Molecular determinants of scaffold-induced linear ubiquitinylation of B cell lymphoma/leukemia 10 (Bcl10) during T cell receptor and oncogenic caspase recruitment domain-containing protein 11 (CARD11) signaling

Journal of Biological Chemistry

Volumn 291, Issue 50, 2016, Pages 25921-25936

  Yang, Yong Kang ^a   Yang, Chao ^a   Chan, Waipan ^a,b   Wang, Zhaoquan ^a   Deibel, Katelynn E ^a   Pomerantz, Joel L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; CELLS; CHAINS; CHEMICAL ACTIVATION; CYTOLOGY; ELECTRIC REACTORS; ENZYMES; ONCOLOGY; PROTEINS; SCAFFOLDS (BIOLOGY); SIGNALING; T-CELLS;

ADAPTIVE IMMUNE RESPONSE; CHAIN ASSEMBLIES; COILED-COIL DOMAINS; DIFFUSE LARGE B-CELL LYMPHOMA; DOMAIN-CONTAINING PROTEINS; INHIBITORY DOMAINS; MOLECULAR DETERMINANTS; MULTICOMPONENT COMPLEXES;

CELL SIGNALING;

CASPASE RECRUITMENT DOMAIN CONTAINING PROTEIN 11; HOIP PROTEIN; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIN(UB)N BCL10 PROTEIN; LINEAR UBIQUITIN CHAIN ASSEMBLY COMPLEX; LYSINE; MALT1 PROTEIN; PROTEIN BCL 10; SCAFFOLD PROTEIN; SHARPIN PROTEIN; T LYMPHOCYTE RECEPTOR; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; BCL10 PROTEIN, HUMAN; CARD11 PROTEIN, HUMAN; CASPASE; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; GUANYLATE CYCLASE; LYMPHOCYTE ANTIGEN RECEPTOR; MALT1 PROTEIN, HUMAN; RNF31 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONJUGATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LARGE CELL LYMPHOMA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UBIQUITINATION; GENETICS; HEK293 CELL LINE; JURKAT CELL LINE; METABOLISM; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARD SIGNALING ADAPTOR PROTEINS; CASPASES; GUANYLATE CYCLASE; HEK293 CELLS; HUMANS; JURKAT CELLS; NEOPLASM PROTEINS; NF-KAPPA B; PROTEIN DOMAINS; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 85002858480     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.754028     Document Type: Article

References (58)

1. Schulze-Luehrmann, J., and Ghosh, S. (2006) Antigen-receptor signaling to nuclear factor κB. Immunity 25, 701-715
2. Vallabhapurapu, S., and Karin, M. (2009) Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733
3. Turvey, S. E., Durandy, A., Fischer, A., Fung, S. Y., Geha, R. S., Gewies, A., Giese, T., Greil, J., Keller, B., McKinnon, M. L., Neven, B., Rozmus, J., Ruland, J., Snow, A. L., Stepensky, P., and Warnatz, K. (2014) The CARD11-BCL10-MALT1 (CBM) signalosome complex: stepping into the limelight of human primary immunodeficiency. J. Allergy Clin. Immunol. 134, 276-284
4. Pérez de Diego, R., Sánchez-Ramón, S., López-Collazo, E., Martínez-Barricarte, R., Cubillos-Zapata, C., Ferreira Cerdán, A., Casanova, J. L., and Puel, A. (2015) Genetic errors of the human caspase recruitment domain-B-cell lymphoma 10-mucosa-associated lymphoid tissue lymphoma-translocation gene 1 (CBM) complex: molecular, immunologic, and clinical heterogeneity. J. Allergy Clin. Immunol. 136, 1139-1149
5. 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-κB activation. Nat. Immunol. 3, 836-843
6. Wang, D., You, Y., Case, S. M., McAllister-Lucas, L. M., Wang, L., DiStefano, P. S., Nuñez, G., Bertin, J., and Lin, X. (2002) A requirement for CARMA1 in TCR-induced NF-κB activation. Nat. Immunol. 3, 830-835
7. Pomerantz, J. L., Denny, E. M., and Baltimore, D. (2002) CARD11 mediates factor-specific activation of NF-κB by the T cell receptor complex. EMBO J. 21, 5184-5194
8. Hara, H., Wada, T., Bakal, C., Kozieradzki, I., Suzuki, S., Suzuki, N., Nghiem, M., Griffiths, E. K., Krawczyk, C., Bauer, B., D'Acquisto, F., Ghosh, S., Yeh, W. C., Baier, G., Rottapel, R., and Penninger, J. M. (2003) The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18, 763-775
9. Jun, J. E., Wilson, L. E., Vinuesa, C. G., Lesage, S., Blery, M., Miosge, L. A., Cook, M. C., Kucharska, E. M., Hara, H., Penninger, J. M., Domashenz, H., Hong, N. A., Glynne, R. J., Nelms, K. A., and Goodnow, C. C. (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
10. 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-κB activation and lymphocyte proliferation. Curr. Biol. 13, 1252-1258
11. Newton, K., and Dixit, V. M. (2003) Mice lacking the CARD of CARMA1 exhibit defective B lymphocyte development and impaired proliferation of their B and T lymphocytes. Curr. Biol. 13, 1247-1251
12. Stepensky, P., Keller, B., Buchta, M., Kienzler, A. K., Elpeleg, O., Somech, R., Cohen, S., Shachar, I., Miosge, L. A., Schlesier, M., Fuchs, I., Enders, A., Eibel, H., Grimbacher, B., and Warnatz, K. (2013) Deficiency of caspase recruitment domain family, member 11 (CARD11), causes profound combined immunodeficiency in human subjects. J. Allergy Clin. Immunol. 131, 477-485
13. Greil, J., Rausch, T., Giese, T., Bandapalli, O. R., Daniel, V., Bekeredjian-Ding, I., Stütz, A. M., Drees, C., Roth, S., Ruland, J., Korbel, J. O., and Kulozik, A. E. (2013) Whole-exome sequencing links caspase recruitment domain 11 (CARD11) inactivation to severe combined immunodeficiency. J. Allergy Clin. Immunol. 131, 1376-1383
14. Hayden, M. S., and Ghosh, S. (2012) NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 26, 203-234
15. McCully, R. R., and Pomerantz, J. L. (2008) The protein kinase C-responsive inhibitory domain of CARD11 functions in NF-κB activation to regulate the association of multiple signaling cofactors that differentially depend on Bcl10 and MALT1 for association. Mol. Cell. Biol. 28, 5668-5686
16. Jattani, R. P., Tritapoe, J. M., and Pomerantz, J. L. (2016) Cooperative control of caspase recruitment domain-containing protein 11 (CARD11) signaling by an unusual array of redundant repressive elements. J. Biol. Chem. 291, 8324-8336
17. Jattani, R. P., Tritapoe, J. M., and Pomerantz, J. L. (2016) Intramolecular interactions and regulation of cofactor binding by the four repressive elements in the caspase recruitment domain-containing protein 11 (CARD11) inhibitory domain. J. Biol. Chem. 291, 8338-8348
18. Sommer, K., Guo, B., Pomerantz, J. L., Bandaranayake, A. D., Moreno-García, M. E., Ovechkina, Y. L., and Rawlings, D. J. (2005) Phosphorylation of the CARMA1 linker controls NF-κB activation. Immunity 23, 561-574
19. 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-κB activation. Immunity 23, 575-585
20. Bidère, N., Ngo, V. N., Lee, J., Collins, C., Zheng, L., Wan, F., Davis, R. E., Lenz, G., Anderson, D. E., Arnoult, D., Vazquez, A., Sakai, K., Zhang, J., Meng, Z., Veenstra, T. D., Staudt, L. M., and Lenardo, M. J. (2009) Casein kinase 1α governs antigen-receptor-induced NF-κB activation and human lymphoma cell survival. Nature 458, 92-96
21. Lim, K. H., Yang, Y., and Staudt, L. M. (2012) Pathogenetic importance and therapeutic implications of NF-κB in lymphoid malignancies. Immunol. Rev. 246, 359-378
22. Davis, R. E., Brown, K. D., Siebenlist, U., and Staudt, L. M. (2001) Constitutive nuclear factor κB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J. Exp. Med. 194, 1861-1874
23. Ngo, V. N., Davis, R. E., Lamy, L., Yu, X., Zhao, H., Lenz, G., Lam, L. T., Dave, S., Yang, L., Powell, J., and Staudt, L. M. (2006) A loss-of-function RNA interference screen for molecular targets in cancer. Nature 441, 106-110
24. 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., Ott, G., Muller-Hermelink, H. K., Gascoyne, R. D., Connors, J. M., Rimsza, L. M., et al. (2008) Oncogenic CARD11 mutations in human diffuse large B cell lymphoma. Science 319, 1676-1679
25. Compagno, M., Lim, W. K., Grunn, A., Nandula, S. V., Brahmachary, M., Shen, Q., Bertoni, F., Ponzoni, M., Scandurra, M., Califano, A., Bhagat, G., Chadburn, A., Dalla-Favera, R., and Pasqualucci, L. (2009) Mutations of multiple genes cause deregulation of NF-κB in diffuse large B-cell lymphoma. Nature 459, 717-721
26. Lohr, J. G., Stojanov, P., Lawrence, M. S., Auclair, D., Chapuy, B., Sougnez, C., Cruz-Gordillo, P., Knoechel, B., Asmann, Y. W., Slager, S. L., Novak, A. J., Dogan, A., Ansell, S. M., Link, B. K., Zou, L., et al. (2012) Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing. Proc. Natl. Acad. Sci. U.S.A. 109, 3879-3884
27. Montesinos-Rongen, M., Schmitz, R., Brunn, A., Gesk, S., Richter, J., Hong, K., Wiestler, O. D., Siebert, R., Küppers, R., and Deckert, M. (2010) Mutations of CARD11 but not TNFAIP3 may activate the NF-κB pathway in primary CNS lymphoma. Acta Neuropathol. 120, 529-535
28. Bu, R., Bavi, P., Abubaker, J., Jehan, Z., Al-Haqawi, W., Ajarim, D., Al-Dayel, F., Uddin, S., and Al-Kuraya, K. S. (2012) Role of NF-κB regulators-TNFAIP3 and CARD11 in Middle Eastern diffuse large B cell lymphoma. Leuk. Lymphoma. 53, 1971-1977
29. Dong, G., Chanudet, E., Zeng, N., Appert, A., Chen, Y. W., Au, W. Y., Hamoudi, R. A., Watkins, A. J., Ye, H., Liu, H., Gao, Z., Chuang, S. S., Srivastava, G., and Du, M. Q. (2011) A20, ABIN-1/2, and CARD11 mutations and their prognostic value in gastrointestinal diffuse large B-cell lymphoma. Clin. Cancer Res. 17, 1440-1451
30. Lamason, R. L., McCully, R. R., Lew, S. M., and Pomerantz, J. L. (2010) Oncogenic CARD11 mutations induce hyperactive signaling by disrupting autoinhibition by the PKC-responsive inhibitory domain. Biochemistry 49, 8240-8250
31. Chan, W., Schaffer, T. B., and Pomerantz, J. L. (2013) A quantitative signaling screen identifies CARD11 mutations in the CARD and LATCH domains that induce Bcl10 ubiquitination and human lymphoma cell survival. Mol. Cell. Biol. 33, 429-443
32. Iwai, K., Fujita, H., and Sasaki, Y. (2014) Linear ubiquitin chains: NF-κB signalling, cell death and beyond. Nat. Rev. Mol. Cell Biol. 15, 503-508
33. Ikeda, F., Deribe, Y. L., Skånland, S. S., Stieglitz, B., Grabbe, C., Franz-Wachtel, M., van Wijk, S. J., Goswami, P., Nagy, V., Terzic, J., Tokunaga, F., Androulidaki, A., Nakagawa, T., Pasparakis, M., Iwai, K., et al. (2011) SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature 471, 637-641
34. Tokunaga, F., Nakagawa, T., Nakahara, M., Saeki, Y., Taniguchi, M., Sakata, S., Tanaka, K., Nakano, H., and Iwai, K. (2011) SHARPIN is a component of the NF-κB-activating linear ubiquitin chain assembly complex. Nature 471, 633-636
35. Gerlach, B., Cordier, S. M., Schmukle, A. C., Emmerich, C. H., Rieser, E., Haas, T. L., Webb, A. I., Rickard, J. A., Anderton, H., Wong, W. W., Nachbur, U., Gangoda, L., Warnken, U., Purcell, A. W., Silke, J., and Walczak, H. (2011) Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471, 591-596
36. Hadian, K., Griesbach, R. A., Dornauer, S., Wanger, T. M., Nagel, D., Metlitzky, M., Beisker, W., Schmidt-Supprian, M., and Krappmann, D. (2011) NF-κB essential modulator (NEMO) interaction with linear and lys-63 ubiquitin chains contributes to NF-κB activation. J. Biol. Chem. 286, 26107-26117
37. Emmerich, C. H., Ordureau, A., Strickson, S., Arthur, J. S., Pedrioli, P. G., Komander, D., and Cohen, P. (2013) Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc. Natl. Acad. Sci. U.S.A. 110, 15247-15252
38. Yang, Y., Schmitz, R., Mitala, J., Whiting, A., Xiao, W., Ceribelli, M., Wright, G. W., Zhao, H., Yang, Y., Xu, W., Rosenwald, A., Ott, G., Gascoyne, R. D., Connors, J. M., Rimsza, L. M., et al. (2014) Essential role of the linear ubiquitin chain assembly complex in lymphoma revealed by rare germline polymorphisms. Cancer Discov. 4, 480-493
39. Dubois, S. M., Alexia, C., Wu, Y., Leclair, H. M., Leveau, C., Schol, E., Fest, T., Tarte, K., Chen, Z. J., Gavard, J., and Bidère, N. (2014) A catalytic-independent role for the LUBAC in NF-κB activation upon antigen receptor engagement and in lymphoma cells. Blood 123, 2199-2203
40. Sasaki, Y., Sano, S., Nakahara, M., Murata, S., Kometani, K., Aiba, Y., Sakamoto, S., Watanabe, Y., Tanaka, K., Kurosaki, T., and Iwai, K. (2013) Defective immune responses in mice lacking LUBAC-mediated linear ubiquitination in B cells. EMBO J. 32, 2463-2476
41. Satpathy, S., Wagner, S. A., Beli, P., Gupta, R., Kristiansen, T. A., Malinova, D., Francavilla, C., Tolar, P., Bishop, G. A., Hostager, B. S., and Choudhary, C. (2015) Systems-wide analysis of BCR signalosomes and downstream phosphorylation and ubiquitylation. Mol. Syst. Biol. 11, 810
42. Yang, Y., Kelly, P., Shaffer, A. L., 3rd, Schmitz, R., Yoo, H. M., Liu, X., Huang da, W., Webster, D., Young, R. M., Nakagawa, M., Ceribelli, M., Wright, G. W., Yang, Y., Zhao, H., Yu, X., et al. (2016) Targeting non-proteolytic protein ubiquitination for the treatment of diffuse large B cell lymphoma. Cancer Cell 29, 494-507
43. Keusekotten, K., Elliott, P. R., Glockner, L., Fiil, B. K., Damgaard, R. B., Kulathu, Y., Wauer, T., Hospenthal, M. K., Gyrd-Hansen, M., Krappmann, D., Hofmann, K., and Komander, D. (2013) OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 153, 1312-1326
44. Rivkin, E., Almeida, S. M., Ceccarelli, D. F., Juang, Y. C., MacLean, T. A., Srikumar, T., Huang, H., Dunham, W. H., Fukumura, R., Xie, G., Gondo, Y., Raught, B., Gingras, A. C., Sicheri, F., and Cordes, S. P. (2013) The linear ubiquitin-specific deubiquitinase gumby regulates angiogenesis. Nature 498, 318-324
45. Komander, D., Reyes-Turcu, F., Licchesi, J. D., Odenwaelder, P., Wilkinson, K. D., and Barford, D. (2009) Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 10, 466-473
46. Wu, C. J., and Ashwell, J. D. (2008) NEMO recognition of ubiquitinated Bcl10 is required for T cell receptor-mediated NF-κB activation. Proc. Natl. Acad. Sci. U.S.A. 105, 3023-3028
47. Jiang, C., and Lin, X. (2012) Regulation of NF-κB by the CARD proteins. Immunol. Rev. 246, 141-153
48. Kirisako, T., Kamei, K., Murata, S., Kato, M., Fukumoto, H., Kanie, M., Sano, S., Tokunaga, F., Tanaka, K., and Iwai, K. (2006) A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25, 4877-4887
49. Tokunaga, F., Sakata, S., Saeki, Y., Satomi, Y., Kirisako, T., Kamei, K., Nakagawa, T., Kato, M., Murata, S., Yamaoka, S., Yamamoto, M., Akira, S., Takao, T., Tanaka, K., and Iwai, K. (2009) Involvement of linear polyubiquitylation of NEMO in NF-κB activation. Nat. Cell Biol. 11, 123-132
50. Paul, S., Kashyap, A. K., Jia, W., He, Y. W., and Schaefer, B. C. (2012) Selective autophagy of the adaptor protein Bcl10 modulates T cell receptor activation of NF-κB. Immunity 36, 947-958
51. Alexia, C., Poalas, K., Carvalho, G., Zemirli, N., Dwyer, J., Dubois, S. M., Hatchi, E. M., Cordeiro, N., Smith, S. S., Castanier, C., Le Guelte, A., Wan, L., Kang, Y., Vazquez, A., Gavard, J., Arnoult, D., and Bidère, N. (2013) The endoplasmic reticulum acts as a platform for ubiquitylated components of nuclear factor κB signaling. Sci. Signal. 6, ra79
52. Smit, J. J., Monteferrario, D., Noordermeer, S. M., van Dijk, W. J., van der Reijden, B. A., and Sixma, T. K. (2012) The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J. 31, 3833-3844
53. Stieglitz, B., Morris-Davies, A. C., Koliopoulos, M. G., Christodoulou, E., and Rittinger, K. (2012) LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep. 13, 840-846
54. Yagi, H., Ishimoto, K., Hiromoto, T., Fujita, H., Mizushima, T., Uekusa, Y., Yagi-Utsumi, M., Kurimoto, E., Noda, M., Uchiyama, S., Tokunaga, F., Iwai, K., and Kato, K. (2012) A non-canonical UBA-UBL interaction forms the linear-ubiquitin-chain assembly complex. EMBO Rep. 13, 462-468
55. Klein, T., Fung, S. Y., Renner, F., Blank, M. A., Dufour, A., Kang, S., Bolger-Munro, M., Scurll, J. M., Priatel, J. J., Schweigler, P., Melkko, S., Gold, M. R., Viner, R. I., Régnier, C. H., Turvey, S. E., and Overall, C. M. (2015) The paracaspase MALT1 cleaves HOIL1 reducing linear ubiquitination by LUBAC to dampen lymphocyte NF-κB signalling. Nat. Commun. 6, 8777
56. Elton, L., Carpentier, I., Staal, J., Driege, Y., Haegman, M., and Beyaert, R. (2016) MALT1 cleaves the E3 ubiquitin ligase HOIL-1 in activated T cells, generating a dominant negative inhibitor of LUBAC-induced NF-κB signaling. FEBS J. 283, 403-412
57. Lamason, R. L., Kupfer, A., and Pomerantz, J. L. (2010) The dynamic distribution of CARD11 at the immunological synapse is regulated by the inhibitor kinesin GAKIN. Mol. Cell 40, 798-809
58. Pedersen, S. M., Chan, W., Jattani, R. P., Mackie, dS., and Pomerantz, J. L. (2015) Negative regulation of CARD11 signaling and lymphoma cell survival by the E3 ubiquitin ligase RNF181. Mol. Cell. Biol. 36, 794-808