Hepatic steatosis exacerbated by endoplasmic reticulum stress-mediated downregulation of FXR in aging mice

Journal of Hepatology

Volumn 60, Issue 4, 2014, Pages 847-854

  Xiong, Xuelian ^a   Wang, Xiaolin ^a   Lu, Yan ^a   Wang, E ^a   Zhang, Zhijian ^a   Yang, Jian ^a   Zhang, Huijie ^a   Li, Xiaoying ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Shanghai Institute of Immunology   (China)

Author keywords

Aging; Endoplasmic reticulum stress; Farnesoid X receptor; Non alcoholic fatty liver disease

Indexed keywords

FARNESOID X RECEPTOR; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; TRIACYLGLYCEROL; CELL RECEPTOR; FARNESOID X-ACTIVATED RECEPTOR; HNF1A PROTEIN, MOUSE; TRANSCRIPTOME;

ADULT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL ACTIVATION; CONTROLLED STUDY; DISEASE EXACERBATION; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; FATTY LIVER; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; LIPID METABOLISM; LIVER CELL; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; LIPOGENESIS; LIVER; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY;

AGING; ANIMALS; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; FEMALE; HEPATOCYTE NUCLEAR FACTOR 1-ALPHA; LIPOGENESIS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NON-ALCOHOLIC FATTY LIVER DISEASE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSCRIPTOME; TRIGLYCERIDES;

EID: 84896388318     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2013.12.003     Document Type: Article

References (43)

1. J.C. Cohen, J.D. Horton, and H.H. Hobbs Human fatty liver disease: old questions and new insights Science 332 2011 1519 1523
2. M.G. Cree, B.R. Newcomer, C.S. Katsanos, M. Sheffield-Moore, D. Chinkes, and A. Aarsland et al. Intramuscular and liver triglycerides are increased in the elderly J Clin Endocrinol Metab 89 2004 3864 3871
3. J.G. Fan, J. Zhu, X.J. Li, L. Chen, L. Li, and F. Dai et al. Prevalence of and risk factors for fatty liver in a general population of Shanghai, China J Hepatol 43 2005 508 514
4. M. Hilden, P. Christoffersen, E. Juhl, and J.B. Dalgaard Liver histology in a 'normal' population - examinations of 503 consecutive fatal traffic casualties Scand J Gastroenterol 12 1977 593 597
5. G. Targher, L. Bertolini, R. Padovani, S. Rodella, R. Tessari, and L. Zenari et al. Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients Diabetes Care 30 2007 1212 1218
6. J. Yang, J.L. Goldstein, R.E. Hammer, Y.A. Moon, M.S. Brown, and J.D. Horton Decreased lipid synthesis in livers of mice with disrupted Site-1 protease gene Proc Natl Acad Sci U S A 98 2001 13607 13612
7. J.D. Horton, J.L. Goldstein, and M.S. Brown SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver J Clin Invest 109 2002 1125 1131
8. I. Shimomura, Y. Bashmakov, and J.D. Horton Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus J Biol Chem 274 1999 30028 30032
9. M. Watanabe, S.M. Houten, L. Wang, A. Moschetta, D.J. Mangelsdorf, and R.A. Heyman et al. Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c J Clin Invest 113 2004 1408 1418
10. T. Yoshikawa, H. Shimano, M. Amemiya-Kudo, N. Yahagi, A.H. Hasty, and T. Matsuzaka et al. Identification of liver X receptor-retinoid X receptor as an activator of the sterol regulatory element-binding protein 1c gene promoter Mol Cell Biol 21 2001 2991 3000
11. T.T. Lu, M. Makishima, J.J. Repa, K. Schoonjans, T.A. Kerr, and J. Auwerx et al. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors Mol Cell 6 2000 507 515
12. C.J. Sinal, M. Tohkin, M. Miyata, J.M. Ward, G. Lambert, and F.J. Gonzalez Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis Cell 102 2000 731 744
13. G. Xu, L.X. Pan, H. Li, B.M. Forman, S.K. Erickson, and S. Shefer et al. Regulation of the farnesoid X receptor (FXR) by bile acid flux in rabbits J Biol Chem 277 2002 50491 50496
14. Y. Zhang, F.Y. Lee, G. Barrera, H. Lee, C. Vales, and F.J. Gonzalez et al. Activation of the nuclear receptor FXR improves hyperglycemia and hyperlipidemia in diabetic mice Proc Natl Acad Sci U S A 103 2006 1006 1011
15. S. Cipriani, A. Mencarelli, G. Palladino, and S. Fiorucci FXR activation reverses insulin resistance and lipid abnormalities and protects against liver steatosis in Zucker (fa/fa) obese rats J Lipid Res 51 2010 771 784
16. Y. Ma, Y. Huang, L. Yan, M. Gao, and D. Liu Synthetic FXR agonist GW4064 prevents diet-induced hepatic steatosis and insulin resistance Pharm Res 30 2013 1447 1457
17. Y. Lu, Z. Ma, Z. Zhang, X. Xiong, X. Wang, and H. Zhang et al. Yin Yang 1 promotes hepatic steatosis through repression of farnesoid X receptor in obese mice Gut 63 2014 170 178
18. Z.X. Yang, W. Shen, and H. Sun Effects of nuclear receptor FXR on the regulation of liver lipid metabolism in patients with non-alcoholic fatty liver disease Hepatol Int 4 2010 741 748
19. D. Duran-Sandoval, G. Mautino, G. Martin, F. Percevault, O. Barbier, and J.C. Fruchart et al. Glucose regulates the expression of the farnesoid X receptor in liver Diabetes 53 2004 890 898
20. J.J. Repa, G. Liang, J. Ou, Y. Bashmakov, J.M. Lobaccaro, and I. Shimomura et al. Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta Genes Dev 14 2000 2819 2830
21. T. Kanayama, M. Arito, K. So, S. Hachimura, J. Inoue, and R. Sato Interaction between sterol regulatory element-binding proteins and liver receptor homolog-1 reciprocally suppresses their transcriptional activities J Biol Chem 282 2007 10290 10298
22. N. Naidoo ER and aging-Protein folding and the ER stress response Ageing Res Rev 8 2009 150 159
23. M.K. Brown, and N. Naidoo The endoplasmic reticulum stress response in aging and age-related diseases Front Physiol 3 2012 263
24. H.L. Kammoun, H. Chabanon, I. Hainault, S. Luquet, C. Magnan, and T. Koike et al. GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice J Clin Invest 119 2009 1201 1215
25. Q. Xie, V.I. Khaoustov, C.C. Chung, J. Sohn, B. Krishnan, and D.E. Lewis et al. Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation Hepatology 36 2002 592 601
26. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, and R.O. Smith et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 2006 1137 1140
27. S.D. Miller, C.M. Greene, C. McLean, M.W. Lawless, C.C. Taggart, and S.J. O'Neill et al. Tauroursodeoxycholic acid inhibits apoptosis induced by Z alpha-1 antitrypsin via inhibition of Bad Hepatology 46 2007 496 503
28. M. Pontoglio, J. Barra, M. Hadchouel, A. Doyen, C. Kress, and J.P. Bach et al. Hepatocyte nuclear factor 1 inactivation results in hepatic dysfunction, phenylketonuria, and renal Fanconi syndrome Cell 84 1996 575 585
29. D.Q. Shih, M. Bussen, E. Sehayek, M. Ananthanarayanan, B.L. Shneider, and F.J. Suchy et al. Hepatocyte nuclear factor-1alpha is an essential regulator of bile acid and plasma cholesterol metabolism Nat Genet 27 2001 375 382
30. F. Urano, X. Wang, A. Bertolotti, Y. Zhang, P. Chung, and H.P. Harding et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 2000 664 666
31. F. Capel, G. Rolland-Valognes, C. Dacquet, M. Brun, M. Lonchampt, and A. Ktorza et al. Analysis of sterol-regulatory element-binding protein 1c target genes in mouse liver during aging and high-fat diet J Nutrigenet Nutrigenomics 6 2013 107 122
32. A. Kuhla, T. Blei, R. Jaster, and B. Vollmar Aging is associated with a shift of fatty metabolism toward lipogenesis J Gerontol A Biol Sci Med Sci 66 2011 1192 1200
33. E. Sanguino, N. Roglans, M. Alegret, R.M. Sánchez, M. Vázquez-Carrera, and J.C. Laguna Atorvastatin reverses age-related reduction in rat hepatic PPARalpha and HNF-4 Br J Pharmacol 145 2005 853 861
34. A. Purushotham, Q. Xu, J. Lu, J.F. Foley, X. Yan, and D.H. Kim et al. Hepatic deletion of SIRT1 decreases hepatocyte nuclear factor 1α/farnesoid X receptor signaling and induces formation of cholesterol gallstones in mice Mol Cell Biol 32 2012 1226 1236
35. S. Wang, and R.J. Kaufman The impact of the unfolded protein response on human disease J Cell Biol 197 2012 857 867
36. R.Y. Hampton ER stress response: getting the UPR hand on misfolded proteins Curr Biol 10 2000 R518 R521
37. U. Ozcan, Q. Cao, E. Yilmaz, A.H. Lee, N.N. Iwakoshi, and E. Ozdelen et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461
38. N. Hosogai, A. Fukuhara, K. Oshima, Y. Miyata, S. Tanaka, and K. Segawa et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation Diabetes 56 2007 901 911
39. D.T. Rutkowski, J. Wu, S.H. Back, M.U. Callaghan, S.P. Ferris, and J. Iqbal et al. UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators Dev Cell 15 2008 829 840
40. R. Ye, D.Y. Jung, J.Y. Jun, J. Li, S. Luo, and H.J. Ko et al. Grp78 heterozygosity promotes adaptive unfolded protein response and attenuates diet-induced obesity and insulin resistance Diabetes 59 2010 6 16
41. A.H. Lee, E.F. Scapa, D.E. Cohen, and L.H. Glimcher Regulation of hepatic lipogenesis by the transcription factor XBP1 Science 320 2008 1492 1496
42. K. Zhang, S. Wang, J. Malhotra, J.R. Hassler, S.H. Back, and G. Wang et al. The unfolded protein response transducer IRE1alpha prevents ER stress-induced hepatic steatosis EMBO J 30 2011 1357 1375
43. K. Yamamoto, K. Takahara, S. Oyadomari, T. Okada, T. Sato, and A. Harada et al. Induction of liver steatosis and lipid droplet formation in ATF6alpha-knockout mice burdened with pharmacological endoplasmic reticulum stress Mol Biol Cell 21 2010 2975 2986