A20 prevents chronic liver inflammation and cancer by protecting hepatocytes from death

Cell Death and Disease

Volumn 7, Issue 6, 2016, Pages

  Catrysse, L ^a,b   Farhang Ghahremani, M ^a,b   Vereecke, L ^a,b   Youssef, S A ^c   Mc Guire, C ^a,b   Sze, M ^a,b   Weber, A ^d   Heikenwalder, M ^e,f   De Bruin, A ^c,g   Beyaert, R ^a,b   Van Loo, G ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; FAS ASSOCIATED DEATH DOMAIN PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN BCL XL; TUMOR NECROSIS FACTOR; UBIQUITIN; UBIQUITIN EDITING PROTEIN A20; UNCLASSIFIED DRUG; CYTOKINE; FADD PROTEIN, MOUSE; STRESS ACTIVATED PROTEIN KINASE; TNFAIP3 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA INDUCED PROTEIN 3;

ACUTE LIVER FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; CELL PROLIFERATION; CELL PROTECTION; CHRONIC HEPATITIS; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FATTY LIVER; GENE EXPRESSION; HYPOTHERMIA; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; KUPFFER CELL; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL; LIVER DEVELOPMENT; LIVER HISTOLOGY; LIVER PROTECTION; MACROPHAGE; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CARCINOGENESIS; CHRONIC DISEASE; DEFICIENCY; DRUG EFFECTS; GENE DELETION; HEPATITIS; INFLAMMATION; KNOCKOUT MOUSE; LIPID DIET; LIVER; LIVER TUMOR; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; CARCINOGENESIS; CHRONIC DISEASE; CYTOKINES; CYTOPROTECTION; DIET, HIGH-FAT; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; GENE DELETION; HEPATITIS; HEPATOCYTES; INFLAMMATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIVER; LIVER NEOPLASMS; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; PHENOTYPE; TUMOR NECROSIS FACTOR ALPHA-INDUCED PROTEIN 3; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84974707630     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2016.154     Document Type: Article

References (50)

1. Luedde T, Kaplowitz N, Schwabe RF. Cell death and cell death responses in liver disease: mechanisms and clinical relevance. Gastroenterology 2014; 147: 765-783, e4.
2. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003; 114: 181-190.
3. Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M et al. Inhibition of JNK activation through NF-kappaB target genes. Nature 2001; 414: 313-317.
4. Schuchmann M, Varfolomeev EE, Hermann F, Rueckert F, Strand D, Koehler H et al. Dominant negative MORT1/FADD rescues mice from CD95 and TNF-induced liver failure. Hepatology 2003; 37: 129-135.
5. Kang T-B, Ben-Moshe T, Varfolomeev EE, Pewzner-Jung Y, Yogev N, Jurewicz A et al. Caspase-8 serves both apoptotic and nonapoptotic roles. J Immunol 2004; 173: 2976-2984.
6. Kaufmann T, Jost PJ, Pellegrini M, Puthalakath H, Gugasyan R, Gerondakis S et al. Fatal hepatitis mediated by tumor necrosis factor TNFalpha requires caspase-8 and involves the BH3-only proteins Bid and Bim. Immunity 2009; 30: 56-66.
7. Luedde T, Schwabe RF. NF-?B in the liver-linking injury, fibrosis and hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol 2011; 8: 108-118.
8. Boone DL, Turer EE, Lee EG, Ahmad R-C,Wheeler MT, Tsui C et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 2004; 5: 1052-1060.
9. Hitotsumatsu O, Ahmad R-C, Tavares R, Wang M, Philpott D, Turer EE et al. The ubiquitinediting enzyme A20 restricts nucleotide-binding oligomerization domain containing 2-triggered signals. Immunity 2008; 28: 381-390.
10. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP et al. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 2000; 289: 2350-2354.
11. Vereecke L, Sze M, Mc Guire C, Rogiers B, Chu Y, Schmidt-Supprian M et al. Enterocytespecific A20 deficiency sensitizes to tumor necrosis factor-induced toxicity and experimental colitis. J Exp Med 2010; 207: 1513-1523.
12. Catrysse L, Vereecke L, Beyaert R, van Loo G. A20 in inflammation and autoimmunity. Trends Immunol 2014; 35: 22-31.
13. De Boer YS, van Gerven NMF, Zwiers A, Verwer BJ, van Hoek B, van Erpecum KJ et al. Genome-wide association study identifies variants associated with autoimmune hepatitis type 1. Gastroenterology 2014; 147: e5.
14. Longo CR, Patel VI, Shrikhande GV, Scali ST, Csizmadia E, Daniel S et al. A20 protects mice from lethal radical hepatectomy by promoting hepatocyte proliferation via a p21waf1-dependent mechanism. Hepatology 2005; 42: 156-164.
15. Damrauer SM, Studer P, da Silva CG, Longo CR, Ramsey HE, Csizmadia E et al. A20 modulates lipid metabolism and energy production to promote liver regeneration. PLoS One 2011; 6: e17715.
16. Da Silva CG, Studer P, Skroch M, Mahiou J, Minussi DC, Peterson CR et al. A20 promotes liver regeneration by decreasing SOCS3 expression to enhance IL-6/STAT3 proliferative signals. Hepatology 2013; 57: 2014-2025.
17. Studer P, da Silva CG, Revuelta Cervantes JM, Mele A, Csizmadia E, Siracuse JJ et al. Significant lethality following liver resection in A20 heterozygous knockout mice uncovers a key role for A20 in liver regeneration. Cell Death Differ 2015; 22: 2068-2077.
18. Arvelo MB, Cooper JT, Longo C, Daniel S, Grey ST, Mahiou J et al. A20 protects mice from D-galactosamine/lipopolysaccharide acute toxic lethal hepatitis. Hepatology 2002; 35: 535-543.
19. Da Silva CG, Cervantes JR, Studer P, Ferran C. A20-an omnipotent protein in the liver: prometheus myth resolved? Adv Exp Med Biol 2014; 809: 117-139.
20. Tronche F, Opherk C, Moriggl R, Kellendonk C, Reimann A, Schwake L et al. Glucocorticoid receptor function in hepatocytes is essential to promote postnatal body growth. Genes Dev 2004; 18: 492-497.
21. Kellendonk C, Opherk C, Anlag K, Schütz G, Tronche F. Hepatocyte-specific expression of Cre recombinase. Genesis 2000; 26: 151-153.
22. Mc Guire C, Volckaert T, Sze M, De Rycke R, Waisman A, Prinz M et al. Oligodendrocytespecific FADD deletion protects mice from autoimmune-mediated demyelination. J Immunol 2010; 185: 7646-7653.
23. Wilson NS, Dixit V, Ashkenazi A. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat Immunol 2009; 10: 348-355.
24. Yeh WC, de la Pompa JL, McCurrach ME, Shu HB, Elia AJ, Shahinian A et al. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 1998; 279: 1954-1958.
25. Zhang J, Cado D, Chen A, Kabra NH, Winoto A. Fas-mediated apoptosis and activationinduced T-cell proliferation are defective in mice lacking FADD/Mort1. Nature 1998; 392: 296-300.
26. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006; 441: 431-436.
27. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004; 431: 461-466.
28. Haybaeck J, Zeller N, Wolf MJ, Weber A, Wagner U, Kurrer MO et al. A lymphotoxin-driven pathway to hepatocellular carcinoma. Cancer Cell 2009; 16: 295-308.
29. Maeda S, Kamata H, Luo J-L, Leffert H, Karin M. IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 2005; 121: 977-990.
30. Wolf MJ, Adili A, Piotrowitz K, Abdullah Z, Boege Y, Stemmer K et al. Metabolic activation of intrahepatic CD8+ T cells and NKT cells causes nonalcoholic steatohepatitis and liver cancer via cross-talk with hepatocytes. Cancer Cell 2014; 26: 549-564.
31. Park EJ, Lee JH, Yu G-Y, He G, Ali SR, Holzer RG et al. Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 2010; 140: 197-208.
32. Vereecke L, Vieira-Silva S, Billiet T, van Es JH, Mc Guire C, Slowicka K et al. A20 controls intestinal homeostasis through cell-specific activities. Nat Commun 2014; 5: 5103.
33. Jin Z, Li Y, Pitti R, Lawrence D, Pham VC, Lill JR et al. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 2009; 137: 721-735.
34. Bellail AC, Olson JJ, Yang X, Chen ZJ, Hao C. A20 ubiquitin ligase-mediated polyubiquitination of RIP1 inhibits caspase-8 cleavage and TRAIL-induced apoptosis in glioblastoma. Cancer Discov 2012; 2: 140-155.
35. WonM, Park KA, Byun HS, Sohn K-C, Kim Y-R, Jeon J et al. Novel anti-apoptotic mechanism of A20 through targeting ASK1 to suppress TNF-induced JNK activation. Cell Death Differ 2010; 17: 1830-1841.
36. Wertz IE, Newton K, Seshasayee D, Kusam S, Lam C, Zhang J et al. Phosphorylation and linear ubiquitin direct A20 inhibition of inflammation. Nature 2015; 528: 1-6.
37. Draber P, Kupka S, Reichert M, Draberova H, Lafont E, de Miguel D et al. LUBAC-recruited CYLD and A20 regulate gene activation and cell death by exerting opposing effects on linear ubiquitin in signaling complexes. Cell Rep 2015; 13: 2258-2272.
38. Luedde T, Beraza N, Kotsikoris V, van Loo G, Nenci A, De Vos R et al. Deletion of NEMO/IKK? in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 2007; 11: 119-132.
39. Bettermann K, Vucur M, Haybaeck J, Koppe C, Janssen J, Heymann F et al. TAK1 suppresses a NEMO-dependent but NF-?B-independent pathway to liver cancer. Cancer Cell 2010; 17: 481-496.
40. Inokuchi S, Aoyama T, Miura K, Osterreicher CH, Kodama Y, Miyai K et al. Disruption of TAK1 in hepatocytes causes hepatic injury, inflammation, fibrosis, carcinogenesis. Proc Natl Acad Sci USA 2010; 107: 844-849.
41. Kato M, Sanada M, Kato I, Sato Y, Takita J, Takeuchi K et al. Frequent inactivation of A20 in B-cell lymphomas. Nature 2009; 459: 712-716.
42. Compagno M, Lim WK, Grunn A, Nandula SV, Brahmachary M, Shen Q et al. Mutations of multiple genes cause deregulation of NF-kappaB in diffuse large B-cell lymphoma. Nature 2009; 459: 717-721.
43. Schmitz R, Hansmann M-L, Bohle V, Martin-Subero JI, Hartmann S, Mechtersheimer G et al. TNFAIP3 (A20) is a tumor suppressor gene in Hodgkin lymphoma and primary mediastinal B cell lymphoma. J Exp Med 2009; 206: 981-989.
44. Shao L, Oshima S, Duong B, Advincula R, Barrera J, Malynn BA et al. A20 restricts wnt signaling in intestinal epithelial cells and suppresses colon carcinogenesis. PLoS One 2013; 8: e62223.
45. Wang CM, Wang Y, Fan CG, Xu FF, Sun WS, Liu YG et al. MiR-29c targets TNFAIP3, inhibits cell proliferation and induces apoptosis in hepatitis B virus-related hepatocellular carcinoma. Biochem Biophys Res Commun 2011; 411: 586-592.
46. Dong B, Lv G, Wang Q, Wei F, Bellail AC, Hao C et al. Targeting A20 enhances TRAILinduced apoptosis in hepatocellular carcinoma cells. Biochem Biophys Res Commun 2012; 418: 433-438.
47. Chen H, Hu L, Luo Z, Zhang J, Zhang C, Qiu B et al. A20 suppresses hepatocellular carcinoma proliferation and metastasis through inhibition of Twist1 expression. Mol Cancer 2015; 14: 186.
48. Hoeroldt B, McFarlane E, Dube A, Basumani P, Karajeh M, Campbell MJ et al. Long-term outcomes of patients with autoimmune hepatitis managed at a nontransplant center. Gastroenterology 2011; 140: 1980-1989.
49. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005; 41: 1313-1321.
50. Hübscher SG. Histological assessment of non-alcoholic fatty liver disease. Histopathology 2006; 49: 450-465.