Critical protein-protein interactions within the CARMA1-BCL10-MALT1 complex: Take-home points for the cell biologist

Egawa, 2003, Requirement for CARMA1 in antigen receptor-induced NF-kappa B activation and lymphocyte proliferation, Curr. Biol., 13, 1252, 10.1016/S0960-9822(03)00491-3 Hara, 2003, The MAGUK family protein CARD11 is essential for lymphocyte activation, Immunity, 18, 763, 10.1016/S1074-7613(03)00148-1 Jun, 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, 10.1016/S1074-7613(03)00141-9 McAllister-Lucas, 2001, Bimp1, a MAGUK family member linking protein kinase C activation to Bcl10-mediated NF-kappaB induction, J. Biol. Chem., 276, 30589, 10.1074/jbc.M103824200 Xue, 2003, Defective development and function of Bcl10-deficient follicular, marginal zone and B1 B cells, Nat. Immunol., 4, 857, 10.1038/ni963 Ruefli-Brasse, 2003, Regulation of NF-kappaB-dependent lymphocyte activation and development by paracaspase, Science, 302, 1581, 10.1126/science.1090769 Ruland, 2001, Bcl10 is a positive regulator of antigen receptor-induced activation of NF-kappaB and neural tube closure, Cell, 104, 33, 10.1016/S0092-8674(01)00189-1 Lenz, 2008, Oncogenic CARD11 mutations in human diffuse large B cell lymphoma, Science, 319, 1676, 10.1126/science.1153629 Zhang, 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, 10.1038/8767 Sanchez-Izquierdo, 2003, MALT1 is deregulated by both chromosomal translocation and amplification in B-cell non-Hodgkin lymphoma, Blood, 101, 4539, 10.1182/blood-2002-10-3236 Zucca, 2016, The spectrum of MALT lymphoma at different sites: biological and therapeutic relevance, Blood, 127, 2082, 10.1182/blood-2015-12-624304 Kataoka, 2015, Integrated molecular analysis of adult T cell leukemia/lymphoma, Nat. Genet., 47, 1304, 10.1038/ng.3415 Wang, 2015, Genomic profiling of Sezary syndrome identifies alterations of key T cell signaling and differentiation genes, Nat. Genet., 47, 1426, 10.1038/ng.3444 da Silva Almeida, 2015, The mutational landscape of cutaneous T cell lymphoma and Sezary syndrome, Nat. Genet., 47, 1465, 10.1038/ng.3442 Matsumoto, 2005, Phosphorylation of CARMA1 plays a critical role in T Cell receptor-mediated NF-kappaB activation, Immunity, 23, 575, 10.1016/j.immuni.2005.10.007 Shinohara, 2005, PKC beta regulates BCR-mediated IKK activation by facilitating the interaction between TAK1 and CARMA1, J. Exp. Med., 202, 1423, 10.1084/jem.20051591 Sommer, 2005, Phosphorylation of the CARMA1 linker controls NF-kappaB activation, Immunity, 23, 561, 10.1016/j.immuni.2005.09.014 Sun, 2004, The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes, Mol. Cell, 14, 289, 10.1016/S1097-2765(04)00236-9 Hailfinger, 2009, Essential role of MALT1 protease activity in activated B cell-like diffuse large B-cell lymphoma, PNAS, 106, 19946, 10.1073/pnas.0907511106 Rebeaud, 2008, The proteolytic activity of the paracaspase MALT1 is key in T cell activation, Nat. Immunol., 9, 272, 10.1038/ni1568 Thome, 2008, Multifunctional roles for MALT1 in T-cell activation, Nat. Rev. Immunol., 8, 495, 10.1038/nri2338 Chan, 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, 10.1128/MCB.00850-12 Rawlings, 2006, The CARMA1 signalosome links the signalling machinery of adaptive and innate immunity in lymphocytes, Nat. Rev. Immunol., 6, 799, 10.1038/nri1944 Jattani, 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, 10.1074/jbc.M115.683714 Jattani, 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, 10.1074/jbc.M116.717322 Holliday, 2019, Structures of autoinhibited and polymerized forms of CARD9 reveal mechanisms of CARD9 and CARD11 activation, Nat. Commun., 10, 3070, 10.1038/s41467-019-10953-z Gaide, 2002, CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-kappa B activation, Nat. Immunol., 3, 836, 10.1038/ni830 Bedsaul, 2018, Mechanisms of regulated and dysregulated CARD11 signaling in adaptive immunity and disease, Front. Immunol., 9, 2105, 10.3389/fimmu.2018.02105 Desjardins, 2018, A unique heterozygous CARD11 mutation combines pathogenic features of both gain- and loss-of-function patients in a four-generation family, Front. Immunol., 9, 2944, 10.3389/fimmu.2018.02944 Brohl, 2015, Germline CARD11 Mutation in a Patient with Severe Congenital B Cell Lymphocytosis, J. Clin. Immunol., 35, 32, 10.1007/s10875-014-0106-4 Gaide, 2001, Carma1, a CARD-containing binding partner of Bcl10, induces Bcl10 phosphorylation and NF-kappaB activation, FEBS Lett., 496, 121, 10.1016/S0014-5793(01)02414-0 Bertin, 2001, CARD11 and CARD14 are novel caspase recruitment domain (CARD)/membrane-associated guanylate kinase (MAGUK) family members that interact with BCL10 and activate NF-kappa B, J. Biol. Chem., 276, 11877, 10.1074/jbc.M010512200 Li, 2012, Structural insights into the assembly of CARMA1 and BCL10, PLoS ONE, 7 Qiao, 2013, Structural architecture of the CARMA1/Bcl10/MALT1 signalosome: nucleation-induced filamentous assembly, Mol. Cell, 51, 766, 10.1016/j.molcel.2013.08.032 Jang, 2013, Novel disulfide bond-mediated dimerization of the CARD domain was revealed by the crystal structure of CARMA1 CARD, PLoS ONE, 8, 10.1371/journal.pone.0079778 Tanner, 2007, CARMA1 coiled-coil domain is involved in the oligomerization and subcellular localization of CARMA1 and is required for T cell receptor-induced NF-kappaB activation, J. Biol. Chem., 282, 17141, 10.1074/jbc.M700169200 Che, 2004, MALT1/paracaspase is a signaling component downstream of CARMA1 and mediates T cell receptor-induced NF-kappaB activation, J. Biol. Chem., 279, 15870, 10.1074/jbc.M310599200 Schulze-Luehrmann, 2006, Antigen-receptor signaling to nuclear factor kappa B, Immunity, 25, 701, 10.1016/j.immuni.2006.10.010 Hara, 2015, Clustering of CARMA1 through SH3-GUK domain interactions is required for its activation of NF-kappaB signalling, Nat. Commun., 6, 5555, 10.1038/ncomms6555 Yan, 1999, mE10, a novel caspase recruitment domain-containing proapoptotic molecule, J. Biol. Chem., 274, 10287, 10.1074/jbc.274.15.10287 Guiet, 2000, Caspase recruitment domain (CARD)-dependent cytoplasmic filaments mediate bcl10-induced NF-kappaB activation, J. Cell Biol., 148, 1131, 10.1083/jcb.148.6.1131 Koseki, 1999, CIPER, a novel NF kappaB-activating protein containing a caspase recruitment domain with homology to Herpesvirus-2 protein E10, J. Biol. Chem., 274, 9955, 10.1074/jbc.274.15.9955 Rossman, 2006, POLKADOTS are foci of functional interactions in T-Cell receptor-mediated signaling to NF-kappaB, Mol. Biol. Cell, 17, 2166, 10.1091/mbc.e05-10-0985 David, 2018, Assembly mechanism of the CARMA1-BCL10-MALT1-TRAF6 signalosome, PNAS, 115, 1499, 10.1073/pnas.1721967115 Schlauderer, 2018, Molecular architecture and regulation of BCL10-MALT1 filaments, Nat. Commun., 9, 4041, 10.1038/s41467-018-06573-8 Park, 2013, Self-oligomerization of the CARD domain prevents complex formation in the CARMA1 signalosome, Int. J. Mol. Med., 31, 1280, 10.3892/ijmm.2013.1307 Seeholzer, 2018, BCL10-CARD11 fusion mimics an active CARD11 seed that triggers constitutive BCL10 oligomerization and lymphocyte activation, Front. Immunol., 9, 2695, 10.3389/fimmu.2018.02695 Uren, 2000, Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma, Mol. Cell, 6, 961 Lucas, 2001, Bcl10 and MALT1, independent targets of chromosomal translocation in malt lymphoma, cooperate in a novel NF-kappa B signaling pathway, J. Biol. Chem., 276, 19012, 10.1074/jbc.M009984200 Langel, 2008, Multiple protein domains mediate interaction between Bcl10 and MALT1, J. Biol. Chem., 283, 32419, 10.1074/jbc.M800670200 Wegener, 2006, Essential role for IkappaB kinase beta in remodeling Carma1-Bcl10-Malt1 complexes upon T cell activation, Mol. Cell, 23, 13, 10.1016/j.molcel.2006.05.027 Wiesmann, 2012, Structural determinants of MALT1 protease activity, J. Mol. Biol., 419, 4, 10.1016/j.jmb.2012.02.018 Cabalzar, 2013, Monoubiquitination and activity of the paracaspase MALT1 requires glutamate 549 in the dimerization interface, PLoS ONE, 8, 10.1371/journal.pone.0072051 Hailfinger, 2011, Malt1-dependent RelB cleavage promotes canonical NF-kappaB activation in lymphocytes and lymphoma cell lines, PNAS, 108, 14596, 10.1073/pnas.1105020108 Coornaert, 2008, T cell antigen receptor stimulation induces MALT1 paracaspase-mediated cleavage of the NF-kappaB inhibitor A20, Nat. Immunol., 9, 263, 10.1038/ni1561 McAllister-Lucas, 2011, MALT1 protease: a new therapeutic target in B lymphoma and beyond?, Cancer Res., 17, 6623 Yu, 2011, Crystal structure of the mucosa-associated lymphoid tissue lymphoma translocation 1 (MALT1) paracaspase region, PNAS, 108, 21004, 10.1073/pnas.1111708108 Lork, 2019, Ubiquitination and phosphorylation of the CARD11-BCL10-MALT1 signalosome in T cells, Cell. Immunol., 340, 10.1016/j.cellimm.2018.11.001 Schairer, 2020, Allosteric activation of MALT1 by its ubiquitin-binding Ig3 domain, PNAS, 117, 3093, 10.1073/pnas.1912681117 Pelzer, 2013, The protease activity of the paracaspase MALT1 is controlled by monoubiquitination, Nat. Immunol., 14, 337, 10.1038/ni.2540 Ferch, 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, 10.1084/jem.20091167 Fontan, 2012, MALT1 small molecule inhibitors specifically suppress ABC-DLBCL in vitro and in vivo, Cancer Cell, 22, 812, 10.1016/j.ccr.2012.11.003 Bardet, 2018, The T-cell fingerprint of MALT1 paracaspase revealed by selective inhibition, Immunol. Cell Biol., 96, 81, 10.1111/imcb.1018 Fontan, 2018, Specific covalent inhibition of MALT1 paracaspase suppresses B cell lymphoma growth, J. Clin. Investig., 128, 4397, 10.1172/JCI99436 Nagel, 2012, Pharmacologic inhibition of MALT1 protease by phenothiazines as a therapeutic approach for the treatment of aggressive ABC-DLBCL, Cancer Cell, 22, 825, 10.1016/j.ccr.2012.11.002 Quancard, 2019, An allosteric MALT1 inhibitor is a molecular corrector rescuing function in an immunodeficient patient, Nat. Chem. Biol., 15, 304, 10.1038/s41589-018-0222-1 Schlauderer, 2013, Structural analysis of phenothiazine derivatives as allosteric inhibitors of the MALT1 paracaspase, Angew. Chem., 52, 10384, 10.1002/anie.201304290 Meloni, 2018, Mepazine inhibits RANK-induced osteoclastogenesis independent of its MALT1 inhibitory function, Molecules, 23, 10.3390/molecules23123144 Lim, 2015, Identification of beta-lapachone analogs as novel MALT1 inhibitors to treat an aggressive subtype of diffuse large B-cell lymphoma, J. Med. Chem., 58, 8491, 10.1021/acs.jmedchem.5b01415 Konczalla, 2020, Biperiden and mepazine effectively inhibit MALT1 activity and tumor growth in pancreatic cancer, Int. J. Cancer, 146, 1618, 10.1002/ijc.32567 Noels, 2007, A Novel TRAF6 binding site in MALT1 defines distinct mechanisms of NF-kappaB activation by API2middle dotMALT1 fusions, J. Biol. Chem., 282, 10180, 10.1074/jbc.M611038200 Kingeter, 2010, Cutting edge: TCR ligation triggers digital activation of NF-kappaB, J. Immunol., 185, 4520, 10.4049/jimmunol.1001051 Bardet, 2018, MALT1 activation by TRAF6 needs neither BCL10 nor CARD11, Biochem. Biophys. Res. Commun., 506, 48, 10.1016/j.bbrc.2018.10.029 Bertin, 2000, CARD9 is a novel caspase recruitment domain-containing protein that interacts with BCL10/CLAP and activates NF-kappa B, J. Biol. Chem., 275, 41082, 10.1074/jbc.C000726200 Juilland, 2016, Role of the CARMA1/BCL10/MALT1 complex in lymphoid malignancies, Curr. Opin. Hematol., 23, 402, 10.1097/MOH.0000000000000257 Yang, 2014, The CBM signalosome: potential therapeutic target for aggressive lymphoma?, Cytokine Growth Factor Rev., 25, 175, 10.1016/j.cytogfr.2013.12.008 Laraia, 2015, Overcoming chemical biological, and computational challenges in the development of inhibitors targeting protein-protein interactions, Chem. Biol., 22, 689, 10.1016/j.chembiol.2015.04.019 Cierpicki, 2015, Targeting protein-protein interactions in hematologic malignancies: still a challenge or a great opportunity for future therapies?, Immunol. Rev., 263, 279, 10.1111/imr.12244