Constitutive expression of bcl-2 in B cells causes a lethal form of lupuslike autoimmune disease after induction of neonatal tolerance to H-2b alloantigens

Journal of Experimental Medicine

Volumn 183, Issue 6, 1996, Pages 2523-2531

  López Hoyos, Marcos ^a   Carrió, Roberto ^a   Merino, Ramón ^b   Buelta, Luis ^a   Izui, Shozo ^c   Núñez, Gabriel ^b   Merino, Jesús ^a  

^a HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; B LYMPHOCYTE DIFFERENTIATION FACTOR;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; AUTOIMMUNITY; CELL DIFFERENTIATION; CELL SURVIVAL; GENE EXPRESSION; GRAFT REJECTION; HUMAN; HUMAN CELL; LUPUS ERYTHEMATOSUS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AGING; ANIMALS; ANIMALS, NEWBORN; AUTOIMMUNE DISEASES; B-LYMPHOCYTES; CROSSES, GENETIC; DEATH; GTP-BINDING PROTEINS; H-2 ANTIGENS; HETEROZYGOTE; IMMUNE TOLERANCE; ISOANTIGENS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPH NODES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENES; SPLEEN;

EID: 0029956023     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.183.6.2523     Document Type: Article

References (35)

1. Hard, R.C., and B. Kullgren. 1970. Etiology, pathogenesis and prevention of a fatal host-versus-graft syndrome in patent F1 mouse chimeras. Am. J. Pathol. 59:203-224.
2. Luzuy, S., J. Merino, H. Engers, S. Izui, and P.H. Lambert. 1986. Autoimmunity after induction of neonatal tolerance to alloantigens: role of B cell chimerism and F1 donor B cell activation. J. Immunol. 136:4420-4426.
3. Schurmans, S., G. Brighouse, G. Kramar, L. Wen, S. Izui, J. Merino, and P.H. Lambert. 1991. Transient T and B cell activation after neonatal induction of tolerance to MHC class II or Mls alloantigens. J. Immunol. 146:2152-2160.
4. González, A.L., C. Conde, C. Revilla, A. Ramos, B. Renedo, and J. Merino. 1993. Autoimmune syndrome after induction of neonatal tolerance to I-E antigens. Eur. J. Immunol. 23: 2353-2357.
5. Ramos, A., R. Merino, and J. Merino. 1994. Differences in non-MHC alloantigens promote tissue rejection but fail to mediate allogeneic co-operation and autoimmunity in mice neonatally injected with semi-allogeneic F1 B cells. Immunology. 82:287-293.
6. Schurmans, S., J. Merino, H.-Y. Qin, G. Kramar, M. Duchosal, O. Skalli, G. Benzonana, G. Gabbiani, and P.H. Lambert. 1991. Autoimmune syndrome after neonatal induction of tolerance to alloantigens: analysis of the specificity and of the cellular and genetic origin of autoantibodies. Autoimmunity. 9:283-291.
7. Merino, J., S. Schurmans, M.A. Duchosal, S. Izui, and P.H. Lambert. 1989. Autoimmune syndrome after induction of neonatal tolerance to alloantigens: T cells from the tolerant host activate autoreactive F1 B cells. J. Immunol. 143:2202-2208.
8. Schurmans, S., C.H. Heusser, H.-Y. Qin, J. Merino, G. Brighouse, and P.H. Lambert. 1990. In vivo effects of anti-IL-4 monoclonal antibody in neonatal induction of tolerance and on an associated autoimmune syndrome. J. Immunol. 145: 2465-2473.
9. Powell, T.J., and J.W. Streinlein. 1990. Neonatal tolerance induction by class II alloantigens activates IL-4 secreting tolerogen-responsive T cells. J. Immunol. 144:854-859.
10. Abramowicz, D., P. Durez, C. Gerard, V. Donckier, Z. Amraoui, T. Velu, and M. Goldman. 1993. Neonatal induction of transplantation tolerance in mice is associated with in vivo expression of IL-4 and IL-10 mRNAs. Transplant. Proc. 25: 312-313.
11. bm12 mice J. Immunol. 145:94-101.
12. Izui, S., P.J. McConahey, A.N. Theofilopoulos, and F.J. Dixon. 1979. Association of circulating retroviral gp70-anti-gp70 immune complexes with murine systemic lupus erythematosus. J. Exp. Med. 149:1099-1116.
13. Florquin, S., D. Abramowicz, E. De Heer, J.A. Bruijn, J.M. Doutrelepont, M. Goldman, and P. Hoedemaeker. 1991. Renal immunopathology in murine host-versus-graft disease. Kidney Int. 40:852-861.
14. Van Der Woude, F.J., N. Rasmussen, S. Lobatto, A. Wiik, H. Permin, L.A. Van Es, M. Van Der Giessen, G.K. Var der Hem, and T.H. The. 1985. Autoantibodies against neutrophils and monocytes: tools for diagnosis and marker of disease activity in Wegener's granulomatosis. Lancet. 1:425-429.
15. Falk, R.J., and J.C. Jeanette. 1988. Anti-neutrophil cytoplasmic autoantibodies with specificity for myeloperoxidase in patients with systemic vasculitis and idiopathic necrotizing and crescentic glomerulonephritis. N. Engl. J. Med. 318:1651-1657.
16. De la Hera, M., A. De la Hera, A. Ramos, L. Buelta, J.L. Alonso, V. Rodríguez-Valverde, and J. Merino. 1992. Self-limited autoimmune disease related to transient donor B cell activation in mice neonatally injected with semi-allogeneic F1 cells. Int. Immunol. 4:67-74.
17. Merino, R., L. Ding, D.J. Veis, S.J. Korsmeyer, and G. Núñez. 1994. Developmental regulation of the Bcl-2 protein and susceptibility to cell death in B lymphocytes. EMBO (Eur. Mol. Biol. Organ.) J. 13:683-691.
18. Li, Y.S., K. Hayakawa, and R.R. Hardy. 1993. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 178:951-960.
19. Pezzella, F., A.G. Tse, J.L. Cardell, K.A. Pulford, K.C. Gatter, and D.Y. Mason. 1990. Expression of the Bcl-2 oncogene protein is not specific for the 14;18 chromosomal translocation. Am. J. Pathol. 137:225-232.
20. Hockenbery, D., M. Zutter, W. Hickey, M. Naham, and S.J. Korsmeyer. 1991. Bcl-2 protein is topographically restricted in tissue characterized by apoptotic cell death. Proc. Natl. Acad. Sci. USA. 88:6961-6965.
21. Nakayama, K., K. Nakayama, I. Nagishi, K. Kuidad, Y. Shinkai, M.C. Louie, L.E. Fields, P.J. Lucas, V. Stewart, F.W. Alt, and D.Y. Loh. 1993. Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science (Wash. DC). 261:1584-1588.
22. Veis, D.J., C.M. Sorenson, J.R. Shutter, and S.J. Korsmeyer. 1993. Bcl-2 deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys and hypopigmented hair. Cell. 75:229-240.
23. McDonnell, T.J., N. Deane, F.M. Watt, G. Núñez, U. Jaeger, J.P. McKearn, and S.J. Korsmeyer. 1989. Bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell. 57:79-88.
24. Strasser, A., S. Wittingham, D.L. Vaux, M.L. Bath, J.M. Adams, S. Cory, and A.W. Harris. 1991. Enforced Bcl-2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl. Acad. Sci. USA. 88: 8661-8665.
25. Katsumata, M., R.M. Siegel, D.C. Louie, T. Miyashita, Y. Tsujimoto, P.C. Nowell, M.I. Greene, and J.C. Reed. 1992. Differential effect of Bcl-2 on T and B cells in transgenic mice. Proc. Natl. Acad. Sci. USA. 89:11376-11380.
26. 1 mice with monoclonal antibody to L3T4. J. Exp. Med. 161:378-391.
27. Merino, R., T. Shibata, S. Kossodo, and S. Izui. 1989. Differential effect of the autoimmune Yaa and lpr genes on the acceleration of lupus-like syndrome in MRL/MpJ mice. Eur. J. Immunol. 19:2131-2137.
28. Stott, D.I., J. Merino, S. Schurmans, and P.H. Lambert. 1988. Expression of anti-DNA clonotypes and the role of helper T-lymphocytes during the autoimmune response in mice tolerant to alloantigens. Autoimmunity. 1:253-266.
29. Rolink, A.G., T. Radaszkiewicz, and F. Meltchers. 1987. The autoantigen-binding B cell repertoires of normal and of chronically graft-versus-host-diseased mice. J. Exp. Med. 165: 1675-1687.
30. Conger, J.D., B.L. Pike, and G.J.V. Nossal. 1987. Clonal analysis of the anti-DNA repertoire of murine B lymphocytes. Proc. Natl. Acad. Sci. USA. 84:2931-2935.
31. Starobinski, M., M. Lacour, L. Reininger, and S. Izui. 1989. Autoantibody repertoire analysis in normal and lupus-prone mice. J. Autoimmun. 2:657-674.
32. Nossal, G.J.V. 1994. Negative selection of lymphocytes. Cell. 76:229-239.
33. Nuñez, G., D. Hockenbery, T.J. McDonnell, C.M. Sorensen, and S.J. Korsmeyer. 1991. Bcl-2 maintains B cell memory. Nature (Lond.). 353:71-73.
34. 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. 72:325-335.
35. 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. 178:1247-1254.