Valproic acid induces CYP3A4 and MDR1 gene expression by activation of constitutive androstane receptor and pregnane X receptor pathways

Drug Metabolism and Disposition

Volumn 35, Issue 7, 2007, Pages 1032-1041

  Cerveny, Lukas ^a   Svecova, Lucie ^a   Anzenbacherova, Eva ^b   Vrzal, Radim ^b   Staud, Frantisek ^a   Dvorak, Zdenek ^b   Ulrichova, Jitka ^b   Anzenbacher, Pavel ^b   Pavek, Petr ^a  

^a Charles University in Prague Faculty of Pharmacy   (Czech Republic)

^b PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

6 (4 CHLOROPHENYL)IMIDAZO[2,1 B][1,3]THIAZOLE 5 CARBALDEHYDE O (3,4 DICHLOROBENZYL)OXIME; CELL NUCLEUS RECEPTOR; CONSTITUTIVE ANDROSTANE RECEPTOR; CYTOCHROME P450 3A4; HETERODIMER; LUCIFERASE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; PREGNANE X RECEPTOR; RETINOID X RECEPTOR ALPHA; RIFAMPICIN; STEROID RECEPTOR; UNCLASSIFIED DRUG; VALPROIC ACID;

ARTICLE; CANCER CELL CULTURE; CATALYSIS; CELL STRAIN HEPG2; COLON ADENOCARCINOMA; CONTROLLED STUDY; DRUG RECEPTOR BINDING; ELEMENTARY PARTICLE; ENZYME ANALYSIS; ENZYME ASSAY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE VECTOR; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTESTINE CELL; LIVER CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANTICONVULSANTS; ARYL HYDROCARBON HYDROXYLASES; CELL LINE, TUMOR; CYTOCHROME P-450 ENZYME SYSTEM; DRUG SYNERGISM; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME INDUCTION; GENES, REPORTER; HEPATOCYTES; HUMANS; HYDROXYLATION; LUCIFERASES; OXIDOREDUCTASES, N-DEMETHYLATING; OXIMES; P-GLYCOPROTEIN; PROMOTER REGIONS (GENETICS); RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID; RETINOID X RECEPTOR ALPHA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIFAMPIN; RNA, MESSENGER; TESTOSTERONE; THIAZOLES; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION; VALPROIC ACID;

EID: 34250758597     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.106.014456     Document Type: Article

References (50)

1. Allen MH, Hirschfeld RM, Wozniak PJ, Baker JD, and Bowden CL (2006) Linear relationship of valproate serum concentration to response and optimal serum levels for acute mania. Am J Psychiatry 163:272-275.
2. Bertilsson G, Heidrich J, Svensson K, Asman M, Jendeberg L, Sydow-Backman M, Ohlsson R, Postlind H, Blomquist P, and Berkenstam A (1998) Identification of a human nuclear receptor defines a new signaling pathway for CYP3A induction. Proc Natl Acad Sci U S A 95:12208-12213.
3. Blaheta RA, Michaelis M, Driever PH, and Cinatl J Jr (2005) Evolving anticancer drug valproic acid: insights into the mechanism and clinical studies. Med Res Rev 25:383-397.
4. Blaheta RA, Nau H, Michaelis M, and Cinatl J Jr (2002) Valproate and valproate-analogues: potent tools to fight against cancer. Curr Med Chem 9:1417-1433.
5. Bosetti F, Bell JM, and Manckam P (2005) Microarray analysis of rat brain gene expression after chronic administration of sodium valproate. Brain Res Bull 65:331-338.
6. Burk O, Arnold KA, Geick A, Tegude H, and Eichelbaum M (2005a) A role for constitutive androstane receptor in the regulation of human intestinal MDR1 expression. Biol Chem 386:503-513.
7. Burk O, Arnold KA, Nussler AK, Schaeffeler E, Efimova E, Avery BA, Avery MA, Fromm MF, and Eichelbaum M (2005b) Antimalarial artemisinin drugs induce cytochrome P450 and MDR1 expression by activation of xenosensors pregnane X receptor and constitutive androstane receptor. Mol Pharmacol 67:1954-1965.
8. Centorrino F, Kelleher JP, Berry JM, Salvatore P, Eakin M, Fogarty KV, Fellman V, and Baldessarini RJ (2003) Pilot comparison of extended-release and standard preparations of divalproex sodium in patients with bipolar and schizoaffective disorders. Am J Psychiatry 160:1348-1350.
9. Chen G, Huang LD, Jiang YM, and Manji HK (1999) The mood-stabilizing agent valproate inhibits the activity of glycogen synthase kinase-3. J Neurochem 72:1327-1330.
10. Davis R, Peters DH, and McTavish D (1994) Valproic acid. A reappraisal of its pharmacological properties and clinical efficacy in epilepsy. Drugs 47:332-372.
11. Eyal S, Lamb JG, Smith-Yockman M, Yagen B, Fibach E, Altschuler Y, White HS, and Bialer M (2006) The antiepileptic and anticancer agent, valproic acid, induces P-glycoprotein in human tumour cell lines and in rat liver. Br J Pharmacol 149:250-260.
12. Faucette SR, Zhang TC, Moore R, Sueyoshi T, Omiecinski CJ, LeCluyse EL, Negishi M, and Wang H (2007) Relative activation of human pregnane X receptor versus constitutive androstane receptor defines distinct classes of CYP2B6 and CYP3A4 inducers. J Pharmacol Exp Ther 320:72-80.
13. Fisher JE, Nau H, and Loscher W (1991) Alterations in the renal excretion of valproate and its metabolites after chronic treatment. Epilepsia 32:146-150.
14. Forman BM, Tzameli I, Choi HS, Chen J, Simha D, Seol W, Evans RM, and Moore DD (1998) Androstane metabolites bind to and deactivate the nuclear receptor CAR-beta. Nature 395:612-615.
15. Frank C, Gonzalez MM, Oinonen C, Dunlop TW, and Carlberg C (2003) Characterization of DNA complexes formed by the nuclear receptor constitutive androstane receptor. J Biol Chem 278:43299-43310.
16. Frank C, Molnar F, Matilainen M, Lempiainen H, and Carlberg C (2004) Agonist-dependent and agonist-independent transactivations of the human constitutive androstane receptor are modulated by specific amino acid pairs. J Biol Chem 279:33558-33566.
17. Geick A, Eichelbaum M, and Burk O (2001) Nuclear receptor response elements mediate induction of intestinal MDR1 by rifampin. J Biol Chem 276:14581-14587.
18. Goodwin B, Hodgson E, D'Costa DJ, Robertson GR, and Liddle C (2002) Transcriptional regulation of the human CYP3A4 gene by the constitutive androstane receptor. Mol Pharmacol 62:359-365.
19. Goodwin B, Hodgson E, and Liddle C (1999) The orphan human pregnane X receptor mediates the transcriptional activation of CYP3A4 by rifampicin through a distal enhancer module. Mol Pharmacol 56:1329-1339.
20. Goodwin B and Moore JT (2004) CAR: detailing new models. Trends Pharmacol Sci 25:437-441.
21. Goodwin B, Moore LB, Stoltz CA, McKee DD, and Kliewer SA (2001) Regulation of the human CYP2B6 gene by the nuclear pregnane X receptor. Mol Pharmacol 60:427-431.
22. Göttlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, et al. (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 20:6969-6978.
23. Guengerich FP, Martin MV, Beaune PH, Kremers P, Wolff T, and Waxman DJ (1986) Characterization of rat and human liver microsomal cytochrome P-450 forms involved in nifedipine oxidation, a prototype for genetic polymorphism in oxidative drug metabolism. J Biol Chem 261:5051-5060.
24. Honkakoski P, Zelko I, Sueyoshi T, and Negishi M (1998) The nuclear orphan receptor CAR-retinoid X receptor heterodimer activates the phenobarbital-responsive enhancer module of the CYP2B gene. Mol Cell Biol 18:5652-5658.
25. Isom HC, Secott T, Georgoff I, Woodworth C, and Mummaw J (1985) Maintenance of differentiated rat hepatocytes in primary culture. Proc Natl Acad Sci U S A 82:3252-3256.
26. Jin S and Scotto KV (1998) Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Mol Cell Biol 18:4377-4384.
27. Jones SA, Moore LB, Shenk JL, Wisely GB, Hamilton GA, McKee DD, Tomkinson NC, LeCluyse EL, Lambert MH, Willson TM, et al. (2000) The pregnane X receptor: a promiscuous xenobiotic receptor that has diverged during evolution. Mol Endocrinol 14:27-39.
28. Kawamoto T, Sueyoshi T, Zelko I, Moore R, Washburn K, and Negishi M (1999) Phenobarbital-responsive nuclear translocation of the receptor CAR in induction of the CYP2B gene. Mol Cell Biol 19:6318-6322.
29. Kramer OH, Zhu P, Ostendorff HP, Golebiewski M, Tiefenbach J, Peters MA, Brill B, Groner B, Bach I, Heinzel T, et al. (2003) The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J 22:3411-3420.
30. Maglich JM, Parks DJ, Moore LB, Collins JL, Goodwin B, Billin AN, Stoltz CA, Kliewer SA, Lambert MH, Willson TM, et al. (2003) Identification of a novel human constitutive androstane receptor (CAR) agonist and its use in the identification of CAR target genes. J Biol Chem 278:17277-17283.
31. Masuyama H, Suwaki N, Tateishi Y, Nakatsukasa H, Segawa T, and Hiramatsu Y (2005) The pregnane X receptor regulates gene expression in a ligand- and promoter-selective fashion. Mol Endocrinol 19:1170-1180.
32. Moore LB, Goodwin B, Jones SA, Wisely GB, Serabjit-Singh CJ, Willson TM, Collins JL, and Kliewer SA (2000a) St. John's wort induces hepatic drug metabolism through activation of the pregnane X receptor. Proc Natl Acad Sci U S A 97:7500-7502.
33. Moore LB, Parks DJ, Jones SA, Bledsoe RK, Consler TG, Stimmel JB, Goodwin B, Liddle C, Blanchard SG, Willson TM, et al. (2000b) Orphan nuclear receptors constitutive androstane receptor and pregnane X receptor share xenobiotic and steroid ligands. J Biol Chem 275:15122-15127.
34. Morrow CS and Nakagawa M (1994) Reversible transcriptional activation of mdr1 by sodium butyrate treatment of human colon cancer cells. J Biol Chem 269:10739-10746.
35. Pascussi JM, Drocourt L, Fabre JM, Maurel P, and Vilarem MJ (2000) Dexamethasone induces pregnane X receptor and retinoid X receptor-alpha expression in human hepatocytes: synergistic increase of CYP3A4 induction by pregnane X receptor activators. Mol Pharmacol 58:361-372.
36. Perucca E (2006) Clinically relevant drug interactions with antiepileptic drugs. Br J Clin Pharmacol 61:246-255.
37. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
38. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, and Klein PS (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276:36734-36741.
39. Pichard-Garcia L, Gerbal-Chaloin S, Ferrini JB, Fabre JM, and Maurel P (2002) Use of long-term cultures of human hepatocytes to study cytochrome P450 gene expression. Methods Enzymol 357:311-321.
40. Raffoux E, Chaibi P, Dombret H, and Degos L (2005) Valproic acid and all-trans retinoic acid for the treatment of elderly patients with acute myeloid leukemia. Haematologica 90:986-988.
41. Rodríguez-Antona C, Bort R, Jover R, Tindberg N, Ingelman-Sundberg M, Gómez-Lechón M, and Castell JV (2003) Transcriptional regulation of human CYP3A4 basal expression by CCAAT enhancer-binding protein. Mol Pharmacol 63:1180-1189.
42. Rogiers V, Akrawi M, Vercruysse A, Phillips IR, and Shephard EA (1995) Effects of the anticonvulsant, valproate, on the expression of components of the cytochrome-P-450-mediated monooxygenase system and glutathione S-transferases. Eur J Biochem 231:337-343.
43. Rogiers V, Callaerts A, Vercruysse A, Akrawi M, Shephard E, and Phillips I (1992) Effects of valproate on xenobiotic biotransformation in rat liver. In vivo and in vitro experiments. Pharm Weekbl Sci 14:127-131.
44. Scotto KV (2003) Transcriptional regulation of ABC drug transporters. Oncogene 22:7496-7511.
45. Staudinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y, Klaassen CD, Brown KK, Reinhard J, et al. (2001) The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc Natl Acad Sci U S A 98:3369-3374.
46. Tanaka E (1999) Clinically significant pharmacokinetic drug interactions between antiepileptic drugs. J Clin Pharm Ther 24:87-92.
47. Wen X, Wang JS, Kivisto KT, Neuvonen PJ, and Backman JT (2001) In vitro evaluation of valproic acid as an inhibitor of human cytochrome P450 isoforms: preferential inhibition of cytochrome P450 2C9 (CYP2C9). Br J Clin Pharmacol 52:547-553.
48. Werling U, Siehler S, Litfin M, Nau H, and Gottlicher M (2001) Induction of differentiation in F9 cells and activation of peroxisome proliferator- activated receptor delta by valproic acid and its teratogenic derivatives. Mol Pharmacol 59:1269-1276.
49. Xiao JJ and Huang Y (2005) Chemoresistance to depsipeptide FK228 [(E)-(1S,4S,10S,21R)-7-[(Z)-ethylidene]-4,21-diisopropyl-2-oxa-12,13-dithia-5,8, 20,23-tetraazabicyclo[8,7,6]-tricos-16-ene-3,6,9,22-pentanone] is mediated by reversible MDR1 induction in human cancer cell lines. J Pharmacol Exp Ther 314:467-475.
50. Xie W, Radominska-Pandya A, Shi Y, Simon CM, Nelson MC, Ong ES, Waxman DJ, and Evans RM (2001) An essential role for nuclear receptors SXR/PXR in detoxification of cholestatic bile acids. Proc Natl Acad Sci U S A 98:3375-3380.