B cell receptor affinity and B cell subset identity integrate to define the effectiveness, affinity threshold, and mechanism of anergy

Journal of Immunology

Volumn 181, Issue 6, 2008, Pages 3834-3840

  Diz, Ramiro ^a   McCray, Suzanne K ^a   Clarke, Stephen H ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD45 ANTIGEN; IMMUNOGLOBULIN M; INTERFERON REGULATORY FACTOR 4; SYNDECAN 1; TOLL LIKE RECEPTOR; X BOX BINDING PROTEIN 1; AUTOANTIBODY; AUTOANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; SM NUCLEAR ANTIGENS; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CLONAL ANERGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RECEPTOR AFFINITY; REGULATORY MECHANISM; SPLEEN CELL; ANIMAL; BIOSYNTHESIS; CELL ADHESION; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; B-LYMPHOCYTE SUBSETS; CELL ADHESION; CELL DIFFERENTIATION; CELLS, CULTURED; CLONAL ANERGY; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; PROTEIN BINDING; RECEPTORS, ANTIGEN, B-CELL; RIBONUCLEOPROTEINS, SMALL NUCLEAR; SELF TOLERANCE;

EID: 56149116164     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.6.3834     Document Type: Article

References (48)

1. 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: 279-368.
2. 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: 999-1008. (Pubitemid 23097389)
3. Nemazee, D., and M. Weigert. 2000. Revising B cell receptors. J. Exp. Med. 191: 1813-1817.
4. Mandik-Nayak, L., A. Bui, H. Noorchashm, A. Eaton, and J. Erikson. 1997. Regulation of anti-double-stranded DNA B cells in nonautoimmune mice: localization to the T-B interface of the splenic follicle. J. Exp. Med. 186: 1257-1267. (Pubitemid 27469021)
5. Cyster, J. G., S. B. Hartley, and C. C. Goodnow. 1994. Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire. Nature 371: 389-395.
6. Culton, D. A., B. P. O'Conner, K. L. Conway, R. Diz, J. Rutan, B. J. Vilen, and S. H. Clarke. 2006. Early preplasma cells define a tolerance checkpoint for autoreactive B cells. J. Immunol. 176: 790-802.
7. William, J., C. Euler, N. Primarolo, and M. J. Shlomchik. 2006. B cell tolerance checkpoints that restrict pathways of antigen-driven differentiation. J. Immunol. 176: 2142-2151. (Pubitemid 43201661)
8. Merrell, K. T., R. J. Benschop, S. B. Gauld, K. Aviszus, D. Decote-Ricardo, L. J. Wysocki, and J. C. Cambier. 2006. Identification of anergic B cells within a wild-type repertoire. Immunity 25: 953-962.
9. Wardemann, H., S. Yurasov, A. Schaefer, J. W. Young, E. Meffre, and M. C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377. (Pubitemid 37075812)
10. Rui, L., J. I. Healy, J. Blasioli, and C. C. Goodnow. 2006. ERK signaling is a molecular switch integrating opposing inputs from B cell receptor and T cell cytokines to control TLR4-driven plasma cell differentiation. J. Immunol. 177: 5337-5346. (Pubitemid 44527606)
11. Rui, L., C. G. Vinuesa, J. Blasioli, and C. C. Goodnow. 2003. Resistance to CpG DNA-induced autoimmunity through tolerogenic B cell antigen receptor ERK signaling. Nat. Immunol. 4: 594-600. (Pubitemid 36701344)
12. Gilbert, M. R., D. G. Carnathan, P. C. Cogswell, L. Lin, A. S. Baldwin, Jr., and B. J. Vilen. 2007. Dendritic cells from lupus-prone mice are defective in repressing immunoglobulin secretion. J. Immunol. 178: 4803-4810.
13. Kilmon, M. A., J. A. Rutan, S. H. Clarke, and B. J. Vilen. 2005. Low-affinity, Smith antigen-specific B cells are tolerized by dendritic cells and macrophages. J. Immunol. 175: 37-41. (Pubitemid 40884299)
14. Kilmon, M. A., N. J. Wagner, A. L. Garland, L. Lin, K. Aviszus, L. J. Wysocki, and B. J. Vilen. 2007. Macrophages prevent the differentiation of autoreactive B cells by secreting CD40 ligand and IL-6. Blood 110: 1595-1602.
15. Borrero, M., and S. H. Clarke. 2002. Low-affinity anti-Smith antigen B cells are regulated by anergy as opposed to developmental arrest or differentiation to B-1. J. Immunol. 168: 13-21. (Pubitemid 34014097)
16. Qian, Y., C. Santiago, M. Borrero, T. F. Tedder, and S. H. Clarke. 2001. Lupus-specific antiribonucleoprotein B cell tolerance in nonautoimmune mice is maintained by differentiation to B-1 and governed by B cell receptor signaling thresholds. J. Immunol. 166: 2412-2419. (Pubitemid 32173476)
17. Qian, Y., H. Wang, and S. H. Clarke. 2004. Impaired clearance of apoptotic cells induces the activation of autoreactive anti-Sm marginal zone and B-1 B cells. J. Immunol. 172: 625-635. (Pubitemid 38020521)
18. Acevedo-Suarez, C. A., C. Hulbert, E. J. Woodward, and J. W. Thomas. 2005. Uncoupling of anergy from developmental arrest in anti-insulin B cells supports the development of autoimmune diabetes. J. Immunol. 174: 827-833.
19. Nguyen, K. A., L. Mandik, A. Bui, J. Kavaler, A. Norvell, J. G. Monroe, J. H. Roark, and J. Erikson. 1997. Characterization of anti-single-stranded DNA B cells in a non-autoimmune background. J. Immunol. 159: 2633-2644. (Pubitemid 127681281)
20. Roark, J. H., A. Bui, K. A. Nguyen, L. Mandik, and J. Erikson. 1997. Persistence of functionally compromised anti-double-stranded DNA B cells in the periphery of non-autoimmune mice. Int. Immunol. 9: 1615-1626.
21. Lopes-Carvalho, T., and J. F. Kearney. 2004. Development and selection of marginal zone B cells. Immunol. Rev. 197: 192-205. (Pubitemid 38142177)
22. Qian, Y., K. L. Conway, X. Lu, H. M. Seitz, G. K. Matsushima, and S. H. Clarke. 2006. Autoreactive MZ and B-1 B-cell activation by Faslpr is coincident with an increased frequency of apoptotic lymphocytes and a defect in macrophage clearance. Blood 108: 974-982. (Pubitemid 44154633)
23. Santulli-Marotto, S., M. W. Retter, R. Gee, M. J. Mamula, and S. H. Clarke. 1998. Autoreactive B cell regulation: peripheral induction of developmental arrest by lupus-associated autoantigens. Immunity 8: 209-219. (Pubitemid 28123748)
24. Arnold, L. W., C. A. Pennell, S. K. McCray, and S. H. Clarke. 1994. Development of B-1 cells: segregation of phosphatidyl choline-specific B cells to the B-1 population occurs after immunoglobulin gene expression. J. Exp. Med. 179: 1585-1595.
25. Iwakoshi, N. N., A. H. Lee, and L. H. Glimcher. 2003. The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response. Immunol. Rev. 194: 29-38. (Pubitemid 36886426)
26. Sciammas, R., A. L. Shaffer, J. H. Schatz, H. Zhao, L. M. Staudt, and H. Singh. 2006. Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25: 225-236. (Pubitemid 44224149)
27. Norvell, A., and J. G. Monroe. 1996. Acquisition of surface IgD fails to protect from tolerance-induction. Both surface IgM- and surface IgD-mediated signals induce apoptosis of immature murine B lymphocytes. J. Immunol. 156: 1328-1332. (Pubitemid 26065838)
28. Sater, R. A., P. C. Sandel, and J. G. Monroe. 1998. B cell receptor-induced apoptosis in primary transitional murine B cells: signaling requirements and modulation by T cell help. Int. Immunol. 10: 1673-1682.
29. Oliver, A. M., F. Martin, G. L. Gartland, R. H. Carter, and J. F. Kearney. 1997. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 27: 2366-2374.
30. Krutzik, P. O., M. R. Clutter, and G. P. Nolan. 2005. Coordinate analysis of murine immune cell surface markers and intracellular phosphoproteins by flow cytometry. J. Immunol. 175: 2357-2365.
31. Tze, L. E., E. A. Baness, K. L. Hippen, and T. W. Behrens. 2000. Ig light chain receptor editing in anergic B cells. J. Immunol. 165: 6796-6802.
32. Wen, L., J. Brill-Dashoff, S. A. Shinton, M. Asano, R. R. Hardy, and K. Hayakawa. 2005. Evidence of marginal-zone B cell-positive selection in spleen. Immunity 23: 297-308. (Pubitemid 41317797)
33. Lau, C. M., C. Broughton, A. S. Tabor, S. Akira, R. A. Flavell, M. J. Mamula, S. R. Christensen, M. J. Shlomchik, G. A. Viglianti, I. R. Rifkin, and A. Marshak-Rothstein. 2005. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202: 1171-1177.
34. Viglianti, G. A., C. M. Lau, T. M. Hanley, B. A. Miko, M. J. Shlomchik, and A. Marshak-Rothstein. 2003. Activation of autoreactive B cells by CpG dsDNA. Immunity 19: 837-847.
35. Huang, H., J. F. Kearney, M. J. Grusby, C. Benoist, and D. Mathis. 2006. Induction of tolerance in arthritogenic B cells with receptors of differing affinity for self-antigen. Proc. Natl. Acad. Sci. USA 103: 3734-3739. (Pubitemid 43376624)
36. Hayakawa, K., M. Asano, S. A. Shinton, M. Gui, L. J. Wen, J. Dashoff, and R. R. Hardy. 2003. Positive selection of anti-thy-1 autoreactive B-1 cells and natural serum autoantibody production independent from bone marrow B cell development. J. Exp. Med. 197: 87-99. (Pubitemid 36110260)
37. Chen, X., F. Martin, K. A. Forbush, R. M. Perlmutter, and J. F. Kearney. 1997. Evidence for selection of a population of multi-reactive B cells into the splenic marginal zone. Int. Immunol. 9: 27-41. (Pubitemid 27062886)
38. Lopes-Carvalho, T., and J. F. Kearney. 2005. Marginal zone B cell physiology and disease. Curr. Dir. Autoimmun. 8: 91-123.
39. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617-629. (Pubitemid 32520872)
40. Li, Y., H. Li, and M. Weigert. 2002. Autoreactive B cells in the marginal zone that express dual receptors. J. Exp. Med. 195: 181-188. (Pubitemid 34461262)
41. Lesley, R., Y. Xu, S. L. Kalled, D. M. Hess, S. R. Schwab, H. B. Shu, and J. G. Cyster. 2004. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20: 441-453. (Pubitemid 38482122)
42. Zhang, J., V. Roschke, K. P. Baker, Z. Wang, G. S. Alarcon, B. J. Fessler, H. Bastian, R. P. Kimberly, and T. Zhou. 2001. Cutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosus. J. Immunol. 166: 6-10. (Pubitemid 32038409)
43. Cheema, G. S., V. Roschke, D. M. Hilbert, and W. Stohl. 2001. Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum. 44: 1313-1319.
44. Acevedo-Suarez, C. A., D. M. Kilkenny, M. B. Reich, and J. W. Thomas. 2006. Impaired intracellular calcium mobilization and NFATc1 availability in tolerant anti-insulin B cells. J. Immunol. 177: 2234-2241.
45. Vilen, B. J., T. Nakamura, and J. C. Cambier. 1999. Antigen-stimulated dissociation of BCR mIg from Ig-α/Ig-β: implications for receptor desensitization. Immunity 10: 239-248.
46. high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J. Immunol. 162: 7198-7207.
47. Attanavanich, K., and J. F. Kearney. 2004. Marginal zone, but not follicular B cells, are potent activators of naive CD4 T cells. J. Immunol. 172: 803-811. (Pubitemid 38113736)
48. Viau, M., N. S. Longo, P. E. Lipsky, L. Bjorck, and M. Zouali. 2004. Specific in vivo deletion of B-cell subpopulations expressing human immunoglobulins by the B-cell superantigen protein L. Infect. Immun. 72: 3515-3523. (Pubitemid 38697778)