Short-lived plasmablasts dominate the early spontaneous rheumatoid factor response: Differentiation pathways, hypermutating cell types, and affinity maturation outside the germinal center

Journal of Immunology

Volumn 174, Issue 11, 2005, Pages 6879-6887

  William, Jacqueline ^a   Euler, Chad ^a   Shlomchik, Mark J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; RHEUMATOID FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; BLAST CELL; CELL DIFFERENTIATION; CELL LABELING; CELL MATURATION; CELL METABOLISM; CELL TYPE; CONTROLLED STUDY; GENE MUTATION; GERMINAL CENTER; LYMPHOCYTE ACTIVATION; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; SOMATIC HYPERMUTATION;

EID: 18944398750     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.11.6879     Document Type: Article

References (54)

1. Lipsky, P. E. 2001. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat. Immunol. 2: 764-766.
2. Goodnow, C. C., S. Adelstein, and A. Basten. 1990. The need for central and peripheral tolerance in the B cell repertoire. Science 248: 1373-1379.
3. Nemazee, D., D. Russell, B. Arnold, G. Haemmerling, J. Allison, J. F. A. P. Miller, G. Morahan, and K. Beurki. 1991. Clonal deletion of autospecific B lymphocytes. Immunol. Rev. 122: 117-132.
4. 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.
5. Chen, C., M. Z. Radic, J. Erikson, S. A. Camper, S. Litwin, R. R. Hardy, and M. Weigert. 1994. Deletion and editing of B cells that express antibodies to DNA. J. Immunol. 152: 1970-1982.
6. 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.
7. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavoie, 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: 676-682.
8. Erikson, J., M. Z. Radic, S. A. Camper, R. R. Hardy, and M. G. Weigert. 1991. Expression of anti-DNA immunoglobulin transgenes in non-autoimmune mice. Nature 349: 331-334.
9. 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.
10. Russell, D. M., Z. Dembic, G. Morahan, J. F. A. P. Miller, K. Burki, and D. Nemazee. 1991. Peripheral deletion of self-reactive B cells. Nature 354: 308-311.
11. 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.
12. Santulli-Marotto, S., Y. Qian, S. Ferguson, and S. H. Clarke. 2001. Anti-Sm B cell differentiation in Ig transgenic MRL/Mp-lpr/lpr mice: altered differentiation and an accelerated response. J. Immunol. 166: 5292-5299.
13. 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.
14. Shlomchik, M. J., D. Zharhary, T. Saunders, S. Camper, and M. Weigert. 1993. A rheumatoid factor transgenic mouse model of autoantibody regulation. Int. Immunol. 5: 1329-1341.
15. 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.
16. 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.
17. Li, Y., H. Li, D. Ni, and M. Weigert. 2002. Anti-DNA B cells in MRL/lpr mice show altered differentiation and editing pattern. J. Exp. Med. 196: 1543-1552.
18. Wang, H., and M. J. Shlomchik. 1999. Autoantigen-specific B cell activation in Fas-deficient rheumatoid factor immunoglobulin transgenic mice. J. Exp. Med. 190: 639-649.
19. Howard, T. W., M. J. Iannini, J. J. Burge, and J. T. Davis. 1991. Rheumatoid factor, cryoglobulinemia, anti-DNA, and renal disease in patients with systemic lupus erythematosus. J. Rheumatol. 18: 826-830.
20. Izui, S., M. Abdelmoula, Y. Gyotoku, G. Lange, and P. H. Lambert. 1984. IgG rheumatoid factors and cryoglobulins in mice bearing the mutant gene lpr (lympholiferation). Rheumatol. Int. 4 (Suppl): 45.
21. Wolfowicz, C. B., P. Sakorasas, T. L. Rothstein, and A. Marshak-Rothstein. 1988. Oligoclonality of rheumatoid factors arising spontaneously in lpr/lpr mice. Clin. Immunol. Immunopathol. 46: 382-395.
22. Shlomchik, M. J., D. Zharhary, T. Saunders, S. A. Camper, and M. G. Weigert. 1993. A rheumatoid factor transgenic mouse model of autoantibody regulation. Int. Immunol. 5: 1329-1341.
23. Hannum, L. G., D. Ni, A. M. Haberman, M. G. Weigert, and M. J. Shlomchik. 1996. A disease-related rheumatoid factor autoantibody is not tolerized in a normal mouse: implications for the origins of autoantibodies in autoimmune disease. J. Exp. Med. 184: 1269.
24. Andrews, B. S., R. A. Eisenberg, A. N. Theofilopoulos, S. Izui, C. B. Wilson, P. J. McConahey, E. D. Murphy, J. B. Roths, and F. J. Dixon. 1978. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J. Exp. Med. 148: 1198.
25. Eisenberg, R. A., S. Y. Craven, R. W. Warren, and P. L. Cohen. 1987. Stochastic control of anti-Sm autoantibodies in MRL/Mp-lpr/lpr mice. J. Clin. Invest. 80: 691-697.
26. Riedy, M. C., K. A. Muirhead, C. P. Jensen, and C. C. Stewart. 1991. Use of a photolabeling technique to identify nonviable cells in fixed homologous or heterologous cell populations. Cytometry 12: 133-139.
27. Hannum, L. G., A. M. Haberman, S. M. Anderson, and M. J. Shlomchik. 2000. Germinal center initiation, variable gene region hypermutation, and mutant B cell selection without detectable immune complexes on follicular dendritic cells. J. Exp. Med. 192: 931-942.
28. hi splenic B cells are an immature developmental intermediate in the production of long-lived marrow-derived B cells. J. Immunol. 151: 4431-4444.
29. Wang, H., and M. J. Shlomchik. 1997. High affinity rheumatoid factor transgenic B cells are eliminated in normal mice. J. Immunol. 159: 1125-1134.
30. Hargreaves, D. C., P. L. Hyman, T. T. Lu, V. N. Ngo, A. Bidgol, G. Suzuki, Y. R. Zou, D. R. Littman, and J. G. Cyster. 2001. A coordinated change in chemokine responsiveness guides plasma cell movements. J. Exp. Med. 194: 45-56.
31. Shaffer, A. L., K. I. Lin, T. C. Kuo, X. Yu, E. M. Hurt, A. Rosenwald, J. M. Giltnane, L. Yang, H. Zhao, K. Calame, and L. M. Staudt. 2002. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17: 51-62.
32. Calame, K. L. 2001. Plasma cells: finding new light at the end of B cell development. Nat. Immunol. 2: 1103-1108.
33. Jego, G., N. Robillard, D. Puthier, M. Amiot, F. Accard, D. Pineau, J.-L. Harousseau, R. Bataille, and C. Pellat-Deceunynck. 1999. Reactive plasmacytoses are expansions of plasmablasts retaining the capacity to differentiate into plasma cells. Blood 94: 701-712.
34. Odendahl, M., A. Jacobi, A. Hansen, E. Feist, F. Hiepe, G. R. Burmester, P. E. Lipsky, A. Radbruch, and T. Dorner. 2000. Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J. Immunol. 165: 5970-5979.
35. MacLennan, I. C. M., K.-M. Toellner, A. F. Cunningham, K. Serre, D. M. Y. Sze, E. Zuniga, M. C. Cook, and C. G. Vinuesa. 2003. Extrafollicular antibody responses. Immunol. Rev. 194: 8-18.
36. Allen, D., T. Simon, F. Sablitzky, K. Rajewsky, and A. Cumano. 1988. Antibody engineering for the analysis of affinity maturation of an anti-hapten response. EMBO J. 7: 1995-2001.
37. Berek, C., and C. Milstein. 1987. Mutation drift and repertoire shift in the maturation of the immune response. Immunol. Rev. 96: 23-41.
38. Shlomchik, M. J., A. H. Aucoin, D. S. Pisetsky, and M. G. Weigert. 1987. Structure and function af anti-DNA antibodies derived from a single autoimmune mouse. Proc. Natl. Acad. Sci. USA 84: 9150-9154.
39. Radic, M. Z., and M. Weigert. 1994. Genetic and structural evidence for antigen selection of anti-DNA antibodies. Ann. Rev. Immunol. 12: 487-520.
40. Jacobson, B. A., J. Sharon, H. Shan, M. Shlomchik, M. G. Weigert, and A. Marshak-Rothstein. 1994. An isotype switched and somatically mutated rheumatoid factor clone isolated from a MRL-lpr/lpr mouse exhibits limited intraclonal affinity maturation. J. Immunol. 152: 4489-4499.
41. 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.
42. Cumano, A., and K. Rajewsky. 1985. Structure of primary anti-(4-hydroxy-3-nitrophenyl)acetyl (NP) antibodies in normal and idiotypically suppressed C57BL/6 mice. Eur. J. Immunol. 15: 512-520.
43. Wehrli, N., D. F. Legier, D. Finke, K. M. Toellner, P. Loetscher, M. Baggiolini, I. C. MacLennan, and H. Acha-Orbea. 2001. Changing responsiveness to chemokines allows medullary plasmablasts to leave lymph nodes. Eur. J. Immunol. 31: 609-616.
44. Hauser, A. E., G. F. Debes, S. Arce, G. Cassese, A. Hamann, A. Radbruch, and R. A. Manz. 2002. Chemotactic responsiveness toward ligands for CXCR3 and CXCR4 is regulated on plasmablasts during the time course of a memory immune response. J. Immunol. 169: 1277-1282.
45. Garcia De Vinuesa, C., A. Gulbranson-Judge, M. Khan, P. O'Leary, M. Cascalho, M. Wabl, G. G. Klaus, M. J. Owen, and I. C. MacLennan. 1999. Dendritic cells associated with plasmablast survival. Eur. J. Immunol. 29: 3712-3721.
46. Balazs, M., F. Martin, T. Zhou, and J. Kearney. 2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17: 341-352.
47. Mackay, F., and J. L. Browning. 2002. BAFF: a fundamental survival factor for B cells. Nat. Rev. Immunol. 2: 465-475.
48. Gross, J. A., J. Johnston, S. Mudri, R. Enselman, S. R. Dillon, K. Madden, W. Xu, J. Parrish-Novak, D. Foster, C. Lofton-Day, et al. 2000. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404: 995-999.
49. Erickson, L. D., L. L. Lin, B. Duan, L. Morel, and R. J. Noelle. 2003. A genetic lesion that arrests plasma cell homing to the bone marrow. Proc. Natl. Acad. Sci. USA 100: 12905-12910.
50. Cambridge, G., M. J. Leandro, J. C. Edwards, M. R. Ehrenstein, M. Salden, M. Bodman-Smith, and A. D. Webster. 2003. Serologic changes following B lymphocyte depletion therapy for rheumatoid arthritis. Arthritis Rheum. 48: 2146-2154.
51. Specks, U., F. C. Fervenza, T. J. McDonald, and M. C. Hogan. 2001. Response of Wegener's granulomatosis to anti-CD20 chimeric monoclonal antibody therapy. Arthritis Rheum. 44: 2836-2840.
52. Kleinstem, S. H., Y. Louzoun, and M. J. Shlomchik. 2003. Estimating hypermutation rates from clonal tree data. J. Immunol. 171: 4639-4649.
53. William, J., C. Euler, E. Leadbetter, A. Marshak-Rothstein, and M. J. Shlomchik. 2005. Visualizing the onset and evolution of an autoantibody response in systemic autoimmunity. J. Immunol. 174: 6872-6878.
54. Hoyer, B. F., K. Moser, A. E. Hauser, A. Peddinghaus, C. Voigt, D. Eilat, A. Radbruch, F. Hiepe, and R. A. Manz. 2004. Short-lived plasmablasts and long-lived plasma cells contribute to chronic humoral autoimmunity in NZB/W mice. J. Exp. Med. 199: 1577-1584.