Autoreactive B cells escape clonal deletion by expressing multiple antigen receptors

Journal of Immunology

Volumn 164, Issue 8, 2000, Pages 4111-4119

  Kenny, James J ^a   Rezanka, Louis J ^a   Lustig, Ana ^a   Fischer, Randy T ^a   Voder, Jeffrey ^a   Marshall, Shannon ^a   Longo, Dan L ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN BCL 2;

ANIMAL CELL; ANTIBODY DETECTION; ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CLONAL ANERGY; CONTROLLED STUDY; GENE OVEREXPRESSION; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; IMMUNOREGULATION; LYMPHOID ORGAN; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 0034655136     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.164.8.4111     Document Type: Article

References (64)

1. Yancopoulos, G. M., and F. W. Alt. 1986. Regulation of the assembly and expression of variable-region genes. Annu. Rev. Immunol. 4:339.
2. Alt, F. W., T. K. Blackwell, and G. D. Yancopoulos. 1987. Development of the primary antibody repertoire. Science 238:1079.
3. Alt, F. W., E. M. Oltz, F. Young, J. Gorman, G. Taccioli, and J. Chen. 1992. VDJ recombination. Immunol. Today 13:306.
4. Storb, U., K. A. Ritchie, R. O'Brien, B. Arp, and R. Brinster. 1986. Expression, allelic exclusion and somatic mutation of mouse immunoglobulin κ genes. Immunol. Rev. 89:85.
5. Storb, U. 1987. Transgenic mice with immunoglobulin genes. Annu. Rev. Immunol. 5:151.
6. Storb, U. 1995. Ig gene expression and regulation in Ig transgenic mice. In Immunoglobulin Genes. T. Honjo and F. Alt, eds. Academic Press, New York, p. 345.
7. Uematsu, Y., S. Ryser, Z. Dembic, P. Borgulya, P. Krimpenfort, A. Berns, H. von Boehmer, and M. Steinmetz. 1988. In transgenic mice the introduced functional TCR βgene prevents expression of endogenous β genes. Cell 52:831.
8. Malissen, M., J. Trucy, J. Jouvin, E. Marche, P. A. Cazenave, R. Scollay, and B. Malissen. 1992. Regulation of TCR α and β gene allelic exclusion during T-cell development. Immunol. Today 13:315.
9. Nussenzweig, M. C., A. C. Shaw, E. Sinn, D. B. Danner, K. L. Holmes, H. C. Morse III, and P. Leder. 1987. Allelic exclusion in transgenic mice that express the membrane form of immunoglobulin. Science 236:816.
10. Nussenzweig, M., A. Shaw, E. Sinn, J. Campos-Torres, and P. Leder. 1988. Allelic exclusion in transgenic mice carrying mutant human IgM genes. J. Exp. Med. 167:1969.
11. Manz, J., K. Denis, O. Witte, R. Brinster, and U. Storb. 1988. Feedback inhibition of immunoglobulin gene rearrangement by membrane μ, but not by secreted μ heavy chains. J. Exp. Med. 168:1363.
12. Bumet, F. M. 1959. The Clonal Selection Theory of Acquired Immunity. Vanderbilt University Press, Nashville.
13. Kenny, J. J., G. Guelde, R. T. Fischer, and D. L. Longo. 1994. Induction of phosphocholine-specific antibodies in X-linked immune deficient mice: in vivo protection against a Streptococcus pneumoniae challenge. Int. Immunol. 6:561.
14. Fischer, R. T., D. L. Longo, and J. J. Kenny. 1995. A novel phosphocholine antigen protects both normal and X-linked immune deficient mice against Streptococcus pneumoniae: comparison of the 6-O-phosphocholine hydroxyhexanoate-conjugate with other phosphocholine-containing vaccines. J. Immunol. 154: 3373.
15. HI heavy chain of anti-phosphocholine antibodies alter binding to and protection against Streptococcus pneumoniae. Int. Immunol. 9:665.
16. Briles, D. E., M. Nahm, K. Schroer, J. Davie, P. Baker, J. F. Kearney, and R. Barletta. 1981. Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 Streptococcus pneumoniae. J. Exp. Med. 153:694.
17. Briles, D. E., C. Forman, S. Hudak, and J. L. Claflin. 1982. Anti-phosphorylcholine antibodies of the T15 idiotype are optimally protective against Streptococcus pneumoniae. J. Exp. Med. 156:1177.
18. Kenny, J. J., A. M. Stall, D. G. Sieckmann, M. C. Lamers, F. Finkleman, L. Finch, and D. L. Longo. 1991. Receptor-mediated elimination of phosphocholine-specific B cells in X-linked immune deficient mice. J. Immunol. 146: 2568.
19. Kenny, J. J., R. T. Fischer, A. Lustig, H. M. Dintzis, M. Katsumata, J. C. Reed, and D. L. Longo. 1996. bcl-2 alters the antigen-driven selection of B cells in μκ but not in μ-only Xid transgenic mice. J. Immunol. 157:1054.
20. Hartley, S. B., M. P. Cooke, D. A. Fulcher, A. W. Harris, S. Cory, A. Basten, and C. C. Goodnow. 1993. Elimination of self-reactive B lymphocytes proceeds in two stages: arrested development and cell death. Cell 72:325.
21. Melamed, D., R. J. Benschopk, J. C. Cambier, D. Nemazee, and R. J. Benschop. 1998. Developmental regulation of B lymphocyte immune tolerance compartmentalizes clonal selection from receptor selection. Cell 92:173.
22. Goodnow, C. C., J. G. Cyster, S. B. Hartley, S. E. Bell, M. P. Cooke, J. I. Healy, S. Akkaraju, J. C. Rathmell, S. L. Pogue, and K. P. Shokat. 1995. Self-tolerance checkpoints in B lymphocyte development. Adv. Immunol. 59:279.
23. Nemazee, D., and K. Buerki. 1989. Clonal deletion of autoreactive B lymphocytes in bone marrow chimeras. Proc. Natl. Acad. Sci. USA 86:8039.
24. Palanda, R., S. Schwers, R. M. Torres, D. Nemazee, and K. Rajewsky. 1997. Receptor editing in a transgenic mouse model: site, efficiency, and role in B cell tolerance and antibody diversity, Immunity 7:765.
25. Chen, C., Z. Nagy, M. Z. Radic, R. R. Hardy, D. Huszar, S. A. Campers, and M, Weigert. 1995 The site and stage of anti-DNA B-cell deletion. Nature 373: 252.
26. Gay, D., T. Saunders, S. Camper, and M. Weigert. 1993. Receptor editing: an approach by autoreactive B cells to escape tolerance. J. Exp. Med. 177:999.
27. Radic, M. Z., J. Erikson, S. Litwin, and M. Weigert. 1993. B lymphocytes may escape tolerance by revising their antigen receptors. J. Exp. Med. 177:1165.
28. Tiegs, S. L., D. M. Russell, and D. Nemazee. 1993. Receptor editing in self-reactive bone marrow B cells. J. Exp. Med. 177:1009.
29. - bone marrow cells in vitro. Immunity 6:429.
30. Melamed, D., and D. Nemazee. 1997. Self-antigen does not accelerate immature B cell apoptosis, but stimulates receptor editing as a consequence of developmental arrest. Proc. Natl. Acad. Sci. USA 94:9267.
31. Andersson, J., F. Melchers, and A. Rolink. 1995. Stimulation by T cell independent antigens can relieve the arrest of differentiation of immature auto-reactive B cells in the bone marrow. Scand. J. Immunol. 42:21.
32. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavioe, S. J. Smith-Gill. R. A. Brink, H. Pritchard-Briscoe, J. S. Wotherspoon, R. H. Loblay, K. Raphael, et al. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334:676.
33. Cooke, M. P., A. W. Heath, K. M. Shokat, Y. Zeng, F. D. Finkelman, P. S. Linsley, M. Howard, and C. C. Goodnow. 1994. Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J. Exp. Med. 179:425.
34. Xu, H., H. Li, E. Suri-Payer, R. R. Hardy, and M. Weigert. 1998. Regulation of anti-DNA B cells in recombination-activation gene deficient mice. J. Exp. Med. 188:1247.
35. Storb, U., C. Pinkert, B. Arp, P. Engler, K. Gollahon, J. Manz, W. Brady, and R. Brinster. 1986. Transgenic mice with μ and κ genes encoding antiphosphorylcholine antibodies. J. Exp. Med. 164:627.
36. Kitamura, D., J. Roes, R. Kuhn, and K. Rajewsky. 1991. A B-cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature 350:423.
37. Kitamura, D., and K. Rajewsky. 1992. Targeted disruption of μ chain membrane exon causes loss of heavy-chain allelic exclusion. Nature 356:154.
38. Kenny, J. J., C. O'Connell, D. G. Sieckmann, R. T. Fischer, and D. L. Longo. 1991. Selection of antigen-specific, idiotype positive B cells in transgenic mice expressing a rearranged M167-μ heavy chain gene. J. Exp. Med. 174:1189.
39. Kenny, J. J., A. M. Stall, R. T. Fischer, E. Derby, M. W. Yang, P. W. Tucker, and D. L. Longo. 1995. Ig(γ)2b transgenes promote B cell development but alternate developmental pathways appear to function in different transgenic lines. J. Immunol. 154:5694.
40. Rao, M., W. Lee, and D. Conrad. 1987. Characterization of a monoclonal antibody directed against the murine B lymphocyte receptor for IgE. J. Immunol. 138:1845.
41. Kenny, J. J., F. Finkleman, F. Macchiarini, W. C. Kopp, U. Storb. and D. L. Longo. 1989. Alteration of the B cell surface phenotype, immune response to phosphocholine and the B cell repertoire in M167 μ plus κ transgenic mice. J. Immunol. 138:1363.
42. Sieckmann, D. G., K. Holmes, P. Hornbeck, E. Martin, G. Guelde, S. Bondada, D. L. Longo, and J. J. Kenny. 1994. B cells from M167 μκ transgenic mice fail to proliferate after stimulation with soluble anti-Ig antibodies. J. Immunol. 152: 4873.
43. Shinkal, Y., G. Rathburn, K. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A. M. Stall, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V-(D)-J rearrangement. Cell 65:855.
44. Murakami, M., T. Tsubata, M. Okamoto, A. Shimizu, S. Kumagai, H. Imura, and T. Honjo. 1992. Antigen-induced apoptotic death of Ly-1 B cells responsible for autoimmune disease in transgenic mice. Nature 357:77.
45. Okamoto, M., M. Murakami, A. Shimizu, S. Ozaki, T. Tsubata, S. Kumagai, and T. Honjo. 1992. A transgenic model of autoimmune hemolytic anemia. J. Exp. Med. 175:71.
46. Nisitani, S., T. Tsubata, M. Murakami, M. Okamoto, and T. Honjo. 1993. The bcl-2 gene product inhibits clonal deletion of self-reactive B lymphocytes in the periphery but not in the bone marrow. J. Exp. Med. 178:1247.
47. Lang, J., B. Arnold, G. Hammerling, A. W. Harris, S. Korsmeyer, D. Russell, A. Strasser, D. Nemazee, G. J. Hammerling, S. J. Korsmeyer, et al. 1997. Enforced bcl-2 expression inhibits antigen-mediated clonal elimination of peripheral B cells in an antigen dose-dependent manner and promotes receptor editing in autoreactive, immature B cells. J. Exp. Med. 186:1513.
48. Lam, K., and K. Rajewsky. 1998. Rapid elimination of mature autoreactive B cells demonstrated by Cre-induced change in B cell antigen receptor specificity in vivo. Proc. Natl. Acad. Sci. USA 95:13171.
49. Stall, A. M., F. G. Kroese, F. T. Gadus, D. G. Sieckmann, and L. A. Herzenberg. 1988. Rearrangement and expression of endogenous immunoglobulin genes occurs in many murine B cells expressing transgenic membrane IgM. Proc. Natl. Acad. Sci. USA 85:3546.
50. Lam, K., L. A. Herzenberg, and A. M. Stall. 1993. A high frequency of hybridomas from M54 μ heavy chain transgenic mice initially co-express transgenic and rearranged endogenous μ genes. Int. Immunol. 5:1011.
51. Roth, P. E., L. Doglio, J. T. Manz, J. Y. Kim, D. Lo, and U. Storb. 1993. Immunoglobulin γ2b transgenes inhibit heavy chain gene rearrangement, but cannot promote B cell development. J. Exp. Med. 178:2007.
52. Chen, J., M. Trounstine, C. Kurahara, F. Young, C. Kuo, Y. Xu, J. F. Loring, F W. Alt, and D. Huszar. 1993. B cell development in mice that lack one or both immunoglobulin κ light chain genes. EMBO J. 12:821.
53. Oka, Y., A. G. Rolink, J. Andersson, M. Kamanaka, J. Uchida, T. Yasui, T. Kishimoto, H. Kikutani, and F. Melchers. 1996. Profound reduction of mature B cell numbers, reactivities and serum Ig levels in mice which simultaneously carry the xid and CD40 deficiency genes. Int. Immunol. 8:1675.
54. Khan, W. N., A. Nilsson, E. Mizoguchi, E. Castigli, J. Forsell, A. K. Bhan, R. Geha, P. Sideras, and F. W. Alt. 1997. Impaired B cell maturation in mice lacking Bruton's tyrosine kinase (Btk) and CD40. Int. Immunol. 9:395.
55. + B cell precursor in B-1 cell differentiation. J. Exp. Med. 187:1325.
56. + B lymphocytes. Im. Immunol. 2:5/5.
57. Iliev, A., L. Spatz. S. Ray, and B. Diamond. 1994. Lack of allelic exclusion permits autoreactive B cells to escape deletion. J. Immunol 153:3551.
58. Gollahon, K., J. Hagman, R. Brinster, and U. Storb. 1988. Ig-producing B cells do not show feedback inhibition of gene rearrangement. J. Immunol. 141:2771.
59. Rudikoff, S. 1983. Immunoglobulin structure-function correlates: antigen binding and idiotypes. Contemp. Top. Mol. Biol. 9:169.
60. Cosenza, H., and H. Kohler. 1972. Specific inhibition of plaque formation to phosphorylcholine by antibody against antibody. Science 176:1027.
61. Claflin, J. L., R. Lieberman, and J. Davie. 1974. Clonal nature of the immune response to phosphorylcholine. I. Specificity, class, and idiotype of phosphorylcholine-binding receptors on lymphoid cells. J. Exp. Med. 139:58.
62. Claflin, J. L., and J. Davie. 1974. Clonal nature of the immune response to phosphorylcholine. IV. Idiotypic uniformity of binding site antigenic determinants among mouse phosphorylcholine antibodies. J. Exp. Med. 140:673.
63. Claflin, J. L. 1976. Uniformity in the clonal repertoire for the immune response to phosphorylcholine in mice. Eur. J. Immunol. 6:669.
64. Gearhart, P. J., N. H. Sigal, and N. R. Klinman. 1977. The monoclonal anti-phosphocholine antibody response in several murine strains: genetic implications of a diverse repertoire. J. Exp. Med. 145:876.