Enforced Bcl-2 expression in B lymphocytes induces rheumatoid factor and anti-DNA production, but the Yaa mutation promotes only anti-DNA production

European Journal of Immunology

Volumn 34, Issue 4, 2004, Pages 1077-1084

  Kuroki, Aki ^a   Moll, Thomas ^a   López Hoyos, Marcos ^b   Fossati Jimack, Liliane ^c   Ibnou Zekri, Nabila ^a   Kikuchi, Shuichi ^a   Merino, Jesús ^d   Merino, Ramón ^b   Izui, Shozo ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^c IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^d UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

Apoptosis; Autoantibody; Immune complexes; Rheumatoid arthritis; Systemic lupus erythematosus

Indexed keywords

AUTOANTIBODY; DNA ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; PROTEIN BCL 2; RHEUMATOID FACTOR; ANTINUCLEAR ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; BLOOD SAMPLING; BONE MARROW CELL; CHIMERA; CONTROLLED STUDY; GENE MUTATION; GENE OVEREXPRESSION; GLOMERULONEPHRITIS; HISTOPATHOLOGY; IMMUNE RESPONSE; LYMPHOCYTE DEPLETION; MALE; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROLOGY; STATISTICAL ANALYSIS; TRANSGENIC MOUSE; ANIMAL; BIOSYNTHESIS; BLOOD; COMPARATIVE STUDY; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODIES, ANTINUCLEAR; APOPTOSIS; ARTHRITIS, RHEUMATOID; B-LYMPHOCYTES; CHIMERA; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLOMERULONEPHRITIS; HUMANS; IMMUNOGLOBULIN G; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICE; MUTATION; PROTO-ONCOGENE PROTEINS C-BCL-2; RHEUMATOID FACTOR;

EID: 2442664892     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200424859     Document Type: Article

References (42)

1. Van Snick, J. L. and Masson, P. L., Age-dependent production of IgA and IgM autoantibodies against IgG2a in a colony of 129/Sv mice. J. Exp. Med. 1979. 149: 1519-1530.
2. Izui, S., Eisenberg, R. A. and Dixon, F. J., IgM rheumatoid factors in mice injected with bacterial lipopolysaccharides. J. Immunol. 1979. 122: 2096-2102.
3. Van Snick, J. and Coulie, P., Rheumatoid factors and secondary immune responses in the mouse. I. Frequent occurrence of hybridomas secreting IgM anti-IgG1 autoantibodies after immunization with protein antigens. Eur. J. Immunol. 1983. 13: 890-894.
4. Nemazee, D. A. and Sato, V. L., Induction of rheumatoid antibodies in the mouse. Regulated production of autoantibody in the secondary humoral response. J. Exp. Med. 1983. 158: 529-545.
5. Theofilopoulos, A. N., Balderas, R. S., Hang, L. and Dixon, F. J., Monoclonal IgM rheumatoid factors derived from arthritic MRL/Mp-lpr/lpr mice. J. Exp. Med. 1983. 158: 901-919.
6. Wolfowicz, C. B., Sakorafas, P., Rothstein, T. L. and Marshak-Rothstein, A., Oligoclonality of rheumatoid factors arising spontaneously in lpr/lpr mice. Clin. Immunol. Immunopathol. 1988. 46: 382-395.
7. Shibata, T., Berney, T., Spertini, F. and Izui, S., Rheumatoid factors in mice bearing the lpr or gld mutation. Selective production of rheumatoid factor cryoglobulins in MRL/MpJ-lpr/lpr mice. Clin. Exp. Immunol. 1992. 87: 190-195.
8. Eisenberg, R. A., Thor, L. T. and Dixon, F. J., Serum-serum interactions in autoimmune mice. Arthritis Rheum. 1979. 22: 1074-1081.
9. Izui, S. and Eisenberg, R. A., Circulating anti-DNA-rheumatoid factor complexes in MRL/l mice. Clin. Immunol. Immunopathol. 1980. 15: 536-551.
10. Kunkel, H. G., Müller-Eberhard, H. J., Fudenberg, H. H. and Tomasi, T. B., Gamma globulin complexes in rheumatoid arthritis and certain other conditions. J. Clin. Invest. 1961. 40: 117.
11. Andrews, B. S., Eisenberg, R. A., Theofilopoulos, A. N., Izui, S., Wilson, C. B., McConahey, P. J., Murphy, E. D., Roths, J. B. and Dixon, F. J., Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J. Exp. Med. 1978. 148: 1198-1215.
12. Barden, J. H. M., Hang, L. M., McConahey, P. J. and Dixon, F. J., Analysis of vascular lesions in murine SLE. J. Immunol. 1983. 130: 1699-1705.
13. Hang, L., Theofilopoulos, A. N. and Dixon, F. J., A spontaneous rheumatoid arthritis-like disease in MRL/l mice. J. Exp. Med. 1982. 155: 1690-1701.
14. Berney, T., Fulpius, T., Shibata, T., Reininger, L., Van Snick, J., Shan, H., Weigert, M., Marshak-Rothstein, A. and Izui, S., Selective pathogenicity of murine rheumatoid factors of the cryoprecipitable IgG3 subclass. Int. Immunol. 1992. 4: 93-99.
15. Kikuchi, S., Pastore, Y., Fossati-Jimack, L., Kuroki, A., Yoshida, H., Fulpius, T., Araki, K., Takahashi, S., Lemoine, R., Reininger, L. and Izui, S., A transgenic mouse model of autoimmune glomerulonephritis and necrotizing arteritis associated with cryoglobulinemia. J. Immunol. 2002. 169: 4644-4650.
16. Merino, R., Shibata, T., de Kossodo, S. and Izui, S., Differential effect of the autoimmune Yaa and lpr genes on the acceleration of lupus-like syndrome in MRL/MpJ mice. Eur. J. Immunol. 1989. 19: 2131-2137.
17. Izui, S., Iwamoto, M., Fossati, L., Merino, R., Takahashi, S. and Ibnou-Zekri, N., The Yaa gene model of systemic lupus erythematosus. Immunol. Rev. 1995. 144: 137-156.
18. Hibbs, M. L., Tarlinton, D. M., Armes, J., Grail, D., Hodgson, G., Maglitto, R., Stacker, S. A. and Dunn, A. R., Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 1995. 83: 301-312.
19. Sato, S., Ono, N., Steeber, D. A., Pisetsky, D. S. and Tedder, T. F., CD19 regulates B lymphocyte signaling thresholds critical for the development of B-1 lineage cells and autoimmunity. J. Immunol. 1996. 157: 4371-4378.
20. O'Keefe, T. L., Williams, G. T., Batista, F. D. and Neuberger, M. S., Deficiency in CD22, a B cell-specific inhibitory receptor, is sufficient to predispose to development of high affinity autoantibodies. J. Exp. Med. 1999. 189: 1307-1313.
21. Bolland, S. and Ravetch, J. V., Spontaneous autoimmune disease in FcγRIIB-deficient mice results from strain-specific epistasis. Immunity 2000. 13: 277-285.
22. Strasser, A., Whittingham, S., Vaux, D. L., Bath, M. L., Adams, J. M., Cory, S. and Harris, A. W., Enforced Bcl2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl. Acad. Sci. USA 1991. 88: 8661-8665.
23. Vyse, T. J. and Kotzin, B. L., Genetic susceptibility to systemic lupus erythematosus. Ann. Rev. Immunol. 1998. 16: 261-292.
24. Izui, S., McConahey, P. J., Clark, J. P., Hang, L. M., Hara, I. and Dixon, F. J., Retroviral gp70 immune complexes in NZB × NZW F2 mice with murine lupus nephritis. J. Exp. Med. 1981. 154: 517-528.
25. Vyse, T. J., Drake, C. G., Rozzo, S. J., Roper, E., Izui, S. and Kotzin, B. L., Genetic linkage of IgG autoantibody production in relation to lupus nephritis in New Zealand hybrid mice. J. Clin. Invest. 1996. 98: 1762-1772.
26. Martinez-Valdez, H., Guret, C., de Bouteiller, O., Fugier, I., Banchereau, J. and Liu, Y. J., Human germinal center B cells express the apoptosis-inducing genes Fas, c-myc, P53, and Bax but not the survival gene bcl-2. J. Exp. Med. 1996. 183: 971-977.
27. Pearse, R. N., Kawabe, T., Bolland, S., Guinamard, R., Kurosaki, T. and Ravetch, J. V., SHIP recruitment attenuates FcγRIIB-induced B cell apoptosis. Immunity 1999. 10: 753-760.
28. Smith, K. G., Weiss, U., Rajewsky, K., Nossal, G. J. V. and Tarlinton, D. M., Bcl-2 increases memory B cell recruitment but does not perturb selection in germinal centers. Immunity 1994. 1: 803-813.
29. Pulendran, B., Kannourakis, G., Nouri, S., Smith, K. G. C. and Nossal, G. J. V., Soluble antigen can cause enhanced apoptosis of germinal-centre B cells. Nature 1995. 375: 331-334.
30. Hande, S., Notidis, E. and Manser, T, Bcl-2 obstructs negative selection of autoreactive, hypermutated antibody V regions during memory B cell development. Immunity 1998. 8: 189-198.
31. Leadbetter, E. A., Rifkin, I. R., Hohlbaum, A. M., Beaudefte, B. C., Shlomchik, M. J. and Marshak-Rothstein, A., Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002. 416: 603-607.
32. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K. and Akira, S., A novel Toll-like receptor that recognizes bacterial DNA. Nature 2000. 408: 740-745.
33. Botto, M., Dell'Agnola, C., Bygrave, A. E., Thompson, E. M., Cook, H. T., Petry, F., Loos, M., Pandolfi, P. P. and Walport, M. J., Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 1998. 19: 56-59.
34. Bickerstaff, M. C. M., Botto, M., Hutchinson, W. L., Herbert, J., Tennent, G. A., Bybee, A., Mitchell, D. A., Cook, H. T., Butler, P. J. G., Walport, M. J. and Pepys, M. B., Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat. Med. 1999. 5: 694-697.
35. Amano, H., Amano, E., Moll, T., Marinkovic, D., Ibnou-Zekri, N., Martinez-Soria, E., Semac, I., Wirth, T., Nitschke, L. and Izui, S., The Yaa mutation promoting murine lupus causes defective development of marginal zone B cells. J. Immunol. 2003. 170: 2293-2301.
36. Izui, S., Higaki, M., Morrow, D. and Merino, R., The Y chromosome from autoimmune BXSB/MpJ mice induces a lupus-like syndrome in (NZW × C57BL/6)F1 male mice, but not in C57BL/6 male mice. Eur. J. Immunol. 1988. 18: 911-915.
37. Merino, R., Iwamoto, M., Fossati, L., Muniesa, P., Araki, K., Takahashi, S., Huarte, J., Yamamura, K.-I., Vassalli, J.-D. and Izui, S., Prevention of systemic lupus erythematosus in autoimmune BXSB mice by a transgene encoding I-E α chain. J. Exp. Med. 1993. 178: 1189-1197.
38. Merino, R., Fossati, L., Iwamoto, M., Takahashi, S., Lemoine, R., Ibnou-Zekri, N., Pugliatti, L., Merino, J. and Izui, S., Effect of long-term anti-CD4 or anti-CD8 treatment on the development of lpr CD4-CD8- double-negative T cells and of the autoimmune syndrome in MRL-lpr/lpr mice. J. Autoimmun. 1995. 8: 33-45.
39. Fossati, L., Sobel, E. S., Iwamoto, M., Cohen, P. L., Eisenberg, R. A. and Izui, S., The Yaa gene-mediated acceleration of murine lupus: Yaa- T cells from non-autoimmune mice collaborate with Yaa+ B cells to produce lupus autoantibodies in vivo. Eur. J. Immunol. 1995. 25: 3412-3417.
40. Luzuy, S., Merino, J., Engers, H., Izui, S. and Lambert, P. H., Autoimmunity after induction of neonatal tolerance to alloantigens: role of B cell chimerism and F1 donor B cell activation. J. Immunol. 1986. 136: 4420-4426.
41. Takahashi, S., Fossati, L., Iwamoto, M., Merino, R., Motta, R., Kobayakawa, T. and Izui, S., Imbalance towards Th1 predominance is associated with acceleration of lupus-like autoimmune syndrome in MRL mice. J. Clin. Invest. 1996. 97: 1597-1604.
42. Merino, R., Fossati, L., Lacour, M., Lemoine, R., Higaki, M. and Izui, S., H-2-linked control of the Yaa gene-induced acceleration of lupus-like autoimmune disease in BXSB mice. Eur. J. Immunol. 1992. 22: 295-299.