A positive feedback loop between RIP3 and JNK controls non-alcoholic steatohepatitis

EMBO Molecular Medicine

Volumn 6, Issue 8, 2014, Pages 1062-1074

  Gautheron, Jérémie ^a   Vucur, Mihael ^a   Reisinger, Florian ^b   Cardenas, David Vargas ^a   Roderburg, Christoph ^a   Koppe, Christiane ^a   Kreggenwinkel, Karina ^a   Schneider, Anne Theres ^a   Bartneck, Matthias ^a   Neumann, Ulf Peter ^a   Canbay, Ali ^c   Reeves, Helen Louise ^d   Luedde, Mark ^e   Tacke, Frank ^a   Trautwein, Christian ^a   Heikenwalder, Mathias ^b   Luedde, Tom ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d FREEMAN HOSPITAL   (United Kingdom)

^e UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

Biliary ductular reaction; Caspase 8; Liver fibrosis; MCP 1; Necroptosis

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CASPASE 8; GLUTAMATE DEHYDROGENASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN; RIP3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CCL2 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, HUMAN; RIPK3 PROTEIN, MOUSE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL DEATH; CHEMOTAXIS; CHOLANGIOCYTE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN TISSUE; INFLAMMATION; LIPID PEROXIDATION; LIVER CELL; LIVER FIBROSIS; LIVER INJURY; MACROPHAGE; MONOCYTE; MOUSE; NECROPTOSIS; NONALCOHOLIC FATTY LIVER; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION; ANIMAL; DISEASE MODEL; GENE EXPRESSION REGULATION; LIVER; METABOLISM; PATHOLOGY;

ANIMALS; CHEMOKINE CCL2; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; LIVER; MAP KINASE KINASE 4; MICE; NON-ALCOHOLIC FATTY LIVER DISEASE; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES;

EID: 84905239992     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201403856     Document Type: Review

References (52)

1. Anstee QM, Concas D, Kudo H, Levene A, Pollard J, Charlton P, Thomas HC, Thursz MR, Goldin RD (2010) Impact of pan-caspase inhibition in animal models of established steatosis and non-alcoholic steatohepatitis. J Hepatol 53: 542-550
2. Baeck C, Wehr A, Karlmark KR, Heymann F, Vucur M, Gassler N, Huss S, Klussmann S, Eulberg D, Luedde T et al (2012) Pharmacological inhibition of the chemokine CCL2 (MCP-1) diminishes liver macrophage infiltration and steatohepatitis in chronic hepatic injury. Gut 61: 416-426
3. Bhala N, Angulo P, van der Poorten D, Lee E, Hui JM, Saracco G, Adams LA, Charatcharoenwitthaya P, Topping JH, Bugianesi E et al (2011) The natural history of nonalcoholic fatty liver disease with advanced fibrosis or cirrhosis: an international collaborative study. Hepatology 54: 1208-1216
4. Bonnet MC, Preukschat D, Welz PS, van Loo G, Ermolaeva MA, Bloch W, Haase I, Pasparakis M (2011) The adaptor protein FADD protects epidermal keratinocytes from necroptosis in vivo and prevents skin inflammation. Immunity 35: 572-582
5. Chakraborty JB, Oakley F, Walsh MJ (2012) Mechanisms and biomarkers of apoptosis in liver disease and fibrosis. Int J Hepatol 2012: 648915
6. Chang HY, Yang X (2000) Proteases for cell suicide: functions and regulation of caspases. Microbiol Mol Biol Rev 64: 821-846
7. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137: 1112-1123
8. Csak T, Dolganiuc A, Kodys K, Nath B, Petrasek J, Bala S, Lippai D, Szabo G (2011) Mitochondrial antiviral signaling protein defect links impaired antiviral response and liver injury in steatohepatitis in mice. Hepatology 53: 1917-1931
9. Das M, Sabio G, Jiang F, Rincon M, Flavell RA, Davis RJ (2009) Induction of hepatitis by JNK-mediated expression of TNF-alpha. Cell 136: 249-260
10. Degterev A, Maki JL, Yuan J (2013) Activity and specificity of necrostatin-1, small-molecule inhibitor of RIP1 kinase. Cell Death Differ 20: 366
11. Dixon LJ, Flask CA, Papouchado BG, Feldstein AE, Nagy LE (2013) Caspase-1 as a central regulator of high fat diet-induced non-alcoholic steatohepatitis. PLoS ONE 8: e56100
12. Estaquier J, Vallette F, Vayssiere JL, Mignotte B (2012) The mitochondrial pathways of apoptosis. Adv Exp Med Biol 942: 157-183
13. Feldstein AE, Canbay A, Angulo P, Taniai M, Burgart LJ, Lindor KD, Gores GJ (2003) Hepatocyte apoptosis and fas expression are prominent features of human nonalcoholic steatohepatitis. Gastroenterology 125: 437-443
14. Feldstein AE, Gores GJ (2005) Apoptosis in alcoholic and nonalcoholic steatohepatitis. Front Biosci 10: 3093-3099
15. Han J, Zhong CQ, Zhang DW (2011) Programmed necrosis: backup to and competitor with apoptosis in the immune system. Nat Immunol 12: 1143-1149
16. Hatting M, Zhao G, Schumacher F, Sellge G, Al Masaoudi M, Gabetaler N, Boekschoten M, Muller M, Liedtke C, Cubero FJ et al (2013) Hepatocyte caspase-8 is an essential modulator of steatohepatitis in rodents. Hepatology 57: 2189-2201
17. He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137: 1100-1111
18. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, Caspary T, Mocarski ES (2011) RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471: 368-372
19. Kellendonk C, Opherk C, Anlag K, Schutz G, Tronche F (2000) Hepatocyte-specific expression of Cre recombinase. Genesis 26: 151-153
20. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp-Arida A et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41: 1313-1321
21. Li J, McQuade T, Siemer AB, Napetschnig J, Moriwaki K, Hsiao YS, Damko E, Moquin D, Walz T, McDermott A et al (2012) The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 150: 339-350
22. Liu K, Czaja MJ (2013) Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ 20: 3-11
23. Malhi H, Gores GJ (2008) Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease. Semin Liver Dis 28: 360-369
24. Najimi M, Smets F, Sokal E (2009) Hepatocyte apoptosis. Methods Mol Biol 481: 59-74
25. Newton K, Sun X, Dixit VM (2004) Kinase RIP3 is dispensable for normal NF-kappa Bs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol Cell Biol 24: 1464-1469
26. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939
27. Poelstra K, Schuppan D (2011) Targeted therapy of liver fibrosis/cirrhosis and its complications. J Hepatol 55: 726-728
28. Postic C, Shiota M, Niswender KD, Jetton TL, Chen Y, Moates JM, Shelton KD, Lindner J, Cherrington AD, Magnuson MA (1999) Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J Biol Chem 274: 305-315
29. Ratziu V, Sheikh MY, Sanyal AJ, Lim JK, Conjeevaram H, Chalasani N, Abdelmalek M, Bakken A, Renou C, Palmer M et al (2012) A phase 2, randomized, double-blind, placebo-controlled study of GS-9450 in subjects with nonalcoholic steatohepatitis. Hepatology 55: 419-428
30. Richardson MM, Jonsson JR, Powell EE, Brunt EM, Neuschwander-Tetri BA, Bhathal PS, Dixon JB, Weltman MD, Tilg H, Moschen AR et al (2007) Progressive fibrosis in nonalcoholic steatohepatitis: association with altered regeneration and a ductular reaction. Gastroenterology 133: 80-90
31. Roychowdhury S, McMullen MR, Pisano SG, Liu X, Nagy LE (2013) Absence of receptor interacting protein kinase 3 prevents ethanol-induced liver injury. Hepatology 57: 1773-1783
32. Salmena L, Lemmers B, Hakem A, Matysiak-Zablocki E, Murakami K, Au PY, Berry DM, Tamblyn L, Shehabeldin A, Migon E et al (2003) Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev 17: 883-895
33. Schattenberg JM, Singh R, Wang Y, Lefkowitch JH, Rigoli RM, Scherer PE, Czaja MJ (2006) JNK1 but not JNK2 promotes the development of steatohepatitis in mice. Hepatology 43: 163-172
34. Schattenberg JM, Schuppan D (2011) Nonalcoholic steatohepatitis: the therapeutic challenge of a global epidemic. Curr Opin Lipidol 22: 479-488
35. Schuppan D, Afdhal NH (2008) Liver cirrhosis. Lancet 371: 838-851
36. Schuppan D, Kim YO (2013) Evolving therapies for liver fibrosis. J Clin Invest 123: 1887-1901
37. Seifert EL, Estey C, Xuan JY, Harper ME (2010) Electron transport chain-dependent and -independent mechanisms of mitochondrial H2O2 emission during long-chain fatty acid oxidation. J Biol Chem 285: 5748-5758
38. Seki E, de Minicis S, Inokuchi S, Taura K, Miyai K, van Rooijen N, Schwabe RF, Brenner DA (2009) CCR2 promotes hepatic fibrosis in mice. Hepatology 50: 185-197
39. Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X et al (2012) Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148: 213-227
40. Tacke F, Luedde T, Trautwein C (2008) Inflammatory pathways in liver homeostasis and liver injury. Clin Rev Allergy Immunol 36: 4-12
41. Vernon G, Baranova A, Younossi ZM (2011) Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 34: 274-285
42. Vucur M, Reisinger F, Gautheron J, Janssen J, Roderburg C, Cardenas DV, Kreggenwinkel K, Koppe C, Hammerich L, Hakem R et al (2013) RIP3 inhibits inflammatory hepatocarcinogenesis but promotes cholestasis by controlling caspase-8- and JNK-dependent compensatory cell proliferation. Cell Rep 4: 776-790
43. Weinlich R, Oberst A, Dillon CP, Janke LJ, Milasta S, Lukens JR, Rodriguez DA, Gurung P, Savage C, Kanneganti TD et al (2013) Protective roles for caspase-8 and cFLIP in adult homeostasis. Cell Rep 5: 340-348
44. Welz PS, Wullaert A, Vlantis K, Kondylis V, Fernandez-Majada V, Ermolaeva M, Kirsch P, Sterner-Kock A, van Loo G, Pasparakis M (2011) FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 477: 330-334
45. Wieckowska A, Zein NN, Yerian LM, Lopez AR, McCullough AJ, Feldstein AE (2006) In vivo assessment of liver cell apoptosis as a novel biomarker of disease severity in nonalcoholic fatty liver disease. Hepatology 44: 27-33
46. Witek RP, Stone WC, Karaca FG, Syn WK, Pereira TA, Agboola KM, Omenetti A, Jung Y, Teaberry V, Choi SS et al (2009) Pan-caspase inhibitor VX-166 reduces fibrosis in an animal model of nonalcoholic steatohepatitis. Hepatology 50: 1421-1430
47. Wree A, Broderick L, Canbay A, Hoffman HM, Feldstein AE (2013) From NAFLD to NASH to cirrhosis-new insights into disease mechanisms. Nat Rev Gastroenterol Hepatol 10: 627-636
48. Yang L, Roh YS, Song J, Zhang B, Liu C, Loomba R, Seki E (2014) Transforming growth factor beta signaling in hepatocytes participates in steatohepatitis through regulation of cell death and lipid metabolism in mice. Hepatology 59: 483-495
49. Younossi ZM, Jarrar M, Nugent C, Randhawa M, Afendy M, Stepanova M, Rafiq N, Goodman Z, Chandhoke V, Baranova A (2008) A novel diagnostic biomarker panel for obesity-related nonalcoholic steatohepatitis (NASH). Obes Surg 18: 1430-1437
50. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU (2006) Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 8: 1124-1132
51. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325: 332-336
52. Zimmermann HW, Tacke F (2011) Modification of chemokine pathways and immune cell infiltration as a novel therapeutic approach in liver inflammation and fibrosis. Inflamm Allergy Drug Targets 10: 509-536