B Cell activating factor (BAFF) and T cells cooperate to breach B cell tolerance in lupus-prone New Zealand Black (NZB) mice

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Chang, Nan Hua ^a   Cheung, Yui Ho ^a,b   Loh, Christina ^a,b   Pau, Evelyn ^a,b   Roy, Valerie ^a   Cai, Yong Chun ^a   Wither, Joan ^b,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; ENZYME ANTIBODY; IMMUNOGLOBULIN G; LYSOZYME; MESSENGER RNA; AUTOANTIBODY; HEN EGG LYSOZYME;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; BREEDING; CELL COMPARTMENTALIZATION; CELL SURVIVAL; CLONAL ANERGY; CONTROLLED STUDY; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTE TRANSFER; MOUSE; NEW ZEALAND BLACK MOUSE; NONHUMAN; PHENOTYPE; RECIPIENT; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; TRANSGENE; ANIMAL; BLOOD; GENETICS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

ANIMALS; AUTOANTIBODIES; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; IMMUNE TOLERANCE; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, TRANSGENIC; MURAMIDASE; T-LYMPHOCYTES;

EID: 77955392498     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011691     Document Type: Article

References (51)

1. Theofilopoulos AN, Dixon FJ (1985) Murine models of systemic lupus erythematosus. Adv Immunol 37: 269-390.
2. Izui S, McConahey PJ, Dixon FJ (1978) Increased spontaneous polyclonal activation of B lymphocytes in mice with spontaneous autoimmune disease. J Immunol 121: 2213-9.
3. Wither JE, Roy V, Brennan LA (2000) Activated B cells express increased levels of costimulatory molecules in young autoimmune NZB and (NZB x NZW)F(1) mice. Clin Immunol 94: 51-63.
4. Manny N, Datta SK, Schwartz RS (1979) Synthesis of IgM by cells of NZB and SWR mice and their crosses. J Immunol 122: 1220-7.
5. Moutsopoulos HM, Boehm-Truitt M, Kassan SS, Chused TM (1977) Demonstration of activation of B lymphocytes in New Zealand black mice at birth by an immunoradiometric assay for murine IgM. J Immunol 119: 1639-44.
6. Raveche ES, Steinberg AD, DeFranco AL, Tjio JH (1982) Cell cycle analysis of lymphocyte activation in normal and autoimmune strains of mice. J Immunol 129: 1219-26.
7. Wangel AG, Milton A, Egan JB (1982) Spontaneous plaque forming cells in the peripheral blood of patients with systemic lupus erythematosus. Clin Exp Immunol 49: 41-9.
8. Goodnow CC, Cyster JG, Hartley SB, Bell SE, Cooke MP, et al. (1995) Selftolerance checkpoints in B lymphocyte development. Adv Immunol 59: 279-368.
9. Halverson R, Torres RM, Pelanda R (2004) Receptor editing is the main mechanism of B cell tolerance toward membrane antigens. Nat Immunol 5: 645-50.
10. Hippen KL, Schram BR, Tze LE, Pape KA, Jenkins MK, et al. (2005) In vivo assessment of the relative contributions of deletion, anergy, and editing to B cell self-tolerance. J Immunol 175: 909-16.
11. Roy V, Chang NH, Cai Y, Bonventi G, Wither J (2005) Aberrant IgM signaling promotes survival of transitional T1 B cells and prevents tolerance induction in lupus-prone New Zealand black mice. J Immunol 175: 7363-71.
12. Hartley SB, Cooke MP, Fulcher DA, Harris AW, Cory S, et al. (1993) Elimination of self-reactive B lymphocytes proceeds in two stages: arrested development and cell death. Cell 72: 325-35.
13. Fang W, Weintraub BC, Dunlap B, Garside P, Pape KA, et al. (1998) Selfreactive B lymphocytes overexpressing Bcl-xL escape negative selection and are tolerized by clonal anergy and receptor editing. Immunity 9: 35-45.
14. Cyster JG, Hartley SB, Goodnow CC (1994) Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire. Nature 371: 389-95.
15. Batten M, Groom J, Cachero TG, Qian F, Schneider P, et al. (2000) BAFF mediates survival of peripheral immature B lymphocytes. J Exp Med 192: 1453-66.
16. Cheema GS, Roschke V, Hilbert DM, Stohl W (2001) Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum 44: 1313-9.
17. Stohl W, Metyas S, Tan SM, Cheema GS, Oamar B, et al. (2003) B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum 48: 3475-86.
18. Zhang J, Roschke V, Baker KP, Wang Z, Alarcon GS, et al. (2001) Cutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosus. J Immunol 166: 6-10.
19. Khare SD, Sarosi I, Xia XZ, McCabe S, Miner K, et al. (2000) Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc Natl Acad Sci U S A 97: 3370-5.
20. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, et al. (1999) Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 190: 1697-710.
21. Thien M, Phan TG, Gardam S, Amesbury M, Basten A, et al. (2004) Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 20: 785-98.
22. Goodnow CC, Crosbie J, Adelstein S, Lavoie TB, Smith-Gill SJ, et al. (1988) Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334: 676-82.
23. Roy V, Bonventi G, Cai Y, MacLeod R, Wither JE (2007) Immune mechanisms leading to abnormal B cell selection and activation in New Zealand Black mice. Eur J Immunol 37: 2645-56.
24. Culton DA, O'Conner BP, Conway KL, Diz R, Rutan J, et al. (2006) Early preplasma cells define a tolerance checkpoint for autoreactive B cells. J Immunol 176: 790-802.
25. Fulcher DA, Basten A (1994) Reduced life span of anergic self-reactive B cells in a double-transgenic model. J Exp Med 179: 125-34.
26. Fulcher DA, Lyons AB, Korn SL, Cook MC, Koleda C, et al. (1996) The fate of self-reactive B cells depends primarily on the degree of antigen receptor engagement and availability of T cell help. J Exp Med 183: 2313-28.
27. Cornall RJ, Cyster JG, Hibbs ML, Dunn AR, Otipoby KL, et al. (1998) Polygenic autoimmune traits: Lyn, CD22, and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity 8: 497-508.
28. Inaoki M, Sato S, Weintraub BC, Goodnow CC, Tedder TF (1997) CD19- regulated signaling thresholds control peripheral tolerance and autoantibody production in B lymphocytes. J Exp Med 186: 1923-31.
29. Cooke MP, Heath AW, Shokat KM, Zeng Y, Finkelman FD, et al. (1994) Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J Exp Med 179: 425-38.
30. Rathmell JC, Fournier S, Weintraub BC, Allison JP, Goodnow CC (1998) Repression of B7.2 on self-reactive B cells is essential to prevent proliferation and allow Fas-mediated deletion by CD4(+) T cells. J Exp Med 188: 651-9.
31. Chang NH, MacLeod R, Wither JE (2004) Autoreactive B cells in lupus-prone New Zealand black mice exhibit aberrant survival and proliferation in the presence of self-antigen in vivo. J Immunol 172: 1553-60.
32. Lesley R, Xu Y, Kalled SL, Hess DM, Schwab SR, et al. (2004) Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20: 441-53.
33. Craxton A, Draves KE, Gruppi A, Clark EA (2005) BAFF regulates B cell survival by downregulating the BH3-only family member Bim via the ERK pathway. J Exp Med 202: 1363-74.
34. Do RK, Hatada E, Lee H, Tourigny MR, Hilbert D, et al. (2000) Attenuation of apoptosis underlies B lymphocyte stimulator enhancement of humoral immune response. J Exp Med 192: 953-64.
35. Hsu BL, Harless SM, Lindsley RC, Hilbert DM, Cancro MP (2002) Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators. J Immunol 168: 5993-6.
36. Meyer-Bahlburg A, Andrews SF, Yu KO, Porcelli SA, Rawlings DJ (2008) Characterization of a late transitional B cell population highly sensitive to BAFFmediated homeostatic proliferation. J Exp Med 205: 155-68.
37. Mandik-Nayak L, Nayak S, Sokol C, Eaton-Bassiri A, Madaio MP, et al. (2000) The origin of anti-nuclear antibodies in bcl-2 transgenic mice. Int Immunol 12: 353-64.
38. Jongstra-Bilen J, Vukusic B, Boras K, Wither JE (1997) Resting B cells from autoimmune lupus-prone New Zealand Black and (New Zealand Black x New Zealand White)F1 mice are hyper-responsive to T cell-derived stimuli. J Immunol 159: 5810-20.
39. Avery DT, Kalled SL, Ellyard JI, Ambrose C, Bixler SA, et al. (2003) BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J Clin Invest 112: 286-97.
40. O'Connor BP, Raman VS, Erickson LD, Cook WJ, Weaver LK, et al. (2004) BCMA is essential for the survival of long-lived bone marrow plasma cells. J Exp Med 199: 91-8.
41. Hase H, Kanno Y, Kojima M, Hasegawa K, Sakurai D, et al. (2004) BAFF/ BLyS can potentiate B-cell selection with the B-cell coreceptor complex. Blood 103: 2257-65.
42. Rahman ZS, Manser T (2005) Failed up-regulation of the inhibitory IgG Fc receptor Fc gamma RIIB on germinal center B cells in autoimmune-prone mice is not associated with deletion polymorphisms in the promoter region of the Fc gamma RIIB gene. J Immunol 175: 1440-9.
43. Sasaki Y, Casola S, Kutok JL, Rajewsky K, Schmidt-Supprian M (2004) TNF family member B cell-activating factor (BAFF) receptor-dependent and - independent roles for BAFF in B cell physiology. J Immunol 173: 2245-52.
44. Shulga-Morskaya S, Dobles M, Walsh ME, Ng LG, Mackay F, et al. (2004) B cell-activating factor belonging to the TNF family acts through separate receptors to support B cell survival and T cell-independent antibody formation. J Immunol 173: 2331-41.
45. Groom JR, Fletcher CA, Walters SN, Grey ST, Watt SV, et al. (2007) BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J Exp Med 204: 1959-71.
46. Jiang Y, Hirose S, Sanokawa-Akakura R, Abe M, Mi X, et al. (1999) Genetically determined aberrant down-regulation of FcgammaRIIB1 in germinal center B cells associated with hyper-IgG and IgG autoantibodies in murine systemic lupus erythematosus. Int Immunol 11: 1685-91.
47. Xiu Y, Nakamura K, Abe M, Li N, Wen XS, et al. (2002) Transcriptional regulation of Fcgr2b gene by polymorphic promoter region and its contribution to humoral immune responses. J Immunol 169: 4340-6.
48. McGaha TL, Sorrentino B, Ravetch JV (2005) Restoration of tolerance in lupus by targeted inhibitory receptor expression. Science 307: 590-3.
49. Brownlie RJ, Lawlor KE, Niederer HA, Cutler AJ, Xiang Z, et al. (2008) Distinct cell-specific control of autoimmunity and infection by FcgammaRIIb. J Exp Med 205: 883-95.
50. Xiang Z, Cutler AJ, Brownlie RJ, Fairfax K, Lawlor KE, et al. (2007) FcgammaRIIb controls bone marrow plasma cell persistence and apoptosis. Nat Immunol 8: 419-29.
51. Wakeland E, Morel L, Achey K, Yui M, Longmate J (1997) Speed congenics: a classic technique in the fast lane (relatively speaking). Immunol Today 18: 472-7.