Scoparone potentiates transactivation of the bile salt export pump gene and this effect is enhanced by cytochrome P450 metabolism but abolished by a PKC inhibitor

British Journal of Pharmacology

Volumn 164, Issue 5, 2011, Pages 1547-1557

  Yang, Dongfang ^a   Yang, Jian ^a   Shi, Deshi ^a   Deng, Ruitang ^a   Yan, Bingfang ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

bile salt export pump (BSEP); CAR; CYP1A2; CYP2B6; FXR; GF109203X; phosphorylation; potentiation of BSEP expression; scoparone

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; BILE SALT EXPORT PUMP PROTEIN; CHENODEOXYCHOLIC ACID; CYTOCHROME P450 1A2; GLUCURONOSYLTRANSFERASE 1A1; LIPID TRANSFER PROTEIN; MESSENGER RNA; PROTEIN KINASE C INHIBITOR; SCOPARONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILE SALT EXPORT PUMP GENE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG MECHANISM; DRUG METABOLISM; DRUG POTENTIATION; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME METABOLISM; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LIVER CELL; LIVER CELL CARCINOMA; LIVER MICROSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; TRANSACTIVATION; TRANSIENT TRANSFECTION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; CELL LINE, TUMOR; CHOLAGOGUES AND CHOLERETICS; COUMARINS; CYTOCHROME P-450 CYP1A2; CYTOCHROME P-450 ENZYME SYSTEM; DRUG SYNERGISM; GENES, REPORTER; GLUCURONOSYLTRANSFERASE; HEPATOCYTES; HUMANS; MICE; MICROSOMES, LIVER; PROMOTER REGIONS, GENETIC; PROTEIN KINASE INHIBITORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 80054051468     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01522.x     Document Type: Article

References (64)

1. Baiocchi L, Tisone G, Russo MA, Longhi C, Palmieri G, Volpe A, et al,. (2008). TUDCA prevents cholestasis and canalicular damage induced by ischemia-reperfusion injury in the rat, modulating PKCalpha-ezrin pathway. Transpl Int 21: 792-800.
2. Basu NK, Kole L, Owens IS, (2003). Evidence for phosphorylation requirement for human bilirubin UDP-glucuronosyltransferase (UGT1A1) activity. Biochem Biophys Res Commun 303: 98-104. (Pubitemid 36338213)
3. Bock KW, Bock-Hennig BS, (2010). UDP-glucuronosyltransferases (UGTs): from purification of Ah-receptor-inducible UGT1A6 to coordinate regulation of subsets of CYPs, UGTs, and ABC transporters by nuclear receptors. Drug Metab Rev 42: 5-12.
4. Bodin K, Lindbom U, Diczfalusy U, (2005). Novel pathways of bile acid metabolism involving CYP3A4. Biochim Biophys Acta 1687: 84-93. (Pubitemid 40228988)
5. Brites D, Rodrigues CM, van-Zeller H, Brito A, Silva R, (1998). Relevance of serum bile acid profile in the diagnosis of intrahepatic cholestasis of pregnancy in a high incidence area: Portugal. Eur J Obstet Gynecol Reprod Biol 80: 31-38. (Pubitemid 29272016)
6. Calderon RM, Cubeddu LX, Goldberg RB, Schiff ER, (2010). Statins in the treatment of dyslipidemia in the presence of elevated liver aminotransferase levels: a therapeutic dilemma. Mayo Clin Proc 85: 349-356.
7. Cederbaum AI, Lu Y, Wu D, (2009). Role of oxidative stress in alcohol-induced liver injury. Arch Toxicol 83: 519-548.
8. Chen SP, Tian LL, Liu FL, (2009). Clinical observation of Yinzhihuang Oral Liquid on prevention of the premature infantile jaundice. Chin J Integr Med 15: 299-302.
9. Crocenzi FA, Sánchez Pozzi EJ, Ruiz ML, Zucchetti AE, Roma MG, Mottino AD, (2008). Ca(2+)-dependent protein kinase C isoforms are critical to estradiol 17beta-D-glucuronide-induced cholestasis in the rat. Hepatology 48: 1885-1895.
10. Cuperus FJ, Hafkamp AM, Hulzebos CV, Verkade HJ, (2009). Pharmacological therapies for unconjugated hyperbilirubinemia. Curr Pharm Des 15: 2927-2938.
11. Deng R, Yang D, Yang J, Yan B, (2006). Cholesterol oxylsterol transcriptionally induces the expression of the bile salt efflux pump through the farnesoid X receptor but not the liver X receptor. J Pharmacol Exp Ther 317: 317-325.
12. Deng R, Yang D, Radke A, Yang J, Yan B, (2007). Hypolipidemic agent guggulsterone regulates BSEP expression: dominance of transactivation over FXR-antagonism. J Pharmacol Exp Ther 320: 1277-1286.
13. Dolz C, Xiol X, Abad A, Cabré E, González-Huix F, Giné JJ, et al,. (1989). Changes in liver function tests in patients with inflammatory bowel disease on enteral nutrition. JPEN J Parenter Enteral Nutr 13: 401-405. (Pubitemid 19203165)
14. Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K, Blei AT, (2002). Hepatic encephalopathy-definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 35: 716-721. (Pubitemid 34183979)
15. Ferri C, Govoni M, Calabrese L, (2010). The A, B, Cs of viral hepatitis in the biologic era. Curr Opin Rheumatol 22: 443-450.
16. Fiorucci S, Baldelli F, (2009). Farnesoid X receptor agonists in biliary tract disease. Curr Opin Gastroenterol 25: 252-259.
17. Fiorucci S, Clerici C, Antonelli E, Orlandi S, Goodwin B, Sadeghpour BM, et al,. (2005). Protective effects of 6-ethyl chenodeoxycholic acid, a farnesoid X receptor ligand, in estrogen-induced cholestasis. J Pharmacol Exp Ther 313: 604-612. (Pubitemid 40604160)
18. Gineste R, Sirvent A, Paumelle R, Helleboid S, Aquilina A, Darteil R, et al,. (2008). Phosphorylation of farnesoid X receptor by protein kinase C promotes its transcriptional activity. Mol Endocrinol 22: 2433-2447.
19. Hirouchi M, Suzuki H, Sugiyama Y, (2005). Treatment of hyperbilirubinemia in Eisai hyperbilirubinemic rat by transfecting human MRP2/ABCC2 gene. Pharm Res 22: 661-666. (Pubitemid 40603264)
20. Ho RH, Leake BF, Kilkenny DM, Meyer Zu Schwabedissen HE, Glaeser H, Kroetz DL, et al,. (2010). Polymorphic variants in the human bile salt export pump (BSEP; ABCB11): functional characterization and interindividual variability. Pharmacogenet Genomics 20: 45-57.
21. Huang W, Zhang J, Moore DD, (2004). A traditional herbal medicine enhances bilirubin clearance by activating the nuclear receptor CAR. J Clin Invest 113: 137-143. (Pubitemid 38541640)
22. Ieiri I, Suzuki H, Kimura M, Takane H, Nishizato Y, Irie S, et al,. (2004). Influence of common variants in the pharmacokinetic genes (OATP-C, UGT1A1, and MRP2) on serum bilirubin levels in healthy subjects. Hepatol Res 30: 91-95. (Pubitemid 41115270)
23. IPA (2007). Top 20 causes of mortality throughout the world.
24. Jung D, Elferink MG, Stellaard F, Groothuis GM, (2007). Analysis of bile acid-induced regulation of FXR target genes in human liver slices. Liver Int 27: 137-144. (Pubitemid 46139438)
25. Jyrkkärinne J, Windshügel B, Mäkinen J, Ylisirniö M, Peräkylä M, Poso A, et al,. (2005). Amino acids important for ligand specificity of the human constitutive androstane receptor. J Biol Chem 280: 5960-5971. (Pubitemid 40280080)
26. Kagawa T, Watanabe N, Mochizuki K, Numari A, Ikeno Y, Itoh J, (2008). Phenotypic differences in PFIC2 and BRIC2 correlate with protein stability of mutant Bsep and impaired taurocholate secretion in MDCK II cells. Am J Physiol Gastrointest Liver Physiol 294: G58-G67.
27. Kaimal R, Song X, Yan B, King R, Deng R, (2009). Differential modulation of farnesoid X receptor signaling pathway by the thiazolidinediones. J Pharmacol Exp Ther 330: 125-134.
28. Keitel V, Burdelski M, Warskulat U, Kühlkamp T, Keppler D, Häussinger D, et al,. (2005). Expression and localization of hepatobiliary transport proteins in progressive familial intrahepatic cholestasis. Hepatology 41: 1160-1172. (Pubitemid 40593925)
29. Kis E, Ioja E, Nagy T, Szente L, Herédi-Szabõ K, Krajcsi P, (2009). Effect of membrane cholesterol on BSEP/Bsep activity: species specificity studies for substrates and inhibitors. Drug Metab Dispos 37: 1878-1886.
30. 2+-dependent protein kinase C isoforms induce cholestasis in rat liver. J Biol Chem 279: 10323-10330. (Pubitemid 38372639)
31. Lee TY, Chang HH, Chen JH, Hsueh ML, Kuo JJ, (2007). Herb medicine Yin-Chen-Hao-Tang ameliorates hepatic fibrosis in bile duct ligation rats. J Ethnopharmacol 109: 318-324.
32. Li W, Shen J, Liu G, Tang Y, Hoshino T, (2011). Exploring coumarin egress channels in human cytochrome P450 2A6 by random acceleration and steered molecular dynamics simulations. Proteins 79: 271-281.
33. Liver Foundation (2009). Liver awareness month.
34. Ma Y, Song X, Sachdeva K, Liu J, Li Y, Yang D, et al,. (2005). Clofibrate and perfluorodecanoate both up-regulate the expression of the pregnane X receptor but only clofibrate enhances its ligand-dependent induction of cytochrome P4503A23. Biochem Pharmacol 69: 1 363-1 371.
35. Mennes WC, van Holsteijn CW, Timmerman A, Noordhoek J, Blaauboer BJ, (1991). Biotransformation of scoparone used to monitor changes in cytochrome P450 activities in primary hepatocyte cultures derived from rats, hamsters and monkeys. Biochem Pharmacol 41: 1203-1208.
36. Meyer RP, Hagemeyer CE, Knoth R, Kurz G, Volk B, (2001). Oxidative hydrolysis of scoparone by cytochrome p450 CYP2C29 reveals a novel metabolite. Biochem Biophys Res Commun 285: 32-39. (Pubitemid 32912506)
37. Meyer Zu Schwabedissen HE, Böttcher K, Chaudhry A, Kroemer HK, Schuetz EG, Kim RB, (2001). Liver X receptor α and farnesoid X receptor are major transcriptional regulators of OATP1B1. Hepatology 52: 1797-1807.
38. Murat Bilgin H, Atmaca M, Deniz Obay B, Ozekinci S, TaÅdemir E, Ketani A, (2011). Protective effects of coumarin and coumarin derivatives against carbon tetrachloride-induced acute hepatotoxicity in rats. Exp Toxicol Pathol 63: 325-330.
39. Paul IM, Phillips TA, Widome MD, Hollenbeak CS, (2004). Cost-effectiveness of postnatal home nursing visits for prevention of hospital care for jaundice and dehydration. Pediatrics 114: 1015-1022. (Pubitemid 41529767)
40. Paumgartner G, (2010). Biliary physiology and disease: reflections of a physician-scientist. Hepatology 51: 1095-1106.
41. Pérez Fernández T, Lõpez Serrano P, Tomás E, Gutiérrez ML, Lledõ JL, Cacho G, et al,. (2004). Diagnostic and therapeutic approach to cholestatic liver disease. Rev Esp Enferm Dig 96: 60-73. (Pubitemid 38292446)
42. Perez MJ, Briz O, (2009). Bile-acid-induced cell injury and protection. World J Gastroenterol 15: 1677-1689.
43. Pietrangelo A, (2009). Inherited metabolic disease of the liver. Curr Opin Gastroenterol 25: 209-214.
44. Rodrigues CM, Solá S, Brito MA, Brites D, Moura JJ, (2002). Bilirubin directly disrupts membrane lipid polarity and fluidity, protein order, and redox status in rat mitochondria. J Hepatol 36: 335-341. (Pubitemid 34194792)
45. Romero-Gõmez M, Boza F, García-Valdecasas MS, García E, Aguilar-Reina J, (2001). Subclinical hepatic encephalopathy predicts the development of overt hepatic encephalopathy. Am J Gastroenterol 96: 2718-2723.
46. Santoro A, Mancini E, Ferramosca E, Faenza S, (2007). Liver support systems. Contrib Nephrol 156: 396-404.
47. Schaap FG, van der Gaag NA, Gouma DJ, Jansen PL, (2009). High expression of the bile salt-homeostatic hormone fibroblast growth factor 19 in the liver of patients with extrahepatic cholestasis. Hepatology 49: 1228-1235.
48. Stieger B, (2010). Role of the bile salt export pump, BSEP, in acquired forms of cholestasis. Drug Metab Rev 42: 437-445.
49. Stross C, Helmer A, Weissenberger K, Görg B, Keitel V, Häussinger D, et al,. (2010). Protein kinase C induces endocytosis of the sodium taurocholate cotransporting polypeptide. Am J Physiol Gastrointest Liver Physiol 299: G320-G328.
50. Tan XJ, Li Q, Chen XH, Wang ZW, Shi ZY, Bi KS, et al,. (2008). Simultaneous determination of 13 bioactive compounds in Herba Artemisiae Scopariae (Yin Chen) from different harvest seasons by HPLC-DAD. J Pharm Biomed Anal 47: 847-853.
51. Tandon BN, (2003). Hepatic encephalopathy syndromes. Indian J Gastroenterol 22 (Suppl. 2): S4-S6. (Pubitemid 38282241)
52. Trauner M, Fickert P, Halilbasic E, Moustafa T, (2008). Lessons from the toxic bile concept for the pathogenesis and treatment of cholestatic liver diseases. Wien Med Wochenschr 158: 542-548.
53. Villarroya F, Domingo P, Giralt M, (2010). Drug-induced lipotoxicity: lipodystrophy associated with HIV-1 infection and antiretroviral treatment. Biochim Biophys Acta 1801: 392-399.
54. Vítek L, Ostrow JD, (2009). Bilirubin chemistry and metabolism; harmful and protective aspects. Curr Pharm Des 15: 2869-2883.
55. Wagner M, Zollner G, Trauner M, (2010). Nuclear receptor regulation of the adaptive response of bile acid transporters in cholestasis. Semin Liver Dis 30: 160-177.
56. Wang H, Faucette S, Moore R, Sueyoshi T, Negishi M, LeCluyse E, (2004). Human constitutive androstane receptor mediates induction of CYP2B6 gene expression by phenytoin. J Biol Chem 279: 29295-29301. (Pubitemid 38915806)
57. Wang JM, Wang H, Xu LN, Zou SQ, (2005). Hepatic injury in rats with obstructive jaundice: roles of the protein kinase C signal pathway and cytoprotection of fructose. Hepatobiliary Pancreat Dis Int 4: 577-581. (Pubitemid 41723815)
58. Wang N, Li P, Wang Y, Peng W, Wu Z, Tan S, et al,. (2008). Hepatoprotective effect of Hypericum japonicum extract and its fractions. J Ethnopharmacol 116: 1-6.
59. Wimmer R, Hohenester S, Pusl T, Denk GU, Rust C, Beuers U, (2008). Tauroursodeoxycholic acid exerts anticholestatic effects by a cooperative cPKC alpha-/PKA-dependent mechanism in rat liver. Gut 57: 1448-1454.
60. Yang J, Shi D, Yang D, Song X, Yan B, (2007). Interleukin-6 suppresses the expression of carboxylesterases HCE1 and HCE2 through transcriptional repression. Mol Pharmacol 72: 686-694. (Pubitemid 47347303)
61. Yang YJ, Lee HJ, Choi DH, Huang HS, Lim SC, Lee MK, (2008). Effect of scoparone on neurite outgrowth in PC12 cells. Neurosci Lett 440: 14-18.
62. Yang YJ, Lee HJ, Huang HS, Lee BK, Choi HS, Lim SC, et al,. (2009). Effects of scoparone on dopamine biosynthesis and L-DOPA-induced cytotoxicity in PC12 cells. J Neurosci Res 87: 1929-1937.
63. Yu ZG, Wang Q, Li K, Li YQ, Gao XX, (2007). Determination and pharmacokinetics of 6,7 dimethoxycoumarin in rat plasma after intragastric administration of different decoctions of yinchenhao tang. J Chromatogr Sci 45: 544-548. (Pubitemid 47396518)
64. Zhu W, Song L, Zhang H, Matoney L, LeCluyse E, Yan B, (2000). Dexamethasone differentially regulates expression of carboxylesterase genes in humans and rats. Drug Metab Dispos 28: 186-191. (Pubitemid 30069003)