Nuclear receptors in regulation of biotransformation enzymes and drug transporters in the placental barrier

References

• Adcock IM, Ito K, Barnes PJ. (2004). Glucocorticoids: Effects on gene transcription. Proc Am Thorac Soc 1:247–254
   PubMedGoogle Scholar
• Avery ML, Meek CE, Audus KL. (2003). The presence of inducible cytochrome P450 types 1A1 and 1A2 in the BeWo cell line. Placenta 24:45–52
   PubMed Web of Science ®Google Scholar
• Avila E, Diaz L, Barrera D, et al. (2007). Regulation of Vitamin D hydroxylases gene expression by 1,25-dihydroxyvitamin D3 and cyclic AMP in cultured human syncytiotrophoblasts. J Steroid Biochem Mol Biol 103:90–96
   PubMed Web of Science ®Google Scholar
• Avila E, Diaz L, Halhali A, Larrea F. (2004). Regulation of 25-hydroxyvitamin D3 1alpha-hydroxylase, 1,25-dihydroxyvitamin D3 24-hydroxylase and vitamin D receptor gene expression by 8-bromo cyclic AMP in cultured human syncytiotrophoblast cells. J Steroid Biochem Mol Biol 89–90:115–119
   PubMed Web of Science ®Google Scholar
• Baes M, Gulick T, Choi HS, et al. (1994). A new orphan member of the nuclear hormone receptor superfamily that interacts with a subset of retinoic acid response elements. Mol Cell Biol 14:1544–1552
   PubMed Web of Science ®Google Scholar
• Barrera D, Avila E, Hernandez G, et al. (2008). Calcitriol affects hCG gene transcription in cultured human syncytiotrophoblasts. Reprod Biol Endocrinol 6:3
   PubMed Web of Science ®Google Scholar
• Beaune P, Dansette P, Flinois JP, et al. (1979). Partial purification of human liver cytochrome P 450. Biochem Biophys Res Commun 88:826–832
   PubMed Web of Science ®Google Scholar
• Belkacemi L, Zuegel U, Steinmeyer A, et al. (2005). Calbindin-D28k (CaBP28k) identification and regulation by 1,25-dihydroxyvitamin D3 in human choriocarcinoma cell line JEG-3. Mol Cell Endocrinol 236:31–41
   PubMed Web of Science ®Google Scholar
• Bieche I, Narjoz C, Asselah T, et al. (2007). Reverse transcriptase-PCR quantification of mRNA levels from cytochrome (CYP)1, CYP2 and CYP3 families in 22 different human tissues. Pharmacogenet Genomics 17:731–742
   PubMed Web of Science ®Google Scholar
• Bruchova H, Vasikova A, Merkerova M, et al. (2008). Effect of maternal tobacco smoke exposure on the placental transcriptome. Placenta 31:186–191
   Web of Science ®Google Scholar
• Burton PJ, Waddell BJ. (1999). Dual function of 11beta-hydroxysteroid dehydrogenase in placenta: Modulating placental glucocorticoid passage and local steroid action. Biol Reprod 60:234–240
   PubMed Web of Science ®Google Scholar
• Chan CC, Lao TT, Ho PC, et al. (2003). The effect of mifepristone on the expression of steroid hormone receptors in human decidua and placenta: A randomized placebo-controlled double-blind study. J Clin Endocrinol Metab 88:5846–5850
   PubMed Web of Science ®Google Scholar
• Chen Y, Tang Y, Guo C, et al. (2012). Nuclear receptors in the multidrug resistance through the regulation of drug-metabolizing enzymes and drug transporters. Biochem Pharmacol 83:1112–1126
   PubMed Web of Science ®Google Scholar
• Chen YH, Wang JP, Wang H, et al. (2005). Lipopolysaccharide treatment downregulates the expression of the pregnane X receptor, cyp3a11 and mdr1a genes in mouse placenta. Toxicology 211:242–252
   PubMed Web of Science ®Google Scholar
• Collier AC, Ganley NA, Tingle MD, et al. (2002a). UDP-glucuronosyltransferase activity, expression and cellular localization in human placenta at term. Biochem Pharmacol 63:409–419
   PubMed Web of Science ®Google Scholar
• Collier AC, Tingle MD, Paxton JW, et al. (2002b). Metabolizing enzyme localization and activities in the first trimester human placenta: The effect of maternal and gestational age, smoking and alcohol consumption. Hum Reprod 17:2564–2572
   PubMed Web of Science ®Google Scholar
• Conney AH, Miller EC, Miller JA. (1957). Substrate-induced synthesis and other properties of benzpyrene hydroxylase in rat liver. J Biol Chem 228:753–766
   PubMed Web of Science ®Google Scholar
• di Masi A, De Marinis E, Ascenzi P, Marino M. (2009). Nuclear receptors CAR and PXR: Molecular, functional, and biomedical aspects. Mol Aspects Med 30:297–343
   PubMed Web of Science ®Google Scholar
• Dolwick KM, Schmidt JV, Carver LA, et al. (1993). Cloning and expression of a human Ah receptor cDNA. Mol Pharmacol 44:911–917
   PubMed Web of Science ®Google Scholar
• Driver PM, Kilby MD, Bujalska I, et al. (2001). Expression of 11 beta-hydroxysteroid dehydrogenase isozymes and corticosteroid hormone receptors in primary cultures of human trophoblast and placental bed biopsies. Mol Hum Reprod 7:357–363
   PubMed Web of Science ®Google Scholar
• Drocourt L, Ourlin JC, Pascussi JM, et al. (2002). Expression of CYP3A4, CYP2B6, and CYP2C9 is regulated by the vitamin D receptor pathway in primary human hepatocytes. J Biol Chem 277:25125–25132
   PubMed Web of Science ®Google Scholar
• Dusso AS, Brown AJ, Slatopolsky E. (2005). Vitamin D. Am J Physiol Renal Physiol 289:F8–28
   PubMed Web of Science ®Google Scholar
• Dvorak Z, Pavek P. (2010). Regulation of drug-metabolizing cytochrome P450 enzymes by glucocorticoids. Drug Metab Rev 42:621–635
   PubMed Web of Science ®Google Scholar
• Ema M, Matsushita N, Sogawa K, et al. (1994). Human arylhydrocarbon receptor: Functional expression and chromosomal assignment to 7p21. J Biochem 116:845–851
   PubMed Web of Science ®Google Scholar
• Enders AC, Blankenship TN. (1999). Comparative placental structure. Adv Drug Deliv Rev 38:3–15
   PubMed Web of Science ®Google Scholar
• Evseenko DA, Paxton JW, Keelan JA. (2007). Independent regulation of apical and basolateral drug transporter expression and function in placental trophoblasts by cytokines, steroids, and growth factors. Drug Metab Dispos 35:595–601
   PubMed Web of Science ®Google Scholar
• Filiberto AC, Maccani MA, Koestler D, et al. (2011). Birthweight is associated with DNA promoter methylation of the glucocorticoid receptor in human placenta. Epigenetics 6:566–572
   PubMed Web of Science ®Google Scholar
• Gahir SS, Piquette-Miller M. (2011). Gestational and pregnane X receptor-mediated regulation of placental ATP-binding cassette drug transporters in mice. Drug Metab Dispos 39:465–471
   PubMed Web of Science ®Google Scholar
• Geenes VL, Dixon PH, Chambers J, et al. (2011). Characterisation of the nuclear receptors FXR, PXR and CAR in normal and cholestatic placenta. Placenta 32:535–537
   PubMed Web of Science ®Google Scholar
• Geick A, Eichelbaum M, Burk O. (2001). Nuclear receptor response elements mediate induction of intestinal MDR1 by rifampin. J Biol Chem 276:14581–14587
   PubMed Web of Science ®Google Scholar
• Gerbal-Chaloin S, Pascussi JM, Pichard-Garcia L, et al. (2001). Induction of CYP2C genes in human hepatocytes in primary culture. Drug Metab Dispos 29:242–251
   PubMed Web of Science ®Google Scholar
• Giacomini KM, Huang SM, Tweedie DJ, et al. (2010). Membrane transporters in drug development. Nat Rev Drug Discov 9:215–236
   PubMed Web of Science ®Google Scholar
• Gonzalez FJ. (1988). The molecular biology of cytochrome P450s. Pharmacol Rev 40:243–288
   PubMed Web of Science ®Google Scholar
• Gronemeyer H, Gustafsson JA, Laudet V. (2004). Principles for modulation of the nuclear receptor superfamily. Nat Rev Drug Discov 3:950–964
   PubMed Web of Science ®Google Scholar
• Guengerich FP, Tang Z, Cheng Q, Salamanca-Pinzon SG. (2011). Approaches to deorphanization of human and microbial cytochrome P450 enzymes. Biochim Biophys Acta 1814:139–145
   PubMed Web of Science ®Google Scholar
• Guibourdenche J, Alsat E, Soncin F, et al. (1998). Retinoid receptors expression in human term placenta: Involvement of RXR alpha in retinoid induced-hCG secretion. J Clin Endocrinol Metab 83:1384–1387
   PubMed Web of Science ®Google Scholar
• Hakkola J, Pasanen M, Hukkanen J, et al. (1996a). Expression of xenobiotic-metabolizing cytochrome P450 forms in human full-term placenta. Biochem Pharmacol 51:403–411
   PubMed Web of Science ®Google Scholar
• Hakkola J, Pasanen M, Pelkonen O, et al. (1997). Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis 18:391–397
   PubMed Web of Science ®Google Scholar
• Hakkola J, Raunio H, Purkunen R, et al. (1996b). Detection of cytochrome P450 gene expression in human placenta in first trimester of pregnancy. Biochem Pharmacol 52:379–383
   PubMed Web of Science ®Google Scholar
• Hallman M, Peltoniemi O, Kari MA. (2010). Enhancing functional maturity before preterm birth. Neonatology 97:373–378
   PubMed Web of Science ®Google Scholar
• Handschin C, Meyer UA. (2003). Induction of drug metabolism: The role of nuclear receptors. Pharmacol Rev 55:649–673
   PubMed Web of Science ®Google Scholar
• Hemauer SJ, Patrikeeva SL, Wang X, et al. (2010). Role of transporter-mediated efflux in the placental biodisposition of bupropion and its metabolite, OH-bupropion. Biochem Pharmacol 80:1080–1086
   PubMed Web of Science ®Google Scholar
• Hinson JA, Forkert PG. (1995). Phase II enzymes and bioactivation. Can J Physiol Pharmacol 73:1407–1413
   PubMed Web of Science ®Google Scholar
• Hodyl NA, Wyper H, Osei-Kumah A, et al. (2010). Sex-specific associations between cortisol and birth weight in pregnancies complicated by asthma are not due to differential glucocorticoid receptor expression. Thorax 65:677–683
   PubMed Web of Science ®Google Scholar
• Huuskonen P, Storvik M, Reinisalo M, et al. (2008). Microarray analysis of the global alterations in the gene expression in the placentas from cigarette-smoking mothers. Clin Pharmacol Ther 83:542–550
   PubMed Web of Science ®Google Scholar
• Ietta F, Wu Y, Winter J, et al. (2006). Dynamic HIF1A regulation during human placental development. Biol Reprod 75:112–121
   PubMed Web of Science ®Google Scholar
• Jiang YZ, Wang K, Fang R, Zheng J. (2010). Expression of aryl hydrocarbon receptor in human placentas and fetal tissues. J Histochem Cytochem 58:679–685
   PubMed Web of Science ®Google Scholar
• Johnson RF, Rennie N, Murphy V, et al. (2008). Expression of glucocorticoid receptor messenger ribonucleic acid transcripts in the human placenta at term. J Clin Endocrinol Metab 93:4887–4893
   PubMed Web of Science ®Google Scholar
• Kauffmann HM, Pfannschmidt S, Zöller H, et al. (2002). Influence of redox-active compounds and PXR-activators on human MRP1 and MRP2 gene expression. Toxicology 171:137–146
   PubMed Web of Science ®Google Scholar
• Kawajiri K, Fujii-Kuriyama Y. (2007). Cytochrome P450 gene regulation and physiological functions mediated by the aryl hydrocarbon receptor. Arch Biochem Biophys 464:207–212
   PubMed Web of Science ®Google Scholar
• Kohle C, Bock KW. (2007). Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2. Biochem Pharmacol 73:1853–1862
   PubMed Web of Science ®Google Scholar
• Kolwankar D, Glover DD, Ware JA, Tracy TS. (2005). Expression and function of ABCB1 and ABCG2 in human placental tissue. Drug Metab Dispos 33:524–529
   PubMed Web of Science ®Google Scholar
• Lamba V, Yasuda K, Lamba JK, et al. (2004). PXR (NR1I2): Splice variants in human tissues, including brain, and identification of neurosteroids and nicotine as PXR activators. Toxicol Appl Pharmacol 199:251–265
   PubMed Web of Science ®Google Scholar
• Lee MJ, Wang Z, Yee H, et al. (2005). Expression and regulation of glucocorticoid receptor in human placental villous fibroblasts. Endocrinology 146:4619–4626
   PubMed Web of Science ®Google Scholar
• Lehmann JM, McKee DD, Watson MA, et al. (1998). The human orphan nuclear receptor PXR is activated by compounds that regulate CYP3A4 gene expression and cause drug interactions. J Clin Invest 102:1016–1023
   PubMed Web of Science ®Google Scholar
• Lehrmann C, Ullrich V, Rummel W. (1973). Phenobarbital inducible drug monooxygenase activity in the small intestine of mice. Naunyn Schmiedebergs Arch Pharmacol 276:89–98
   PubMed Web of Science ®Google Scholar
• Liu NQ, Hewison M. (2012). Vitamin D, the placenta and pregnancy. Arch Biochem Biophys 523:37–47
   PubMed Web of Science ®Google Scholar
• Lu NZ, Wardell SE, Burnstein KL, et al. (2006). International Union of Pharmacology. LXV. The pharmacology and classification of the nuclear receptor superfamily: Glucocorticoid, mineralocorticoid, progesterone, and androgen receptors. Pharmacol Rev 58:782–797
   PubMed Web of Science ®Google Scholar
• Maezawa K, Matsunaga T, Takezawa T, et al. (2010). Cytochrome P450 3As gene expression and testosterone 6 beta-hydroxylase activity in human fetal membranes and placenta at full term. Biol Pharm Bull 33:249–254
   PubMed Web of Science ®Google Scholar
• Maglich JM, Stoltz CM, Goodwin B, et al. (2002). Nuclear pregnane x receptor and constitutive androstane receptor regulate overlapping but distinct sets of genes involved in xenobiotic detoxification. Mol Pharmacol 62:638–646
   PubMed Web of Science ®Google Scholar
• Makishima M, Lu TT, Xie W, et al. (2002). Vitamin D receptor as an intestinal bile acid sensor. Science 296:1313–1316
   PubMed Web of Science ®Google Scholar
• Manceau S, Giraud C, Decleves X, et al. (2012). ABC drug transporter and nuclear receptor expression in human cytotrophoblasts: Influence of spontaneous syncytialization and induction by glucocorticoids. Placenta 33:927–932
   PubMed Web of Science ®Google Scholar
• Manchester DK, Gordon SK, Golas CL, et al. (1987). Ah receptor in human placenta: Stabilization by molybdate and characterization of binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin, 3-methylcholanthrene, and benzo(a)pyrene. Cancer Res 47:4861–4868
   PubMed Web of Science ®Google Scholar
• Manchester DK, Wilson VL, Hsu IC, et al. (1990). Synchronous fluorescence spectroscopic, immunoaffinity chromatographic and 32P-postlabeling analysis of human placental DNA known to contain benzo[a]pyrene diol epoxide adducts. Carcinogenesis 11:553–559
   PubMed Web of Science ®Google Scholar
• Mandl M, Ghaffari-Tabrizi N, Haas J, et al. (2006). Differential glucocorticoid effects on proliferation and invasion of human trophoblast cell lines. Reproduction 132:159–167
   PubMed Web of Science ®Google Scholar
• Mark PJ, Waddell BJ. (2006). P-glycoprotein restricts access of cortisol and dexamethasone to the glucocorticoid receptor in placental BeWo cells. Endocrinology 147:5147–5152
   PubMed Web of Science ®Google Scholar
• Masuyama H, Hiramatsu Y, Mizutani Y, et al. (2001). The expression of pregnane X receptor and its target gene, cytochrome P450 3A1, in perinatal mouse. Mol Cell Endocrinol 172:47–56
   PubMed Web of Science ®Google Scholar
• Mathias AA, Hitti J, Unadkat JD. (2005). P-glycoprotein and breast cancer resistance protein expression in human placentae of various gestational ages. Am J Physiol Regul Integr Comp Physiol 289:R963–969
   PubMed Web of Science ®Google Scholar
• May K, Minarikova V, Linnemann K, et al. (2008). Role of the multidrug transporter proteins ABCB1 and ABCC2 in the diaplacental transport of talinolol in the term human placenta. Drug Metab Dispos 36:740–744
   PubMed Web of Science ®Google Scholar
• McRobie DJ, Glover DD, Tracy TS. (1998). Effects of gestational and overt diabetes on human placental cytochromes P450 and glutathione S-transferase. Drug Metab Dispos 26:367–371
   PubMed Web of Science ®Google Scholar
• Meyer zu Schwabedissen HE, Grube M, Dreisbach A, et al. (2006). Epidermal growth factor-mediated activation of the map kinase cascade results in altered expression and function of ABCG2 (BCRP). Drug Metab Dispos 34:524–533
   PubMed Web of Science ®Google Scholar
• Meyer Zu Schwabedissen HE, Grube M, Heydrich B, et al. (2005). Expression, localization, and function of MRP5 (ABCC5), a transporter for cyclic nucleotides, in human placenta and cultured human trophoblasts: Effects of gestational age and cellular differentiation. Am J Pathol 166:39–48
   PubMed Web of Science ®Google Scholar
• Moore DD, Kato S, Xie W, et al. (2006). International Union of Pharmacology. LXII. The NR1H and NR1I receptors: Constitutive androstane receptor, pregnene X receptor, farnesoid X receptor alpha, farnesoid X receptor beta, liver X receptor alpha, liver X receptor beta, and vitamin D receptor. Pharmacol Rev 58:742–759
   PubMed Web of Science ®Google Scholar
• Muller F, Fromm MF. (2011). Transporter-mediated drug--drug interactions. Pharmacogenomics 12:1017–1037
   PubMed Web of Science ®Google Scholar
• Myllynen P, Pasanen M, Vahakangas K. (2007). The fate and effects of xenobiotics in human placenta. Expert Opin Drug Metab Toxicol 3:331–346
   PubMed Web of Science ®Google Scholar
• Myllynen P, Vahakangas K. (2013). Placental transfer and metabolism: An overview of the experimental models utilizing human placental tissue. Toxicol In Vitro 27:507–512
   PubMed Web of Science ®Google Scholar
• Nakanishi T, Ross DD. (2012). Breast cancer resistance protein (BCRP/ABCG2): Its role in multidrug resistance and regulation of its gene expression. Chin J Cancer 31:73–99
   PubMed Web of Science ®Google Scholar
• Nebert DW, Gelboin HV. (1968). Substrate-inducible microsomal aryl hydroxylase in mammalian cell culture. II. Cellular responses during enzyme induction. J Biol Chem 243:6250–6261
   PubMed Web of Science ®Google Scholar
• Nishimura M, Naito S. (2006). Tissue-specific mRNA expression profiles of human phase I metabolizing enzymes except for cytochrome P450 and phase II metabolizing enzymes. Drug Metab Pharmacokinet 21:357–374
   PubMed Web of Science ®Google Scholar
• Nishimura M, Naito S, Yokoi T. (2004). Tissue-specific mRNA expression profiles of human nuclear receptor subfamilies. Drug Metab Pharmacokinet 19:135–149
   PubMedGoogle Scholar
• Nishimura M, Yaguti H, Yoshitsugu H, et al. (2003). Tissue distribution of mRNA expression of human cytochrome P450 isoforms assessed by high-sensitivity real-time reverse transcription PCR. Yakugaku Zasshi 123:369–375
   PubMed Web of Science ®Google Scholar
• Okey AB, Giannone JV, Smart W, et al. (1997). Binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin to AH receptor in placentas from normal versus abnormal pregnancy outcomes. Chemosphere 34:1535–1547
   PubMed Web of Science ®Google Scholar
• Paakki P, Kirkinen P, Helin H, et al. (2000). Antepartum glucocorticoid therapy suppresses human placental xenobiotic and steroid metabolizing enzymes. Placenta 21:241–246
   PubMed Web of Science ®Google Scholar
• Pasanen M, Helin-Martikainen HL, Pelkonen O, Kirkinen P. (1997). Intrahepatic cholestasis of pregnancy impairs the activities of human placental xenobiotic and steroid metabolizing enzymes in vitro. Placenta 18:37–41
   PubMed Web of Science ®Google Scholar
• Pascussi JM, Gerbal-Chaloin S, Drocourt L, et al. (2003). The expression of CYP2B6, CYP2C9 and CYP3A4 genes: A tangle of networks of nuclear and steroid receptors. Biochim Biophys Acta 1619:243–253
   PubMed Web of Science ®Google Scholar
• Patel FA, Funder JW, Challis JR. (2003). Mechanism of cortisol/progesterone antagonism in the regulation of 15-hydroxyprostaglandin dehydrogenase activity and messenger ribonucleic acid levels in human chorion and placental trophoblast cells at term. J Clin Endocrinol Metab 88:2922–2933
   PubMed Web of Science ®Google Scholar
• Pavek P, Cerveny L, Svecova L, et al. (2007). Examination of Glucocorticoid receptor alpha-mediated transcriptional regulation of P-glycoprotein, CYP3A4, and CYP2C9 genes in placental trophoblast cell lines. Placenta 28:1004–1011
   PubMed Web of Science ®Google Scholar
• Pavek P, Dvorak Z. (2008). Xenobiotic-induced transcriptional regulation of xenobiotic metabolizing enzymes of the cytochrome P450 superfamily in human extrahepatic tissues. Curr Drug Metab 9:129–143
   PubMed Web of Science ®Google Scholar
• Pavek P, Pospechova K, Svecova L, et al. (2010). Intestinal cell-specific vitamin D receptor (VDR)-mediated transcriptional regulation of CYP3A4 gene. Biochem Pharmacol 79:277–287
   PubMed Web of Science ®Google Scholar
• Pavek P, Staud F, Fendrich Z, et al. (2003). Examination of the functional activity of P-glycoprotein in the rat placental barrier using rhodamine 123. J Pharmacol Exp Ther 305:1239–1250
   PubMed Web of Science ®Google Scholar
• Pospechova K, Rozehnal V, Stejskalova L, et al. (2009). Expression and activity of vitamin D receptor in the human placenta and in choriocarcinoma BeWo and JEG-3 cell lines. Mol Cell Endocrinol 299:178–187
   PubMed Web of Science ®Google Scholar
• Prouillac C, Koraichi F, Videmann B, et al. (2012). In vitro toxicological effects of estrogenic mycotoxins on human placental cells: Structure activity relationships. Toxicol Appl Pharmacol 259:366–375
   PubMed Web of Science ®Google Scholar
• Rasheed A, Hines RN, McCarver-May DG. (1997). Variation in induction of human placental CYP2E1: Possible role in susceptibility to fetal alcohol syndrome? Toxicol Appl Pharmacol 144:396–400
   PubMed Web of Science ®Google Scholar
• Remmer H. (1959). [The acceleration of evipan oxidation and the demethylation of methylaminopyrine by barbiturates]. Naunyn Schmiedebergs Arch Exp Pathol Pharmakol 237:296–307
   PubMedGoogle Scholar
• Rosenfeld MG, Lunyak VV, Glass CK. (2006). Sensors and signals: A coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev 20:1405–1428
   PubMed Web of Science ®Google Scholar
• Ryan AJ, James MO, Ben-Zvi Z, et al. (1976). Hepatic and extrahepatic metabolism of 14C-styrene oxide. Environ Health Perspect 17:135–144
   PubMed Web of Science ®Google Scholar
• Schmiedlin-Ren P, Thummel KE, Fisher JM, et al. (1997). Expression of enzymatically active CYP3A4 by Caco-2 cells grown on extracellular matrix-coated permeable supports in the presence of 1alpha,25-dihydroxyvitamin D3. Mol Pharmacol 51:741–754
   PubMed Web of Science ®Google Scholar
• Schroder HJ. (1995). Comparative aspects of placental exchange functions. Eur J Obstet Gynecol Reprod Biol 63:81–90
   PubMed Web of Science ®Google Scholar
• Schuetz EG, Wrighton SA, Barwick JL, Guzelian PS. (1984). Induction of cytochrome P-450 by glucocorticoids in rat liver. I. Evidence that glucocorticoids and pregnenolone 16 alpha-carbonitrile regulate de novo synthesis of a common form of cytochrome P-450 in cultures of adult rat hepatocytes and in the liver in vivo. J Biol Chem 259:1999–2006
   PubMed Web of Science ®Google Scholar
• Seckl JR, Holmes MC. (2007). Mechanisms of disease: Glucocorticoids, their placental metabolism and fetal ‘programming' of adult pathophysiology. Nat Clin Pract Endocrinol Metab 3:479–488
   PubMedGoogle Scholar
• Seliskar M, Rozman D. (2007). Mammalian cytochromes P450–importance of tissue specificity. Biochim Biophys Acta 1770:458–466
   PubMed Web of Science ®Google Scholar
• Serrano MA, Macias RI, Briz O, et al. (2007). Expression in human trophoblast and choriocarcinoma cell lines, BeWo, Jeg-3 and JAr of genes involved in the hepatobiliary-like excretory function of the placenta. Placenta 28:107–117
   PubMed Web of Science ®Google Scholar
• Sesardic D, Pasanen M, Pelkonen O, Boobis AR. (1990). Differential expression and regulation of members of the cytochrome P450IA gene subfamily in human tissues. Carcinogenesis 11:1183–1188
   PubMed Web of Science ®Google Scholar
• Shin JS, Choi MY, Longtine MS, Nelson DM. (2010). Vitamin D effects on pregnancy and the placenta. Placenta 31:1027–1034
   PubMed Web of Science ®Google Scholar
• Speeg KV, Jr, Harrison RW. (1979). The ontogony of the human placental glucocorticoid receptor and inducibility of heat-stable alkaline phosphatase. Endocrinology 104:1364–1368
   PubMed Web of Science ®Google Scholar
• Spink DC, Eugster HP, Lincoln DW, 2nd, et al. (1992). 17 beta-estradiol hydroxylation catalyzed by human cytochrome P450 1A1: A comparison of the activities induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in MCF-7 cells with those from heterologous expression of the cDNA. Arch Biochem Biophys 293:342–348
   PubMed Web of Science ®Google Scholar
• Staudinger JL, Woody S, Sun M, Cui W. (2013). Nuclear-receptor-mediated regulation of drug- and bile-acid-transporter proteins in gut and liver. Drug Metab Rev 45:48–59
   PubMed Web of Science ®Google Scholar
• Stejskalova L, Pavek P. (2011). The function of cytochrome P450 1A1 enzyme (CYP1A1) and aryl hydrocarbon receptor (AhR) in the placenta. Curr Pharm Biotechnol 12:715–730
   PubMed Web of Science ®Google Scholar
• Stejskalova L, Vecerova L, Perez LM, et al. (2011). Aryl hydrocarbon receptor and aryl hydrocarbon nuclear translocator expression in human and rat placentas and transcription activity in human trophoblast cultures. Toxicol Sci 123:26–36
   PubMed Web of Science ®Google Scholar
• Stejskalova L, Vrzal R, Rulcova A, et al. (2013). Effects of glucocorticoids on cytochrome P450 1A1 (CYP1A1) expression in isolated human placental trophoblast. J Appl Biomed. [Epub ahead of print]. doi:10.2478/v10136-012-0022-y
   Google Scholar
• Sun M, Kingdom J, Baczyk D, et al. (2006). Expression of the multidrug resistance P-glycoprotein, (ABCB1 glycoprotein) in the human placenta decreases with advancing gestation. Placenta 27:602–609
   PubMed Web of Science ®Google Scholar
• Sun M, Ramirez M, Challis JR, Gibb W. (1996). Immunohistochemical localization of the glucocorticoid receptor in human fetal membranes and decidua at term and preterm delivery. J Endocrinol 149:243–248
   PubMed Web of Science ®Google Scholar
• Syme MR, Paxton JW, Keelan JA. (2004). Drug transfer and metabolism by the human placenta. Clin Pharmacokinet 43:487–514
   PubMed Web of Science ®Google Scholar
• Tan KP, Wang B, Yang M, et al. (2010). Aryl hydrocarbon receptor is a transcriptional activator of the human breast cancer resistance protein (BCRP/ABCG2). Mol Pharmacol 78:175–185
   PubMed Web of Science ®Google Scholar
• Teng S., Piquette-Miller M. (2008). Regulation of transporters by nuclear hormone receptors: Implications during inflammation. Mol Pharm 5:67-76
   PubMed Web of Science ®Google Scholar
• Tirona RG, Kim RB. (2005). Nuclear receptors and drug disposition gene regulation. J Pharm Sci 94:1169–1186
   PubMed Web of Science ®Google Scholar
• Tirona RG, Leake BF, Wolkoff AW, Kim RB. (2003). Human organic anion transporting polypeptide-C (SLC21A6) is a major determinant of rifampin-mediated pregnane X receptor activation. J Pharmacol Exp Ther 304:223–228
   PubMed Web of Science ®Google Scholar
• Tomi M, Nishimura T, Nakashima E. (2011). Mother-to-fetus transfer of antiviral drugs and the involvement of transporters at the placental barrier. J Pharm Sci 100:3708--18
   Google Scholar
• Ugele B, Bahn A, Rex-Haffner M. (2008). Functional differences in steroid sulfate uptake of organic anion transporter 4 (OAT4) and organic anion transporting polypeptide 2B1 (OATP2B1) in human placenta. J Steroid Biochem Mol Biol 111:1–6
   PubMed Web of Science ®Google Scholar
• Vahakangas K, Myllynen P. (2009). Drug transporters in the human blood-placental barrier. Br J Pharmacol 158:665–678
   PubMed Web of Science ®Google Scholar
• Vahakangas K, Raunio H, Pasanen M, et al. (1989). Comparison of the formation of benzo[a]pyrene diolepoxide-DNA adducts in vitro by rat and human microsomes: Evidence for the involvement of P-450IA1 and P-450IA2. J Biochem Toxicol 4:79–86
   PubMedGoogle Scholar
• Vaught JB, Gurtoo HL, Parker NB, et al. (1979). Effect of smoking on benzo(a)pyrene metabolism by human placental microsomes. Cancer Res 39:3177–3183
   PubMed Web of Science ®Google Scholar
• Vondracek J, Umannova L, Machala M. (2011). Interactions of the aryl hydrocarbon receptor with inflammatory mediators: Beyond CYP1A regulation. Curr Drug Metab 12:89–103
   PubMed Web of Science ®Google Scholar
• Vrzal R, Stejskalova L, Monostory K, et al. (2009). Dexamethasone controls aryl hydrocarbon receptor (AhR)-mediated CYP1A1 and CYP1A2 expression and activity in primary cultures of human hepatocytes. Chem Biol Interact 179:288–296
   PubMed Web of Science ®Google Scholar
• Waddell BJ, Benediktsson R, Brown RW, Seckl JR. (1998). Tissue-specific messenger ribonucleic acid expression of 11beta-hydroxysteroid dehydrogenase types 1 and 2 and the glucocorticoid receptor within rat placenta suggests exquisite local control of glucocorticoid action. Endocrinology 139:1517–1523
   PubMed Web of Science ®Google Scholar
• Wang H, Lee EW, Zhou L, et al. (2008). Progesterone receptor (PR) isoforms PRA and PRB differentially regulate expression of the breast cancer resistance protein in human placental choriocarcinoma BeWo cells. Mol Pharmacol 73:845–854
   PubMed Web of Science ®Google Scholar
• Wang H, Zhou L, Gupta A, et al. (2006). Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am J Physiol Endocrinol Metab 290:E798–807
   PubMed Web of Science ®Google Scholar
• Welch RM, Harrison YE, Conney AH, et al. (1968). Cigarette smoking: Stimulatory effect on metabolism of 3,4-benzpyrene by enzymes in human placenta. Science 160:541–542
   PubMed Web of Science ®Google Scholar
• Whyatt RM, Bell DA, Jedrychowski W, et al. (1998). Polycyclic aromatic hydrocarbon-DNA adducts in human placenta and modulation by CYP1A1 induction and genotype. Carcinogenesis 19:1389–1392
   PubMed Web of Science ®Google Scholar
• Whyatt RM, Garte SJ, Cosma G, et al. (1995). CYP1A1 messenger RNA levels in placental tissue as a biomarker of environmental exposure. Cancer Epidemiol Biomarkers Prev 4:147–153
   PubMed Web of Science ®Google Scholar
• Xu C, Li CY, Kong AN. (2005). Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 28:249–268
   PubMed Web of Science ®Google Scholar
• Yamamoto J, Ihara K, Nakayama H, et al. (2004). Characteristic expression of aryl hydrocarbon receptor repressor gene in human tissues: Organ-specific distribution and variable induction patterns in mononuclear cells. Life Sci 74:1039–1049
   PubMed Web of Science ®Google Scholar
• Yoshinari K, Yoda N, Toriyabe T, Yamazoe Y. (2012). Constitutive androstane receptor transcriptionally activates human CYP1A1 and CYP1A2 genes through a common regulatory element in the 5′-flanking region. Biochem Pharmacol 79:261–269
   Web of Science ®Google Scholar
• Zhu BT, Cai MX, Spink DC, et al. (2002). Stimulatory effect of cigarette smoking on the 15 alpha-hydroxylation of estradiol by human term placenta. Clin Pharmacol Ther 71:311–324
   PubMed Web of Science ®Google Scholar