REV-ERBα Activates C/EBP Homologous Protein to Control Small Heterodimer Partner–Mediated Oscillation of Alcoholic Fatty Liver

American Journal of Pathology

Volumn 186, Issue 11, 2016, Pages 2909-2920

  Yang, Zhihong ^a,b   Tsuchiya, Hiroyuki ^c   Zhang, Yuxia ^d   Lee, Sangmin ^a   Liu, Chune ^a   Huang, Yi ^a,e   Vargas, Gymar M ^a   Wang, Li ^a,b,e,f  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^e WENZHOU MEDICAL UNIVERSITY   (China)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACTIN; ACTIVATING TRANSCRIPTION FACTOR 4; ALANINE AMINOTRANSFERASE; ALCOHOL; ASPARTATE AMINOTRANSFERASE; BETA ACTIN; CCAAT ENHANCER BINDING PROTEIN; CELL NUCLEUS RECEPTOR; FATTY ACID SYNTHASE; GENOMIC DNA; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HETERODIMER; MALTOSE; NUCLEAR RECEPTOR NR1D1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SHORT HAIRPIN RNA; SMALL HETERODIMER PARTNER NUCLEAR RECEPTOR; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRANSLATION INITIATION FACTOR 2 ALPHA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CELL RECEPTOR; NR1D1 PROTEIN, MOUSE; NUCLEAR RECEPTOR SUBFAMILY 0, GROUP B, MEMBER 2; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ALCOHOLIC FATTY LIVER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; GENETIC TRANSCRIPTION; LIPID LIVER LEVEL; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; MOUSE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; UPREGULATION; WILD TYPE MOUSE; ANIMAL; C57BL MOUSE; DISEASE MODEL; FATTY LIVER, ALCOHOLIC; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LIVER; MALE; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ETHANOL; FATTY LIVER, ALCOHOLIC; GENE EXPRESSION REGULATION; HUMANS; LIPID METABOLISM; LIPOGENESIS; LIVER; MALE; MICE; MICE, INBRED C57BL; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; PROMOTER REGIONS, GENETIC; RECEPTORS, CYTOPLASMIC AND NUCLEAR; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTION FACTOR CHOP; UP-REGULATION;

EID: 84994879711     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2016.07.014     Document Type: Article

References (37)

1. 1 Williams, J.A., Manley, S., Ding, W.X., New advances in molecular mechanisms and emerging therapeutic targets in alcoholic liver diseases. World J Gastroenterol 20 (2014), 12908–12933.
2. 2 You, M., Jogasuria, A., Lee, K., Wu, J., Zhang, Y., Lee, Y.K., Taylor, C., Sadana, P., Signal transduction mechanisms of alcoholic fatty liver disease: emerging role of lipin-1. Curr Mol Pharmacol, 2015 [Epub ahead of print] doi: 10.2174/1874467208666150817112109.
3. 3 Ji, C., Mechanisms of alcohol-induced endoplasmic reticulum stress and organ injuries. Biochem Res Int, 2012, 2012, 216450.
4. 4 Malhi, H., Kaufman, R.J., Endoplasmic reticulum stress in liver disease. J Hepatol 54 (2011), 795–809.
5. 5 Tsuchiya, H., da Costa, K.A., Lee, S., Renga, B., Jaeschke, H., Yang, Z., Orena, S.J., Goedken, M.J., Zhang, Y., Kong, B., Lebofsky, M., Rudraiah, S., Smalling, R., Guo, G., Fiorucci, S., Zeisel, S.H., Wang, L., Interactions between nuclear receptor SHP and FOXA1 maintain oscillatory homocysteine homeostasis in mice. Gastroenterology 148 (2015), 1012–1023.e14.
6. 6 Rudraiah, S., Zhang, X., Wang, L., Nuclear receptors as therapeutic targets in liver disease: are we there yet?. Annu Rev Pharmacol Toxicol 56 (2016), 605–626.
7. 7 Zhang, Y., Hagedorn, C.H., Wang, L., Role of nuclear receptor SHP in metabolism and cancer. Biochim Biophys Acta 1812 (2011), 893–908.
8. 8 Zhou, T., Zhang, Y., Macchiarulo, A., Yang, Z., Cellanetti, M., Coto, E., Xu, P., Pellicciari, R., Wang, L., Novel polymorphisms of nuclear receptor SHP associated with functional and structural changes. J Biol Chem 285 (2010), 24871–24881.
9. 9 Wang, L., Lee, Y.K., Bundman, D., Han, Y., Thevananther, S., Kim, C.S., Chua, S.S., Wei, P., Heyman, R.A., Karin, M., Moore, D.D., Redundant pathways for negative feedback regulation of bile acid production. Dev Cell 2 (2002), 721–731.
10. 10 Zhang, Y., Xu, N., Xu, J., Kong, B., Copple, B., Guo, G.L., Wang, L., E2F1 is a novel fibrogenic gene that regulates cholestatic liver fibrosis through the Egr-1/SHP/EID1 network. Hepatology 60 (2014), 919–930.
11. 11 Huang, J., Iqbal, J., Saha, P.K., Liu, J., Chan, L., Hussain, M.M., Moore, D.D., Wang, L., Molecular characterization of the role of orphan receptor small heterodimer partner in development of fatty liver. Hepatology 46 (2007), 147–157.
12. 12 Pan, X., Zhang, Y., Wang, L., Hussain, M.M., Diurnal regulation of MTP and plasma triglyceride by CLOCK is mediated by SHP. Cell Metab 12 (2010), 174–186.
13. 13 Wang, L., Liu, J., Saha, P., Huang, J., Chan, L., Spiegelman, B., Moore, D.D., The orphan nuclear receptor SHP regulates PGC-1alpha expression and energy production in brown adipocytes. Cell Metab 2 (2005), 227–238.
14. 14 Lee, S.M., Zhang, Y., Tsuchiya, H., Smalling, R., Jetten, A.M., Wang, L., Small heterodimer partner/neuronal PAS domain protein 2 axis regulates the oscillation of liver lipid metabolism. Hepatology 61 (2015), 497–505.
15. 15 Bertola, A., Mathews, S., Ki, S.H., Wang, H., Gao, B., Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat Protoc 8 (2013), 627–637.
16. 16 Zhang, Y., Liu, C., Barbier, O., Smalling, R., Tsuchiya, H., Lee, S., Delker, D., Zou, A., Hagedorn, C.H., Wang, L., Bcl2 is a critical regulator of bile acid homeostasis by dictating Shp and lncRNA H19 function. Sci Rep, 6, 2016, 20559.
17. 17 Yang, Z., Zhang, Y., Wang, L., A feedback inhibition between miRNA-127 and TGFbeta/c-Jun cascade in HCC cell migration via MMP13. PLoS One, 8, 2013, e65256.
18. 18 Chen, P., Miyamoto, Y., Mazagova, M., Lee, K.C., Eckmann, L., Schnabl, B., Microbiota protects mice against acute alcohol-induced liver injury, alcoholism. Clin Exp Res 39 (2015), 2313–2323.
19. 19 Roh, Y.S., Zhang, B., Loomba, R., Seki, E., TLR2 and TLR9 contribute to alcohol-mediated liver injury through induction of CXCL1 and neutrophil infiltration. Am J Physiol Gastrointest Liver Physiol 309 (2015), G30–G41.
20. 20 Watanabe, M., Houten, S.M., Wang, L., Moschetta, A., Mangelsdorf, D.J., Heyman, R.A., Moore, D.D., Auwerx, J., Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J Clin Invest 113 (2004), 1408–1418.
21. 21 Ferre, P., Foufelle, F., Hepatic steatosis: a role for de novo lipogenesis and the transcription factor SREBP-1c, diabetes. Obesity Metab 12:Suppl 2 (2010), 83–92.
22. 22 Purohit, V., Gao, B., Song, B.J., Molecular mechanisms of alcoholic fatty liver, alcoholism. Clin Exp Res 33 (2009), 191–205.
23. 23 Ji, C., New insights into the pathogenesis of alcohol-induced ER stress and liver diseases. Int J Hepatol, 2014, 2014, 513787.
24. 24 Hyoda, K., Hosoi, T., Horie, N., Okuma, Y., Ozawa, K., Nomura, Y., PI3K-Akt inactivation induced CHOP expression in endoplasmic reticulum-stressed cells. Biochem Biophys Res Commun 340 (2006), 286–290.
25. 25 Averous, J., Bruhat, A., Jousse, C., Carraro, V., Thiel, G., Fafournoux, P., Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J Biol Chem 279 (2004), 5288–5297.
26. 26 Harding, H.P., Lazar, M.A., The orphan receptor Rev-ErbA alpha activates transcription via a novel response element. Mol Cell Biol 13 (1993), 3113–3121.
27. 27 Wang, J., Yin, L., Lazar, M.A., The orphan nuclear receptor Rev-erb alpha regulates circadian expression of plasminogen activator inhibitor type 1. J Biol Chem 281 (2006), 33842–33848.
28. 28 Guillaumond, F., Dardente, H., Giguere, V., Cermakian, N., Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J Biol Rhythms 20 (2005), 391–403.
29. 29 Yerian, L., Histopathological evaluation of fatty and alcoholic liver diseases. J Dig Dis 12 (2011), 17–24.
30. 30 Udoh, U.S., Valcin, J.A., Gamble, K.L., Bailey, S.M., The molecular circadian clock and alcohol-induced liver injury. Biomolecules 5 (2015), 2504–2537.
31. 31 Everitt, H., Hu, M., Ajmo, J.M., Rogers, C.Q., Liang, X., Zhang, R., Yin, H., Choi, A., Bennett, E.S., You, M., Ethanol administration exacerbates the abnormalities in hepatic lipid oxidation in genetically obese mice. Am J Physiol Gastrointest Liver Physiol 304 (2013), G38–G47.
32. 32 Datta, S., Wang, L., Moore, D.D., Osborne, T.F., Regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase promoter by nuclear receptors liver receptor homologue-1 and small heterodimer partner: a mechanism for differential regulation of cholesterol synthesis and uptake. J Biol Chem 281 (2006), 807–812.
33. 33 Han, S., Kim, G., Lee, S.K., Kwon, C.H., Gwak, M., Lee, S., Ha, S., Park, C.K., Ko, J.S., Joh, J., Comparison of the tolerance of hepatic ischemia/reperfusion injury in living donors: macrosteatosis versus microsteatosis. Liver Transpl 20 (2014), 775–783.
34. 34 Duez, H., Staels, B., Rev-erb-alpha: an integrator of circadian rhythms and metabolism. J Appl Physiol 107 (2009), 1972–1980.
35. 35 Cho, H., Zhao, X., Hatori, M., Yu, R.T., Barish, G.D., Lam, M.T., Chong, L.W., DiTacchio, L., Atkins, A.R., Glass, C.K., Liddle, C., Auwerx, J., Downes, M., Panda, S., Evans, R.M., Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 485 (2012), 123–127.
36. 36 Bugge, A., Feng, D., Everett, L.J., Briggs, E.R., Mullican, S.E., Wang, F., Jager, J., Lazar, M.A., Rev-erbalpha and Rev-erbbeta coordinately protect the circadian clock and normal metabolic function. Genes Dev 26 (2012), 657–667.
37. 37 Duez, H., van der Veen, J.N., Duhem, C., Pourcet, B., Touvier, T., Fontaine, C., Derudas, B., Bauge, E., Havinga, R., Bloks, V.W., Wolters, H., van der Sluijs, F.H., Vennstrom, B., Kuipers, F., Staels, B., Regulation of bile acid synthesis by the nuclear receptor Rev-erbalpha. Gastroenterology 135 (2008), 689–698.