Liver-specific gene inactivation of the transcription factor ATF4 alleviates alcoholic liver steatosis in mice

Journal of Biological Chemistry

Volumn 291, Issue 35, 2016, Pages 18536-18546

  Li, Kai ^a   Xiao, Yuzhong ^a   Yu, Junjie ^a   Xia, Tingting ^a   Liu, Bin ^a   Guo, Yajie ^a   Deng, Jiali ^a   Chen, Shanghai ^a   Wang, Chunxia ^a   Guo, Feifan ^a  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; ETHANOL; FATTY ACIDS; MAMMALS; TRANSCRIPTION; TRANSCRIPTION FACTORS;

ACTIVATING TRANSCRIPTION FACTOR; AMP-ACTIVATED PROTEIN KINASE; BIOLOGICAL FUNCTIONS; CARNITINE PALMITOYLTRANSFERASE; FATTY ACID SYNTHASE; HEPATOCYTES; LIVER STEATOSIS; LIVER-SPECIFIC GENES;

ENZYME INHIBITION;

ACTIVATING TRANSCRIPTION FACTOR 4; ALCOHOL; CARNITINE PALMITOYLTRANSFERASE I; FATTY ACID SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PEPTIDES AND PROTEINS; PROTEIN TRB3; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ATF4 PROTEIN, MOUSE; CELL CYCLE PROTEIN; TRB3 PROTEIN, MOUSE;

ALCOHOLIC FATTY LIVER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE INACTIVATION; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; CELL LINE; GENETICS; KNOCKOUT MOUSE; LIVER; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTOR 4; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL CYCLE PROTEINS; CELL LINE; ETHANOL; FATTY LIVER, ALCOHOLIC; HEPATOCYTES; LIVER; MALE; MICE; MICE, KNOCKOUT; ORGAN SPECIFICITY; SIGNAL TRANSDUCTION; TRIGLYCERIDES;

EID: 84984680138     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.726836     Document Type: Article

References (52)

1. Purohit, V., Gao, B., and Song, B. J. (2009) Molecular mechanisms of alcoholic fatty liver. Alcohol. Clin. Exp. Res. 33, 191-205
2. Rasineni, K., and Casey, C. A. (2012) Molecular mechanism of alcoholic fatty liver. Indian J. Pharmacol. 44, 299-303
3. Yin, H., Hu, M., Liang, X., Ajmo, J. M., Li, X., Bataller, R., Odena, G., Stevens, S. M., Jr., and You, M. (2014) Deletion of SIRT1 from hepatocytes in mice disrupts lipin-1 signaling and aggravates alcoholic fatty liver. Gastroenterology 146, 801-811
4. You, M., Fischer, M., Deeg, M. A., and Crabb, D. W. (2002) Ethanol induces fatty acid synthesis pathways by activation of sterol regulatory element-binding protein (SREBP). J. Biol. Chem. 277, 29342-29347
5. Lieber, C. S., and Leo., M. A., Wang, X., and Decarli, L. M. (2008) Effect of chronic alcohol consumption on Hepatic SIRT1 and PGC-1α in rats. Biochem. Biophys. Res. Commun. 370, 44-48
6. You, M., Matsumoto, M., Pacold, C. M., and Cho., W. K., and Crabb, D. W. (2004) The role of AMP-activated protein kinase in the action of ethanol in the liver. Gastroenterology 127, 1798-1808
7. Shen, Z., Liang, X., Rogers, C. Q., Rideout, D., and You, M. (2010) Involvement of adiponectin-SIRT1-AMPK signaling in the protective action of rosiglitazone against alcoholic fatty liver in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G364-G374
8. Hu, M., Wang, F., Li, X., Rogers, C. Q., Liang, X., and Finck., B. N., Mitra, M. S., Zhang, R., Mitchell, D. A., and You, M. (2012) Regulation of hepatic lipin-1 by ethanol: role of AMP-activated protein kinase/sterol regulatory element-binding protein 1 signaling in mice. Hepatology 55, 437-446
9. Winder, W. W., and Hardie, D. G. (1996) Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am. J. Physiol. 270, E299-E304
10. Kudo, N., and Barr., A. J., Barr, R. L., Desai, S., and Lopaschuk, G. D. (1995) High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 5'-AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J. Biol. Chem. 270, 17513-17520
11. Tomita, K., Tamiya, G., Ando, S., Kitamura, N., Koizumi, H., Kato, S., Horie, Y., Kaneko, T., Azuma, T., Nagata, H, Ishii, H., and Hibi, T. (2005) AICAR, an AMPK activator, has protective effects on alcohol-induced fatty liver in rats. Alcohol. Clin. Exp. Res. 29, 240S-245S
12. Bergheim, I., Guo, L., Davis, M. A., and Lambert., J. C., Beier, J. I., Duveau, I., Luyendyk, J. P., and Roth., R. A., and Arteel, G. E. (2006) Metformin prevents alcohol-induced liver injury in the mouse: critical role of plasminogen activator inhibitor-1. Gastroenterology 130, 2099-2112
13. Karpinski, B. A., and Morle., G. D., Huggenvik, J., Uhler, M. D., and Leiden, J. M. (1992) Molecular cloning of human CREB-2: an ATF/CREB transcription factor that can negatively regulate transcription from the cAMP response element. Proc. Natl. Acad. Sci. U.S.A. 89, 4820-4824
14. Vallejo, M., Ron, D., Miller, C. P., and Habener, J. F. (1993) C/ATF, a member of the activating transcription factor family of DNA-binding proteins, dimerizes with CAAT/enhancer-binding proteins and directs their binding to cAMP response elements. Proc. Natl. Acad. Sci. U.S.A. 90, 4679-4683
15. Yang, X., Matsuda, K., Bialek, P., Jacquot, S., and Masuoka., H. C., Schinke, T., Li, L., Brancorsini, S., Sassone-Corsi, P., Townes, T. M., Hanauer, A., and Karsenty, G. (2004) ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry syndrome. Cell 117, 387-398
16. Lange, P. S., and Chavez., J. C., Pinto, J. T., Coppola, G., Sun, C. W., and Townes., T. M., Geschwind, D. H, and Ratan, R. R. (2008) ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J. Exp. Med. 205, 1227-1242
17. Wang, C, Li, H, Meng, Q., Du, Y., Xiao, F., Zhang, Q., Yu, J., Li, K., Chen, S., Huang, Z., Liu, B., and Guo, F. (2014) ATF4 deficiency protects hepatocytes from oxidative stress via inhibiting CYP2E1 expression. J. Cell Mol. Med. 18, 80-90
18. Li, H., Meng, Q., Xiao, F., Chen, S., Du, Y., Yu, J., Wang, C, and Guo, F. (2011) ATF4 deficiency protects mice from high-carbohydrate-diet-induced liver steatosis. Biochem. J. 438, 283-289
19. Wang, C, Huang, Z., Du, Y., Cheng, Y., Chen, S., and Guo, F. (2010) ATF4 regulates lipid metabolism and thermogenesis. Cell Res. 20, 174-184
20. Zhang, Q., Yu, J., Liu, B., Lv, Z., Xia, T., Xiao, F., Chen, S., and Guo, F. (2013) Central activating transcription factor 4 (ATF4) regulates hepatic insulin resistance in mice via S6K1 signaling and the vagus nerve. Diabetes 62, 2230-2239
21. Xiao, G., Zhang, T., Yu, S., Lee, S., Calabuig-Navarro, V., Yamauchi, J., Ringquist, S., and Dong, H. H. (2013) ATF4 protein deficiency protects against high fructose-induced hypertriglyceridemia in mice. J. Biol. Chem. 288, 25350-25361
22. Magne, L., Blanc, E., Legrand, B., Lucas, D., Barouki, R., Rouach, H, and Garlatti, M. (2011) ATF4 and the integrated stress response are induced by ethanol and cytochrome P450 2E1 in human hepatocytes. J. Hepatol. 54, 729-737
23. Chen, Y., Gao, H, Yin, Q., Chen, L., Dong, P., Zhang, X., and Kang, J. (2013) ER stress activating ATF4/CHOP-TNF-α signaling pathway contributes to alcohol-induced disruption of osteogenic lineage of multipotential mesenchymal stem cell. Cell Physiol. Biochem. 32, 743-754
24. Sun, Q., Zhong, W., Zhang, W., Li, Q., Sun, X., Tan, X., Sun, X., Dong, D., and Zhou, Z. (2015) Zinc deficiency mediates alcohol-induced apoptotic cell death in the liver of rats through activating ER and mitochondrial cell death pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 308, G757-G766
25. Carraro, V., Maurin, A. C, Lambert-Langlais, S., Averous, J., Chaveroux, C., Parry, L., Jousse, C, Ord, D., Ord, T., Fafournoux, P., and Bruhat, A. (2010) Amino acid availability controls TRB3 transcription in liver through the GCN2/eIF2α/ATF4 pathway. PLoS One 5, e15716
26. Li, K., Zhang, J., Yu, J., Liu, B., Guo, Y., Deng, J., Chen, S., Wang, C, and Guo, F. (2015) MicroRNA-214 suppresses gluconeogenesis by targeting activating transcriptional factor 4. J. Biol. Chem. 290, 8185-8195
27. Kahn, B. B., Alquier, T., Carling, D., and Hardie, D. G. (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. CellMetab. 1, 15-25
28. Browning, J. D., and Horton, J. D. (2004) Molecular mediators of hepatic steatosis and liver injury. J. Clin. Invest. 114, 147-152
29. Jousse, C, Deval, C, Maurin, A. C, Parry, L., Chérasse, Y., Chaveroux, C, Lefloch, R., Lenormand, P., Bruhat, A., and Fafournoux, P. (2007) TRB3 inhibits the transcriptional activation of stress-regulated genes by a negative feedback on the ATF4 pathway. J. Biol. Chem. 282, 15851-15861
30. Ord, D., Meerits, K., and Ord, T. (2007) TRB3 protects cells against the growth inhibitory and cytotoxic effect of ATF4. Exp. Cell Res. 313, 3556-3567
31. Yao, X. H., and Nyomba, B. L. (2008) Hepatic insulin resistance induced by prenatal alcohol exposure is associated with reduced PTEN and TRB3 acetylation in adult rat offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1797-R1806
32. 2+/calmodulin-dependent protein kinase kinase-β acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2, 21-33
33. Du, K., Herzig, S., Kulkarni, R. N., and Montminy, M. (2003) TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300, 1574-1577
34. Chen, G., Ma, C, and Bower., K. A., Shi, X., Ke, Z., and Luo, J. (2008) Ethanol promotes endoplasmic reticulum stress-induced neuronal death: involvement of oxidative stress. J. Neurosci. Res. 86, 937-946
35. Xu, F., and Wang., Y. L., Chang, J. J., Du, S. C, Diao, L., Jiang, N., Wang, H. J., Ma, D., and Zhang, J. (2014) Mammalian sterile 20-like kinase 1/2 inhibits the Wnt/β-catenin signalling pathway by directly binding casein kinase 1e. Biochem. J. 458, 159-169
36. Yoshizawa, T., Hinoi, E., Jung, D. Y., Kajimura, D., Ferron, M., Seo, J., Graff, J. M., and Kim., J. K., and Karsenty, G. (2009) The transcription factor ATF4 regulates glucose metabolism in mice through its expression in osteoblasts. J. Clin. Invest. 119, 2807-2817
37. Malhi, H, and Kaufman, R. J. (2011) Endoplasmic reticulum stress in liver disease. J. Hepatol. 54, 795-809
38. García-Villafranca, J., Guillen, A., and Castro, J. (2008) Ethanol consumption impairs regulation of fatty acid metabolism by decreasing the activity of AMP-activated protein kinase in rat liver. Biochimie 90, 460-466
39. Bi, L., Jiang, Z., and Zhou, J. (2015) The role of lipin-1 in the pathogenesis of alcoholic fatty liver. Alcohol Alcohol. 50, 146-151
40. Jiang, Z., Zhou, J., Zhou, D., Zhu, Z., Sun, L., and Nanji, A. A. (2015) The adiponectin-SIRT1-AMPK pathway in alcoholic fatty liver disease in the rat. Alcohol. Clin. Exp. Res. 39, 424-433
41. Zhu, S., Ma, L., Wu, Y., Ye, X., Zhang, T., Zhang, Q., Rasoul, L. M., Liu, Y., Guo, M., Zhou, B., Ren, G., and Li, D. (2014) FGF21 treatment ameliorates alcoholic fatty liver through activation of AMPK-SIRT1 pathway. Acta Biochim. Biophys. Sin. 46, 1041-1048
42. He, L., and Simmen., F. A., Mehendale, H. M., Ronis, M. J., and Badger, T. M. (2006) Chronic ethanol intake impairs insulin signaling in rats by disrupting Akt association with the cell membrane: role of TRB3 in inhibition of Akt/protein kinase B activation. J. Biol. Chem. 281, 11126-11134
43. Koh, H. J., and Arnolds., D. E., Fujii, N., Tran, T. T., and Rogers., M. J., Jessen, N., Li, Y., Liew, C. W., and Ho., R. C., Hirshman, M. F., Kulkarni, R. N., and Kahn., C. R., and Goodyear, L. J. (2006) Skeletal muscle-selective knockout of LKB1 increases insulin sensitivity, improves glucose homeostasis, and decreases TRB3. Mol. Cell Biol. 26, 8217-8227
44. Vara, D., Salazar, M., Olea-Herrero, N., Guzmán, M., Velasco, G., and Díaz-Laviada, I. (2011) Anti-tumoral action of cannabinoids on hepatocellular carcinoma: role of AMPK-dependent activation of autophagy. Cell Death Differ. 18, 1099-1111
45. Wang, D., and Sul, H. S. (1998) Insulin stimulation of the fatty acid synthase promoter is mediated by the phosphatidylinositol 3-kinase pathway. Involvement of protein kinase B/Akt. J. Biol. Chem. 273, 25420-25426
46. Whitney, M. L., and Jefferson., L. S., and Kimball, S. R. (2009) ATF4is necessary and sufficient for ER stress-induced upregulation of REDD1 expression. Biochem. Biophys. Res. Commun. 379, 451-455
47. Ji, C. (2014) New insights into the pathogenesis of alcohol-induced ER stress and liver diseases. Int. J. Hepatol. 2014, 513787
48. Bertola, A., Mathews, S., Ki, S. H., Wang, H., and Gao, B. (2013) Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat. Protoc. 8, 627-637
49. Wang, Q., Jiang, L., Wang, J., Li, S., Yu, Y., You, J., Zeng, R., Gao, X., Rui, L., Li, W., and Liu, Y. (2009) Abrogation of hepatic ATP-citrate lyase protects against fatty liver and ameliorates hyperglycemia in leptin receptor-deficient mice. Hepatology 49, 1166-1175
50. Yu, J., Xiao, F., Guo, Y., Deng, J., Liu, B., Zhang, Q., Li, K., Wang, C., Chen, S., and Guo, F. (2015) Hepatic phosphoserine aminotransferase 1 regulates insulin sensitivity in mice via Tribbles homolog 3. Diabetes 64, 1591-1602
51. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509
52. Xiao, Y., Liu, H., Yu, J., Zhao, Z., Xiao, F., Xia, T., Wang, C., Li, K., Deng, J., Guo, Y., Chen, S., Chen, Y., and Guo, F. (2016) Activation of ERK1/2 ameliorates liver steatosis in leptin receptor-deficient (db/db) mice via stimulating ATG7-dependent autophagy. Diabetes 65, 393-405