Roles of TRAF3 in T cells: many surprises

References

• Hu HM, O'Rourke K, Bogusi MS, Dixit VM. A novel RING finger protein interacts with the cytoplasmic domain of CD40. J Biol Chem 1994; 269: 30069–72; PMID:7527023
   PubMed Web of Science ®Google Scholar
• Sato T, Irie S, Reed JC. A novel member of the TRAF family of putative signal transducing proteins binds to the cytosolic domain of CD40. FEBS Lett 1995; 358: 113–8; PMID:7530216; http://dx.doi.org/10.1016/0014-5793(94)01406-Q
   PubMed Web of Science ®Google Scholar
• Cheng G, Cleary AM, Ye Z-S, Hong DI, Lederman S, Baltimore D. Involvement of CRAF1, a relative of TRAF, in CD40 signaling. Science 1995; 267: 1494–8; PMID:7533327; http://dx.doi.org/10.1126/science.7533327
   PubMed Web of Science ®Google Scholar
• Mosialos G, Birkenbach M, Yalamanchili R, VanArsdale T, Ware C, Kie E. The EBV transforming protein LMP1 engages signaling proteins for the TNFR family. Cell 1995; 80: 389–99; PMID:7859281; http://dx.doi.org/10.1016/0092-8674(95)90489-1
   PubMed Web of Science ®Google Scholar
• Wajant H, Henkler F, Scheurich P. The TRAF family. Scaffold molecules for cytokine receptors, kinases and their regulators. Cell Signal 2001; 13: 389–400; PMID:11384837; http://dx.doi.org/10.1016/S0898-6568(01)00160-7
   PubMed Web of Science ®Google Scholar
• Ha H, Han D, Choi Y. TRAF-mediated TNFR-family signaling. Curr Protoc Immunol 2009; Chapter 11: Unit11.9D; PMID:19918944
   PubMedGoogle Scholar
• Hildebrand JM, Yi Z, Buchta CM, Poovassery J, Stunz LL, Bishop GA. Roles TRAF3 and TRAF5 in immune cell functions. Immunol Rev 2011; 244: 55–74; PMID:22017431; http://dx.doi.org/10.1111/j.1600-065X.2011.01055.x
   PubMed Web of Science ®Google Scholar
• Hans Häcker, Ping-Hui Tseng, Michael Karin. Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat Rev Immunol 2011; 11: 457–68; PMID:21660053; http://dx.doi.org/10.1038/nri2998
   PubMed Web of Science ®Google Scholar
• Xie P. TRAF molecules in cell signaling and in human diseases. J Mol Signal 2013; 8: 7; PMID:23758787; http://dx.doi.org/10.1186/1750-2187-8-7
   PubMedGoogle Scholar
• Chung JY, Park YC, Ye H, Wu H. All TRAFs are not created equal: common and distinct molecular mechanisms of TRAF-mediated signal transduction. J Cell Sci 2002; 115: 679–88; PMID:11865024
   PubMed Web of Science ®Google Scholar
• Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on TLRs. Nat Immunol 2010; 11: 373–84; PMID:20404851; http://dx.doi.org/10.1038/ni.1863
   PubMed Web of Science ®Google Scholar
• Saleh M. The machinery of Nod-like receptors: refining the paths to immunity and cell death. Immunol Rev 2011; 243: 235–46; PMID:21884180; http://dx.doi.org/10.1111/j.1600-065X.2011.01045.x
   PubMed Web of Science ®Google Scholar
• Yu M, Levine SJ. TLR, RIG-I-like receptors and the NLRP3 inflammasome: key modulators of innate immune responses to double-stranded RNA viruses. Cytokine Growth Factor Rev 2011; 22: 63–72; PMID:21466970; http://dx.doi.org/10.1016/j.cytogfr.2011.02.001
   PubMed Web of Science ®Google Scholar
• Zhu S, Pan W, Shi P, Gao H, Zhao F, Song X, Liu Y, Zhao L, Li X, Shi Y, et al. Modulation of experimental autoimmune encephalomyelitis through TRAF3-mediated suppression of IL-17R signaling. J Exp Med 2010; 207: 2647–62; PMID:21078888; http://dx.doi.org/10.1084/jem.20100703
   PubMed Web of Science ®Google Scholar
• Yi Z, Lin WW, Stunz LL, Bishop GA. The adaptor TRAF3 restrains the lineage determination of thymic regulatory T cells by modulating signaling via the receptor for IL-2. Nat Immunol 2014; 15: 866–74; PMID:25029551; http://dx.doi.org/10.1038/ni.2944
   PubMed Web of Science ®Google Scholar
• Bishop GA, Xie P. Multiple roles of TRAF3 signaling in lymphocyte function. Immunol Res 2007; 39: 22–32; PMID:17917053; http://dx.doi.org/10.1007/s12026-007-0068-1
   PubMed Web of Science ®Google Scholar
• Bishop GA. The multifaceted roles of TRAFs in the regulation of B-cell function. Nat Rev Immunol 2004; 4: 775–86; PMID:15459669; http://dx.doi.org/10.1038/nri1462
   PubMed Web of Science ®Google Scholar
• Bishop GA. The many faces of TRAF molecules in immune regulation. J Immunol 2013; 191: 3483–5; PMID:24058190; http://dx.doi.org/10.4049/jimmunol.1390048
   PubMed Web of Science ®Google Scholar
• He JQ, Oganesyan G, Saha SK, Zarnegar B, Cheng G. TRAF3 and its biological function. Adv Exp Med Biol 2007; 597: 48–59; PMID:17633016; http://dx.doi.org/10.1007/978-0-387-70630-6_4
   PubMed Web of Science ®Google Scholar
• Ni CZ, Welsh K, Leo E, Chiou CK, Wu H, Reed JC, Ely KR. Molecular basis for CD40 signaling mediated by TRAF3. Proc Natl Acad Sci U S A 2000; 97: 10395–9; PMID:10984535; http://dx.doi.org/10.1073/pnas.97.19.10395
   PubMed Web of Science ®Google Scholar
• Ni CZ, Welsh K, Zheng J, Havert M, Reed JC, Ely KR. Crystallization and preliminary X-ray analysis of the TRAF domain of TRAF3. Acta Crystallogr D Biol Crystallogr 2002; 58: 1340–2; PMID:12136149; http://dx.doi.org/10.1107/S0907444902008958
   PubMedGoogle Scholar
• Ely KR, Kodandapani R, Wu S. Protein-protein interactions in TRAF3. Adv Exp Med Biol 2007; 597: 114–21; PMID:17633021; http://dx.doi.org/10.1007/978-0-387-70630-6_9
   PubMed Web of Science ®Google Scholar
• Li C, Norris PS, Ni CZ, Havert ML, Chiong EM, Tran BR, Cabezas E, Reed JC, Satterthwait AC, Ware CF, et al. Structurally distinct recognition motifs in lymphotoxin-b receptor and CD40 for TRAF-mediated signaling. J Biol Chem 2003; 278: 50523–9; PMID:14517219; http://dx.doi.org/10.1074/jbc.M309381200
   PubMed Web of Science ®Google Scholar
• Ni CZ, Oganesyan G, Welsh K, Zhu X, Reed JC, Satterthwait AC, Cheng G, Ely KR. Key molecular contacts promote recognition of the BAFF receptor by TRAF3: Implications for intracellular signaling regulation. J Immunol 2004; 173: 7394–400; PMID:15585864; http://dx.doi.org/10.4049/jimmunol.173.12.7394
   PubMed Web of Science ®Google Scholar
• Li C, Ni CZ, Havert ML, Cabezas E, He J, Kaiser D, Reed JC, Satterthwait AC, Cheng G, Ely KR. Downstream regulator TANK binds to the CD40 recognition site on TRAF3. Structure 2002; 10: 403–11; PMID:12005438; http://dx.doi.org/10.1016/S0969-2126(02)00733-5
   PubMed Web of Science ®Google Scholar
• Wu S, Xie P, Welsh K, Li C, Ni CZ, Zhu X, Reed JC, Satterthwait AC, Bishop GA, Ely KR. LMP1 protein from the Epstein Barr virus is a structural CD40 decoy in B lymphocytes for binding to TRAF3. J Biol Chem 2005; 280: 33620–6; PMID:16009714; http://dx.doi.org/10.1074/jbc.M502511200
   PubMed Web of Science ®Google Scholar
• Kayagaki N, Phung Q, Chan S, Chaudhari R, Quan C, O'Rourke KM, Eby M, Pietras E, Cheng G, Bazan JF, et al. DUBA: a deubiquitinase that regulates type I interferon production. Science 2007; 318: 1628–32; PMID:17991829; http://dx.doi.org/10.1126/science.1145918
   PubMed Web of Science ®Google Scholar
• Lin WW, Hildebrand JM, Bishop GA. A Complex relationship between TRAF3 and non-canonical NF-κB2 activation in B Lymphocytes. Front Immunol 2013; 4: 477; PMID:24391649; http://dx.doi.org/10.3389/fimmu.2013.00477
   PubMed Web of Science ®Google Scholar
• Kawamata S, Hori T, Imura A, Takaori-Kondo A, Uchiyama T. Activation of OX40 signal transduction pathways leads to TRAF2- and TRAF5-mediated NF-kB activation. J Biol Chem 1998; 273: 5808–14; PMID:9488716; http://dx.doi.org/10.1074/jbc.273.10.5808
   PubMed Web of Science ®Google Scholar
• Kwon B, Yu KY, Ni J, Yu GL, Jang IK, Kim YJ, Xing L, Liu D, Wang SX, Kwon BS. Identification of a novel activation-inducible protein of the TNFR superfamily and its ligands. J Biol Chem 1999; 274: 6056–61; PMID:10037686; http://dx.doi.org/10.1074/jbc.274.10.6056
   PubMed Web of Science ®Google Scholar
• Rothe M, Sarma V, Dixit VM, Goeddel DV. TRAF2-mediated activation of NF-kB by TNFR2 and CD40. Science 1995; 269: 1424–7; PMID:7544915; http://dx.doi.org/10.1126/science.7544915
   PubMed Web of Science ®Google Scholar
• Ishida T, Mizushima Si, Azuma S, Kobayashi N, Tojo T, Suzuki K, Aizawa S, Watanabe T, Mosialos G, Kieff E, et al. Identification of TRAF6, a novel TRAF protein that mediates signaling from an amino-terminal domain of the CD40 cytoplasmic region. J Biol Chem 1996; 271: 28745–8; PMID:8910514; http://dx.doi.org/10.1074/jbc.271.46.28745
   PubMed Web of Science ®Google Scholar
• Xu Y, Cheng G, Baltimore D. Targeted disruption of TRAF3 leads to postnatal lethality and defective T-dependent immune responses. Immunity 1996; 5: 407–15; PMID:8934568; http://dx.doi.org/10.1016/S1074-7613(00)80497-5
   PubMed Web of Science ®Google Scholar
• Xie P, Hostager BS, Bishop GA. Requirement for TRAF3 in signaling by LMP1 but not CD40 in B lymphocytes. J Exp Med 2004; 199: 661–71; PMID:14981114; http://dx.doi.org/10.1084/jem.20031255
   PubMed Web of Science ®Google Scholar
• Hostager BS, Bishop GA. Cutting edge: contrasting roles of TRAF2 and TRAF3 in CD40-mediated B lymphocyte activation. J Immunol 1999; 162: 6307–11; PMID:10352240
   PubMed Web of Science ®Google Scholar
• Haxhinasto SA, Bishop GA. A novel interaction between protein kinase D and TRAF molecules regulates B cell receptor-CD40 synergy. J Immunol 2003; 171: 4655–62; PMID:14568940; http://dx.doi.org/10.4049/jimmunol.171.9.4655
   PubMed Web of Science ®Google Scholar
• Xie P, Stunz LL, Larison KD, Yang B, Bishop GA. TRAF3 is a critical regulator of B cell homeostasis in secondary lymphoid organs. Immunity 2007; 27: 253–67; PMID:17723217; http://dx.doi.org/10.1016/j.immuni.2007.07.012
   PubMed Web of Science ®Google Scholar
• Gardam S, Sierro F, Basten A, Mackay F, Brink R. TRAF2 and TRAF3 signal adapters act cooperatively to control the maturation and survival signals delivered to B cells by the BAFF receptor. Immunity 2008; 28: 391–401; PMID:18313334; http://dx.doi.org/10.1016/j.immuni.2008.01.009
   PubMed Web of Science ®Google Scholar
• Xie P, Poovassery J, Stunz LL, Smith SM, Schultz ML, Carlin LE, Bishop GA. Enhanced TLR responses of TRAF3-deficient B lymphocytes. J Leukoc Biol 2011; 90: 1149–57; PMID:21971520; http://dx.doi.org/10.1189/jlb.0111044
   PubMed Web of Science ®Google Scholar
• Xie P, Kraus ZJ, Stunz LL, Liu Y, Bishop GA. TRAF3 is required for T cell-mediated immunity and TCR/CD28 signaling. J Immunol 2011; 186: 143–55; PMID:21084666; http://dx.doi.org/10.4049/jimmunol.1000290
   PubMed Web of Science ®Google Scholar
• Lalani AI, Moore CR, Luo C, Kreider BZ, Liu Y, Morse HC 3rd, Xie P. Myeloid cell TRAF3 regulates immune responses and inhibits inflammation and tumor development in mice. J Immunol 2015; 194: 334–48; PMID:25422508; http://dx.doi.org/10.4049/jimmunol.1401548
   PubMed Web of Science ®Google Scholar
• Yi Z, Lin WW, Stunz LL, Bishop GA. Roles for TRAF3 in lymphocyte functions. Cytokine Growth Factor Rev 2014; 25: 147–56; PMID:24433987; http://dx.doi.org/10.1016/j.cytogfr.2013.12.002
   PubMed Web of Science ®Google Scholar
• He JQ, Zarnegar B, Oganesyan G, Saha SK, Yamazaki S, Doyle SE, Dempsey PW, Cheng G. Rescue of TRAF3-null mice by p100 NF-kB deficiency. J Exp Med 2006; 203: 2413–8; PMID:17015635; http://dx.doi.org/10.1084/jem.20061166
   PubMed Web of Science ®Google Scholar
• Yi Z, Stunz LL, Lin WW, Bishop GA. TRAF3 regulates homeostasis of CD8+ central memory T cells. PLoS One 2014; 9: e102120
   PubMed Web of Science ®Google Scholar
• Yi Z, Stunz LL, Bishop GA. TRAF3 plays a key role in development and function of iNKT cells. J Exp Med 2013; 210: 1079–86; PMID:23650438; http://dx.doi.org/10.1084/jem.20122135
   PubMed Web of Science ®Google Scholar
• Das R, Sant'Angelo DB, Nichols KE. Transcriptional control of iNKT cell development. Immunol Rev 2010; 238: 195–215; PMID:20969594; http://dx.doi.org/10.1111/j.1600-065X.2010.00962.x
   PubMed Web of Science ®Google Scholar
• Godfrey DI, Berzins SP. Control points in NKT-cell development. Nat Rev Immunol 2007; 7: 505–18; PMID:17589542; http://dx.doi.org/10.1038/nri2116
   PubMed Web of Science ®Google Scholar
• D'Cruz LM, Yang CY, Goldrath AW. Transcriptional regulation of NKT cell development and homeostasis. Curr Opin Immunol 2010; 22: 199–205; http://dx.doi.org/10.1016/j.coi.2010.01.014
   PubMed Web of Science ®Google Scholar
• Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, Biron CA, Gapin L, Glimcher LH. T-bet regulates the terminal maturation and homeostasis of NK and Va14 iNKT cells. Immunity 2004; 20: 477–94; PMID:15084276; http://dx.doi.org/10.1016/S1074-7613(04)00076-7
   PubMed Web of Science ®Google Scholar
• Chang JH, Hu H, Jin J, Puebla-Osorio N, Xiao Y, Gilbert BE, Brink R, Ullrich SE, Sun SC. TRAF3 regulates the effector function of regulatory T cells and humoral immune responses. J Exp Med 2014; 211: 137–51; PMID:24378539; http://dx.doi.org/10.1084/jem.20131019
   PubMed Web of Science ®Google Scholar
• Yu A, Zhu L, Altman NH, Malek TR. A low IL-2R signaling threshold supports the development and homeostasis of T regulatory cells. Immunity 2009; 30: 204–17; PMID:19185518; http://dx.doi.org/10.1016/j.immuni.2008.11.014
   PubMed Web of Science ®Google Scholar
• Mahmud SA, Manlove LS, Schmitz HM, Xing Y, Wang Y, Owen DL, Schenkel JM, Boomer JS, Green JM, Yagita H, et al. Costimulation via the TNFR superfamily couples TCR signal strength to the thymic differentiation of regulatory T cells. Nat Immunol 2014; 15: 473–81; PMID:24633226; http://dx.doi.org/10.1038/ni.2849
   PubMed Web of Science ®Google Scholar
• Rowe AM, Murray SE, Raué HP, Koguchi Y, Slifka MK, Parker DC. A cell-intrinsic requirement for NF-κB-inducing kinase in CD4 and CD8 T cell memory. J Immunol 2013; 191: 3663–72; PMID:24006459; http://dx.doi.org/10.4049/jimmunol.1301328
   PubMed Web of Science ®Google Scholar
• Sun L, Deng L, Ea CK, Xia ZP, Chen ZJ. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol cell 2004; 14: 289–301; PMID:15125833; http://dx.doi.org/10.1016/S1097-2765(04)00236-9
   PubMed Web of Science ®Google Scholar
• Xie JJ, Liang JQ, Diao LH, Altman A, Li Y. TRAF6 regulates TCR signaling via interaction with and modification of the LAT adapter. J Immunol 2013; 190: 4027–36; PMID:23514740; http://dx.doi.org/10.4049/jimmunol.1202742
   PubMed Web of Science ®Google Scholar
• Johnston JA, Bacon CM, Riedy MC, O'Shea JJ. Signaling by IL-2 and related cytokines: JAKs, STATs, and relationship to immunodeficiency. J Leukoc Biol 1996; 60: 441–52; PMID:8864127
   PubMed Web of Science ®Google Scholar
• Minami Y, Taniguchi T. IL-2 signaling: recruitment and activation of multiple protein tyrosine kinases by the components of the IL-2 receptor. Curr Opin Cell Biol 1995; 7: 156–62; PMID:7612266; http://dx.doi.org/10.1016/0955-0674(95)80023-9
   PubMed Web of Science ®Google Scholar
• Burns LA, Karnitz LM, Sutor SL, Abraham RT. IL-2-induced tyrosine phosphorylation of p52shc in T lymphocytes. J Biol Chem 1993; 268: 17659–61; PMID:7688728
   PubMed Web of Science ®Google Scholar
• Zhou YJ, Magnuson KS, Cheng TP, Gadina M, Frucht DM, Galon J, Candotti F, Geahlen RL, Changelian PS, O'Shea JJ. Hierarchy of protein tyrosine kinases in IL-2 signaling: activation of Syk depends on Jak3; however, neither Syk nor Lck is required for IL-2-mediated STAT activation. Mol Cell Biol 2000; 20: 4371–80; PMID:10825200; http://dx.doi.org/10.1128/MCB.20.12.4371-4380.2000
   PubMed Web of Science ®Google Scholar
• Sporri B, Kovanen PE, Sasaki A, Yoshimura A, Leonard WJ. JAB/SOCS1/SSI-1 is an IL-2-induced inhibitor of IL-2 signaling. Blood 2001; 97: 221–6; PMID:11133764; http://dx.doi.org/10.1182/blood.V97.1.221
   PubMed Web of Science ®Google Scholar
• Yu CR, Mahdi RM, Ebong S, Vistica BP, Gery I, Egwuagu CE. SOCS3 regulates proliferation and activation of T-helper cells. J Biol Chem 2003; 278: 29752–9; PMID:12783879; http://dx.doi.org/10.1074/jbc.M300489200
   PubMed Web of Science ®Google Scholar
• Migone TS, Cacalano NA, Taylor N, Yi T, Waldmann TA, Johnston JA. Recruitment of SH2-containing protein tyrosine phosphatase SHP-1 to the IL-2R; loss of SHP-1 expression in human T-lymphotropic virus type I-transformed T cells. Proc Natl Acad Sci U S A 1998; 95: 3845–50; PMID:9520455; http://dx.doi.org/10.1073/pnas.95.7.3845
   PubMed Web of Science ®Google Scholar
• Simoncic PD, Lee-Loy A, Barber DL, Tremblay ML, McGlade CJ. The TCPTP is a negative regulator of Jaks 1 and 3. Curr Biol 2002; 12: 446–53; PMID:11909529; http://dx.doi.org/10.1016/S0960-9822(02)00697-8
   PubMed Web of Science ®Google Scholar
• Ibarra-Sánchez MJ, Simoncic PD, Nestel FR, Duplay P, Lapp WS, Tremblay ML. The TCPTP. Semin Immunol 2000; 12: 379–86; http://dx.doi.org/10.1006/smim.2000.0220
   PubMed Web of Science ®Google Scholar
• Wiede F, Shields BJ, Chew SH, Kyparissoudis K, van Vliet C, Galic S, Tremblay ML, Russell SM, Godfrey DI, Tiganis T. TCPTP attenuates T cell signaling to maintain tolerance in mice. J Clin Invest 2011; 121: 4758–74; PMID:22080863; http://dx.doi.org/10.1172/JCI59492
   PubMed Web of Science ®Google Scholar
• Motegi H, Shimo Y, Akiyama T, Inoue J. TRAF6 negatively regulates the Jak1-Erk pathway in IL-2 signaling. Genes Cells 2011; 16: 179–89; PMID:21155952; http://dx.doi.org/10.1111/j.1365-2443.2010.01474.x
   PubMed Web of Science ®Google Scholar
• Walsh PT, Buckler JL, Zhang J, Gelman AE, Dalton NM, Taylor DK, Bensinger SJ, Hancock WW, Turka LA. PTEN inhibits IL-2 receptor-mediated expansion of CD4+CD25+ Tregs. J Clin Invest 2006; 116: 2521–31; PMID:16917540
   PubMed Web of Science ®Google Scholar
• Zheng Y, Josefowicz SZ, Kas A, Chu TT, Gavin MA, Rudensky AY. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 2007; 445: 936–40; PMID:17237761; http://dx.doi.org/10.1038/nature05563
   PubMed Web of Science ®Google Scholar
• Wortzman ME, Clouthier DL, McPherson AJ, Lin GH, Watts TH. The contextual role of TNFR family members in CD8+ T-cell control of viral infections. Immunol Rev 2013; 255: 125–48; PMID:23947352; http://dx.doi.org/10.1111/imr.12086
   PubMed Web of Science ®Google Scholar
• Marsters SA, Ayres TM, Skubatch M, Gray CL, Rothe M, Ashkenazi A. HVEM, a member of the TNFR family, interacts with members of the TRAF family and activates the transcription factors NF-kB and AP-1. J Biol Chem 1997; 272: 14029–32; PMID:9162022; http://dx.doi.org/10.1074/jbc.272.22.14029
   PubMed Web of Science ®Google Scholar
• Munroe ME. Functional roles for T cell CD40 in infection and autoimmune disease: the role of CD40 in lymphocyte homeostasis. Semin Immunol 2009; 21: 283–8; PMID:19539498; http://dx.doi.org/10.1016/j.smim.2009.05.008
   PubMed Web of Science ®Google Scholar
• Munroe ME, Bishop GA. A costimulatory function for T cell CD40. J Immunol 2007; 178: 671–82; PMID:17202327; http://dx.doi.org/10.4049/jimmunol.178.2.671
   PubMed Web of Science ®Google Scholar
• Hauer J, Püschner S, Ramakrishnan P, Simon U, Bongers M, Federle C, Engelmann H. TRAF3 serves as an inhibitor of TRAF2/5-mediated activation of the noncanonical NF-kB pathway by TRAF-binding TNFRs. Proc Natl Acad Sci U S A 2005; 102: 2874–9; PMID:15708970; http://dx.doi.org/10.1073/pnas.0500187102
   PubMed Web of Science ®Google Scholar
• Jang IK, Lee ZH, Kim YJ, Kim SH, Kwon BS. Human 4-1BB (CD137) signals are mediated by TRAF2 and activate NF-kB. Biochem Biophys Res Commun 1998; 242: 613–20; PMID:9464265; http://dx.doi.org/10.1006/bbrc.1997.8016
   PubMed Web of Science ®Google Scholar
• Saoulli K, Lee SY, Cannons JL, Yeh WC, Santana A, Goldstein MD, Bangia N, DeBenedette MA, Mak TW, Choi Y, et al. CD28-independent, TRAF2-dependent costimulation of resting T cells by 4-1BB ligand. J Exp Med 1998; 187: 1849–62; PMID:9607925; http://dx.doi.org/10.1084/jem.187.11.1849
   PubMed Web of Science ®Google Scholar
• Yi Z, Stunz LL, Bishop GA. CD40-mediated maintenance of immune homeostasis in the adipose tissue microenvironment. Diabetes 2014; 63: 2751–60; PMID:24647739; http://dx.doi.org/10.2337/db13-1657
   PubMed Web of Science ®Google Scholar
• Weih DS, Yilmaz ZB, Weih F. Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J Immunol 2001; 167: 1909–19; PMID:11489970; http://dx.doi.org/10.4049/jimmunol.167.4.1909
   PubMed Web of Science ®Google Scholar
• Franzoso G, Carlson L, Poljak L, Shores EW, Epstein S, Leonardi A, Grinberg A, Tran T, Scharton-Kersten T, Anver M, et al. Mice deficient in NF-kB/p52 present with defects in humoral responses, germinal center reactions, and splenic microarchitecture. J Exp Med 1998; 187: 147–59; PMID:9432973; http://dx.doi.org/10.1084/jem.187.2.147
   PubMed Web of Science ®Google Scholar
• Jin W, Zhou XF, Yu J, Cheng X, Sun SC. Regulation of Th17 cell differentiation and EAE induction by the MAP3K NIK. Blood 2009; 113: 6603–10; PMID:19411637; http://dx.doi.org/10.1182/blood-2008-12-192914
   PubMed Web of Science ®Google Scholar
• Hofmann J, Mair F, Greter M, Schmidt-Supprian M, Becher B. NIK signaling in dendritic cells but not in T cells is required for the development of effector T cells and cell-mediated immune responses. J Exp Med 2011; 208: 1917–29; PMID:21807870; http://dx.doi.org/10.1084/jem.20110128
   PubMed Web of Science ®Google Scholar
• Zhu M, Chin RK, Christiansen PA, Lo JC, Liu X, Ware C, Siebenlist U, Fu YX. NF-kB2 is required for the establishment of central tolerance through an Aire-dependent pathway. J Clin Invest 2006; 116: 2964–71; PMID:17039258; http://dx.doi.org/10.1172/JCI28326
   PubMed Web of Science ®Google Scholar
• Boehm T, Scheu S, Pfeffer K, Bleul CC. Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoimmunity require lympho-epithelial cross talk via LTbR. J Exp Med 2003; 198: 757–69; PMID:12953095; http://dx.doi.org/10.1084/jem.20030794
   PubMed Web of Science ®Google Scholar
• Zarnegar BJ, Wang Y, Mahoney DJ, Dempsey PW, Cheung HH, He J, Shiba T, Yang X, Yeh WC, Mak TW, et al. Noncanonical NF-kB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol 2008; 9: 1371–8; PMID:18997794; http://dx.doi.org/10.1038/ni.1676
   PubMed Web of Science ®Google Scholar
• Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, Wang H, Vignali DA, Bergsagel PL, Karin M. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kB signaling. Nat Immunol 2008; 9: 1364–70; PMID:18997792; http://dx.doi.org/10.1038/ni.1678
   PubMed Web of Science ®Google Scholar
• Michel M, Wilhelmi I, Schultz AS, Preussner M, Heyd F. Activation-induced Traf3 alternative splicing controls the noncanonical NF-kB pathway and chemokine expression in human T cells. J Biol Chem 2014; 289: 13651–60; PMID:24671418; http://dx.doi.org/10.1074/jbc.M113.526269
   PubMed Web of Science ®Google Scholar