The three CARMA sisters: So different, so similar: A portrait of the three CARMA proteins and their involvement in human disorders

Journal of Cellular Physiology

Volumn 229, Issue 8, 2014, Pages 990-997

  Scudiero, Ivan ^a   Vito, Pasquale ^b,c   Stilo, Romania ^a,b  

^a Grande Ospedale Metropolitano   (Italy)

^b UNIVERSITY OF SANNIO   (Italy)

^c Qatar University   (Qatar)

Author keywords

[No Author keywords available]

Indexed keywords

CARMA 1 PROTEIN; CARMA 2 PROTEIN; CARMA 3 PROTEIN; GUANYLATE KINASE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ISOPROTEIN; POLYPEPTIDE; PROTEASOME; PROTEIN; PROTEIN BCL 10; PROTEIN P50; PROTEIN P52; TRANSCRIPTION FACTOR REL; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL GROWTH; CELL SURVIVAL; CYTOPLASM; ENZYME MECHANISM; GENETIC ANALYSIS; HUMAN; IMMUNE RESPONSE; INFLAMMATION; LYMPHOID TISSUE; LYMPHOPROLIFERATIVE DISEASE; MAMMAL CELL; MISSENSE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

CARD SIGNALING ADAPTOR PROTEINS; GENE EXPRESSION REGULATION; GUANYLATE CYCLASE; HUMANS; INFLAMMATION; MEMBRANE PROTEINS; NEOPLASMS;

EID: 84899088247     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24543     Document Type: Article

References (67)

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. Bertin J, Wang L, Guo Y, Jacobson MD, Poyet JL, Srinivasula SM, Merriam S, DiStefano PS, Alnemri ES. 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 276:11877-11882.
3. Bidère N, Ngo VN, Lee J, Collins C, Zheng L, Wan F, Davis RE, Lenz G, Anderson DE, Arnoult D, Vazquez A, Sakai K, Zhang J, Meng Z, Veenstra TD, Staudt LM, Lenardo MJ. 2009. Casein kinase 1alpha governs antigen-receptor-induced NF-kappaB activation and human lymphoma cell survival. Nature 458:92-96.
4. Blonska M, Lin X. 2011. NF-κB signaling pathways regulated by CARMA family of scaffold proteins. Cell Res 21:55-70.
5. Blumer JB, Smrcka AV, Lanier SM. 2007. Mechanistic pathways and biological roles for receptor-independent activators of G-protein signaling. Pharmacol Ther 113:488-506.
6. Bohers E, Mareschal S, Bouzelfen A, Marchand V, Ruminy P, Maingonnat C, Ménard AL, Etancelin P, Bertrand P, Dubois S, Alcantara M, Bastard C, Tilly H, Jardin F. 2014. Targetable activating mutations are very frequent in GCB and ABC diffuse large B-cell lymphoma. Genes Chromosomes Cancer 53:144-153.
7. Brenner D, Brechmann M, Röhling S, Tapernoux M, Mock T, Winter D, Lehmann WD, Kiefer F, Thome M, Krammer PH, Arnold R. 2009. Phosphorylation of CARMA1 by HPK1 is critical for NF-κB activation in T cells. Proc Natl Acad Sci USA 106:14508-14513.
8. Compagno M, Lim WK, Grunn A, Nandula SV, Brahmachary M, Shen Q, Bertoni F, Ponzoni M, Scandurra M, Califano A, Bhagat G, Chadburn A, Dalla-Favera R, Pasqualucci L. 2009. Mutations of multiple genes cause deregulation of NF-kappaB in diffuse large B-cell lymphoma. Nature 459:717-721.
9. Costanzo A, Guiet C, Vito P. 1999. c-E10 is a caspase-recruiting domain-containing protein that interacts with components of death receptors signaling pathway and activates nuclear factor-kappaB. J Biol Chem 274:20127-20132.
10. Davis RE, Brown KD, Siebenlist U, Staudt LM. 2001. Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J Exp Med 194:1861-1874.
11. Dong G, Chanudet E, Zeng N, Appert A, Chen YW, Au WY, Hamoudi RA, Watkins AJ, Ye H, Liu H, Gao Z, Chuang SS, Srivastava G, Du MQ. 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.
12. Düwel M, Welteke V, Oeckinghaus A, Baens M, Kloo B, Ferch U, Darnay BG, Ruland J, Marynen P, Krappmann D. 2009. A20 negatively regulates T cell receptor signaling to NF-kappaB by cleaving Malt1 ubiquitin chains. J Immunol 182:7718-7728.
13. Eitelhuber AC, Warth S, Schimmack G, Düwel M, Hadian K, Demski K, Beisker W, Shinohara H, Kurosaki T, Heissmeyer V, Krappmann D. 2011. Dephosphorylation of Carma1 by PP2A negatively regulates T-cell activation. EMBO J 30:594-605.
14. 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.
15. Feng X, Miao G, Han Y, Xu Y. 2013. CARMA3 is overexpressed in human glioma and promotes cell invasion through MMP9 regulation in A172 cell line. Tumour Biol In press.
16. Fuchs-Telem D, Sarig O, van Steensel MA, Isakov O, Israeli S, Nousbeck J, Richard K, Winnepenninckx V, Vernooij M, Shomron N, Uitto J, Fleckman P, Richard G, Sprecher E. 2012. Familial pityriasis rubra pilaris is caused by mutations in CARD14. Am J Hum Genet 91:163-170.
17. Gaide O, Martinon F, Micheau O, Bonnet D, Thome M, Tschopp J. 2001. Carma1, a CARD-containing binding partner of Bcl10, induces Bcl10 pho- sphorylation and NF-kappaB activation. FEBS Lett 496:121-127.
18. 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.
19. Greil J, Rausch T, Giese T, Bandapalli OR, Daniel V, Bekeredjian-Ding I, Stütz AM, Drees C, Roth S, Ruland J, Korbel JO, Kulozik AE. 2013. Whole-exome sequencing links caspase recruitment domain 11 (CARD11) inactivation to severe combined immunodeficiency. J Allergy Clin Immunol 131:1376-1383.
20. Guiet C, Vito P. 2000. Caspase recruitment domain (CARD)-dependent cytoplasmic filaments mediate bcl10-induced NF-kappaB activation. J Cell Biol 148:1131-1140.
21. 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.
22. Hayden MS, Ghosh S. 2008. Shared principles in NF-kappaB signaling. Cell 132:344-362.
23. Jeelall YS, Wang JQ, Law HD, Domaschenz H, Fung HK, Kallies A, Nutt SL, Goodnow CC, Horikawa K. 2012. Human lymphoma mutations reveal CARD11 as the switch between self-antigen-induced B cell death or proliferation and autoantibody production. J Exp Med 209:1907-1917.
24. Jiang T, Grabiner B, Zhu Y, Jiang C, Li H, You Y, Lang J, Hung MC, Lin X. 2011. CARMA3 is crucial for EGFR-Induced activation of NF-κB and tumor progression. Cancer Res 71:2183-2192.
25. Jordan CT, Cao L, Roberson ED, Pierson KC, Yang CF, Joyce CE, Ryan C, Duan S, Helms CA, Liu Y, Chen Y, McBride AA, Hwu WL, Wu JY, Chen YT, Menter A, Goldbach-Mansky R, Lowes MA, Bowcock AM. 2012a. PSORS2 is due to mutations in CARD14. Am J Hum Genet 90:784-795.
26. Jordan CT, Cao L, Roberson ED, Duan S, Helms CA, Nair RP, Duffin KC, Stuart PE, Goldgar D, Hayashi G, Olfson EH, Feng BJ, Pullinger CR, Kane JP, Wise CA, Goldbach-Mansky R, Lowes MA, Peddle L, Chandran V, Liao W, Rahman P, Krueger GG, Gladman D, Elder JT, Menter A, Bowcock AM. 2012b. Rare and common variants in CARD14, encoding an epidermal regulator of NF-kappaB, in psoriasis. Am J Hum Genet 90:796-808.
27. Koseki T, Inohara N, Chen S, Carrio R, Merino J, Hottiger MO, Nabel GJ, Núñez G. 1999. CIPER, a novel NF-kappaB-activating protein containing a caspase recruitment domain with homology to Herpesvirus-2 protein E10. J Biol Chem 274:9955-9961.
28. Lee KY, D'Acquisto F, Hayden MS, Shim JH, Ghosh S. 2005. PDK1 nucleates T cell receptor-indiced signaling complex for NF-kappaB activation. Science 308:114-118.
29. Lenz G, Davis RE, Ngo VN, Lam L, George TC, Wright GW, Dave SS, Zhao H, Xu W, Rosenwald A, Ott G, Muller-Hermelink HK, Gascoyne RD, Connors JM, Rimsza LM, Campo E, Jaffe ES, Delabie J, Smeland EB, Fisher RI, Chan WC, Staudt LM. 2008. Oncogenic CARD11 mutations in human diffuse large B cell lymphoma. Science 319:1676-1679.
30. Lowes MA, Bowcock AM, Krueger JG. 2007. Pathogenesis and therapy of psoriasis. Nature 445:866-873.
31. Marasco D, Stilo R, Sandomenico A, Monti SM, Tizzano B, de Capua A, Varricchio E, Liguoro D, Zotti T, Formisano S, Ruvo M, Vito P. 2009. Generation and functional characterization of a BCL10-inhibitory peptide that represses NF-kappaB activation. Biochem J 422:553-561.
32. 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.
33. Li Z, Qu L, Dong Q, Huang B, Li H, Tang Z, Xu Y, Luo W, Liu L, Qiu X, Wang E. 2012. Overexpression of CARMA3 in non-small-cell lung cancer is linked for tumor progression. PLoS ONE 7:e36903.
34. Lohr JG, Stojanov P, Lawrence MS, Auclair D, Chapuy B, Sougnez C, Cruz-Gordillo P, Knoechel B, Asmann YW, Slager SL, Novak AJ, Dogan A, Ansell SM, Link BK, Zou L, Gould J, Saksena G, Stransky N, Rangel-Escareño C, Fernandez-Lopez JC, Hidalgo-Miranda A, Melendez-Zajgla J, Hernández-Lemus E, Schwarz-Cruz y Celis A, Imaz-Rosshandler I, Ojesina AI, Jung J, Pedamallu CS, Lander ES, Habermann TM, Cerhan JR, Shipp MA, Getz G, Golub TR. 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.
35. McAllister-Lucas LM, Inohara N, Lucas PC, Ruland J, Benito A, Li Q, Chen S, Chen FF, Yamaoka S, Verma IM, Mak TW, Núñez G. 2001. Bimp1, a MAGUK family member linking protein kinase C activation to Bcl10-mediated NF-kappaB induction. J Biol Chem 276:30589-30597.
36. McAllister-Lucas LM, Ruland J, Siu K, Jin X, Gu S, Kim DS, Kuffa P, Kohrt D, Mak TW, Nuñez G, Lucas PC. 2007. CARMA3/Bcl10/MALT1-dependent NF-kappaB activation mediates angiotensin II-responsive inflammatory signaling in nonim-mune cells. Proc Natl Acad Sci USA 104:139-144.
37. McCully RR, Pomerantz JL. 2008. The protein kinase C-responsive inhibitory domain of CARD11 functions in NF-kappaB activation to regulate the association of multiple signaling cofactors that differentially depend on Bcl10 and MALT1 for association. Mol Cell Biol 28:5668-5686.
38. Miao Z, Zhao T, Wang Z, Xu Y, Song Y, Wu J, Xu H. 2012. CARMA3 is overexpressed in colon cancer and regulates NF-κB activity and cyclin D1 expression. Biochem Biophys Res Commun 425:781-787.
39. Montesinos-Rongen M, Schmitz R, Brunn A, Gesk S, Richter J, Hong K, Wiestler OD, Siebert R, Küppers R, Deckert M. 2010. Mutations of CARD11 but not TNFAIP3 may activate the NF-κB pathway in primary CNS lymphoma. Acta Neuropathol 120:529-535.
40. Nograles KE, Brasington RD, Bowcock AM. 2009. New insights into the pathogenesis and genetics of psoriatic arthritis. Nat Clin Pract Rheumatol 5:83-91.
41. Nakamura S, Nakamura S, Matsumoto T, Yada S, Hirahashi M, Suekane H, Yao T, Goda K, Iida M. 2005. Overexpression of caspase recruitment domain (CARD) membrane-associated guanylate kinase 1 (CARMA1) and CARD9 in primary gastric B-cell lymphoma. Cancer 104:1885-1893.
42. Newton K, Dixit V. 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.
43. 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.
44. Oshiro A, Tagawa H, Ohshima K, Karube K, Uike N, Tashiro Y, Utsunomiya A, Masuda M, Takasu N, Nakamura S, Morishima Y, Seto M. 2006. Identification of subtype-specific genomic alterations in aggressive adult T-cell leukemia/lymphoma. Blood 107:4500-4507.
45. 2+-dependent phosphatase calcineurin controls the formation of the Carma1-Bcl10-Malt1 complex during T cell receptor-induced NF-kappaB activation. J Biol Chem 286:7522-7534.
46. Park Y, Jin HS, Liu YC. 2013. Regulation of T cell function by the ubiquitin-specific protease USP9X via modulating the Carma1-Bcl10-Malt1 complex. Proc Natl Acad Sci U S A 110:9433-9438.
47. Qiao Q, Yang C, Zheng C, Fontán L, David L, Yu X, Bracken C, Rosen M, Melnick A, Egelman EH, Wu H. 2013. Structural architecture of the CARMA1/Bcl10/MALT1 signalosome: Nucleation-induced filamentous assembly. Mol Cell 51:766-779.
48. Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, Fisher RI, Gascoyne RD, Muller-Hermelink HK, Smeland EB, Giltnane JM, Hurt EM, Zhao H, Averett L, Yang L, Wilson WH, Jaffe ES, Simon R, Klausner RD, Powell J, Duffey PL, Longo DL, Greiner TC, Weisenburger DD, Sanger WG, Dave BJ, Lynch JC, Vose J, Armitage JO, Montserrat E, López-Guillermo A, Grogan TM, Miller TP, LeBlanc M, Ott G, Kvaloy S, Delabie J, Holte H, Krajci P, Stokke T, Staudt LM. 2002. Lymphoma/leukemia molecular profiling project. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med 346:1937-1947.
49. 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.
50. Scudiero I, Zotti T, Ferravante A, Vessichelli M, Vito P, Stilo R. 2011. Alternative splicing of CARMA2/CARD14 transcripts generates protein variants with differential effect on NF-κB activation and endoplasmic reticulum stress-induced cell death. J Cell Physiol 226:3121-3131.
51. Shinohara H, Yasuda T, Aiba Y, Sanjo H, Hamadate M, Watarai H, Sakurai H, Kurosaki T. 2005. PKC beta regulates BCR-mediated IKK activation by facilitating the interaction between TAK1 and CARMA1 J Exp Med 2005:1423-1431.
52. Snow AL, Xiao W, Stinson JR, Lu W, Chaigne-Delalande B, Zheng L, Pittaluga S, Matthews HF, Schmitz R, Jhavar S, Kuchen S, Kardava L, Wang W, Lamborn IT, Jing H, Raffeld M, Moir S, Fleisher TA, Staudt LM, Su HC, Lenardo MJ. 2012. Congenital B cell lymphocytosis explained by novel germline CARD11 mutations. J Exp Med 209:2247-2261.
53. 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.
54. Srinivasula SM, Ahmad M, Lin JH, Poyet JL, Fernandes-Alnemri T, Tsichlis PN, Alnemri ES. 1999. CLAP, a novel caspase recruitment domain-containing protein in the tumor necrosis factor receptor pathway, regulates NF-kappaB activation and apoptosis. J Biol Chem 274:17946-17954.
55. Stepensky P, Keller B, Buchta M, Kienzler AK, Elpeleg O, Somech R, Cohen S, Shachar I, Miosge LA, Schlesier M, Fuchs I, Enders A, Eibel H, Grimbacher B, 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.
56. Stilo R, Liguoro D, Di Jeso B, Formisano S, Consiglio E, Leonardi A, Vito P. 2004. Physical and functional interaction of CARMA1 and CARMA 3 with Ikappa Kinase gamma-NF-kappaB essential modulator. J Biol Chem 279:34323-34331.
57. Stilo R, Varricchio E, Liguoro D, Leonardi A, Vito P. 2008. A20 is a negative regulator of BCL10- and CARMA3-mediated activation of NF-kappaB. J Cell Sci 121:1165-1171.
58. 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.
59. Sun SC, Ley SC. 2008. New insights into NF-kappaB regulation and function. Trends Immunol 29:469-478.
60. Sun J. 2010. CARMA3: A novel scaffold protein in regulation of NF-κB activation and diseases. World J Biol Chem 1:353-361.
61. Tanner MJ, Hanel W, Gaffen SL, Lin X. 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 282:17141-17147.
62. The non-hodgkin's lymphoma classification project. 1997. Blood 89:3909.
63. Vessichelli M, Ferravante A, Zotti T, Reale C, Scudiero I, Picariello G, Vito P, Stilo R. 2012. Neuroepithelial transforming gene 1 (Net1) binds to caspase activation and recruitment domain (CARD)- and membrane-associated guanylate kinase-like domain-containing (CARMA) proteins and regulates nuclear factor κB activation. J Biol Chem 287:13722-13730.
64. Wang L, Guo Y, Huang WJ, Ke X, Poyet JL, Manji GA, Merriam S, Glucksmann MA, DiStefano PS, Alnemri ES, Bertin J. 2001. Card10 is a novel caspase recruitment domain/membrane-associated guanylate kinase family member that interacts with BCL10 and activates NF-kappa B. J Biol Chem 276:21405-21409.
65. 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 lymphomas and mutated in multiple tumor types. Cell 96:35-45.
66. Wu CJ, Ashwell JD. 2008. NEMO recognition of ubiquitinated Bcl10 is required for T cell receptor-mediated NF-κB activation. Proc Natl Acad Sci USA 105:3023-3028.
67. 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 mutation and overexpression of BCL10, a caspase recruitment domain-containing gene, in MALT lymphoma with t(1;14)(p22;q32). Nat Genet 22:63-68.