TAK1 regulates hepatic lipid homeostasis through SREBP

Oncogene

Volumn 35, Issue 29, 2016, Pages 3829-3838

  Morioka, S ^a,c   Sai, K ^a,b   Omori, E ^a   Ikeda, Y ^a   Matsumoto, K ^b   Ninomiya Tsuji, J ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NAGOYA UNIVERSITY   (Japan)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA FETOPROTEIN; CHOLESTEROL; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JANUS KINASE; REX PROTEIN; RNA H19; STEROL REGULATORY ELEMENT BINDING PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1A; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRIACYLGLYCEROL; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PROTEIN BINDING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; FATTY LIVER; FEMALE; GENE DELETION; IN VIVO STUDY; INFLAMMATION; LIPID HOMEOSTASIS; LIPID LIVER LEVEL; LIPID STORAGE; LIPOGENESIS; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; RISK ASSESSMENT; RISK FACTOR; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; ANIMAL; C57BL MOUSE; CELL LINE; GENETICS; HEK293 CELL LINE; HEP-G2 CELL LINE; HOMEOSTASIS; HUMAN; IMMUNOBLOTTING; KNOCKOUT MOUSE; LIPID METABOLISM; LIVER; LIVER CELL; LIVER TUMOR; METABOLISM; RNA INTERFERENCE; TRANSGENIC MOUSE;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE; FATTY LIVER; FEMALE; HEK293 CELLS; HEP G2 CELLS; HEPATOCYTES; HOMEOSTASIS; HUMANS; IMMUNOBLOTTING; LIPID METABOLISM; LIVER; LIVER NEOPLASMS; MALE; MAP KINASE KINASE KINASES; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEIN BINDING; RISK FACTORS; RNA INTERFERENCE; STEROL REGULATORY ELEMENT BINDING PROTEINS;

EID: 84961218902     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.453     Document Type: Article

References (70)

1. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 2002; 109: 1125-1131.
2. Brown MS, Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997; 89: 331-340.
3. Shimano H, Shimomura I, Hammer RE, Herz J, Goldstein JL, Brown MS et al. Elevated levels of SREBP-2 and cholesterol synthesis in livers of mice homozygous for a targeted disruption of the SREBP-1 gene. J Clin Invest 1997; 100: 2115-2124.
4. Yang T, Espenshade PJ, Wright ME, Yabe D, Gong Y, Aebersold R et al. Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 2002; 110: 489-500.
5. Goldstein JL, DeBose-Boyd RA, Brown MS. Protein sensors for membrane sterols. Cell 2006; 124: 35-46.
6. Sundqvist A, Ericsson J. Transcription-dependent degradation controls the stability of the SREBP family of transcription factors. Proc Natl Acad Sci USA 2003; 100: 13833-13838.
7. Sundqvist A, Bengoechea-Alonso MT, Ye X, Lukiyanchuk V, Jin J, Harper JW et al. Control of lipid metabolism by phosphorylation-dependent degradation of the SREBP family of transcription factors by SCF(Fbw7). Cell Metab 2005; 1: 379-391.
8. Peterson TR, Sengupta SS, Harris TE, Carmack AE, Kang SA, Balderas E et al. mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 2011; 146: 408-420.
9. Laplante M, Sabatini DM. mTORC1 activates SREBP-1c and uncouples lipogenesis from gluconeogenesis. Proc Natl Acad Sci USA 2010; 107: 3281-3282.
10. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 2010; 39: 171-183.
11. Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S et al. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 2008; 8: 224-236.
12. Yecies JL, Zhang HH, Menon S, Liu S, Yecies D, Lipovsky AI et al. Akt stimulates hepatic SREBP1c and lipogenesis through parallel mTORC1-dependent and independent pathways. Cell Metab 2011; 14: 21-32.
13. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R et al. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 2000; 6: 1355-1364.
14. Kammoun HL, Chabanon H, Hainault I, Luquet S, Magnan C, Koike T et al. GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice. J Clin Invest 2009; 119: 1201-1215.
15. Schuck S, Prinz WA, Thorn KS, Voss C, Walter P. Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J Cell Biol 2009; 187: 525-536.
16. Ron D, Hampton RY. Membrane biogenesis and the unfolded protein response. J Cell Biol 2004; 167: 23-25.
17. Li Y, Xu S, Mihaylova MM, Zheng B, Hou X, Jiang B et al. AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in dietinduced insulin-resistant mice. Cell Metab 2011; 13: 376-388.
18. Mihaly SR, Ninomiya-Tsuji J, Morioka S. TAK1 control of cell death. Cell Death Differ 2014; 21: 1667-1676.
19. Morioka S, Inagaki M, Komatsu Y, Mishina Y, Matsumoto K, Ninomiya-Tsuji J. TAK1 kinase signaling regulates embryonic angiogenesis by modulating endothelial cell survival and migration. Blood 2012; 120: 3846-3857.
20. Omori E, Matsumoto K, Sanjo H, Sato S, Akira S, Smart RC et al. TAK1 is a master regulator of epidermal homeostasis involving skin inflammation and apoptosis. J Biol Chem 2006; 281: 19610-19617.
21. Kajino-Sakamoto R, Inagaki M, Lippert E, Akira S, Robine S, Matsumoto K et al. Enterocyte-derived TAK1 signaling prevents epithelium apoptosis and the development of ileitis and colitis. J Immunol 2008; 181: 1143-1152.
22. Ikeda Y, Morioka S, Matsumoto K, Ninomiya-Tsuji J. TAK1 binding protein 2 is essential for liver protection from stressors. PLoS ONE 2014; 9: e88037.
23. Inokuchi S, Aoyama T, Miura K, Osterreicher CH, Kodama Y, Miyai K et al. Disruption of TAK1 in hepatocytes causes hepatic injury, inflammation, fibrosis, and carcinogenesis. Proc Natl Acad Sci USA 2010; 107: 844-849.
24. 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.
25. Morioka S, Broglie P, Omori E, Ikeda Y, Takaesu G, Matsumoto K et al. TAK1 kinase switches cell fate from apoptosis to necrosis following TNF stimulation. J Cell Biol 2014; 204: 607-623.
26. Yang L, Inokuchi S, Roh YS, Song J, Loomba R, Park EJ et al. Transforming growth factor-signaling in hepatocytes promotes hepatic fibrosis and carcinogenesis in mice with hepatocyte-specific deletion of TAK1. Gastroenterology 2013; 144: 1042-1054 e1044.
27. Das M, Garlick DS, Greiner DL, Davis RJ. The role of JNK in the development of hepatocellular carcinoma. Genes Dev 2011; 25: 634-645.
28. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009; 9: 537-549.
29. Luedde T, Beraza N, Kotsikoris V, van Loo G, Nenci A, De Vos R et al. Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 2007; 11: 119-132.
30. Maeda S, Kamata H, Luo JL, Leffert H, Karin M. IKK couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 2005; 121: 977-990.
31. Karin M. Nuclear factor-B in cancer development and progression. Nature 2006; 441: 431-436.
32. Sohda T, Iwata K, Soejima H, Kamimura S, Shijo H, Yun K. In situ detection of insulin-like growth factor II (IGF2) and H19 gene expression in hepatocellular carcinoma. J Hum Genet 1998; 43: 49-53.
33. Matouk IJ, DeGroot N, Mezan S, Ayesh S, Abu-lail R, Hochberg A et al. The H19 non-coding RNA is essential for human tumor growth. PLoS ONE 2007; 2: e845.
34. Braeuning A, Jaworski M, Schwarz M, Kohle C. Rex3 (reduced in expression 3) as a new tumor marker in mouse hepatocarcinogenesis. Toxicology 2006; 227: 127-135.
35. Inokuchi-Shimizu S, Park EJ, Roh YS, Yang L, Zhang B, Song J et al. TAK1-mediated autophagy and fatty acid oxidation prevent hepatosteatosis and tumorigenesis. J Clin Invest 2014; 124: 3566-3578.
36. Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science 2011; 332: 1519-1523.
37. Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest 2004; 114: 147-152.
38. Sabio G, Cavanagh-Kyros J, Ko HJ, Jung DY, Gray S, Jun JY et al. Prevention of steatosis by hepatic JNK1. Cell Metab 2009; 10: 491-498.
39. Momcilovic M, Hong SP, Carlson M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem 2006; 281: 25336-25343.
40. Kajino T, Omori E, Ishii S, Matsumoto K, Ninomiya-Tsuji J. TAK1 MAPK kinase kinase mediates transforming growth factor-signaling by targeting SnoN oncoprotein for degradation. J Biol Chem 2007; 282: 9475-9481.
41. Takaesu G, Kishida S, Hiyama A, Yamaguchi K, Shibuya H, Irie K et al. TAB2, a novel adaptor protein, mediates activation of TAK1 MAPKKK by linking TAK1 to TRAF6 in the IL-1 signal transduction pathway. Mol Cell 2000; 5: 649-658.
42. Kishimoto K, Matsumoto K, Ninomiya-Tsuji J. TAK1 mitogen-activated protein kinase kinase kinase is activated by autophosphorylation within its activation loop. J Biol Chem 2000; 275: 7359-7364.
43. Scholz R, Sidler CL, Thali RF, Winssinger N, Cheung PC, Neumann D. Autoactivation of transforming growth factor-activated kinase 1 is a sequential bimolecular process. J Biol Chem 2010; 285: 25753-25766.
44. Kamisuki S, Mao Q, Abu-Elheiga L, Gu Z, Kugimiya A, Kwon Y et al. A small molecule that blocks fat synthesis by inhibiting the activation of SREBP. Chem Biol 2009; 16: 882-892.
45. Glass CK, Olefsky JM. Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab 2012; 15: 635-645.
46. Zhang HH, Halbleib M, Ahmad F, Manganiello VC, Greenberg AS. Tumor necrosis factor-stimulates lipolysis in differentiated human adipocytes through activation of extracellular signal-related kinase and elevation of intracellular cAMP. Diabetes 2002; 51: 2929-2935.
47. Fon Tacer K, Kuzman D, Seliskar M, Pompon D, Rozman D. TNF-interferes with lipid homeostasis and activates acute and proatherogenic processes. Physiol Genomics 2007; 31: 216-227.
48. Oliner JD, Andresen JM, Hansen SK, Zhou SL, Tjian R. SREBP transcriptional activity is mediated through an interaction with the CREB-binding protein. Genes Dev 1996; 10: 2903-2911.
49. Osborne TF. Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J Biol Chem 2000; 275: 32379-32382.
50. Junttila MR, Li SP, Westermarck J. Phosphatase-mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J 2008; 22: 954-965.
51. Kim SI, Kwak JH, Wang L, Choi ME. Protein phosphatase 2A is a negative regulator of transforming growth factor-1-induced TAK1 activation in mesangial cells. J Biol Chem 2008; 283: 10753-10763.
52. Kajino T, Ren H, Iemura S, Natsume T, Stefansson B, Brautigan DL et al. Protein phosphatase 6 down-regulates TAK1 kinase activation in the IL-1 signaling pathway. J Biol Chem 2006; 281: 39891-39896.
53. Shimomura I, Hammer RE, Richardson JA, Ikemoto S, Bashmakov Y, Goldstein JL et al. Insulin resistance and diabetes mellitus in transgenic mice expressing nuclear SREBP-1c in adipose tissue: model for congenital generalized lipodystrophy. Genes Dev 1998; 12: 3182-3194.
54. Nakayama H, Otabe S, Ueno T, Hirota N, Yuan X, Fukutani T et al. Transgenic mice expressing nuclear sterol regulatory element-binding protein 1c in adipose tissue exhibit liver histology similar to nonalcoholic steatohepatitis. Metabolism 2007; 56: 470-475.
55. Takahashi Y, Soejima Y, Fukusato T. Animal models of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. World J Gastroenterol 2012; 18: 2300-2308.
56. Campbell JS, Hughes SD, Gilbertson DG, Palmer TE, Holdren MS, Haran AC et al. Platelet-derived growth factor C induces liver fibrosis, steatosis, and hepatocellular carcinoma. Proc Natl Acad Sci USA 2005; 102: 3389-3394.
57. Heindryckx F, Colle I, Van Vlierberghe H. Experimental mouse models for hepatocellular carcinoma research. Int J Exp Pathol 2009; 90: 367-386.
58. Farazi PA, DePinho RA. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer 2006; 6: 674-687.
59. Zhang L, Yang F, Yuan JH, Yuan SX, Zhou WP, Huo XS et al. Epigenetic activation of the MiR-200 family contributes to H19-mediated metastasis suppression in hepatocellular carcinoma. Carcinogenesis 2013; 34: 577-586.
60. 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.
61. Postic C, Shiota M, Niswender KD, Jetton TL, Chen Y, Moates JM et al. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic cell-specific gene knock-outs using Cre recombinase. J Biol Chem 1999; 274: 305-315.
62. Pfeffer K, Matsuyama T, Kundig TM, Wakeham A, Kishihara K, Shahinian A et al. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 1993; 73: 457-467.
63. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, Matsumoto K. The kinase TAK1 can activate the NIK-IB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 1999; 398: 252-256.
64. Toth JI, Datta S, Athanikar JN, Freedman LP, Osborne TF. Selective coactivator interactions in gene activation by SREBP-1a and-1c. Mol Cell Biol 2004; 24: 8288-8300.
65. Hua X, Nohturfft A, Goldstein JL, Brown MS. Sterol resistance in CHO cells traced to point mutation in SREBP cleavage-activating protein. Cell 1996; 87: 415-426.
66. Uemura N, Kajino T, Sanjo H, Sato S, Akira S, Matsumoto K et al. TAK1 is a component of the Epstein-Barr virus LMP1 complex and is essential for activation of JNK but not of NF-B. J Biol Chem 2006; 281: 7863-7872.
67. Morioka S, Omori E, Kajino T, Kajino-Sakamoto R, Matsumoto K, Ninomiya-Tsuji J. TAK1 kinase determines TRAIL sensitivity by modulating reactive oxygen species and cIAP. Oncogene 2009; 28: 2257-2265.
68. 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.
69. Smith JR, Osborne TF, Goldstein JL, Brown MS. Identification of nucleotides responsible for enhancer activity of sterol regulatory element in low density lipoprotein receptor gene. J Biol Chem 1990; 265: 2306-2310.
70. Ringseis R, Rauer C, Rothe S, Gessner DK, Schutz LM, Luci S et al. Sterol regulatory element-binding proteins are regulators of the NIS gene in thyroid cells. Mol Endocrinol 2013; 27: 781-800.