TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts

Blood - Tập 111 - Trang 1004-1012 - 2008
Claudia Bossen1, Teresa G. Cachero2, Aubry Tardivel1, Karine Ingold1, Laure Willen1, Max Dobles2, Martin L. Scott2, Aris Maquelin1, Elodie Belnoue3, Claire-Anne Siegrist3, Stéphane Chevrier1, Hans Acha-Orbea1, Helen Leung4, Fabienne Mackay4, Jürg Tschopp1, Pascal Schneider1
1Department of Biochemistry, University of Lausanne, Epalinges, Switzerland
2BiogenIdec, Cambridge, MA;
3Department of Pathology-Immunology and Pediatrics, University of Geneva, Geneva, Switzerland; and
4Garvan Institute of Medical Research, Darlinghurst, Australia

Tóm tắt

Abstract The cytokine BAFF binds to the receptors TACI, BCMA, and BAFF-R on B cells, whereas APRIL binds to TACI and BCMA only. The signaling properties of soluble trimeric BAFF (BAFF 3-mer) were compared with those of higher-order BAFF oligomers. All forms of BAFF bound BAFF-R and TACI, and elicited BAFF-R–dependent signals in primary B cells. In contrast, signaling through TACI in mature B cells or plasmablasts was only achieved by higher-order BAFF and APRIL oligomers, all of which were also po-tent activators of a multimerization-dependent reporter signaling pathway. These results indicate that, although BAFF-R and TACI can provide B cells with similar signals, only BAFF-R, but not TACI, can respond to soluble BAFF 3-mer, which is the main form of BAFF found in circulation. BAFF 60-mer, an efficient TACI agonist, was also detected in plasma of BAFF transgenic and nontransgenic mice and was more than 100-fold more active than BAFF 3-mer for the activation of multimerization-dependent signals. TACI supported survival of activated B cells and plasmablasts in vitro, providing a rational basis to explain the immunoglobulin deficiency reported in TACI-deficient persons.

Tài liệu tham khảo

Bossen, 2006, BAFF, APRIL and their receptors: structure, function and signaling., Semin Immunol, 18, 263, 10.1016/j.smim.2006.04.006 Kalled, 2005, The role of BAFF in immune function and implications for autoimmunity., Immunol Rev, 204, 43, 10.1111/j.0105-2896.2005.00219.x Treml, 2006, BLyS receptor signatures resolve homeostatically independent compartments among naive and antigen-experienced B cells., Semin Immunol, 18, 297, 10.1016/j.smim.2006.07.001 Scapini, 2005, Proinflammatory mediators elicit secretion of the intracellular B-lymphocyte stimulator pool (BLyS) that is stored in activated neutrophils: implications for inflammatory diseases., Blood, 105, 830, 10.1182/blood-2004-02-0564 Nardelli, 2001, Synthesis and release of B-lymphocyte stimulator from myeloid cells., Blood, 97, 198, 10.1182/blood.V97.1.198 Gorelik, 2003, Normal B cell homeostasis requires B cell activation factor production by radiation–resistant cells., J Exp Med, 198, 937, 10.1084/jem.20030789 Craxton, 2003, Macrophage- and dendritic cell–dependent regulation of human B-cell proliferation requires the TNF family ligand BAFF., Blood, 101, 4464, 10.1182/blood-2002-10-3123 Moore, 1999, BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator., Science, 285, 260, 10.1126/science.285.5425.260 Schneider, 1999, BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth., J Exp Med, 189, 1747, 10.1084/jem.189.11.1747 Bodmer, 2002, The molecular architecture of the TNF superfamily., Trends Biochem Sci, 27, 19, 10.1016/S0968-0004(01)01995-8 Karpusas, 2002, Crystal structure of extracellular human BAFF, a TNF family member that stimulates B lymphocytes., J Mol Biol, 315, 1145, 10.1006/jmbi.2001.5296 Liu, 2002, Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands., Cell, 108, 383, 10.1016/S0092-8674(02)00631-1 Cachero, 2006, Formation of virus-like clusters is an intrinsic property of the tumor necrosis factor family member BAFF (B cell activating factor)., Biochemistry, 45, 2006, 10.1021/bi051685o Ingold, 2005, Identification of proteoglycans as the APRIL-specific binding partners., J Exp Med, 201, 1375, 10.1084/jem.20042309 O'Connor, 2004, BCMA is essential for the survival of long-lived bone marrow plasma cells., J Exp Med, 199, 91, 10.1084/jem.20031330 Gorelik, 2004, Cutting edge: BAFF regulates CD21/35 and CD23 expression independent of its B cell survival function., J Immunol, 172, 762, 10.4049/jimmunol.172.2.762 Hsu, 2002, Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators., J Immunol, 168, 5993, 10.4049/jimmunol.168.12.5993 Batten, 2000, BAFF mediates survival of peripheral immature B lymphocytes., J Exp Med, 192, 1453, 10.1084/jem.192.10.1453 Tardivel, 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, 10.1002/eji.200324692 Shulga-Morskaya, 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, 10.4049/jimmunol.173.4.2331 Castigli, 2004, Impaired IgA class switching in APRIL–deficient mice., Proc Natl Acad Sci U S A, 101, 3903, 10.1073/pnas.0307348101 Varfolomeev, 2004, APRIL–deficient mice have normal immune system development., Mol Cell Biol, 24, 997, 10.1128/MCB.24.3.997-1006.2004 von Bülow, 2001, Regulation of the T–independent humoral response by TACI., Immunity, 14, 573, 10.1016/S1074-7613(01)00130-3 Seshasayee, 2003, Loss of TACI causes fatal lymphoproliferation and autoimmunity, establishing TACI as an inhibitory BLyS receptor., Immunity, 18, 279, 10.1016/S1074-7613(03)00025-6 Salzer, 2005, Mutations in TNFRSF13B encoding TACI are associated with common variable immunodeficiency in humans., Nat Genet, 37, 820, 10.1038/ng1600 Castigli, 2005, TACI is mutant in common variable immunodeficiency and IgA deficiency., Nat Genet, 37, 829, 10.1038/ng1601 Mackay, 1999, Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations., J Exp Med, 190, 1697, 10.1084/jem.190.11.1697 Schneider, 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, 10.1084/jem.194.11.1691 Schneider, 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, 10.1084/jem.187.8.1205 Held, 1993, Superantigen-reactive CD4+ T cells are required to stimulate B cells after infection with mouse mammary tumor virus., J Exp Med, 177, 359, 10.1084/jem.177.2.359 Pihlgren, 2006, Reduced ability of neonatal and early-life bone marrow stromal cells to support plasmablast survival., J Immunol, 176, 165, 10.4049/jimmunol.176.1.165 Pihlgren, 2003, CpG-motifs enhance initial and sustained primary tetanus-specific antibody secreting cell responses in spleen and bone marrow, but are more effective in adult than in neonatal mice., Vaccine, 21, 2492, 10.1016/S0264-410X(03)00052-5 Holler, 2003, Two adjacent trimeric Fas ligands are required for Fas signaling and formation of a death-inducing signaling complex., Mol Cell Biol, 23, 1428, 10.1128/MCB.23.4.1428-1440.2003 Liu, 2003, Ligand-receptor binding revealed by the TNF family member TALL-1., Nature, 423, 49, 10.1038/nature01543 Ng, 2004, B cell-activating factor belonging to the TNF family (BAFF)-R is the principal BAFF receptor facilitating BAFF costimulation of circulating T and B cells., J Immunol, 173, 807, 10.4049/jimmunol.173.2.807 Bossen, 2006, Interactions of tumor necrosis factor (TNF) and TNF receptor family members in the mouse and human., J Biol Chem, 281, 13964, 10.1074/jbc.M601553200 Yang, 2005, B cell maturation antigen, the receptor for a proliferation–inducing ligand and B cell-activating factor of the TNF family, induces antigen presentation in B cells., J Immunol, 175, 2814, 10.4049/jimmunol.175.5.2814 Kreuz, 2001, NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling., Mol Cell Biol, 21, 3964, 10.1128/MCB.21.12.3964-3973.2001 Grell, 1995, The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor., Cell, 83, 793, 10.1016/0092-8674(95)90192-2 Kim, 2003, Crystal structure of the BAFF-BAFF-R complex and its implications for receptor activation., Nat Struct Biol, 10, 342, 10.1038/nsb925 Ye, 2000, Thermodynamic characterization of the interaction between TRAF2 and TNFR peptides by isothermal titration calorimetry., Proc Natl Acad Sci U S A, 97, 8961, 10.1073/pnas.160241997 Baud, 1999, Signaling by proinflammatory cytokines: oligomerization of TRAF2 and TRAF6 is sufficient for JNK and IKK activation and target gene induction via an amino-terminal effector domain., Genes Dev, 13, 1297, 10.1101/gad.13.10.1297 Avery, 2003, BAFF selectively enhances the survival and effector function of CD38+ plasmablasts generated from activated human memory B cells., J Clin Invest, 112, 286, 10.1172/JCI18025 Sakurai, 2007, TACI attenuates antibody production costimulated by BAFF-R and CD40., Eur J Immunol, 37, 110, 10.1002/eji.200636623 Sakurai, 2007, TACI regulates IgA production by APRIL in collaboration with HSPG., Blood, 109, 2961, 10.1182/blood-2006-08-041772 Bischof, 2006, Selective activation of TACI by syndecan-2., Blood, 107, 3235, 10.1182/blood-2005-01-0256 Zhang, 2005, BAFF supports human B cell differentiation in the lymphoid follicles through distinct receptors., Int Immunol, 17, 779, 10.1093/intimm/dxh259 Novak, 2004, Expression of BCMA, TACI, and BAFF-R in multiple myeloma: a mechanism for growth and survival., Blood, 103, 689, 10.1182/blood-2003-06-2043 Hoyer, 2004, Short-lived plasmablasts and long-lived plasma cells contribute to chronic humoral autoimmunity in NZB/W mice., J Exp Med, 199, 1577, 10.1084/jem.20040168