukuyama, H., M. Adachi, S. Suematsu, K. Miwa, T. Suda, N. Yoshida, and S. Nagata. 1998. Transgenic expression of Fas in T cells blocks lymphoproliferation but not autoimmune disease in MRL-lpr mice. J. Immunol. 160: 3805-3811. (Pubitemid 28176084)
46. Fukuyama, H., M. Adachi, S. Suematsu, K. Miwa, T. Suda, N. Yoshida, and S. Nagata. 2002. Requirement of Fas expression in B cells for tolerance induction. Eur. J. Immunol. 32: 223-230.
47. Rubio, C. F., J. Kench, D. M. Russell, R. Yawger, and D. Nemazee. 1996. Analysis of central B cell tolerance in autoimmune-prone MRL/lpr mice bearing autoantibody transgenes. J. Immunol. 157: 65-71.
48. Rathmell, J. C., and C. C. Goodnow. 1994. Effects of the lpr mutation on elimination and inactivation of self-reactive B cells. J. Immunol. 153: 2831-2842.
49. Lamoureux, J. L., L. C. Watson, M. Cherrier, P. Skog, D. Nemazee, and A. J. Feeney. 2007. Reduced receptor editing in lupus-prone MRL/lpr mice. J. Exp. Med. 204: 2853-2864.
50. Rathmell, J. C., M. P. Cooke, W. Y. Ho, J. Grein, S. E. Townsend, M. M. Davis, and C. C. Goodnow. 1995. CD95 (Fas)-dependent elimination of self-reactive B cells upon interaction with CD4+ T cells. Nature 376: 181-184.
51. Mandik-Nayak, L., S. J. Seo, C. Sokol, K. M. Potts, A. Bui, and J. Erikson. 1999. MRL-lpr/lpr mice exhibit a defect in maintaining developmental arrest and follicular exclusion of anti-double-stranded DNA B cells. J. Exp. Med. 189: 1799-1814.
52. Paul, E., J. Lutz, J. Erikson, and M. C. Carroll. 2004. Germinal center checkpoints in B cell tolerance in 3H9 transgenic mice. Int. Immunol. 16: 377-384.
53. Brard, F., M. Shannon, E. L. Prak, S. Litwin, and M. Weigert. 1999. Somatic mutation and light chain rearrangement generate autoimmunity in anti-single-stranded DNA transgenic MRL/lpr mice. J. Exp. Med. 190: 691-704.
54. Hao, Z., G. S. Duncan, J. Seagal, Y. W. Su, C. Hong, J. Haight, N. J. Chen, A. Elia, A. Wakeham, W. Y. Li, et al. 2008. Fas Receptor Expression in Germinal-Center B Cells Is Essential for T and B Lymphocyte Homeostasis. Immunity 29: 615-627.
55. Smith, K. G., G. J. Nossal, and D. M. Tarlinton. 1995. FAS is highly expressed in the germinal center but is not required for regulation of the B-cell response to antigen. Proc. Natl. Acad. Sci. USA 92: 11628-11632.
56. Alabyev, B., R. Vuyyuru, and T. Manser. 2008. Influence of Fas on the regulation of the response of an anti-nuclear antigen B cell clonotype to foreign antigen. Int. Immunol. 20: 1279-1287.
57. Takahashi, Y., H. Ohta, and T. Takemori. 2001. Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 14: 181-192. (Pubitemid 32206520)
58. William, J., C. Euler, S. Christensen, and M. J. Shlomchik. 2002. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science 297: 2066-2070.
59. Tiller, T., M. Tsuiji, S. Yurasov, K. Velinzon, M. C. Nussenzweig, and H. Wardemann. 2007. Autoreactivity in human IgG+ memory B cells. Immunity 26: 205-213. (Pubitemid 46329436)
60. Tsuiji, M., S. Yurasov, K. Velinzon, S. Thomas, M. C. Nussenzweig, and H. Wardemann. 2006. A checkpoint for autoreactivity in human IgM+ memory B cell development. J. Exp. Med. 203: 393-400.
61. Chiorazzi, N. 1987. Stimulation of lymphocytes with antibodies to surface membrane-bound antigen receptors. Methods Enzymol. 150: 92-104.
62. Manning, D. D. 1977. Complete humoral immunosuppression of mice by rabbit anti-mu antibodies passing the murine placenta. J. Immunol. 118: 1109-1112. (Pubitemid 8064704)
63. Bazin, H., B. Platteau, A. Beckers, and R. Pauwels. 1978. Differential effect of neonatal injections of anti-mu or anti-delta antibodies on the synthesis of IgM, IgD, IgE, IgA, IgG1, IgG2a, IgG2b, and IgG2c immunoglobulin classes. J. Immunol. 121: 2083-2087. (Pubitemid 9053617)
64. Gause, A., N. Yoshida, C. Kappen, and K. Rajewsky. 1987. In vivo generation and function of B cells in the presence of a monoclonal anti-IgM antibody: implications for B cell tolerance. Eur. J. Immunol. 17: 981-990.
65. Duong, B. H., T. Ota, D. Aït-Azzouzene, M. Aoki-Ota, J. L. Vela, C. Huber, K. Walsh, A. L. Gavin, and D. Nemazee. 2010. Peripheral B cell tolerance and function in transgenic mice expressing an IgD superantigen. J. Immunol. 184: 4143-4158.
66. Marshak-Rothstein, A., and I. R. Rifkin. 2007. Immunologically active autoantigens: the role of toll-like receptors in the development of chronic inflammatory disease. Annu. Rev. Immunol. 25: 419-441.
67. Tian, J., A. M. Avalos, S. Y. Mao, B. Chen, K. Senthil, H. Wu, P. Parroche, S. Drabic, D. Golenbock, C. Sirois, et al. 2007. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat. Immunol. 8: 487-496.
68. Baccala, R., K. Hoebe, D. H. Kono, B. Beutler, and A. N. Theofilopoulos. 2007. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat. Med. 13: 543-551.
69. Kumar, K. R., L. Li, M. Yan, M. Bhaskarabhatla, A. B. Mobley, C. Nguyen, J. M. Mooney, J. D. Schatzle, E. K. Wakeland, and C. Mohan. 2006. Regulation of B cell tolerance by the lupus susceptibility gene Ly108. Science 312: 1665-1669.
70. Yurasov, S., H. Wardemann, J. Hammersen, M. Tsuiji, E. Meffre, V. Pascual, and M. C. Nussenzweig. 2005. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 201: 703-711.
71. Cappione, A., 3rd, J. H. Anolik, A. Pugh-Bernard, J. Barnard, P. Dutcher, G. Silverman, and I. Sanz. 2005. Germinal center exclusion of autoreactive B cells is defective in human systemic lupus erythematosus. J. Clin. Invest. 115: 3205-3216.