Transforming growth factor beta signaling in hepatocytes participates in steatohepatitis through regulation of cell death and lipid metabolism in mice

Hepatology

Volumn 59, Issue 2, 2014, Pages 483-495

  Yang, Ling ^a,b   Roh, Yoon Seok ^a   Song, Jingyi ^a   Zhang, Bi ^a   Liu, Cheng ^a   Loomba, Rohit ^a   Seki, Ekihiro ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DIACYLGLYCEROL ACYLTRANSFERASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PALMITIC ACID; REACTIVE OXYGEN METABOLITE; SMAD2 PROTEIN; SMAD3 PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; FATTY ACID OXIDATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; INFLAMMATORY INFILTRATE; INTRACELLULAR SIGNALING; LIPID LIVER LEVEL; LIPID METABOLISM; LIPID PEROXIDATION; LIPID STORAGE; LIPOGENESIS; LIVER BIOPSY; LIVER CELL; LIVER FIBROSIS; LIVER PARENCHYMA; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VITAMIN DEFICIENCY;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CHOLINE DEFICIENCY; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FATTY LIVER; GENE DELETION; HEPATOCYTES; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84893636304     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26698     Document Type: Article

References (38)

1. Day CP. Non-alcoholic fatty liver disease: a massive problem. Clin Med 2011;11:176-178.
2. Kneeman JM, Misdraji J, Corey KE. Secondary causes of nonalcoholic fatty liver disease. Therap Adv Gastroenterol 2012;5:199-207.
3. Ratziu V, Bellentani S, Cortez-Pinto H, Day C, Marchesini G. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol 2010;53:372-384.
4. Sanyal AJ, Brunt EM, Kleiner DE, Kowdley KV, Chalasani N, Lavine JE, et al. Endpoints and clinical trial design for nonalcoholic steatohepatitis. Hepatology 2011;54:344-353.
5. Tiniakos DG, Vos MB, Brunt EM. Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu Rev Pathol 2010;5:145-171.
6. Loomba R, Abraham M, Unalp A, Wilson L, Lavine J, Doo E, Bass NM. Association between diabetes, family history of diabetes, and risk of nonalcoholic steatohepatitis and fibrosis. Hepatology 2012;56:943-951.
7. Achyut BR, Yang L. Transforming growth factor-beta in the gastrointestinal and hepatic tumor microenvironment. Gastroenterology 2011;141:1167-1178.
8. Dooley S, Weng H, Mertens PR. Hypotheses on the role of transforming growth factor-beta in the onset and progression of hepatocellular carcinoma. Dig Dis 2009;27:93-101.
9. Dooley S, ten Dijke P. TGF-beta in progression of liver disease. Cell Tissue Res 2012;347:245-256.
10. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005;115:209-218.
11. Klein S, Mittendorfer B, Eagon JC, Patterson B, Grant L, Feirt N, et al. Gastric bypass surgery improves metabolic and hepatic abnormalities associated with nonalcoholic fatty liver disease. Gastroenterology 2006;130:1564-1572.
12. Cayon A, Crespo J, Mayorga M, Guerra A, Pons-Romero F. Increased expression of Ob-Rb and its relationship with the overexpression of TGF-beta1 and the stage of fibrosis in patients with nonalcoholic steatohepatitis. Liver Int 2006;26:1065-1071.
13. Lin HM, Lee JH, Yadav H, Kamaraju AK, Liu E, Zhigang D, et al. Transforming growth factor-beta/Smad3 signaling regulates insulin gene transcription and pancreatic islet beta-cell function. J Biol Chem 2009;284:12246-12257.
14. Yadav H, Quijano C, Kamaraju AK, Gavrilova O, Malek R, Chen W, et al. Protection from obesity and diabetes by blockade of TGF-beta/Smad3 signaling. Cell Metab 2011;14:67-79.
15. Tan CK, Leuenberger N, Tan MJ, Yan YW, Chen Y, Kambadur R, et al. Smad3 deficiency in mice protects against insulin resistance and obesity induced by a high-fat diet. Diabetes 2011;60:464-476.
16. Miura K, Kodama Y, Inokuchi S, Schnabl B, Aoyama T, Ohnishi H, et al. Toll-like receptor 9 promotes steatohepatitis by induction of interleukin-1beta in mice. Gastroenterology 2010;139:323-334.e7.
17. Miura K, Yang L, van Rooijen N, Brenner DA, Ohnishi H, Seki E. TLR2 and palmitic acid cooperatively contribute to the development of nonalcoholic steatohepatitis through inflammasome activation. Hepatology 2013;57:577-589.
18. Miura K, Yang L, van Rooijen N, Ohnishi H, Seki E. Hepatic recruitment of macrophages promotes nonalcoholic steatohepatitis through CCR2. Am J Physiol Gastrointest Liver Physiol 2012;302:G1310-1321.
19. De Minicis S, Seki E, Oesterreicher C, Schnabl B, Schwabe RF, Brenner DA. Reduced nicotinamide adenine dinucleotide phosphate oxidase mediates fibrotic and inflammatory effects of leptin on hepatic stellate cells. Hepatology 2008;48:2016-2026.
20. Cazanave SC, Mott JL, Elmi NA, Bronk SF, Werneburg NW, Akazawa Y, et al. JNK1-dependent PUMA expression contributes to hepatocyte lipoapoptosis. J Biol Chem 2009;284:26591-26602.
21. 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.
22. Permutt Z, Le TA, Peterson MR, Seki E, Brenner DA, Sirlin C, Loomba R. Correlation between liver histology and novel magnetic resonance imaging in adult patients with non-alcoholic fatty liver disease-MRI accurately quantifies hepatic steatosis in NAFLD. Aliment Pharmacol Ther 2012;36:22-29.
23. Le TA, Chen J, Changchien C, Peterson MR, Kono Y, Patton H, et al. Effect of colesevelam on liver fat quantified by magnetic resonance in nonalcoholic steatohepatitis: a randomized controlled trial. Hepatology 2012;56:922-932.
24. Seki E, De Minicis S, Osterreicher CH, Kluwe J, Osawa Y, Brenner DA, Schwabe RF. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 2007;13:1324-1332.
25. Ciuclan L, Ehnert S, Ilkavets I, Weng HL, Gaitantzi H, Tsukamoto H, et al. TGF-beta enhances alcohol dependent hepatocyte damage via down-regulation of alcohol dehydrogenase I. J Hepatol 2010;52:407-416.
26. Ninomiya-Tsuji J, Kajino T, Ono K, Ohtomo T, Matsumoto M, Shiina M, et al. A resorcylic acid lactone, 5Z-7-oxozeaenol, prevents inflammation by inhibiting the catalytic activity of TAK1 MAPK kinase kinase. J Biol Chem 2003;278:18485-18490.
27. Shim JH, Xiao C, Paschal AE, Bailey ST, Rao P, Hayden MS, et al. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 2005;19:2668-2681.
28. Sato S, Sanjo H, Takeda K, Ninomiya-Tsuji J, Yamamoto M, Kawai T, et al. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 2005;6:1087-1095.
29. Kita T, Hata Y, Arita R, Kawahara S, Miura M, Nakao S, et al. Role of TGF-beta in proliferative vitreoretinal diseases and ROCK as a therapeutic target. Proc Natl Acad Sci U S A 2008;105:17504-17509.
30. Gressner AM, Weiskirchen R, Breitkopf K, Dooley S. Roles of TGF-beta in hepatic fibrosis. Front Biosci 2002;7:d793-d807.
31. Kodama Y, Taura K, Miura K, Schnabl B, Osawa Y, Brenner DA. Antiapoptotic effect of c-Jun N-terminal kinase-1 through Mcl-1 stabilization in TNF-induced hepatocyte apoptosis. Gastroenterology 2009;136:1423-1434.
32. Yang L, Inokuchi S, Roh YS, Song J, Loomba R, Park EJ, Seki E. Transforming growth factor-beta signaling in hepatocytes promotes hepatic fibrosis and carcinogenesis in mice with hepatocyte-specific deletion of TAK1. Gastroenterology 2013;144:1042-1054.e4.
33. Carnesecchi S, Deffert C, Donati Y, Basset O, Hinz B, Preynat-Seauve O, et al. A key role for NOX4 in epithelial cell death during development of lung fibrosis. Antioxid Redox Signal 2011;15:607-619.
34. Tomita K, Teratani T, Suzuki T, Oshikawa T, Yokoyama H, Shimamura K, et al. p53/p66Shc-mediated signaling contributes to the progression of non-alcoholic steatohepatitis in humans and mice. J Hepatol 2012;57:837-843.
35. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007;56:1761-1772.
36. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest 2011;121:2111-2117.
37. Ling H, Li X, Jha S, Wang W, Karetskaya L, Pratt B, Ledbetter S. Therapeutic role of TGF-beta-neutralizing antibody in mouse cyclosporin A nephropathy: morphologic improvement associated with functional preservation. J Am Soc Nephrol 2003;14:377-388.
38. Nam JS, Terabe M, Mamura M, Kang MJ, Chae H, Stuelten C, et al. An anti-transforming growth factor beta antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res 2008;68:3835-3843.