Impaired Clearance of Apoptotic Cells Induces the Activation of Autoreactive Anti-Sm Marginal Zone and B-1 B Cells

Journal of Immunology

Volumn 172, Issue 1, 2004, Pages 625-635

  Qian, Ye ^a   Wang, Hongsheng ^a   Clarke, Stephen H ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; ANTINUCLEAR ANTIBODY; RIBONUCLEOPROTEIN; SM ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANTIBODY PRODUCTION; APOPTOSIS; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL DEATH; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; SYSTEMIC LUPUS ERYTHEMATOSUS;

EID: 0346734179     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.1.625     Document Type: Article

References (58)

1. Tan, E. M. 1989. Antinuclear antibodies: diagnostic markers for autoimmune diseases and probes for cell biology. Adv. Immunol. 44:93.
2. Homma, M., T. Mimori, Y. Takeda, H. Akama, T. Yoshida, T. Ogasawara, and M. Akizuki. 1987. Autoantibodies to the Sm antigen: immunological approach to clinical aspects of systemic lupus erythematosus. J. Rheumatol. 14(Suppl. 13): 188.
3. 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.
4. 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.
5. 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.
6. 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.
7. Rosen, A., and L. Casciola-Rosen. 1999. Autoantigens as substrates for apoptotic proteases: implications for the pathogenesis of systemic autoimmune disease. Cell Death Differ. 6:6.
8. Casciola-Rosen, L. A., G. Anhalt, and A. Rosen. 1994. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179:1317.
9. Cocca, B. A., S. N. Seal, P. D'Agnillo, Y. M. Mueller, P. D. Katsikis, J. Rauch, M. Weigert, and M. Z. Radic. 2001. Structural basis for autoantibody recognition of phosphatidylserine-β2 glycoprotein I and apoptotic cells. Proc. Natl. Acad. Sci. USA 98:13826.
10. Mevorach, D., J. L. Zhou, X. Song, and K. B. Elkon. 1998. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med. 188:387.
11. Levine, J. S., R. Subang, J. S. Koh, and J. Rauch. 1998. Induction of antiphospholipid autoantibodies by β2-glycoprotein I bound to apoptotic thymocytes. J. Autoimmun. 11:413.
12. Gensler, T. J., M. Hottelet, C. Zhang, S. Schlossman, P. Anderson, and P. J. Utz. 2001. Monoclonal antibodies derived from BALB/c mice immunized with apoptotic Jurkat T cells recognize known autoantigens. J. Autoimmun. 16:59.
13. Baumann, I., W. Kolowos, R. E. Voll, B. Manger, U. Gaipl, W. L. Neuhuber, T. Kirchner, J. R. Kalden, and M. Herrmann. 2002. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum. 46:191.
14. Lu, Q., and G. Lemke. 2001. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293:306.
15. Scott, R. S., E. J. McMahon, S. M. Pop, E. A. Reap, R. Caricchio, P. L. Cohen, H. S. Earp, and G. K. Matsushima. 2001. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411:207.
16. Cohen, P. L., R. Caricchio, V. Abraham, T. D. Camenisch, J. C. Jennette, R. A. Roubey, H. S. Earp, G. Matsushima, and E. A. Reap. 2002. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196:135.
17. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, and M. J. Walport. 1998. Homozygous Clq deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19:56.
18. Bowness, P., K. A. Davies, P. J. Norsworthy, P. Athanassiou, J. Taylor-Wiedeman, L. K. Borysiewicz, P. A. Meyer, and M. J. Walport. 1994. Hereditary Clq deficiency and systemic lupus erythematosus. Qjm 87:455.
19. 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.
20. Camenisch, T. D., B. H. Koller, H. S. Earp, and G. K. Matsushima. 1999. A novel receptor tyrosine kinase, Mer, inhibits TNF-α production and lipopolysaccharide-induced endotoxic shock. J. Immunol. 162:3498.
21. Grimaldi, C. M., D. J. Michael, and B. Diamond. 2001. Cutting edge: expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. J. Immunol. 167:1886.
22. H CDR3 structures. J. Immunol. 155:2248.
23. Raynal, P., and H. B. Pollard. 1994. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim. Biophys. Acta 1197:63.
24. Vermes, I., C. Haanen, H. Steffens-Nakken, and C. Reutelingsperger. 1995. A novel assay for apoptosis: flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J. Immunol. Methods 184:39.
25. van Engeland, M., F. C. Ramaekers, B. Schutte, and C. P. Reutelingsperger. 1996. A novel assay to measure loss of plasma membrane asymmetry during apoptosis of adherent cells in culture. Cytometry 24:131.
26. Casciola-Rosen, L., A. Rosen, M. Petri, and M. Schlissel. 1996. Surface blebs on apoptotic cells are sites of enhanced procoagulant activity: implications for coagulation events and antigenic spread in systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 93:1624.
27. Kroese, F. G., E. C. Butcher, A. M. Stall, P. A. Lalor, S. Adams, and L. A. Herzenberg. 1989. Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int. Immunol. 1:75.
28. Kroese, F. G., W. A. Ammerlaan, and A. B. Kantor. 1993. Evidence that intestinal IgA plasma cells in μ, κ transgenic mice are derived from B-1 (Ly-1B) cells. Int. Immunol. 5:1317.
29. Watanabe, N., K. Ikuta, S. Fagarasan, S. Yazumi, T. Chiba, and T. Honjo. 2000. Migration and differentiation of autoreactive B-1 cells induced by activated gamma/delta T cells in antierythrocyte immunoglobulin transgenic mice. J. Exp. Med. 192:1577.
30. Watanabe, N., K. Ikuta, S. Nisitani, T. Chiba, and T. Honjo. 2002. Activation and differentiation of autoreactive B-1 cells by interleukin 10 induce autoimmune hemolytic anemia in Fas-deficient antierythrocyte immunoglobulin transgenic mice. J. Exp. Med. 196:141.
31. 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.
32. Ho, F., J. E. Lortan, I. C. MacLennan, and M. Khan. 1986. Distinct short-lived and long-lived antibody-producing cell populations. Eur. J. Immunol. 16:1297.
33. Tew, J. G., R. M. DiLosa, G. F. Burton, M. H. Kosco, L. I. Kupp, A. Masuda, and A. K. Szakal. 1992. Germinal centers and antibody production in bone marrow. Immunol. Rev. 126:99.
34. Smith, K. G., A. Light, G. J. Nossal, and D. M. Tarlinton. 1997. The extent of affinity maturation differs between the memory and antibody-forming cell compartments in the primary immune response. EMBO J. 16:2996.
35. Takahashi, Y., P. R. Dutta, D. M. Cerasoli, and G. Kelsoe. 1998. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. V. Affinity maturation develops in two stages of clonal selection. J. Exp. Med. 187:885.
36. Sze, D. M., K. M. Toellner, C. Garcia de Vinuesa, D. R. Taylor, and I. C. MacLennan. 2000. Intrinsic constraint on plasmablast growth and extrinsic limits of plasma cell survival. J. Exp. Med. 192:813.
37. LeFeber, W. P., D. A. Norris, S. R. Ryan, J. C. Huff, L. A. Lee, M. Kubo, S. T. Boyce, B. L. Kotzin, and W. L. Weston. 1984. Ultraviolet light induces binding of antibodies to selected nuclear antigens on cultured human keratinocytes. J. Clin. Invest. 74:1545.
38. Golan, T. D., K. B. Elkon, A. E. Gharavi, and J. G. Krueger. 1992. Enhanced membrane binding of autoantibodies to cultured keratinocytes of systemic lupus erythematosus patients after ultraviolet B/ultraviolet A irradiation. J. Clin. Invest. 90:1067.
39. Nemazee, D., D. Russell, B. Arnold, G. Haemmerling, J. Allison, J. F. Miller, G. Morahan, and K. Buerki. 1991. Clonal deletion of autospecific B lymphocytes. Immunol. Rev. 122:117.
40. 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.
41. Bikah, G., J. Carey, J. R. Ciallella, A. Tarakhovsky, and S. Bondada. 1996. CD5-mediated negative regulation of antigen receptor-induced growth signals in B-1 B cells. Science 274:1906.
42. Sandel, P. C., and J. G. Monroe. 1999. Negative selection of immature B cells by receptor editing or deletion is determined by site of antigen encounter. Immunity 10:289.
43. 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.
44. Herrmann, M., R. E. Voll, O. M. Zoller, M. Hagenhofer, B. B. Ponner, and J. R. Kalden. 1998. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum. 41:1241.
45. Potter, P. K., J. Cortes-Hernandez, P. Quartier, M. Botto, and M. J. Walport. 2003. Lupus-prone mice have an abnormal response to thioglycolate and an impaired clearance of apoptotic cells. J. Immunol. 170:3223.
46. Li, Y., H. Li, and M. Weigert. 2002. Autoreactive B cells in the marginal zone that express dual receptors. J. Exp. Med. 195:181.
47. 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.
48. Zeng, D., M. K. Lee, J. Tung, A. Brendolan, and S. Strober. 2000. Cutting edge: a role for CD1 in the pathogenesis of lupus in NZB/NZW mice. J. Immunol. 164:5000.
49. Wither, J. E., A. D. Paterson, and B. Vukusic. 2000. Genetic dissection of B cell traits in New Zealand Black mice: the expanded population of B cells expressing up-regulated costimulatory molecules shows linkage to Nba2. Eur. J. Immunol. 30:356.
50. 1 mice. Clin. Immunol. 94:51.
51. Amano, H., E. Amano, T. Moll, D. Marinkovic, N. Ibnou-Zekri, E. Martinez-Soria, I. Semac, T. Wirth, L. Nitschke, and S. Izui. 2003. The Yaa mutation promoting murine lupus causes defective development of marginal zone B cells. J. Immunol. 170:2293.
52. Hayakawa, K., R. R. Hardy, D. R. Parks, and L. A. Herzenberg. 1983. The "Ly-1 B" cell subpopulation in normal immunodefective, and autoimmune mice. J. Exp. Med. 157:202.
53. Hayakawa, K., R. R. Hardy, M. Honda, L. A. Herzenberg, and A. D. Steinberg. 1984. Ly-1 B cells: functionally distinct lymphocytes that secrete IgM autoantibodies. Proc. Natl. Acad. Sci. USA 81:2494.
54. Mohan, C., L. Morel, P. Yang, and E. K. Wakeland. 1998. Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupus-prone mice. Arthritis Rheum. 41:1652.
55. Mohan, C., L. Morel, P. Yang, and E. K. Wakeland. 1997. Genetic dissection of systemic lupus erythematosus pathogenesis: Sle2 on murine chromosome 4 leads to B cell hyperactivity. J. Immunol. 159:454.
56. Reap, E. A., E. S. Sobel, P. L. Cohen, and R. A. Eisenberg. 1993. Conventional B cells, not B-1 cells, are responsible for producing autoantibodies in lpr mice. J. Exp. Med. 177:69.
57. Goodnow, C. C., R. Brink, and E. Adams. 1991. Breakdown of self-tolerance in anergic B lymphocytes. Nature 352:532.
58. 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.