BAFF: A fundamental survival factor for B cells

Nature Reviews Immunology

Volumn 2, Issue 7, 2002, Pages 465-475

  Mackay, Fabienne ^a   Browning, Jeffrey L ^b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR OF THE TUMOR NECROSIS FACTOR FAMILY; PROTEIN; UNCLASSIFIED DRUG; B CELL ACTIVATING FACTOR; B CELL ACTIVATING FACTOR RECEPTOR; MEMBRANE PROTEIN; TNFRSF13C PROTEIN, HUMAN; TNFSF13B PROTEIN, HUMAN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; CELL MATURATION; CELL SURVIVAL; HOMEOSTASIS; IMMUNE RESPONSE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CHEMICAL STRUCTURE; HUMAN; PHYSIOLOGY;

ANIMALS; AUTOIMMUNITY; B-CELL ACTIVATING FACTOR; B-CELL ACTIVATION FACTOR RECEPTOR; B-LYMPHOCYTES; HUMANS; MEMBRANE PROTEINS; MODELS, MOLECULAR; RECEPTORS, TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0036634390     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri844     Document Type: Review

References (79)

1. Grewal, I. S. & Flavell, R. A. CD40 and CD154 in cell-mediated immunity. Annu. Rev. Immunol. 18, 111-135 (1998).
2. Brown, M. A., & Hural, J. Functions of IL-4 and control of its expression. Crit. Rev. Immunol. 17, 1-32 (1997).
3. Stoddart, A., Fleming, H. E. & Paige, C. J. The role of the preBCR, the interleukin-7 receptor and homotypic interactions during B-cell development. Immunol. Rev. 175, 47-58 (2000).
4. Waldmann, T. A., Dubois, S. & Tagaya, Y. Contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for immunotherapy. Immunity 14, 105-110 (2001).
5. Lam, K. P., Kuhn, R. & Rajewsky, K. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid death. Cell 90, 1073-1083 (1997).
6. Chao, D. T. & Korsmeyer, S. J. BCL-2 family: regulators of cell death. Annu. Rev. Immunol. 16, 395-419 (1998).
7. Strasser, A. et al. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl Acad. Sci. USA 88, 8661-8665 (1991). This article shows the importance of Bcl-2 for B-cell survival. Mice that are transgenic for Bcl2 develop autoimmune disorders that are very similar to those of Baff-transgenic mice.
8. Locksley R. M., Killeen, N. & Lenardo, M. J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104, 487-501 (2001).
9. Schneider, P. et al. BAFF, a novel ligand of the tumor. necrosis factor (TNF) family stimulates B-cell growth. J. Exp. Med. 189, 1747-1756 (1999). This paper was the first to describe the discovery of BAFF and its role as a costimulator of B-cell activation.
10. Shu, H.-B., Hu, W.-H. & Johnson, H. TALL-1 is a novel member of the TNF family that is down-regulated by mitogens. J. Leukocyte Biol. 65, 680-683 (1999).
11. 2-terminal kinase. J. Biol. Chem. 274, 15978-15981 (1999).
12. Moore, P. A. et al. BlyS: member of the tumor-necrosis factor family and B-lymphocyte stimulator. Science 285, 260-263 (1999).
13. Gross, J. A. et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404, 995-999 (2000).
14. Karpusas, M. et al. Crystal structure of extracellular human BAFF, a TNF family member that stimulates B lymphocytes. J. Mol. Biol. 315, 1145-1154 (2002).
15. Liu, Y. et al. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF ligands. Cell 108, 383-394 (2002).
16. Mackay, F. et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 190, 1697-1710 (1999). This work showed the development of autoimmunity in mice that overexpress BAFF and the up-regulation of Bcl-2 expression in B cells from Baff-transgenic animals.
17. Nardelli, B. et al. Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 97, 198-204 (2000).
18. Hahne, M. et al. APRIL, a new ligand of the tumor-necrosis factor family, stimulates tumor growth. J. Exp. Med. 188, 1185-1190 (1998).
19. Kelly, K., Manos, E., Jensen, G., Nadauld, L. & Jones, D. A. APRIL/TRDL-1, a tumor-necrosis factor-like ligand, stimulates cell death. Cancer Res. 60, 1021-1027 (2000).
20. Bodmer, J. L., Schneider, P. & Tschopp, J. The molecular architecture of the TNF superfamily. Trends Biochem. Sci. 27, 19-26 (2002).
21. Lopez-Fraga, M., Fernandez, R., Albar, J. P. & Hahne, M. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO J. 2, 945-951 (2001).
22. Laabi, Y. et al. A new gene, BCM, on chromosome 16 is fused to the interleukin-2 gene by t(4;16) (q26;p13) translocation in a malignant T-cell lymphoma. EMBO J. 11, 3897-3904 (1992).
23. Madry, C. et al. The characterization of murine BCMA gene defines it as a new member of the tumor-necrosis factor receptor superfamily. Int. Immunol. 10, 1693-1702 (1998).
24. Von Buelow, G. U. & Bram, R. J. NF-AT activation induced by a CAML-interacting member of the tumor-necrosis factor receptor superfamily. Science 278, 138-141 (1997).
25. Wu, Y. et al. Tumor-necrosis factor (TNF) receptor superfamily member TACi is a high-affinity receptor for TNF family members APRIL and BLyS. J. Biol. Chem. 275, 35478-35485 (2000).
26. Thompson, J. S. et al. BAFF-R, a novel TNF receptor that specifically interacts with BAFF. Science 293, 2108-2111 (2001).
27. Yan, M. et al. 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 (2001).
28. Wiley, S. R. et al. A novel TNF receptor family member binds TWEAK and is implicated in angiogenesis. Immunity 15, 837-846 (2001).
29. Gras, M. P. et al. BCMAp: an integral membrane protein in the golgi apparatus of human mature B lymphocytes. Int. Immunol. 7, 1093-1106 (1995).
30. Bradley, J. R., Thiru, S. & Pober, J. S. Disparate localization of 55-kd and 75-kd tumor-necrosis factor receptors in human endothelial cells. Am. J. Pathol. 146, 27-32 (1995).
31. Zhang, X. D., Franco, A. V., Nguyen, T., Gray, C. P. & Hersey P. Differential localization and regulation of death and decoy receptors for TNF-related apoptosis-inducing ligand (TRAIL) in human melanoma cells. J. Immunol. 164, 3961-3970 (2000).
32. Thompson, J. S. et al. BAFF binds to the TNF receptor-like molecule BCMA and is important for maintaining the peripheral B-cell population. J. Exp. Med. 192, 129-135 (2000).
33. Boilly, B., Vercoutter-Edouart, A. S., Hondermarck, H., Nurcombe, V & Le Bourhis, X. FGF signals for cell proliferation and migration through different pathways. Cytokine Growth Factor Rev. 11, 295-302 (2000).
34. Wajant, H., Henkler, F. & Scheurich, P. The TNF-receptor-associated factor family: scaffold molecules for cytokine receptors, kinases and their regulators. Cell. Signal. 13, 389-400 (2001).
35. Hatzoglou, A. et al. TNF receptor family member BCMA (B-cell maturation) associates with TNF receptor-associated factor (TRAF)1, TRAF2, TRAF3 and activates NF-κB, Elk-1, c-jun N-terminal kinase and p38 mitogen-activated protein kinase. J. Immunol. 165, 1322-1330 (2000).
36. Shu, H.-B. & Johnson, H. B-cell maturation protein is a receptor for the tumor-necrosis factor family member TALL-1. Proc. Natl Acad. Sci. USA 97, 9156-9161 (2000).
37. Marsters, S. A. et al. Interaction of the TNF homologues BLyS and APRIL with TNF receptor homologues BCMA and TACI. Curr. Biol. 10, 785-788 (2000).
38. Xia, X.-Z. et al. TACI is a TRAF-interacting receptor for TALL-1, a tumor-necrosis factor family member involved in B-cell regulation. J. Exp. Med. 192, 137-143 (2000).
39. Senftleben, U. et al. Activation by IKKα of a second, evolutionary conserved, NF-κB signaling pathway. Science 293, 1495-1499 (2001).
40. Kaisho, T. et al. IκB kinase α is essential for mature B-cell development and function. J. Exp. Med. 193, 417-426 (2001).
41. Grossmann, M. et al. The anti-apoptotic activities of rel and RelA required during B-cell maturation involve the regulation of Bcl-2. EMBO J. 19, 6351-6360 (2000).
42. Yamada, T. et al. Abnormal immune function of hemopoietic cells from alymphoplasia (aly) mice, a natural strain with mutant NF-κB-inducing kinase. J. Immunol. 165, 804-812 (2000).
43. Do, R. K. et al. Attenuation of apoptosis underlies B-lymphocyte stimulator enhancement of humoral immune response. J. Exp. Med. 192, 953-964 (2000).
44. Veis, D. J., Sorenson, C. M., Shutter, J. R. & Korsmeyer, S. J. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys and hypopigmented hair. Cell 75, 229-240 (1993).
45. Loder, F. et al. 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 (1999). This study established the distinction between T1 and T2 immature splenic B cells. It also showed the presence of a normal MZ B-cell population in the absence of mature B cells in some mutant mice, which indicates that T2 B cells might differentiate directly into MZ B cells.
46. hi splenic B cells are an immature developmental intermediate in the production of long-lived marrow-derived B cells. J. Immunol. 151, 4431-4444 (1993).
47. Batten, M. et al. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 192, 1453-1465 (2000). This article indicated a role for BAFF in B-cell maturation that was later confirmed In BAFF-deficient animals. This work also supports the possibility that T2 B cells are potential precursors of MZ B cells.
48. Schiemann, B. et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293, 2111-2114 (2001). The first description of BAFF-deficient mice. The maturation of B cells is arrested at the T1 B-cell stage in these animals.
49. Gross, J. A. et al. TACI-Ig neutralizes molecules critical for B-cell development and autoimmune disease: impaired B-cell maturation in mice lacking BLyS. Immunity 15, 289-302 (2001).
50. Schneider, P. et al. Maturation of marginal-zone and follicular B cells requires B-cell activating factor of the tumor-necrosis factor family and is independent of B-cell maturation antigen. J. Exp. Med. 194, 1691-1697 (2001).
51. Xu, S. & Lam, K.-P. B-cell maturation protein, which binds the tumor-necrosis factor family members BAFF and APRIL, is dispensable for humoral immune responses. Mol. Cell. Biol. 21, 4067-4074 (2001).
52. von Buelow, G.-U., van Deursen, J. M. & Bram, R. J. Regulation of the T-independent humoral response by TACI. Immunity 14, 573-582 (2001).
53. Yan, M. et al. Activation and accumulation of B cells in TACI-deficient mice. Nature Immunol. 2, 638-643 (2001).
54. Yu, G. et al. APRIL and TALL-1 and receptors BCMA and TACI: system for regulating humoral immunity. Nature Immunol. 1, 252-256 (2000).
55. Amanna, I. J., Clise-Dwyer, K., Nashold, F. E., Hoag, K. A. & Hayes, C. E. A/WySnJ transitional B cells overexpress the chromosome 15 proapoptotic Blk gene and succumb to premature apoptosis. J. Immunol. 167, 6069-6072 (2001).
56. Harless, S. M. et al. Competition for BLyS-mediated signalling through Bcmd/BR3 regulates peripheral B-lymphocyte numbers. Curr. Biol. 11, 1986-1989 (2001).
57. Khare, S. D. et al. Severe B-cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc. Natl Acad. Sci. USA 97, 3370-3375 (2000).
58. Matsumoto, M., Fu, Y.-X., Molina, H. & Chaplin, D. D. Lymphotoxin-α-deficient and TNF receptor-1-deficient mice define developmental and functional characteristics of germinal centers. Immunol. Rev. 156, 137-144 (1997).
59. Guinamard, R., Okigaki, M., Schlessinger, J. & Ravetch, J. V. Absence of marginal-zone B cells in Pyk-2-deficient mice define their role in the humoral response. Nature Immunol. 1, 37-41 (2000).
60. Groom, J. et al. Association of BAFF/BLyS overexpression and altered B-cell differentiation with Sjögren's syndrome. J. Clin. Invest. 109, 59-68 (2002). This paper provides the first description of MZ-like B cells in inflamed tissues and the potential direct pathogenic role of this subset of B cells in autoimmunity.
61. Yano, H. & Chao, M. V. Neurotrophin receptor structure and interactions. Pharm. Acta Helv. 74, 253-260 (2000).
62. Yan, M. et al. Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nature Immunol. 1, 37-41 (2000).
63. Huard, B., Schneider, P., Mauri, D., Tschopp, J. & French, L. E. T-cell costimulation by the TNF ligand BAFF. J. Immunol. 167, 6225-6231 (2001).
64. Martin, F. & Kearney, J. F. B-cell subsets and the mature preimmune repertoire. Marginal-zone and B1 B cells as part of a 'natural immune memory'. Immunol. Rev. 175, 70-79 (2000).
65. Zhang, J. et al. A role for B-lymphocyte stimulator in systemic lupus erythematosus. J. Immunol. 166, 6-10 (2001). The first description of an association between high serum levels of BAFF and autoimmunity in humans.
66. Cheema, G. S., Roschke, V., Hilbert, D. M. & Stohl, W. Elevated serum B-lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum. 44, 1313-1319 (2001).
67. Jonsson, R., Haga, H.-J. & Gordon, T. P. in Arthritis and Allied Conditions (ed. Koopman, W.) 1826-1849 (Lea and Fabiger, Philadelphia, 2000).
68. Zeng, D., Lee, M.-K., Tung, J., Brendolan, A. & Strober, S. A role for CD1 in the pathogenesis of lupus in NZB/NZW mice. J. Immunol. 164, 5000-5004 (2000).
69. 2-microglobulin-dependent and -independent forms. J. Immunol. 161, 1710-1717 (1998).
70. Grimaldi, C. M., Michael, D. J. & Diamond, B. Expansion and activation of a population of autoreactive marginal-zone B cells in a model of estrogen-induced lupus. J. Immunol. 167, 1886-1890 (2001).
71. Martin, F. & Kearney, J. F. Positive selection from newly formed to marginal-zone B cells depends on the rate of clonal production, CD19 and btk. Immunity 12, 39-49 (2000). The first article to indicate a possible alternative maturation pathway for polyreactive or potentially autoreactive B cells. These cells might preferentially differentiate into MZ B cells.
72. Cariappa, A. et al. The follicular versus marginal-zone B-lymphocyte cell-fate decision is regulated by aiolos, Btk and CD21. Immunity 14, 603-615 (2001).
73. Li, Y., Li, H. & Weigert, M. Autoreactive B cells in the marginal zone that express dual receptors. J. Exp. Med. 195, 181-188 (2002).
74. Chen, X., Martin. F., Forbush, K. A., Perlmutter, R. M. & Kearney, J. K. Evidence for selection of a population of multi-reactive B cells into the splenic marginal zone. Int. Immunol. 9, 27-41 (1997).
75. high splenic B cells enriched in the marginal zone: distinct phenotypes and functions. Curr. Top. Microbiol. Immunol. 246, 45-50 (1999).
76. Kamata, T. et al. Increased frequency of surface IgA-positive plasma cells in the intestinal lamina propria and decreased IgA excretion in hyper IgA (HIGA) mice, a murine model of IgA nephropathy with hyperserum IgA. J. Immunol. 165, 1387-1394 (2000).
77. Briones, J., Timmerman, J. M., Hilbert, D. M. & Levy, R. BLyS and BLyS receptor expression in non-Hodgkin's lymphoma. Exp. Hematol. 30, 135-141 (2002).
78. Thieblemont, C., Berger, F. & Coiffler, B. Mucosa-associated lymphoid tissue lymphomas. Curr. Opin. Oncol. 7, 415-420 (1995).
79. Bannish, G., Fuentes-Panana, E. M., Cambier, J. C., Pear, W. S. & Monroe, J. G. Ligand-independent signaling functions for the B-lymphocyte antigen receptor and their role in positive selection during B lymphopoiesis. J. Exp. Med. 194, 1583-1596 (2001).