Repression of the nuclear receptor small heterodimer partner by steatotic drugs and in advanced nonalcoholic fatty liver disease

Molecular Pharmacology

Volumn 87, Issue 4, 2015, Pages 582-594

  Benet, Marta ^a,b   Guzmán, Carla ^a   Pisonero Vaquero, Sandra ^c   García Mediavilla, M Victoria ^b,c   Sánchez Campos, Sonia ^b,c   Martínez Chantar, M Luz ^b,d   Donato, M Teresa ^a,b,e   Castell, José Vicente ^a,b,e   Joverr, Ramiro ^a,b,e  

^a INSTITUTO DE INVESTIGACIÓN SANITARIA DEL HOSPITAL CLÍNICO SAN CARLOS IDISSC   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF LEÓN   (Spain)

^d CIC BIOGUNE   (Spain)

^e UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CELL NUCLEUS RECEPTOR; CYCLOSPORIN A; DOXYCYCLINE; GLYCINE METHYLTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PHOSPHATIDYLINOSITOL 3 KINASE; SMALL HETERODIMER PARTNER; TETRACYCLINE; UNCLASSIFIED DRUG; VALPROIC ACID; CELL RECEPTOR; CYCLOSPORIN; MITOGEN ACTIVATED PROTEIN KINASE 1; NUCLEAR RECEPTOR SUBFAMILY 0, GROUP B, MEMBER 2; THIAZEPINE DERIVATIVE; TIANEPTINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HEPG2 CELL LINE; HUMAN; LIVER CELL; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; CELL CULTURE; CHEMICALLY INDUCED; FATTY LIVER; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE; PROMOTER REGION;

ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-ALPHA; CELLS, CULTURED; CYCLOSPORINE; DOXYCYCLINE; FATTY LIVER; HUMANS; MALE; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; NON-ALCOHOLIC FATTY LIVER DISEASE; PROMOTER REGIONS, GENETIC; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; TETRACYCLINE; THIAZEPINES; TRANSCRIPTION, GENETIC; VALPROIC ACID;

EID: 84923334801     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.114.096313     Document Type: Article

References (62)

1. Aghazadeh S and Yazdanparast R (2010) Inhibition of JNK along with activation of ERK1/2 MAPK pathways improve steatohepatitis among the rats. Clin Nutr 29:381-385.
2. Anstee QM and Goldin RD (2006) Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Pathol 87:1-16.
3. Båvner A, Sanyal S, Gustafsson JA, and Treuter E (2005) Transcriptional corepression by SHP: molecular mechanisms and physiological consequences. Trends Endocrinol Metab 16:478-488.
4. Begriche K, Massart J, Robin MA, Borgne-Sanchez A, and Fromenty B (2011) Druginduced toxicity on mitochondria and lipid metabolism: mechanistic diversity and deleterious consequences for the liver. J Hepatol 54:773-794.
5. Benet M, Lahoz A, Guzmán C, Castell JV, and Jover R (2010) CCAAT/enhancerbinding protein alpha (C/EBPalpha) and hepatocyte nuclear factor 4alpha (HNF4alpha) synergistically cooperate with constitutive androstane receptor to transactivate the human cytochrome P450 2B6 (CYP2B6) gene: application to the development of a metabolically competent human hepatic cell model. J Biol Chem 285:28457-28471.
6. Benet M, Moya M, Donato MT, Lahoz A, Hervás D, Guzmán C, Gómez-Lechón MJ, Castell JV, and Jover R (2014) A simple transcriptomic signature able to predict drug-induced hepatic steatosis. Arch Toxicol 88:967-982.
7. Boulias K, Katrakili N, Bamberg K, Underhill P, Greenfield A, and Talianidis I (2005) Regulation of hepatic metabolic pathways by the orphan nuclear receptor SHP. EMBO J 24:2624-2633.
8. Cai SY, He H, Nguyen T, Mennone A, and Boyer JL (2010) Retinoic acid represses CYP7A1 expression in human hepatocytes and HepG2 cells by FXR/RXR-dependent and independent mechanisms. J Lipid Res 51:2265-2274.
9. Cano A, Buqué X, Martínez-Uña M, Aurrekoetxea I, Menor A, García-Rodríguez JL, Lu SC, Martínez-Chantar ML, Mato JM, and Ochoa B et al. (2011) Methionine adenosyltransferase 1A gene deletion disrupts hepatic very low-density lipoprotein assembly in mice. Hepatology 54:1975-1986.
10. Chanda D, Lee CH, Kim YH, Noh JR, Kim DK, Park JH, Hwang JH, Lee MR, Jeong KH, and Lee IK et al. (2009) Fenofibrate differentially regulates plasminogen activator inhibitor-1 gene expression via adenosine monophosphate-activated protein kinase-dependent induction of orphan nuclear receptor small heterodimer partner. Hepatology 50:880-892.
11. Chiang JY (2003) Bile acid regulation of hepatic physiology: III. Bile acids and nuclear receptors. Am J Physiol Gastrointest Liver Physiol 284:G349-G356.
12. Donato MT, Jover R, and Gómez-Lechón MJ (2013) Hepatic cell lines for drug hepatotoxicity testing: limitations and strategies to upgrade their metabolic competence by gene engineering. Curr Drug Metab 14:946-968.
13. Donato MT, Tolosa L, Jiménez N, Castell JV, and Gómez-Lechón MJ (2012) Highcontent imaging technology for the evaluation of drug-induced steatosis using a multiparametric cell-based assay. J Biomol Screen 17:394-400.
14. Gao D, Wei C, Chen L, Huang J, Yang S, and Diehl AM (2004) Oxidative DNA damage and DNA repair enzyme expression are inversely related in murine models of fatty liver disease. Am J Physiol Gastrointest Liver Physiol 287:G1070-G1077.
15. Garruti G, Wang HH, Bonfrate L, de Bari O, Wang DQ, and Portincasa P (2012) A pleiotropic role for the orphan nuclear receptor small heterodimer partner in lipid homeostasis and metabolic pathways. J Lipids 2012:304292.
16. Gómez-Lechón MJ, López P, Donato T, Montoya A, Larrauri A, Giménez P, Trullenque R, Fabra R, and Castell JV (1990) Culture of human hepatocytes from small surgical liver biopsies. Biochemical characterization and comparison with in vivo. In Vitro Cell Dev Biol 26:67-74.
17. Gómez-Lechón MJ, Jover R, Donato T, Ponsoda X, Rodriguez C, Stenzel KG, Klocke R, Paul D, Guillén I, and Bort R et al. (1998) Long-term expression of differentiated functions in hepatocytes cultured in three-dimensional collagen matrix. J Cell Physiol 177:553-562.
18. Guzmán C, Benet M, Pisonero-Vaquero S, Moya M, García-Mediavilla MV, Martínez-Chantar ML, González-Gallego J, Castell JV, Sánchez-Campos S, and Jover R (2013) The human liver fatty acid binding protein (FABP1) gene is activated by FOXA1 and PPARa; and repressed by C/EBPa: Implications in FABP1 downregulation in nonalcoholic fatty liver disease. Biochim Biophys Acta 1831:803-818.
19. Hart SN, Li Y, Nakamoto K, Subileau EA, Steen D, and Zhong XB (2010) A comparison of whole genome gene expression profiles of HepaRG cells and HepG2 cells to primary human hepatocytes and human liver tissues. Drug Metab Dispos 38:988-994.
20. Hartman HB, Lai K, and Evans MJ (2009) Loss of small heterodimer partner expression in the liver protects against dyslipidemia. J Lipid Res 50:193-203.
21. He N, Park K, Zhang Y, Huang J, Lu S, and Wang L (2008) Epigenetic inhibition of nuclear receptor small heterodimer partner is associated with and regulates hepatocellular carcinoma growth. Gastroenterology 134:793-802.
22. Hoekstra M, Lammers B, Out R, Li Z, Van Eck M, and Van Berkel TJ (2009) Activation of the nuclear receptor PXR decreases plasma LDL-cholesterol levels and induces hepatic steatosis in LDL receptor knockout mice. Mol Pharm 6:182-189.
23. Huang J, Iqbal J, Saha PK, Liu J, Chan L, Hussain MM, Moore DD, and Wang L (2007) Molecular characterization of the role of orphan receptor small heterodimer partner in development of fatty liver. Hepatology 46:147-157.
24. Imajo K, Yoneda M, Kessoku T, Ogawa Y, Maeda S, Sumida Y, Hyogo H, Eguchi Y, Wada K, and Nakajima A (2013) Rodent models of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. Int J Mol Sci 14:21833-21857.
25. Itagaki H, Shimizu K, Morikawa S, Ogawa K, and Ezaki T (2013) Morphological and functional characterization of non-alcoholic fatty liver disease induced by a methioninecholinedeficient diet in C57BL/6 mice. Int J Clin Exp Pathol 6:2683-2696.
26. Jover R, Bort R, Gómez-Lechón MJ, and Castell JV (1998) Re-expression of C/EBP alpha induces CYP2B6, CYP2C9 and CYP2D6 genes in HepG2 cells. FEBS Lett 431:227-230.
27. Kim HI, Koh YK, Kim TH, Kwon SK, Im SS, Choi HS, Kim KS, and Ahn YH (2007) Transcriptional activation of SHP by PPAR-gamma in liver. Biochem Biophys Res Commun 360:301-306.
28. Kohli R, Pan X, Malladi P, Wainwright MS, and Whitington PF (2007) Mitochondrial reactive oxygen species signal hepatocyte steatosis by regulating the phosphatidylinositol 3-kinase cell survival pathway. J Biol Chem 282:21327-21336.
29. Krausova L, Stejskalova L, Wang H, Vrzal R, Dvorak Z, Mani S, and Pavek P (2011) Metformin suppresses pregnane X receptor (PXR)-regulated transactivation of CYP3A4 gene. Biochem Pharmacol 82:1771-1780.
30. Larrain S and Rinella ME (2012) A myriad of pathways to NASH. Clin Liver Dis 16:525-548.
31. Lee HK, Lee YK, Park SH, Kim YS, Park SH, Lee JW, Kwon HB, Soh J, Moore DD, and Choi HS (1998) Structure and expression of the orphan nuclear receptor SHP gene. J Biol Chem 273:14398-14402.
32. Lee JH, Zhou J, and Xie W (2008) PXR and LXR in hepatic steatosis: a new dog and an old dog with new tricks. Mol Pharm 5:60-66.
33. Li T and Chiang JY (2006) Rifampicin induction of CYP3A4 requires pregnane X receptor cross talk with hepatocyte nuclear factor 4alpha and coactivators, and suppression of small heterodimer partner gene expression. Drug Metab Dispos 34:756-764.
34. Lu SC, Alvarez L, Huang ZZ, Chen L, An W, Corrales FJ, Avila MA, Kanel G, and Mato JM (2001) Methionine adenosyltransferase 1A knockout mice are predisposed to liver injury and exhibit increased expression of genes involved in proliferation. Proc Natl Acad Sci USA 98:5560-5565.
35. Martínez-Chantar ML, Corrales FJ, Martínez-Cruz LA, García-Trevijano ER, Huang ZZ, Chen L, Kanel G, Avila MA, Mato JM, and Lu SC (2002) Spontaneous oxidative stress and liver tumors in mice lacking methionine adenosyltransferase 1A. FASEB J 16:1292-1294.
36. Martínez-Chantar ML, Vázquez-Chantada M, Ariz U, Martínez N, Varela M, Luka Z, Capdevila A, Rodríguez J, Aransay AM, and Matthiesen R et al. (2008) Loss of the glycine N-methyltransferase gene leads to steatosis and hepatocellular carcinoma in mice. Hepatology 47:1191-1199.
37. Nakajima T, Kinoshita S, Sasagawa T, Sasaki K, Naruto M, Kishimoto T, and Akira S (1993) Phosphorylation at threonine-235 by a ras-dependent mitogen-activated protein kinase cascade is essential for transcription factor NF-IL6. Proc Natl Acad Sci USA 90:2207-2211.
38. Nerlov C (2008) C/EBPs: recipients of extracellular signals through proteome modulation. Curr Opin Cell Biol 20:180-185.
39. O'Brien PJ, Irwin W, Diaz D, Howard-Cofield E, Krejsa CM, Slaughter MR, Gao B, Kaludercic N, Angeline A, and Bernardi P et al. (2006) High concordance of druginduced human hepatotoxicity with in vitro cytotoxicity measured in a novel cellbased model using high content screening. Arch Toxicol 80:580-604.
40. Park YJ, Qatanani M, Chua SS, LaRey JL, Johnson SA, Watanabe M, Moore DD, and Lee YK (2008) Loss of orphan receptor small heterodimer partner sensitizes mice to liver injury from obstructive cholestasis. Hepatology 47:1578-1586.
41. Pedersen TA, Bereshchenko O, Garcia-Silva S, Ermakova O, Kurz E, Mandrup S, Porse BT, and Nerlov C (2007) Distinct C/EBPalpha motifs regulate lipogenic and gluconeogenic gene expression in vivo. EMBO J 26:1081-1093.
42. Qiao L, MacDougald OA, and Shao J (2006) CCAAT/enhancer-binding protein alpha mediates induction of hepatic phosphoenolpyruvate carboxykinase by p38 mitogenactivated protein kinase. J Biol Chem 281:24390-24397.
43. Ross SE, Erickson RL, Hemati N, and MacDougald OA (1999) Glycogen synthase kinase 3 is an insulin-regulated C/EBPalpha kinase. Mol Cell Biol 19:8433-8441.
44. Ross SE, Radomska HS, Wu B, Zhang P, Winnay JN, Bajnok L, Wright WS, Schaufele F, Tenen DG, and MacDougald OA (2004) Phosphorylation of C/EBPalpha inhibits granulopoiesis. Mol Cell Biol 24:675-686.
45. Sahai A, Pan X, Paul R, Malladi P, Kohli R, and Whitington PF (2006) Roles of phosphatidylinositol 3-kinase and osteopontin in steatosis and aminotransferase release by hepatocytes treated with methionine-choline-deficient medium. Am J Physiol Gastrointest Liver Physiol 291:G55-G62.
46. Seol W, Choi HS, and Moore DD (1996) An orphan nuclear hormone receptor that lacks a DNA binding domain and heterodimerizes with other receptors. Science 272:1336-1339.
47. Shih DQ, Screenan S, Munoz KN, Philipson L, Pontoglio M, Yaniv M, Polonsky KS, and Stoffel M (2001) Loss of HNF-1alpha function in mice leads to abnormal expression of genes involved in pancreatic islet development and metabolism. Diabetes 50:2472-2480.
48. Takahashi Y, Soejima Y, and Fukusato T (2012) Animal models of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. World J Gastroenterol 18:2300-2308.
49. Trauner M (2007) A little orphan runs to fat: the orphan receptor small heterodimer partner as a key player in the regulation of hepatic lipid metabolism. Hepatology 46:1-5.
50. Tsukada J, Yoshida Y, Kominato Y, and Auron PE (2011) The CCAAT/enhancer (C/EBP) family of basic-leucine zipper (bZIP) transcription factors is a multifaceted highly-regulated system for gene regulation. Cytokine 54:6-19.
51. Van Rooyen DM, Larter CZ, Haigh WG, Yeh MM, Ioannou G, Kuver R, Lee SP, Teoh NC, and Farrell GC (2011) Hepatic free cholesterol accumulates in obese, diabetic mice and causes nonalcoholic steatohepatitis. Gastroenterology 141:1393-1403.
52. Varela-Rey M, Martínez-López N, Fernández-Ramos D, Embade N, Calvisi DF, Woodhoo A, Rodríguez J, Fraga MF, Julve J, and Rodríguez-Millán E et al. (2010) Fatty liver and fibrosis in glycine N-methyltransferase knockout mice is prevented by nicotinamide. Hepatology 52:105-114.
53. Wang GL, Iakova P, Wilde M, Awad S, and Timchenko NA (2004) Liver tumors escape negative control of proliferation via PI3K/Akt-mediated block of C/EBP alpha growth inhibitory activity. Genes Dev 18:912-925.
54. Wang L, Han Y, Kim CS, Lee YK, and Moore DD (2003) Resistance of SHP-null mice to bile acid-induced liver damage. J Biol Chem 278:44475-44481.
55. Wang Z, Yao T, and Song Z (2010a) Extracellular signal-regulated kinases 1/2 suppression aggravates transforming growth factor-beta1 hepatotoxicity: a potential mechanism for liver injury in methionine-choline deficient-diet-fed mice. Exp Biol Med (Maywood) 235:1347-1355.
56. Wang Z, Yao T, and Song Z (2010b) Involvement and mechanism of DGAT2 upregulation in the pathogenesis of alcoholic fatty liver disease. J Lipid Res 51:3158-3165.
57. Xu D, Huang XD, Yuan JP, Wu J, Fan Y, Luo HS, and Yang YH (2011) Impaired activation of phosphatidylinositol 3-kinase by leptin is a novel mechanism of hepatic leptin resistance in NAFLD. Hepatogastroenterology 58:1703-1707.
58. Xu JJ, Henstock PV, Dunn MC, Smith AR, Chabot JR, and de Graaf D (2008) Cellular imaging predictions of clinical drug-induced liver injury. Toxicol Sci 105:97-105.
59. Zhang Y, Hagedorn CH, and Wang L (2011) Role of nuclear receptor SHP in metabolism and cancer. Biochim Biophys Acta 1812:893-908.
60. Zhang Y, Soto J, Park K, Viswanath G, Kuwada S, Abel ED, and Wang L (2010) Nuclear receptor SHP, a death receptor that targets mitochondria, induces apoptosis and inhibits tumor growth. Mol Cell Biol 30:1341-1356.
61. Zhang Y, Xu N, Xu J, Kong B, Copple B, Guo GL, and Wang L (2014) E2F1 is a novel fibrogenic gene that regulates cholestatic liver fibrosis through the Egr-1/SHP/EID1 network. Hepatology 60:919-930.
62. Zhang Y, Xu P, Park K, Choi Y, Moore DD, and Wang L (2008) Orphan receptor small heterodimer partner suppresses tumorigenesis by modulating cyclin D1 expression and cellular proliferation. Hepatology 48:289-298.