BAFF and APRIL: A tutorial on B cell survival

Annual Review of Immunology

Volumn 21, Issue , 2003, Pages 231-264

  Mackay, Fabienne ^a   Schneider, Pascal ^b   Rennert, Paul ^c   Browning, Jeffrey ^c  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c BIOGEN   (United States)

Author keywords

Autoimmunity; B lymphocyte; Maturation; Spleen; TNF family

Indexed keywords

APRIL PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 4; INTERLEUKIN 7; LIGAND; PLASMA PROTEIN; UNCLASSIFIED DRUG; B CELL ACTIVATING FACTOR; B CELL ACTIVATING FACTOR RECEPTOR; IMMUNOGLOBULIN A; MEMBRANE PROTEIN; TNFRSF13C PROTEIN, HUMAN; TNFRSF13C PROTEIN, MOUSE; TNFSF13 PROTEIN, HUMAN; TNFSF13 PROTEIN, MOUSE; TNFSF13B PROTEIN, HUMAN; TNFSF13B PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

AUTOIMMUNITY; AUTOREGULATION; B CELL ACTIVATION FACTOR OF THE TNF FAMILY; B LYMPHOCYTE; CELL DEATH; CELL GROWTH; CELL MATURATION; CELL SURVIVAL; GENE OVEREXPRESSION; HODGKIN DISEASE; HUMAN; IMMUNE SYSTEM; MOUSE; NONHODGKIN LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; CYTOLOGY; DISEASE MODEL; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; AUTOIMMUNITY; B-CELL ACTIVATING FACTOR; B-CELL ACTIVATION FACTOR RECEPTOR; B-LYMPHOCYTES; CELL SURVIVAL; DISEASE MODELS, ANIMAL; HUMANS; IMMUNE TOLERANCE; IMMUNOGLOBULIN A; LIGANDS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 13; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0038692705     PISSN: 07320582     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.immunol.21.120601.141152     Document Type: Review

References (156)

1. Plas DR, Rathmell JC, Thompson CB. 2002. Homeostatic control of lymphocyte survival: potential origins and implications. Nat. Immunol. 3:515-21
2. Mackay FM, Browning JL. 2002. BAFF: A fundamental survival factor for B cells. Nat. Rev. Immunol. 2:465-75
3. Mackay F, Mackay CR. 2002. The role of BAFF in B-cell maturation, T-cell activation and autoimmunity. Trends Immunol. 23:113-15
4. Rolink AG, Melchers F. 2002. BAFFled B cells survive and thrive: roles of BAFF in B-cell development. Curr. Opin. Immunol. 14:266-75
5. Dorner T, Putterman C. 2001. B cells, BAFF/zTNF4, TACI, and systemic lupus erythematosus. Arthritis Res. 3:197-99
6. Khare SD, Hsu H. 2001. The role of TALL-1 and APRIL in immune regulation. Trends Immunol. 22:61-63
7. Laabi Y, Egle A, Strasser A. 2001. TNF cytokine family: more BAFF-ling complexities. Curr. Biol. 11:R1013-16
8. Do RK, Chen-Kiang S. 2002. Mechanism of BLyS action in B cell immunity. Cytokine Growth Factor Rev. 13:19-25
9. Ware CF. 2000. APRIL and BAFF connect autoimmunity and cancer. J. Exp. Med. 192:F35-F38
10. Zouali M. 2002. B cell diversity and longevity in systemic autoimmunity. Mol. Immunol. 38:895-901
11. Stohl W. 2002. Systemic lupus erythematosus: a blissless disease of too much BLyS (B lymphocyte stimulator) protein. Curr. Opin. Immunol. 14:522-28
12. Kalled S. 2002. BAFF: a novel target for autoimmunity. Curr. Opin. Invest. Drugs 3:1005-10
13. Schneider P, MacKay F, Steiner V, Hofmann K, Bodmer JL, Holler N, Ambrose C, Lawton P, Bixler S, Acha-Orbea H, Valmori D, Romero P, Werner-Favre C, Zubler RH, Browning JL, Tschopp J. 1999. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J. Exp. Med. 189:1747-56
14. Hahne M, Kataoka T, Schroter M, Hofmann K, Irmler M, Bodmer JL, Schneider P, Bornand T, Holler N, French LE, Sordat B, Rimoldi D, Tschopp J. 1998. APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J. Exp. Med. 188:1185-90
15. Shu HB, Hu WH, Johnson H. 1999. TALL-1 is a novel member of the TNF family that is down-regulated by mitogens. J. Leukocyte Biol. 65:680-83
16. Mukhopadhyay A, Ni J, Zhai Y, Yu GL, Aggarwal BB. 1999. Identification and characterization of a novel cytokine, THANK, a TNF homologue that activates apoptosis, nuclear factor-kappaB, and c-Jun NH2-terminal kinase. J. Biol. Chem. 274:15978-81
17. Moore PA, Belvedere O, Orr A, Pieri K, LaFleur DW, Feng P, Soppet D, Charters M, Gentz R, Parmelee D, Li Y, Galperina O, Giri J, Roschke V, Nardelli B, Carrell J, Sosnovtseva S, Greenfield W, Ruben SM, Olsen HS, Fikes J, Hilbert DM. 1999. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science 285:260-63
18. Gross JA, Johnston J, Mudri S, Enselman R, Dillon SR, Madden K, Xu W, Parrish-Novak J, Foster D, Lofton-Day C, Moore M, Littau A, Grossman A, Haugen H, Foley K, Blumberg H, Harrison K, Kindsvogel W, Clegg CH. 2000. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404:995-99
19. Jiang Y, Ohtsuji M, Abe M, Li N, Xiu Y, Wen S, Shirai T, Hirose S. 2001. Polymorphism and chromosomal mapping of the mouse gene for B-cell activating factor belonging to the tumor necrosis factor family (Baff) and association with the autoimmune phenotype. Immunogenetics 53:810-13
20. Berger R, Le Coniat M, Derre J, Vecchione D. 1989. Secondary nonrandom chromosomal abnormalities of band 13q34 in Burkitt lymphoma-leukemia. Genes Chromosomes Cancer 1:115-18
21. Kelly K, Manos E, Jensen G, Nadauld L, Jones DA. 2000. APRIL/TRDL-1, a tumor necrosis factor-like ligand, stimulates cell death. Cancer Res. 60:1021-27
22. Nishida T, Kaneko F, Kitagawa M, Yasuda H. 2001. Characterization of a novel mammalian SUMO-1/Smt3-specific isopeptidase, a homologue of rat axam, which is an axin-binding protein promoting beta-catenin degradation. J. Biol. Chem. 276:39060-66
23. Bodmer J-L, Schneider P, Tschopp J. 2002. The molecular architecture of the TNF superfamily. Trends Biol. Sci. 27:18-26
24. Locksley RM, Killeen N, Lenardo MJ. 2001. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487-501
25. Kanakaraj P, Migone TS, Nardelli B, Ullrich S, Li Y, Olsen HS, Salcedo TW, Kaufman T, Cochrane E, Gan Y, Hilbert DM, Giri J. 2001. BLyS binds to B cells with high affinity and induces activation of the transcription factors NF-kappaB and ELF-1. Cytokine 13:25-31
26. Lopez-Fraga M, Fernandez R, Albar JP, Hahne M. 2001. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO J. 2:945-51
27. Chen Y, Molloy SS, Thomas L, Gambee J, Bachinger HP, Ferguson B, Zonana J, Thomas G, Morris NP. 2001. Mutations within a furin consensus sequence block proteolytic release of ectodysplasin-A and cause X-linked hypohidrotic ectodermal dysplasia. Proc. Natl. Acad. Sci. USA 98:7218-23
28. Schneider P, Street SL, Gaide O, Hertig S, Tardivel A, Tschopp J, Runkel L, Alevizopoulos K, Ferguson BM, Zonana J. 2001. Mutations leading to X-linked hypohidrotic ectodermal dysplasia affect three major functional domains in the tumor necrosis factor family member ectodysplasin-A. J. Biol. Chem. 276:18819-27
29. Chicheportiche Y, Bourdon PR, Xu H, Hsu YM, Scott H, Hession C, Garcia I, Browning JL. 1997. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J. Biol. Chem. 272:32401-10
30. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, Schneider P, Tschopp J, Browning JL. 1999. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 190:1697-710
31. Groom J, Kalled SL, Cutler AH, Olson C, Woodcock SA, Schneider P, Tschopp J, Cachero TG, Batten M, Wheway J, Mauri D, Cavill D, Gordon TP, Mackay CR, Mackay F. 2002. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. J. Clin. Invest. 109:59-68
32. Zhang J, Roschke V, Baker KP, Wang Z, Alarcon GS, Fessler BJ, Bastian H, Kimberly RP, Zhou T 2001. Cutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosus. J. Immunol. 166:6-10
33. 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. 44:1313-19
34. Nardelli B, Belvedere O, Roschke V, Moore PA, Olsen HS, Migone TS, Sosnovtseva S, Carrell JA, Feng P, Giri JG, Hilbert DM. 2001. Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 97:198-204
35. Karpusas M, Cachero TG, Qian F, Boriack-Sjodin A, Mullen C, Strauch K, Hsu YM, Kalled SL. 2002. Crystal structure of extracellular human BAFF, a TNF family member that stimulates B lymphocytes. J. Mol. Biol. 315:1145-54
36. Oren DA, Li Y, Volovik Y, Morris TS, Dharia C, Das K, Galperina O, Gentz R, Arnold E. 2002. Structural basis of BLyS receptor recognition. Nat. Struct. Biol. 9:288-92
37. Liu Y, Xu L, Opalka N, Kappler J, Shu HB, Zhang G. 2002. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Cell 108:383-94
38. Igaki T, Kanda H, Yamamoto-Goto Y, Kanuka H, Kuranaga E, Aigaki T, Miura M. 2002. Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J. 21:3009-18
39. Kanda H, Igaki T, Kanuka H, Yagi T, Miura M. 2002. Wengen, a member of the drosophila TNF receptor superfamily, is required for Eiger signaling. J. Biol. Chem. 277(32):28372-75
40. Hymowitz SG, Christinger HW, Fuh G, Ultsch M, O'Connell M, Kelley RF, Ashkenazi A, de Vos AM. 1999. Triggering cell death: the crystal structure of Apo2L/TRAIL in a complex with death receptor 5. Mol. Cell 4:563-71
41. Schneider P, Holler N, Bodmer JL, Hahne M, Frei K, Fontana A, Tschopp J. 1998. Conversion of membrane-bound Fas(CD95) ligand to its soluble form is associated with downregulation of its proapoptotic activity and loss of liver toxicity. J. Exp. Med. 187:1205-13
42. Marsters SA, Yan M, Pitti RM, Haas PE, Dixit VM, Ashkenazi A. 2000. Interaction of the TNF homologues BLyS and APRIL with the TNF receptor homologues BCMA and TACI. Curr. Biol. 10:785-88
43. Rennert P, Schneider P, Cachero TG, Thompson J, Trabach L, Hertig S, Holler N, Qian F, Mullen C, Strauch K, Browning JL, Ambrose C, Tschopp J. 2000. A soluble form of B cell maturation antigen, a receptor for the tumor necrosis factor family member APRIL, inhibits tumor cell growth. J. Exp. Med. 192:1677-84
44. Thompson JS, Schneider P, Kalled SL, Wang L, Lefevre EA, Cachero TG, MacKay F, Bixler SA, Zafari M, Liu ZY, Woodcock SA, Qian F, Batten M, Madry C, Richard Y, Benjamin CD, Browning JL, Tsapis A, Tschopp J, Ambrose C. 2000. BAFF binds to the tumor necrosis factor receptor-like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population. J. Exp. Med. 192:129-35
45. Wu Y, Bressette D, Carrell JA, Kaufman T, Feng P, Taylor K, Gan Y, Cho YH, Garcia AD, Gollatz E, Dimke D, LaFleur D, Migone TS, Nardelli B, Wei P, Ruben SM, Ullrich SJ, Olsen HS, Kanakaraj P, Moore PA, Baker KP. 2000. Tumor necrosis factor (TNF) receptor superfamily member TACI is a high affinity receptor for TNF family members APRIL and BLyS. J. Biol. Chem. 275:35478-85
46. Xu S, Lam KP. 2001. B-cell maturation protein, which binds the tumor necrosis factor family members BAFF and APRIL, is dispensable for humoral immune responses. Mol. Cell. Biol. 21:4067-74
47. Yu G, Boone T, Delaney J, Hawkins N, Kelley M, Ramakrishnan M, McCabe S, Qiu WR, Kornuc M, Xia XZ, Guo J, Stolina M, Boyle WJ, Sarosi I, Hsu H, Senaldi G, Theill LE. 2000. APRIL and TALL-I and receptors BCMA and TACI: system for regulating humoral immunity. Nat. Immunol. 1:252-56
48. Laabi Y, Gras MP, Carbonnel F, Brouet JC, Berger R, Larsen CJ, Tsapis A. 1992. A new gene, BCM, on chromosome 16 is fused to the interleukin 2 gene by a t(4;16)(q26;p13) translocation in a malignant T cell lymphoma. EMBO J. 11:3897-904
49. von Bulow GU, Bram RJ. 1997. NF-AT activation induced by a CAML-interacting member of the tumor necrosis factor receptor superfamily. Science 278:138-41
50. Thompson JS, Bixler SA, Qian F, Vora K, Scott ML, Cachero TG, Hession C, Schneider P, Sizing ID, Mullen C, Strauch K, Zafari M, Benjamin CD, Tschopp J, Browning JL, Ambrose C. 2001. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 293:2108-11
51. Yan M, Brady JR, Chan B, Lee WP, Hsu B, Harless S, Cancro M, Grewal IS, Dixit VM. 2001. Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency. Curr. Biol. 11:1547-52
52. Kawasaki A, Tsuchiya N, Fukazawa T, Hashimoto H, Tokunaga K. 2001. Presence of four major haplotypes in human BCMA gene: lack of association with systemic lupus erythematosus and rheumatoid arthritis. Genes Immun. 2:276-79
53. Wiley SR, Cassiano L, Lofton T, Davis-Smith T, Winkles JA, Lindner V, Liu H, Daniel TO, Smith CA, Fanslow WC. 2001. A novel TNF recpetor family member binds TWEAK and is implicated in angiogenesis. Immunity 15:837-46
54. Banner DW, D'Arcy A, Janes W, Gentz R, Schoenfeld HJ, Broger C, Loetscher H, Lesslauer W. 1993. Crystal structure of the soluble human 55 kd TNF receptor-human TNF beta complex: implications for TNF receptor activation. Cell 73:431-45
55. Wilson-Rawls J, Deutscher SL, Wold WS. 1994. The signal-anchor domain of adenovirus E3-6.7K, a type III integral membrane protein, can direct adenovirus E3-gp19K, a type I integral membrane protein, into the membrane of the endoplasmic reticulum. Virology 201:66-76
56. Gras MP, Laabi Y, Linares-Cruz G, Blondel MO, Rigaut JP, Brouet JC, Leca G, Haguenauer-Tsapis R, Tsapis A. 1995. BCMAp: an integral membrane protein in the Golgi apparatus of human mature B lymphocytes. Int. Immunol. 7:1093-106
57. Bradley JR, Thiru S, Pober JS. 1995. Disparate localization of 55-kd and 75-kd tumor necrosis factor receptors in human endothelial cells. Am. J. Pathol. 146:27-32
58. Zhang XD, Franco AV, Nguyen T, Gray CP, Hersey P. 2000. Differential localization and regulation of death and decoy receptors for TNF-related apoptosis-inducing ligand (TRAIL) in human melanoma cells. J. Immunol. 164:3961-70
59. Schneider P, Takatsuka H, Wilson A, Mackay F, Tardivel A, Lens S, Cachero TG, Finke D, Beermann F, Tschopp J. 2001. 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. 194:1691-97
60. Yan M, Wang H, Chan B, Roose-Girma M, Erickson S, Baker T, Tumas D, Grewal IS, Dixit VM. 2001. Activation and accumulation of B cells in TACI-deficient mice. Nat. Immunol. 2:638-43
61. McDermott MF, Aksentijevich I, Galon J, McDermott EM, Ogunkolade BW, Centola M, Mansfield E, Gadina M, Karenko L, Pettersson T, McCarthy J, Frucht DM, Aringer M, Torosyan Y, Teppo AM, Wilson M, Karaarslan HM, Wan Y, Todd I, Wood G, Schlimgen R, Kumarajeewa TR, Cooper SM, Vella JP, Kastner DL, et al. 1999. Germline mutations in the extracellular domains of the 55 kDa TNF receptor, TNFR1, define a family of dominantly inherited autoinflammatory syndromes. Cell 97:133-44
62. Karin M, Ben-Neriah Y. 2000. Phosphorylation meets ubiquitination: the control of NF-kappaB activity. Annu. Rev. Immunol. 18:621-63
63. Baud V, Karin M. 2001. Signal transduction by tumor necrosis and its relatives. Trends Cell Biol. 11:372-77
64. Hatzoglou A, Roussel J, Bourgeade MF, Rogier E, Madry C, Inoue J, Devergne O, Tsapis A. 2000. TNF receptor family member BCMA (B cell maturation) associates with TNF receptor-associated factor (TRAF) 1, TRAF2, and TRAF3 and activates NF-kappa B, elk-1, c-Jun N-terminal kinase, and p38 mitogen-activated protein kinase. J. Immunol. 165:1322-30
65. Xia XZ, Treanor J, Senaldi G, Khare SD, Boone T, Kelley M, Theill LE, Colombero A, Solovyev I, Lee F, McCabe S, Elliott R, Miner K, Hawkins N, Guo J, Stolina M, Yu G, Wang J, Delaney J, Meng SY, Boyle WJ, Hsu H. 2000. TACI is a TRAF-interacting receptor for TALL-1, a tumor necrosis factor family member involved in B cell regulation. J. Exp. Med. 192:137-43
66. Weitzer S, Uhlmann F. 2002. Chromosome segregation: playing polo in prophase. Dev. Cell 2:381-82
67. Verger A, Duterque-Coquillaud M. 2002. When Ets transcription factors meet their partners. BioEssays 24:362-70
68. von Bulow GU, van Deursen JM, Bram RJ. 2001. Regulation of the T-independent humoral response by TACI. Immunity 14:573-82
69. Schiemann B, Gommerman JL, Vora K, Cachero TG, Shulga-Morskaya S, Dobles M, Frew E, Scott ML. 2001. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293:2111-14
70. Gross JA, Dillon SR, Mudri S, Johnston J, Littau A, Roque R, Rixon M, Schou O, Foley KP, Haugen H, McMillen S, Waggie K, Schreckhise RW, Shoemaker K, Vu T, Moore M, Grossman A, Clegg CH. 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
71. Khare SD, Sarosi I, Xia XZ, McCabe S, Miner K, Solovyev I, Hawkins N, Kelley M, Chang D, Van G, Ross L, Delaney J, Wang L, Lacey D, Boyle WJ, Hsu H. 2000. Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc. Natl. Acad. Sci. USA 97:3370-75
72. Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, Cory S, Harris AW. 1991. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl. Acad. Sci. USA 88:8661-65
73. Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Kontgen F, Adams JM, Strasser A. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286:1735-38
74. Do RK, Hatada E, Lee H, Tourigny MR, Hilbert D, Chen-Kiang S. 2000. Attenuation of apoptosis underlies B lymphocyte stimulator enhancement of humoral immune response. J. Exp. Med. 192:953-64
75. 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. 168:5993-96
76. Grossmann M, O'Reilly LA, Gugasyan R, Strasser A, Adams JM, Gerondakis S. 2000. The anti-apoptotic activities of Rel and RelA required during B-cell maturation involve the regulation of Bcl-2 expression. EMBO J. 19:6351-60
77. Su TT, Rawlings DJ. 2002. Transitional B lymphocyte subsets operate as distinct checkpoints in murine splenic B cell development. J. Immunol. 168:2101-10
78. Lentz VM, Hayes CE, Cancro MP. 1998. Bcmd decreases the life span of B-2 but not B-1 cells in A/WySnJ mice. J. Immunol. 160:3743-47
79. Amanna IJ, Clise-Dwyer K, Nashold FE, Hoag KA, Hayes CE. 2001. Cutting edge: A/WySnJ transitional B cells overexpress the chromosome 15 proapoptotic Blk gene and succumb to premature apoptosis. J. Immunol. 167:6069-72
80. Ghosh S, Karin M. 2002. Missing pieces in the NF-κb puzzle. Cell 109:581-96
81. Senftleben U, Cao Y, Xiao G, Greten FR, Krahn G, Bonizzi G, Chen Y, Hu Y, Fong A, Sun SC, Karin M. 2001. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 293:1495-99
82. Kaisho T, Takeda K, Tsujimura T, Kawai T, Nomura F, Terada N, Akira S. 2001. IkappaB kinase alpha is essential for mature B cell development and function. J. Exp. Med. 193:417-26
83. Yamada T, Mitani T, Yorita K, Uchida D, Matsushima A, Iwamasa K, Fujita S, Matsumoto M. 2000. Abnormal immune function of hemopoietic cells from alymphoplasia (aly) mice, a natural strain with mutant NF-kappa B-inducing kinase. J. Immunol. 165:804-12
84. Yan M, Marsters SA, Grewal IS, Wang H, Ashkenazi A, Dixit VM. 2000. Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nat. Immunol. 1:37-41
85. Xiao G, Harhaj EW, Sun SC. 2001. NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol. Cell 7:401-9
86. Loder F, Mutschler B, Ray RJ, Paige CJ, Sideras P, Torres R, Lamers MC, Carsetti R. 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
87. Allman D, Lindsley RC, DeMuth W, Rudd K, Shinton SA, Hardy RR. 2001. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167:6834-40
88. Batten M, Groom J, Cachero TG, Qian F, Schneider P, Tschopp J, Browning JL, Mackay F. 2000. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 192:1453-66
89. Rolink AG, Tschopp J, Schneider P, Melchers F. 2002. BAFF is a survival and maturation factor for mouse B cells. Eur. J. Immunol. 32:2004-10
90. Schlaeger EJ. 1996. The protein hydrolysate, Primatone RL, is a cost-effective multiple growth promoter of mammalian cell culture in serum-containing and serum-free media and displays anti-apoptosis properties. J. Immunol. Methods 194:191-99
91. Harless SM, Lentz VM, Sah AP, Hsu BL, Clise-Dwyer K, Hilbert DM, Hayes CE, Cancro MP. 2001. Competition for BLyS-mediated signaling through Bcmd/BR3 regulates peripheral B lymphocyte numbers. Curr. Biol. 11:1986-89
92. Martin F, Kearney JF. 2002. Marginal-zone B cells. Nat. Rev. Immunol. 2:323-35
93. Fu YX, Chaplin DD. 1999. Development and maturation of secondary lymphoid tissues. Annu. Rev. Immunol. 17:399-433
94. Korner H, Winkler TH, Sedgwick JD, Rollinghoff M, Basten A, Cook MC. 2001. Recirculating and marginal zone B cell populations can be established and maintained independently of primary and secondary follicles. Immunol. Cell Biol. 79:54-61
95. Hao Z, Rajewsky K. 2001. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J. Exp. Med. 194:1151-64
96. Berland R, Wortis HH. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20:253-300
97. Carvalho TL, Mota-Santos T, Cumano A, Demengeot J, Vieira P. 2001. Arrested B lymphopoiesis and persistence of activated B cells in adult interleukin 7(-/)-mice. J. Exp. Med. 194:1141-50
98. Stein JV, Lopez-Fraga M, Elustondo FA, Carvalho-Pinto CE, Rodriguez D, Gomez-Caro R, De Jong J, Martinez AC, Medema JP, Hahne M. 2002. APRIL modulates B and T cell immunity. J. Clin. Invest. 109:1587-98
99. Parry TJ, Riccobene TA, Strawn SJ, Williams R, Daoud R, Carrell J, Sosnovtseva S, Miceli RC, Poortman CM, Sekut L, Li Y, Fikes J, Sung C. 2001. Pharmacokinetics and immunological effects of exogenously administered recombinant human B lymphocyte stimulator (BLyS) in mice. J. Pharmacol. Exp. Ther. 296:396-404
100. Koni PA, Flavell RA. 1999. Lymph node germinal centers form in the absence of follicular dendritic cell networks. J. Exp. Med. 189:855-64
101. Toellner KM, Jenkinson WE, Taylor DR, Khan M, Sze DM, Sansom DM, Vinuesa CG, MacLennan IC. 2002. Low-level hypermutation in T cell-independent germinal centers compared with high mutation rates associated with T cell-dependent germinal centers. J. Exp. Med. 195:383-89
102. Hannum LG, Haberman AM, Anderson SM, Shlomchik MJ. 2000. Germinal center initiation, variable gene region hypermutation, and mutant B cell selection without detectable immune complexes on follicular dendritic cells. J. Exp. Med. 192:931-42
103. Wang H, Marsters SA, Baker T, Chan B, Lee WP, Fu L, Tumas D, Yan M, Dixit VM, Ashkenazi A, Grewal IS. 2001. TACI-ligand interactions are required for T cell activation and collagen-induced arthritis in mice. Nat. Immunol. 2:632-37
104. Huard B, Schneider P, Mauri D, Tschopp J, French LE. 2001. T cell costimulation by the TNF ligand BAFF. J. Immunol. 167:6225-31
105. Anderton S, Burkhart C, Metzler B, Wraith D. 1999. Mechanisms of central and peripheral T-cell tolerance: lessons from experimental models of multiple sclerosis. Immunol. Rev. 169:123-37
106. Goodnow CC, Cyster JG, Hartley SB, Bell SE, Cooke MP, Healy JI, Akkaraju S, Rathmell JC, Pogue SL, Shokat KP. 1995. Self-tolerance checkpoints in B lymphocyte development. Adv. Immunol. 59:279-368
107. Monroe JG. 2000. B-cell antigen receptor signaling in immature-stage B cells: integrating intrinsic and extrinsic signals. Curr. Top. Microbiol. Immunol. 245:1-29
108. Majeti R, Xu Z, Parslow TG, Olson JL, Daikh DI, Killeen N, Weiss A. 2000. An inactivating point mutation in the inhibitory wedge of CD45 causes lymphoproliferation and autoimmunity. Cell 103:1059-70
109. Tedder TF, Inaoki M, Sato S. 1997. The CD19-CD21 complex regulates signal transduction thresholds governing humoral immunity and autoimmunity. Immunity 6:107-18
110. Zeng D, Lee MK, Tung J, Brendolan A, Strober S. 2000. Cutting edge: a role for CD1 in the pathogenesis of lupus in NZB/NZW mice. J. Immunol. 164:5000-4
111. Grimaldi CM, Michael DJ, Diamond B. 2001. Cutting edge: expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. J. Immunol. 167:1886-90
112. Li Y, Li H, Weigert M. 2002. Autoreactive B cells in the marginal zone that express dual receptors. J. Exp. Med. 195:181-88
113. Chen X, Martin F, Forbush KA, Perlmutter RM, Kearney JF. 1997. Evidence for selection of a population of multireactive B cells into the splenic marginal zone. Int. Immunol. 9:27-41
114. Fagarasan S, Honjo T. 2000. T-independent immune response: new aspects of B cell biology. Science 290:89-92
115. Ochsenbein AF, Zinkernagel RM. 2000. Natural antibodies and complement link innate and acquired immunity. Immunol. Today 21:624-30
116. Segundo C, Rodriguez C, Garcia-Poley A, Aguilar M, Gavilan I, Bellas C, Brieva JA. 2001. Thyroid-infiltrating B lymphocytes in Graves' disease are related to marginal zone and memory B cell compartments. Thyroid 11:525-30
117. Bendelac A, Bonneville M, Kearney JF. 2001. Autoreactivity by design: innate B and T lymphocytes. Nat. Rev. Immunol. 1:177-86
118. Chan OT, Hannum LG, Haberman AM, Madaio MP, Shlomchik MJ. 1999. A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J. Exp. Med. 189:1639-48
119. Kalled SL, Cutler AH, Datta SK, Thomas DW. 1998. Anti-CD40 ligand antibody treatment of SNF1 mice with established nephritis: preservation of kidney function. J. Immunol. 160:2158-65
120. Early GS, Zhao W, Burns CM. 1996. Anti-CD40 ligand antibody treatment prevents the development of lupus-like nephritis in a subset of New Zealand black x New Zealand white mice. Response correlates with the absence of an anti-antibody response. J. Immunol. 157:3159-64
121. Fagarasan S, Kinoshita K, Muramatsu M, Ikuta K, Honjo T. 2001. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413:639-43
122. Ji H, Ohmura K, Mahmood U, Lee DM, Hofhuis FM, Boackle SA, Takahashi K, Holers VM, Walport M, Gerard C, Ezekowitz A, Carroll MC, Brenner M, Weissleder R, Verbeek JS, Duchatelle V, Degott C, Benoist C, Mathis D. 2002. Arthritis critically dependent on innate immune system players. Immunity 16:157-68
123. Maccioni M, Zeder-Lutz G, Huang H, Ebel C, Gerber P, Hergueux J, Marchal P, Duchatelle V, Degott C, van Regenmortel M, Benoist C, Mathis D. 2002. Arthritogenic monoclonal antibodies from K/BxN mice. J. Exp. Med. 195:1071-77
124. Jonsson R, Haga H-J, Gordon TP. 2000. Sjogren's syndrome. In Arthritis and Allied Conditions, ed. WJ Koopman, pp. 1826-49. Philadelphia: Lea & Febiger
125. Rose NR. 1998. The role of infection in the pathogenesis of autoimmune disease. Semin. Immunol. 10:5-13
126. Sekigawa I, Kaneko H, Hishikawa T, Hashimoto H, Hirose S, Kaneko Y, Maruyama N. 1998. HIV infection and SLE: their pathogenic relationship. Clin. Exp. Rheumatol. 16:175-80
127. Stohl J, Cheema G, Briggs W, Xu D, Sosnovtseva S, Roschke V, Ferrara D, Labat K, Sattler F, Pierangeli S, Hilbert D. 2002. B lymphocyte stimulator protein: Associated increase in circulating autoantibody levels may require CD4(+) T cells: Lessons from HIV-infected patients. Clin. Immunol. 104:115-22
128. Davies K, Stiehm ER, Woo P, Murray KJ. 2001. Juvenile idiopathic polyarticular arthritis and IgA deficiency in the 22q11 deletion syndrome. J. Rheumatol. 28:2326-34
129. Briones J, Timmerman JM, Hilbert DM, Levy R. 2002. BLyS and BLyS receptor expression in non-Hodgkin's lymphoma. Exp. Hematol. 30:135-41
130. 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. 100:2973-79
131. Morse HC 3rd, Kearney JF, Isaacson PG, Carroll M, Fredrickson TN, Jaffe ES. 2001. Cells of the marginal zone - origins, function and neoplasia. Leuk. Res. 25:169-78
132. Bafico A, Gazit A, Wu-Morgan SS, Yaniv A, Aaronson SA. 1998. Characterization of Wnt-1 and Wnt-2 induced growth alterations and signaling pathways in NIH3T3 fibroblasts. Oncogene 16:2819-25
133. Roth W, Wagenknecht B, Klumpp A, Naumann U, Hahne M, Tschopp J, Weller M. 2001. APRIL, a new member of the tumor necrosis factor family, modulates death ligand-induced apoptosis. Cell Death Differ. 8:403-10
134. Yeh WC, Itie A, Elia AJ, Ng M, Shu HB, Wakeham A, Mirtsos C, Suzuki N, Bonnard M, Goeddel DV, Mak TW. 2000. Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12:633-42
135. Yeh WC, Pompa JL, McCurrach ME, Shu HB, Elia AJ, Shahinian A, Ng M, Wakeham A, Khoo W, Mitchell K, El-Deiry WS, Lowe SW, Goeddel DV, Mak TW. 1998. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279:1954-58
136. Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS, Mett IL, Rebrikov D, Brodianski VM, Kemper OC, Kollet O, Lapidot T, Soffer D, Sobe T, Avraham KB, Goncharov T, Holtmann H, Lonai P, Wallach D. 1998. Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9:267-76
137. Prlic M, Lefrancois L, Jameson SC. 2002. Multiple choices: regulation of memory CD8 T cell generation and homeostasis by interleukin (IL)-7 and IL-15. J. Exp. Med. 195:F49-52
138. Bertram EM, Lau P, Watts TH. 2002. Temporal segregation of 4-1BB versus CD28-mediated costimulation: 4-1BB ligand influences T cell numbers late in the primary response and regulates the size of the T cell memory response following influenza infection. J. Immunol. 168:3777-85
139. Cannons JL, Lau P, Ghumman B, DeBenedette MA, Yagita H, Okumura K, Watts TH. 2001. 4-1BB ligand induces cell division, sustains survival, and enhances effector function of CD4 and CD8 T cells with similar efficacy. J. Immunol. 167:1313-24
140. Honda K, Nakano H, Yoshida H, Nishikawa S, Rennert P, Ikuta K, Tamechika M, Yamaguchi K, Fukumoto T, Chiba T, Nishikawa SI. 2001. Molecular basis for hematopoietic/mesenchymal interaction during initiation of Peyer's patch organogenesis. J. Exp. Med. 193:621-30
141. Theill LE, Boyle WJ, Penninger IM. 2002. RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu. Rev. Immunol. 20:795-823
142. Cao Y, Bonizzi G, Seagroves TN, Greten FR, Johnson R, Schmidt EV, Karin M. 2001. IKKalpha provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 107:763-75
143. Laurikkala J, Pispa J, Jung HS, Nieminen P, Mikkola M, Wang X, Saarialho-Kere U, Galceran J, Grosschedl R, Thesleff I. 2002. Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar. Development 129:2541-53
144. Jernvall J, Thesleff I. 2000. Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech. Dev. 92:19-29
145. Lynch CN, Wang YC, Lund JK, Chen YW, Leal JA, Wiley SR. 1999. TWEAK induces angiogenesis and proliferation of endothelial cells. J. Biol. Chem. 274:8455-59
146. Jakubowski A, Browning B, Lukashev M, Sizing I, Thompson JS, Benjamin CD, Hsu YM, Ambrose C, Zheng TS, Burkly LC. 2002. Dual role for TWEAK in angiogenic regulation. J. Cell Sci. 115:267-74
147. Weih F, Durham SK, Barton DS, Sha WC, Baltimore D, Bravo R. 1997. p50-NF-kappaB complexes partially compensate for the absence of RelB: severely increased pathology in p50(-/-)relB (-/-) double-knockout mice. J. Exp. Med. 185:1359-70
148. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Negishi I, Senju S, Zhang Q, Fujii S, et al. 1995. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267:1506-10
149. Franzoso G, Carlson L, Poljak L, Shores EW, Epstein S, Leonardi A, Grinberg A, Tran T, Scharton-Kersten T, Anver M, Love P, Brown K, Siebenlist U. 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. 187:147-59
150. Caamano JH, Rizzo CA, Durham SK, Barton DS, Raventos-Suarez C, Snapper CM, Bravo R. 1998. Nuclear factor (NF)-kappa B2 (p100/p52) is required for normal splenic microarchitecture and B cell-mediated immune responses. J. Exp. Med. 187:185-96
151. Franzoso G, Carlson L, Scharton-Kersten T, Shores EW, Epstein S, Grinberg A, Tran T, Shacter E, Leonardi A, Anver M, Love P, Sher A, Siebenlist U. 1997. Critical roles for the Bcl-3 oncoprotein in T cell-mediated immunity, splenic microarchitecture, and germinal center reactions. Immunity 6:479-90
152. Poe JC, Hasegawa M, Tedder TF. 2001. CD19, CD21, and CD22: multifaceted response regulators of B lymphocyte signal transduction. Int. Rev. Immunol. 20:739-62
153. Weir DS, Yilmaz ZB, Weih F. 2001. Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J. Immunol. 167:1909-19
154. Cariappa A, Liou HC, Horwitz BH, Pillai S. 2000. Nuclear factor kappa B is required for the development of marginal zone B lymphocytes. J. Exp. Med. 192:1175-82
155. Wardemann H, Boehm T, Dear N, Carsetti R. 2002. B-1a B cells that link the innate and adaptive immune responses are lacking in the absence of the spleen. J. Exp. Med. 195:771-80
156. Franzoso G, Carlson L, Xing L, Poljak L, Shores EW, Brown KD, Leonardi A, Tran T, Boyce BF, Siebenlist U. 1997. Requirement for NF-kappaB in osteoclast and B-cell development. Genes Dev. 11:3482-96