Malt1 ubiquitination triggers NF-κB signaling upon T-cell activation

EMBO Journal

Volumn 26, Issue 22, 2007, Pages 4634-4645

  Oeckinghaus, Andrea ^a,b,c   Wegener, Elmar ^a   Welteke, Verena ^a   Ferch, Uta ^d   Arslan, Seda Çöl ^b   Ruland, Jürgen ^d   Scheidereit, Claus ^b   Krappmann, Daniel ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Malt1; NF B; Regulatory ubiquitination; T cell signaling

Indexed keywords

DOCKING PROTEIN; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; MUCOSA ASSOCIATED LYMPHOID TISSUE 1 PROTEIN; MUTANT PROTEIN; PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; ENZYME ACTIVATION; ENZYME MECHANISM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS REGULATORY PROTEINS; CARD SIGNALING ADAPTOR PROTEINS; CASPASES; CELL LINE; GUANYLATE CYCLASE; HUMANS; I-KAPPA B KINASE; INTERLEUKIN-2; JURKAT CELLS; NEOPLASM PROTEINS; NF-KAPPA B; T-LYMPHOCYTES; TNF RECEPTOR-ASSOCIATED FACTOR 6; UBIQUITINATION;

EID: 36249008032     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601897     Document Type: Article

References (48)

1. Akagi T, Motegi M, Tamura A, Suzuki R, Hosokawa Y, Suzuki H, Ota H, Nakamura S, Morishima Y, Taniwaki M, Seto M (1999) A novel gene, MALT1 at 18q21, is involved in t(11;18) (q21;q21) found in low-grade B-cell lymphoma of mucosa-associated lymphoid tissue. Oncogene 18: 5785-5794
2. Bi K, Tanaka Y, Coudronniere N, Sugie K, Hong S, van Stipdonk MJ, Altman A (2001) Antigen-induced translocation of PKC-theta to membrane rafts is required for T cell activation. Nat Immunol 2: 556-563
3. Bidere N, Snow AL, Sakai K, Zheng L, Lenardo MJ (2006) Caspase-8 regulation by direct interaction with TRAF6 in T cell receptor-induced NF-kappaB activation. Curr Biol 16: 1666-1671
4. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ (2006) Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 22: 245-257
5. Egawa T, Albrecht B, Favier B, Sunshine MJ, Mirchandani K, O'Brien W, Thome M, Littman DR (2003) Requirement for CARMA1 in antigen receptor-induced NF-kappa B activation and lymphocyte proliferation. Curr Biol 13: 1252-1258
6. Gaide O, Favier B, Legler DF, Bonnet D, Brissoni B, Valitutti S, Bron C, Tschopp J, Thome M (2002) CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-kappa B activation. Nat Immunol 3: 836-843
7. Ghosh S, May MJ, Kopp EB (1998) NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16: 225-260
8. Grabiner BC, Blonska M, Lin PC, You Y, Wang D, Sun J, Darnay BG, Dong C, Lin X (2007) CARMA3 deficiency abrogates G protein-coupled receptor-induced NF-{kappa}B activation. Genes Dev 21: 984-996
9. Gross O, Gewies A, Finger K, Schafer M, Sparwasser T, Peschel C, Forster I, Ruland J (2006) Card9 controls a non-TLR signalling pathway for innate antifungal immunity. Nature 442: 651-656
10. Hara H, Wada T, Bakal C, Kozieradzki I, Suzuki S, Suzuki N, Nghiem M, Griffiths EK, Krawczyk C, Bauer B, D'Acquisto F, Ghosh S, Yeh WC, Baier G, Rottapel R, Penninger JM (2003) The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18: 763-775
11. Hayden MS, Ghosh S (2004) Signaling to NF-kappaB. Genes Dev 18: 2195-2224
12. Jun JE, Wilson LE, Vinuesa CG, Lesage S, Blery M, Miosge LA, Cook MC, Kucharska EM, Hara H, Penninger JM, Domashenz H, Hong NA, Glynne RJ, Nelms KA, Goodnow CC (2003) Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity 18: 751-762
13. Kanayama A, Seth RB, Sun L, Ea CK, Hong M, Shaito A, Chiu YH, Deng L, Chen ZJ (2004) TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol Cell 15: 535-548
14. King CG, Kobayashi T, Cejas PJ, Kim T, Yoon K, Kim GK, Chiffoleau E, Hickman SP, Walsh PT, Turka LA, Choi Y (2006) TRAF6 is a T cell-intrinsic negative regulator required for the maintenance of immune homeostasis. Nat Med 12: 1088-1092
15. Klemm S, Zimmermann S, Peschel C, Mak TW, Ruland J (2007) Bcl10 and Malt1 control lysophosphatidic acid-induced NF-kappaB activation and cytokine production. Proc Natl Acad Sci USA 104: 134-138
16. Lee KY, D'Acquisto F, Hayden MS, Shim JH, Ghosh S (2005) PDK1 nucleates T cell receptor-induced signaling complex for NF-kappaB activation. Science 308: 114-118
17. Li H, Kobayashi M, Blonska M, You Y, Lin X (2006) Ubiquitination of RIP is required for tumor necrosis factor alpha-induced NF-kappaB activation. J Biol Chem 281: 13636-13643
18. Matsumoto R, Wang D, Blonska M, Li H, Kobayashi M, Pappu B, Chen Y, Wang D, Lin X (2005) Phosphorylation of CARMA1 plays a critical role in T cell receptor-mediated NF-kappaB activation. Immunity 23: 575-585
19. McAllister-Lucas LM, Inohara N, Lucas PC, Ruland J, Benito A, Li Q, Chen S, Chen FF, Yamaoka S, Verma IM, Mak TW, Nunez G (2001) Bimp1, a MAGUK family member linking protein kinase C activation to Bcl10-mediated NF-kappaB induction. J Biol Chem 276: 30589-30597
20. McAllister-Lucas LM, Ruland J, Siu K, Jin X, Gu S, Kim DS, Kuffa P, Kohrt D, Mak TW, Nunez G, Lucas PC (2007) CARMA3/Bcl10/ MALT1-dependent NF-kappaB activation mediates angiotensin II-responsive inflammatory signaling in nonimmune cells. Proc Natl Acad Sci USA 104: 139-144
21. Monks CR, Kupfer H, Tamir I, Barlow A, Kupfer A (1997) Selective modulation of protein kinase C-theta during T-cell activation. Nature 385: 83-86
22. Morgan JA, Yin Y, Borowsky AD, Kuo F, Nourmand N, Koontz JI, Reynolds C, Soreng L, Griffin CA, Graeme-Cook F, Harris NL, Weisenburger D, Pinkus GS, Fletcher JA, Sklar J (1999) Breakpoints of the t(11;18)(q21;q21) in mucosa-associated lymphoid tissue (MALT) lymphoma lie within or near the previously undescribed gene MALT1 in chromosome 18. Cancer Res 59: 6205-6213
23. Ngo VN, Davis RE, Lamy L, Yu X, Zhao H, Lenz G, Lam LT, Dave S, Yang L, Powell J, Staudt LM (2006) A loss-of-function RNA interference screen for molecular targets in cancer. Nature 441: 106-110
24. Okamura H, Rao A (2001) Transcriptional regulation in lymphocytes. Curr Opin Cell Biol 13: 239-243
25. Passmore LA, Barford D (2004) Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem J 379 (Part 3): 513-525
26. Rawlings DJ, Sommer K, Moreno-Garcia ME (2006) The CARMA1 signalosome links the signalling machinery of adaptive and innate immunity in lymphocytes. Nat Rev Immunol 6: 799-812
27. Ruefli-Brasse AA, French DM, Dixit VM (2003) Regulation of NF-kappaB-dependent lymphocyte activation and development by paracaspase. Science 302: 1581-1584
28. Ruland J, Duncan GS, Elia A, del Barco Barrantes I, Nguyen L, Plyte S, Millar DG, Bouchard D, Wakeham A, Ohashi PS, Mak TW (2001) Bcl10 is a positive regulator of antigen receptor-induced activation of NF-kappaB and neural tube closure. Cell 104: 33-42
29. Ruland J, Duncan GS, Wakeham A, Mak TW (2003) Differential requirement for Malt1 in T and B cell antigen receptor signaling. Immunity 19: 749-758
30. Scharschmidt E, Wegener E, Heissmeyer V, Rao A, Krappmann D (2004) Degradation of Bcl10 induced by T-cell activation negatively regulates NF-kappa B signaling. Mol Cell Biol 24: 3860-3873
31. Schulze-Luehrmann J, Ghosh S (2006) Antigen-receptor signaling to nuclear factor kappa B. Immunity 25: 701-715
32. Shambharkar PB, Blonska M, Pappu BP, Li H, You Y, Sakurai H, Darnay BG, Hara H, Penninger J, Lin X (2007) Phosphorylation and ubiquitination of the IkappaB kinase complex by two distinct signaling pathways. EMBO J 26: 1794-1805
33. Sommer K, Guo B, Pomerantz JL, Bandaranayake AD, Moreno-García ME, Ovechkina YL, Rawlings DJ (2005) Phosphorylation of the CARMA1 linker controls NF-kappaB activation. Immunity 23: 561-574
34. Su H, Bidere N, Zheng L, Cubre A, Sakai K, Dale J, Salmena L, Hakem R, Straus S, Lenardo M (2005) Requirement for caspase-8 in NF-kappaB activation by antigen receptor. Science 307: 1465-1468
35. Sun L, Deng L, Ea CK, Xia ZP, Chen ZJ (2004) The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol Cell 14: 289-301
36. Sun Z, Arendt CW, Ellmeier W, Schaeffer EM, Sunshine MJ, Gandhi L, Annes J, Petrzilka D, Kupfer A, Schwartzberg PL, Littman DR (2000) PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes. Nature 404: 402-407
37. van der Merwe PA (2002) Formation and function of the immunological synapse. Curr Opin Immunol 14: 293-298
38. Wan YY, Chi H, Xie M, Schneider MD, Flavell RA (2006) The kinase TAK1 integrates antigen and cytokine receptor signaling for Tcell development, survival and function. Nat Immunol 7: 851-858
39. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412: 346-351
40. Wang D, You Y, Lin PC, Xue L, Morris SW, Zeng H, Wen R, Lin X (2007) Bcl10 plays a critical role in NF-kappaB activation induced by G protein-coupled receptors. Proc Natl Acad Sci USA 104: 145-150
41. Wegener E, Oeckinghaus A, Papadopoulou N, Lavitas L, Schmidt-Supprian M, Ferch U, Mak TW, Ruland J, Heissmeyer V, Krappmann D (2006) Essential role for IkappaB kinase beta in remodeling Carma1-Bcl10-Malt1 complexes upon T cell activation. Mol Cell 23: 13-23
42. Weil R, Israel A (2006) Deciphering the pathway from the TCR to NF-kappaB. Cell Death Differ 13: 826-833
43. Willis TG, Jadayel DM, Du MQ, Peng H, Perry AR, Abdul-Rauf M, Price H, Karran L, Majekodunmi O, Wlodarska I, Pan L, Crook T, Hamoudi R, Isaacson PG, Dyer MJ (1999) Bcl10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumor types. Cell 96: 35-45
44. Wu CJ, Conze DB, Li T, Srinivasula SM, Ashwell JD (2006) Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat Cell Biol 8: 398-406
45. Yamamoto M, Okamoto T, Takeda K, Sato S, Sanjo H, Uematsu S, Saitoh T, Yamamoto N, Sakurai H, Ishii KJ, Yamaoka S, Kawai T, Matsuura Y, Takeuchi O, Akira S (2006) Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat Immunol 7: 962-970
46. Zhang Q, Siebert R, Yan M, Hinzmann B, Cui X, Xue L, Rakestraw KM, Naeve CW, Beckmann G, Weisenburger DD, Sanger WG, Nowotny H, Vesely M, Callet-Bauchu E, Salles G, Dixit VM, Rosenthal A, Schlegelberger B, Morris SW (1999) Inactivating mutations and overexpression of BCL10, a caspase recruitment domain-containing gene, in MALT lymphoma with t(1;14) (p22;q32). Nat Genet 22: 63-68
47. Zhou H, Du MQ, Dixit VM (2005) Constitutive NF-kappaB activation by the t(11;18)(q21;q21) product in MALT lymphoma is linked to deregulated ubiquitin ligase activity. Cancer Cell 7: 425-431
48. Zhou H, Wertz I, O'Rourke K, Ultsch M, Seshagiri S, Eby M, Xiao W, Dixit VM (2004) Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature 427: 167-171