Crucial role for BAFF-BAFF-R signaling in the survival and maintenance of mature B cells

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Rauch, Melanie ^a   Tussiwand, Roxane ^a   Bosco, Nabil ^a   Rolink, Antonius G ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; B CELL ACTIVATING FACTOR RECEPTOR; MONOCLONAL ANTIBODY; PROTEIN BCL 2; TNFRSF13C PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELL SPECIFICITY; CELL SURVIVAL; COMPLEMENT SYSTEM; CONTROLLED STUDY; CYTOLYSIS; FEMALE; HUMORAL IMMUNITY; INHIBITION KINETICS; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; MEMORY CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; ENZYME IMMUNOASSAY; FLOW CYTOMETRY; IMMUNIZATION; IMMUNOLOGY; LEWIS RAT; METABOLISM; PHYSIOLOGY; SPLEEN; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL; B-CELL ACTIVATING FACTOR; B-CELL ACTIVATION FACTOR RECEPTOR; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; IMMUNIZATION; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, INBRED LEW; SPLEEN;

EID: 65549087544     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005456     Document Type: Article

References (58)

1. Osmond DG (1991) Proliferation kinetics and the lifespan of B cells in central and peripheral lymphoid organs. Curr Opin Immunol 3: 179-185.
2. Osmond DG (1993) The turnover of B-cell populations. Immunol Today 14: 34-37.
3. Rolink AG, Andersson J, Melchers F (1998) Characterization of immature B cells by a novel monoclonal antibody, by turnover and by mitogen reactivity. Eur J Immunol 28: 3738-3748.
4. Allman DM, Ferguson SE, Cancro MP (1992) Peripheral B cell maturation. I. Immature peripheral B cells in adults are heat-stable antigenhi and exhibit unique signaling characteristics. J Immunol 149: 2533-2540.
5. Loder F, Mutschler B, Ray RJ, Paige CJ, Sideras P, et al. (1999) B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J Exp Med 190: 75-89.
6. Allman D, Lindsley RC, DeMuth W, Rudd K, Shinton SA, et al. (2001) Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J Immunol 167: 6834-6840.
7. Forster I, Rajewsky K (1990) The bulk of the peripheral B-cell pool in mice is stable and not rapidly renewed from the bone marrow. Proc Natl Acad Sci U S A 87: 4781-4784.
8. Merrell KT, Benschop RJ, Gauld SB, Aviszus K, Decote-Ricardo D, et al. (2006) Identification of anergic B cells within a wild-type repertoire. Immunity 25: 953-962.
9. Schiemann B, Gommerman JL, Vora K, Cachero TG, Shulga-Morskaya S, et al. (2001) An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293: 2111-2114.
10. Gross JA, Johnston J, Mudri S, Enselman R, Dillon SR, et al. (2000) TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404: 995-999.
11. 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: 2331-2341.
12. 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: 2245-2252.
13. Yan M, Brady JR, Chan B, Lee WP, Hsu B, et al. (2001) Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency. Curr Biol 11: 1547-1552.
14. 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: 1697-1710.
15. 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: 3370-3375.
16. 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: 1453-1466.
17. 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: 953-964.
18. Tardivel A, Tinel A, Lens S, Steiner QG, Sauberli E, et al. (2004) The anti-apoptotic factor Bcl-2 can functionally substitute for the B cell survival but not for the marginal zone B cell differentiation activity of BAFF. Eur J Immunol 34: 509-518.
19. Sasaki Y, Derudder E, Hobeika E, Pelanda R, Reth M, et al. (2006) Canonical NF-kappaB activity, dispensable for B cell development, replaces BAFF-receptor signals and promotes B cell proliferation upon activation. Immunity 24: 729-739.
20. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV (1994) FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 76: 519-529.
21. Domen J, Gandy KL, Weissman IL (1998) Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood 91: 2272-2282.
22. Benson MJ, Dillon SR, Castigli E, Geha RS, Xu S, et al. (2008) Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J Immunol 180: 3655-3659.
23. Gross JA, Dillon SR, Mudri S, Johnston J, Littau A, et al. (2001) TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease. impaired B cell maturation in mice lacking BLyS. Immunity 15: 289-302.
24. Kalled SL (2005) The role of BAFF in immune function and implications for autoimmunity. Immunol Rev 204: 43-54.
25. Lin WY, Gong Q, Seshasayee D, Lin Z, Ou Q, et al. (2007) Anti-BR3 antibodies: a new class of B-cell immunotherapy combining cellular depletion and survival blockade. Blood 110: 3959-3967.
26. Gorelik L, Cutler AH, Thill G, Miklasz SD, Shea DE, et al. (2004) Cutting edge: BAFF regulates CD21/35 and CD23 expression independent of its B cell survival function. J Immunol 172: 762-766.
27. Lam KP, Kuhn R, Rajewsky K (1997) In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90: 1073-1083.
28. Siebenlist U, Brown K, Claudio E (2005) Control of lymphocyte development by nuclear factor-kappaB. Nat Rev Immunol 5: 435-445.
29. Gerondakis S, Strasser A (2003) The role of Rel/NF-kappaB transcription factors in B lymphocyte survival. Semin Immunol 15: 159-166.
30. Hayden MS, Ghosh S (2004) Signaling to NF-kappaB. Genes Dev 18: 2195-2224.
31. Weih F, Durham SK, Barton DS, Sha WC, Baltimore D, et al. (1997) p50-NF-kappaB complexes partially compensate for the absence of RelB: severely increased pathology in p50(-/-)relB(-/-) double-knockout mice. J Exp Med 185: 1359-1370.
32. Senftleben U, Cao Y, Xiao G, Greten FR, Krahn G, et al. (2001) Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 293: 1495-1499.
33. Kaisho T, Takeda K, Tsujimura T, Kawai T, Nomura F, et al. (2001) IkappaB kinase alpha is essential for mature B cell development and function. J Exp Med 193: 417-426.
34. Grossmann M, O'Reilly LA, Gugasyan R, Strasser A, Adams JM, et al. (2000) The anti-apoptotic activities of Rel and RelA required during B-cell maturation involve the regulation of Bcl-2 expression. Embo J 19: 6351-6360.
35. Franzoso G, Carlson L, Xing L, Poljak L, Shores EW, et al. (1997) Requirement for NF-kappaB in osteoclast and B-cell development. Genes Dev 11: 3482-3496.
36. Franzoso G, Carlson L, Poljak L, Shores EW, Epstein S, et al. (1998) Mice deficient in nuclear factor (NF)-kappa B/p52 present with defects in humoral responses, germinal center reactions, and splenic microarchitecture. J Exp Med 187: 147-159.
37. Caamano JH, Rizzo CA, Durham SK, Barton DS, Raventos-Suarez C, et al. (1998) Nuclear factor (NF)-kappa B2 (p100/p52) is required for normal splenic microarchitecture and B cell-mediated immune responses. J Exp Med 187: 185-196.
38. Rolink AG, Tschopp J, Schneider P, Melchers F (2002) BAFF is a survival and maturation factor for mouse B cells. Eur J Immunol 32: 2004-2010.
39. 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: 5993-5996.
40. Mecklenbrauker I, Kalled SL, Leitges M, Mackay F, Tarakhovsky A (2004) Regulation of B-cell survival by BAFF-dependent PKCdelta-mediated nuclear signalling. Nature 431: 456-461.
41. Clayton E, Bardi G, Bell SE, Chantry D, Downes CP, et al. (2002) A crucial role for the p110delta subunit of phosphatidylinositol 3-kinase in B cell development and activation. J Exp Med 196: 753-763.
42. Otero DC, Anzelon AN, Rickert RC (2003) CD19 function in early and late B cell development: I. Maintenance of follicular and marginal zone B cells requires CD19-dependent survival signals. J Immunol 170: 73-83.
43. Casola S, Otipoby KL, Alimzhanov M, Humme S, Uyttersprot N, et al. (2004) B cell receptor signal strength determines B cell fate. Nat Immunol 5: 317-327.
44. Anzelon AN, Wu H, Rickert RC (2003) Pten inactivation alters peripheral B lymphocyte fate and reconstitutes CD19 function. Nat Immunol 4: 287-294.
45. Hozumi K, Negishi N, Suzuki D, Abe N, Sotomaru Y, et al. (2004) Delta-like 1 is necessary for the generation of marginal zone B cells but not T cells in vivo. Nat Immunol 5: 638-644.
46. Saito T, Chiba S, Ichikawa M, Kunisato A, Asai T, et al. (2003) Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18: 675-685.
47. 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: 1313-1319.
48. He B, Chadburn A, Jou E, Schattner EJ, Knowles DM, et al. (2004) Lymphoma B cells evade apoptosis through the TNF family members BAFF/ BLyS and APRIL. J Immunol 172: 3268-3279.
49. Kern C, Cornuel JF, Billard C, Tang R, Rouillard D, et al. (2004) Involvement of BAFF and APRIL in the resistance to apoptosis of B-CLL through an autocrine pathway. Blood 103: 679-688.
50. Novak AJ, Bram RJ, Kay NE, Jelinek DF (2002) Aberrant expression of B-lymphocyte stimulator by B chronic lymphocytic leukemia cells: a mechanism for survival. Blood 100: 2973-2979.
51. Novak AJ, Darce JR, Arendt BK, Harder B, Henderson K, et al. (2004) Expression of BCMA, TACI, and BAFF-R in multiple myeloma: a mechanism for growth and survival. Blood 103: 689-694.
52. 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.
53. Rolink A, Melchers F, Andersson J (1996) The SCID but not the RAG-2 gene product is required for S mu-S epsilon heavy chain class switching. Immunity 5: 319-330.
54. Niman HL, Houghten RA, Walker LE, Reisfeld RA, Wilson IA, et al. (1983) Generation of protein-reactive antibodies by short peptides is an event of high frequency: implications for the structural basis of immune recognition. Proc Natl Acad Sci U S A 80: 4949-4953.
55. Steller H, Pirrotta V (1985) A transposable P vector that confers selectable G418 resistance to Drosophila larvae. Embo J 4: 167-171.
56. Wallny HJ, Sollami G, Karjalainen K (1995) Soluble mouse major histocompatibility complex class II molecules produced in Drosophila cells. Eur J Immunol 25: 1262-1266.
57. Goronzy J, Weyand CM, Fathman CG (1986) Long-term humoral unresponsiveness in vivo, induced by treatment with monoclonal antibody against L3T4. J Exp Med 164: 911-925.
58. Schubart DB, Rolink A, Kosco-Vilbois MH, Botteri F, Matthias P (1996) B-cell-specific coactivator OBF-1/OCA-B/Bob1 required for immune response and germinal centre formation. Nature 383: 538-542.