Interplay between BCL10, MALT1 and IκBα during T-cell-receptor-mediated NFκB activation

Journal of Cell Science

Volumn 123, Issue 14, 2010, Pages 2375-2380

  Carvalho, Gabrielle ^a,b   Le Guelte, Armelle ^c   Demian, Catherine ^a,b,d   Vazquez, Aimé ^a,b   Gavard, Julie ^c   Bidère, Nicolas ^a,b  

^a HÔPITAL PAUL BROUSSE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c INSTITUT COCHIN   (France)

^d ENCPB   (France)

Author keywords

Lymphocyte; NF B; Signalling; Ubiquitylation

Indexed keywords

HETERODIMER; I KAPPA B; I KAPPA B ALPHA; I KAPPA B KINASE; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEASOME; PROTEIN BCL 10; PROTEIN CARMA1; PROTEIN CK1ALPHA; PROTEIN MALT1; PROTEIN SERINE THREONINE KINASE; SMALL INTERFERING RNA; SYNAPTOTAGMIN I; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; MICROENVIRONMENT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARD SIGNALING ADAPTOR PROTEINS; CASEIN KINASE IALPHA; CASPASES; GUANYLATE CYCLASE; HUMANS; I-KAPPA B PROTEINS; JURKAT CELLS; MEMBRANE MICRODOMAINS; MULTIPROTEIN COMPLEXES; NEOPLASM PROTEINS; NF-KAPPA B; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RECEPTORS, ANTIGEN, T-CELL; RNA, SMALL INTERFERING; T-LYMPHOCYTES; TRANSCRIPTIONAL ACTIVATION; UBIQUITINATION;

EID: 77954925971     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.069476     Document Type: Article

References (36)

1. Bidere, N., Snow, A. L., Sakai, K., Zheng, L. and Lenardo, M. J. (2006). Caspase-8 regulation by direct interaction with TRAF6 in T cell receptor-induced NF-kappaB activation. Curr. Biol. 16, 1666-1671.
2. Bidere, N., Ngo, V. N., Lee, J., Collins, C., Zheng, L., Wan, F., Davis, R. E., Lenz, G., Anderson, D. E., Arnoult, D. et al. (2009). Casein kinase 1alpha governs antigen-receptor- induced NF-kappaB activation and human lymphoma cell survival. Nature 458, 92-96.
3. Blonska, M., Pappu, B. P., Matsumoto, R., Li, H., Su, B., Wang, D. and Lin, X. (2007). The CARMA1-Bcl10 signaling complex selectively regulates JNK2 kinase in the T cell receptor-signaling pathway. Immunity 26, 55-66.
4. Che, T., You, Y., Wang, D., Tanner, M. J., Dixit, V. M. and Lin, X. (2004). MALT1/paracaspase is a signaling component downstream of CARMA1 and mediates T cell receptor-induced NF-kappaB activation. J. Biol. Chem. 279, 15870-15876.
5. Chen, C. L., Singh, N., Yull, F. E., Strayhorn, D., Van Kaer, L. and Kerr, L. D. (2000). Lymphocytes lacking I kappa B-alpha develop normally, but have selective defects in proliferation and function. J. Immunol. 165, 5418-5427.
6. Compagno, M., Lim, W. K., Grunn, A., Nandula, S. V., Brahmachary, M., Shen, Q., Bertoni, F., Ponzoni, M., Scandurra, M., Califano, A. et al. (2009). Mutations of multiple genes cause deregulation of NF-kappaB in diffuse large B-cell lymphoma. Nature 459, 717-721.
7. Duwel, M., Welteke, V., Oeckinghaus, A., Baens, M., Kloo, B., Ferch, U., Darnay, B. G., Ruland, J., Marynen, P. and Krappmann, D. (2009). A20 negatively regulates T cell receptor signaling to NF-kappaB by cleaving Malt1 ubiquitin chains. J. Immunol. 182, 7718-7728.
8. Egawa, T., Albrecht, B., Favier, B., Sunshine, M. J., Mirchandani, K., O'Brien, W., Thome, M. and Littman, D. R. (2003). Requirement for CARMA1 in antigen receptor-induced NF-kappa B activation and lymphocyte proliferation. Curr. Biol. 13, 1252-1258.
9. Ferch, U., Kloo, B., Gewies, A., Pfander, V., Duwel, M., Peschel, C., Krappmann, D. and Ruland, J. (2009). Inhibition of MALT1 protease activity is selectively toxic for activated B cell-like diffuse large B cell lymphoma cells. J. Exp. Med. 206, 2313-2320.
10. Gaide, O., Favier, B., Legler, D. F., Bonnet, D., Brissoni, B., Valitutti, S., Bron, C., Tschopp, J. and Thome, M. (2002). CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-kappa B activation. Nat. Immunol. 3, 836-843.
11. Ghosh, S. and Hayden, M. S. (2008). New regulators of NF-kappaB in inflammation. Nat. Rev Immunol. 8, 837-848.
12. Hailfinger, S., Lenz, G., Ngo, V., Posvitz-Fejfar, A., Rebeaud, F., Guzzardi, M., Penas, E. M., Dierlamm, J., Chan, W. C., Staudt, L. M. et al. (2009). Essential role of MALT1 protease activity in activated B cell-like diffuse large B-cell lymphoma. Proc. Natl. Acad. Sci. USA 106, 19946-19951.
13. Lenz, G., Davis, R. E., Ngo, V. N., Lam, L., George, T. C., Wright, G. W., Dave, S. S., Zhao, H., Xu, W., Rosenwald, A. et al. (2008). Oncogenic CARD11 mutations in human diffuse large B cell lymphoma. Science 319, 1676-1679.
14. Lobry, C., Lopez, T., Israel, A. and Weil, R. (2007). Negative feedback loop in T cell activation through IkappaB kinase-induced phosphorylation and degradation of Bcl10. Proc. Natl. Acad. Sci. USA 104, 908-913.
15. Matsumoto, R., Wang, D., Blonska, M., Li, H., Kobayashi, M., Pappu, B., Chen, Y., Wang, D. and Lin, X. (2005). Phosphorylation of CARMA1 plays a critical role in T Cell receptor-mediated NF-kappaB activation. Immunity 23, 575-585.
16. Matsuzawa, A., Tseng, P. H., Vallabhapurapu, S., Luo, J. L., Zhang, W., Wang, H., Vignali, D. A., Gallagher, E. and Karin, M. (2008). Essential cytoplasmic translocation of a cytokine receptor-assembled signaling complex. Science 321, 663-668.
17. Moreno-Garcia, M. E., Sommer, K., Haftmann, C., Sontheimer, C., Andrews, S. F. and Rawlings, D. J. (2009). Serine 649 phosphorylation within the protein kinase C-regulated domain down-regulates CARMA1 activity in lymphocytes. J. Immunol. 183, 7362-7370.
18. Ngo, V. N., Davis, R. E., Lamy, L., Yu, X., Zhao, H., Lenz, G., Lam, L. T., Dave, S., Yang, L., Powell, J. et al. (2006). A loss-of-function RNA interference screen for molecular targets in cancer. Nature 441, 106-110.
19. Oeckinghaus, A., Wegener, E., Welteke, V., Ferch, U., Arslan, S. C., Ruland, J., Scheidereit, C. and Krappmann, D. (2007). Malt1 ubiquitination triggers NF-kappaB signaling upon T-cell activation. EMBO J. 26, 4634-4645. (Pubitemid 350126802)
20. Rawlings, D. J., Sommer, K. and Moreno-Garcia, M. E. (2006). The CARMA1 signalosome links the signalling machinery of adaptive and innate immunity in lymphocytes. Nat. Rev. Immunol. 6, 799-812. (Pubitemid 44631649)
21. Rebeaud, F., Hailfinger, S., Posevitz-Fejfar, A., Tapernoux, M., Moser, R., Rueda, D., Gaide, O., Guzzardi, M., Iancu, E. M., Rufer, N. et al. (2008). The proteolytic activity of the paracaspase MALT1 is key in T cell activation. Nat. Immunol. 9, 272-281.
22. Rossman, J. S., Stoicheva, N. G., Langel, F. D., Patterson, G. H., Lippincott-Schwartz, J. and Schaefer, B. C. (2006). POLKADOTS are foci of functional interactions in T-Cell receptor-mediated signaling to NF-kappaB. Mol. Biol. Cell 17, 2166-2176. (Pubitemid 44011733)
23. Ruland, J., Duncan, G. S., Elia, A., del Barco Barrantes, I., Nguyen, L., Plyte, S., Millar, D. G., Bouchard, D., Wakeham, A., Ohashi, P. S. et al. (2001). Bcl10 is a positive regulator of antigen receptor-induced activation of NF-kappaB and neural tube closure. Cell 104, 33-42.
24. Ruland, J., Duncan, G. S., Wakeham, A. and Mak, T. W. (2003). Differential requirement for Malt1 in T and B cell antigen receptor signaling. Immunity 19, 749-758. (Pubitemid 37490799)
25. Scharschmidt, E., Wegener, E., Heissmeyer, V., Rao, A. and Krappmann, D. (2004). Degradation of Bcl10 induced by T-cell activation negatively regulates NF-kappa B signaling. Mol. Cell. Biol. 24, 3860-3873. (Pubitemid 38496164)
26. Sebald, A., Mattioli, I. and Schmitz, M. L. (2005). T cell receptor-induced lipid raft recruitment of the I kappa B kinase complex is necessary and sufficient for NF-kappa B activation occurring in the cytosol. Eur J. Immunol. 35, 318-325. (Pubitemid 40123878)
27. Sommer, K., Guo, B., Pomerantz, J. L., Bandaranayake, A. D., Moreno-Garcia, M. E., Ovechkina, Y. L. and Rawlings, D. J. (2005). Phosphorylation of the CARMA1 linker controls NF-kappaB activation. Immunity 23, 561-574. (Pubitemid 41779479)
28. Sun, L., Deng, L., Ea, C. K., Xia, Z. P. and Chen, Z. J. (2004). The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell 14, 289-301. (Pubitemid 38591401)
29. Tergaonkar, V., Correa, R. G., Ikawa, M. and Verma, I. M. (2005). Distinct roles of IkappaB proteins in regulating constitutive NF-kappaB activity. Nat. Cell Biol. 7, 921-923. (Pubitemid 41486295)
30. Wan, F. and Lenardo, M. J. (2010). The nuclear signaling of NF-kappaB: current knowledge, new insights, and future perspectives. Cell Res. 20, 24-33.
31. Wang, D., You, Y., Case, S. M., McAllister-Lucas, L. M., Wang, L., DiStefano, P. S., Nunez, G., Bertin, J. and Lin, X. (2002). A requirement for CARMA1 in TCR-induced NF-kappa B activation. Nat. Immunol. 3, 830-835.
32. Wang, D., Matsumoto, R., You, Y., Che, T., Lin, X. Y., Gaffen, S. L. and Lin, X. (2004). CD3/CD28 costimulation-induced NF-kappaB activation is mediated by recruitment of protein kinase C-theta, Bcl10, and IkappaB kinase beta to the immunological synapse through CARMA1. Mol. Cell. Biol. 24, 164-171. (Pubitemid 38010044)
33. Wegener, E., Oeckinghaus, A., Papadopoulou, N., Lavitas, L., Schmidt-Supprian, M., Ferch, U., Mak, T. W., Ruland, J., Heissmeyer, V. and Krappmann, D. (2006). Essential role for IkappaB kinase beta in remodeling Carma1-Bcl10-Malt1 complexes upon T cell activation. Mol. Cell 23, 13-23. (Pubitemid 43963448)
34. Welteke, V., Eitelhuber, A., Duwel, M., Schweitzer, K., Naumann, M. and Krappmann, D. (2009). COP9 signalosome controls the Carma1-Bcl10-Malt1 complex upon T-cell stimulation. EMBO Rep. 10, 642-648.
35. Wu, C. J. and Ashwell, J. D. (2008). NEMO recognition of ubiquitinated Bcl10 is required for T cell receptor-mediated NF-kappaB activation. Proc. Natl. Acad. Sci. USA 105, 3023-3028.
36. Zeng, H., Di, L., Fu, G., Chen, Y., Gao, X., Xu, L., Lin, X. and Wen, R. (2007). Phosphorylation of Bcl10 negatively regulates T-cell receptor-mediated NF-kappaB activation. Mol. Cell. Biol. 27, 5235-5245.