Transcription factor-mediated regulation of the BCRP/ABCG2 efflux transporter: a review across tissues and species

References

• Doyle LA, Yang W, Abruzzo LV, et al. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15665–15670.
   Google Scholar
• Khunweeraphong N, Stockner T, Kuchler K. The structure of the human ABC transporter ABCG2 reveals a novel mechanism for drug extrusion. Sci Rep. 2017 Oct 23;7(1):13767.
   Google Scholar
• Rosenberg MF, Bikadi Z, Chan J, et al. The human breast cancer resistance protein (BCRP/ABCG2) shows conformational changes with mitoxantrone. Structure. 2010 Mar 14;18(4):482–493.
   Google Scholar
• Mao Q. BCRP/ABCG2 in the placenta: expression, function and regulation. Pharm Res. 2008 Jun;25(6):1244–1255.
   Google Scholar
• Ni Z, Bikadi Z, Rosenberg MF, et al. Structure and function of the human breast cancer resistance protein (BCRP/ABCG2). Curr Drug Metab. 2010 Sep;11(7):603–617.
   Google Scholar
• Maliepaard M, Scheffer GL, Faneyte IF, et al. Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res. 2001 Apr 15;61(8):3458–3464.
   Google Scholar
• Natarajan K, Xie Y, Baer MR, et al. Role of breast cancer resistance protein (BCRP/ABCG2) in cancer drug resistance. Biochem Pharmacol. 2012 Apr 15;83(8):1084–1103.
   Google Scholar
• Jonker JW, Smit JW, Brinkhuis RF, et al. Role of breast cancer resistance protein in the bioavailability and fetal penetration of topotecan. J Natl Cancer Inst. 2000 Oct 18;92(20):1651–1656.
   Google Scholar
• Mao Q, Unadkat JD. Role of the breast cancer resistance protein (BCRP/ABCG2) in drug transport–an update. Aaps J. 2015 Jan;17(1):65–82.
   Google Scholar
• Imai Y, Nakane M, Kage K, et al. C421A polymorphism in the human breast cancer resistance protein gene is associated with low expression of Q141K protein and low-level drug resistance. Mol Cancer Ther. 2002 Jun;1(8):611–616.
   Google Scholar
• Bircsak KM, Moscovitz JE, Wen X, et al. Interindividual regulation of the breast cancer resistance protein/ABCG2 transporter in term human placentas. Drug Metab Dispos. 2018 May;46(5):619–627.
   Google Scholar
• Sparreboom A, Loos WJ, Burger H, et al. Effect of ABCG2 genotype on the oral bioavailability of topotecan. Cancer Biol Ther. 2005 Jun;4(6):650–658.
   Google Scholar
• Sparreboom A, Gelderblom H, Marsh S, et al. Diflomotecan pharmacokinetics in relation to ABCG2 421C>A genotype. Clin Pharmacol Ther. 2004 Jul;76(1):38–44.
   Google Scholar
• Woodward OM, Kottgen A, Coresh J, et al. Identification of a urate transporter, ABCG2, with a common functional polymorphism causing gout. Proc Natl Acad Sci U S A. 2009 Jun 23;106(25):10338–10342.
   Google Scholar
• Anzai N, Kanai Y, Endou H. New insights into renal transport of urate. Curr Opin Rheumatol. 2007 Mar;19(2):151–157.
   Google Scholar
• Stiburkova B, Pavelcova K, Zavada J, et al. Functional non-synonymous variants of ABCG2 and gout risk. Rheumatology (Oxford). 2017 Nov 1;56(11):1982–1992.
   Google Scholar
• Matsuo H, Takada T, Ichida K, et al. ABCG2/BCRP dysfunction as a major cause of gout. Nucleosides Nucleotides Nucleic Acids. 2011 Dec;30(12):1117–1128.
   Google Scholar
• Woodward OM. ABCG2: the molecular mechanisms of urate secretion and gout. Am J Physiol Renal Physiol. 2015 Sep 15;309(6):F485–8.
   Google Scholar
• Evseenko DA, Paxton JW, Keelan JA. ABC drug transporter expression and functional activity in trophoblast-like cell lines and differentiating primary trophoblast. Am J Physiol Regul Integr Comp Physiol. 2006 May;290(5):R1357–65.
   Google Scholar
• Prouillac C, Videmann B, Mazallon M, et al. Induction of cells differentiation and ABC transporters expression by a myco-estrogen, zearalenone, in human choriocarcinoma cell line (BeWo). Toxicology. 2009 Sep 19;263(2–3):100–107.
   Google Scholar
• Lye P, Bloise E, Nadeem L, et al. Glucocorticoids modulate multidrug resistance transporters in the first trimester human placenta. J Cell Mol Med. 2018 Jul;22(7):3652–3660.
   Google Scholar
• Evseenko DA, Paxton JW, Keelan JA. The xenobiotic transporter ABCG2 plays a novel role in differentiation of trophoblast-like BeWo cells. Placenta. 2007 Apr;28(Suppl A):S116–20.
   Google Scholar
• Ruebner M, Langbein M, Strissel PL, et al. Regulation of the human endogenous retroviral Syncytin-1 and cell-cell fusion by the nuclear hormone receptors PPARgamma/RXRalpha in placentogenesis. J Cell Biochem. 2012 Jul;113(7):2383–2396.
   Google Scholar
• Jebbink J, Veenboer G, Boussata S, et al. Total bile acids in the maternal and fetal compartment in relation to placental ABCG2 expression in preeclamptic pregnancies complicated by HELLP syndrome. Biochim Biophys Acta. 2015 Jan;1852(1):131–136.
   Google Scholar
• Evseenko DA, Murthi P, Paxton JW, et al. The ABC transporter BCRP/ABCG2 is a placental survival factor, and its expression is reduced in idiopathic human fetal growth restriction. Faseb J. 2007 Nov;21(13):3592–3605.
   Google Scholar
• Ding R, Jin S, Pabon K, et al. A role for ABCG2 beyond drug transport: regulation of autophagy. Autophagy. 2016 May 3;12(5):737–751.
   Google Scholar
• Erdei Z, Sarkadi B, Brozik A, et al. Dynamic ABCG2 expression in human embryonic stem cells provides the basis for stress response. Eur Biophys J. 2013 Mar;42(2–3):169–179.
   Google Scholar
• Ning ZF, Huang YJ, Lin TX, et al. Subpopulations of stem-like cells in side population cells from the human bladder transitional cell cancer cell line T24. J Int Med Res. 2009 May-Jun;37(3):621–630.
   Google Scholar
• Ingram WJ, Crowther LM, Little EB, et al. ABC transporter activity linked to radiation resistance and molecular subtype in pediatric medulloblastoma. Exp Hematol Oncol. 2013 Oct 4;2(1):26.
   Google Scholar
• Li X, Huang J, Yi P, et al. Single-chain estrogen receptors (ERs) reveal that the ERalpha/beta heterodimer emulates functions of the ERalpha dimer in genomic estrogen signaling pathways. Mol Cell Biol. 2004 Sep;24(17):7681–7694.
   Google Scholar
• Marino M, Galluzzo P, Ascenzi P. Estrogen signaling multiple pathways to impact gene transcription. Curr Genomics. 2006;7(8):497–508.
   Google Scholar
• Monroe DG, Secreto FJ, Subramaniam M, et al. Estrogen receptor alpha and beta heterodimers exert unique effects on estrogen- and tamoxifen-dependent gene expression in human U2OS osteosarcoma cells. Mol Endocrinol. 2005 Jun;19(6):1555–1568.
   Google Scholar
• Ee PL, He X, Ross DD, et al. Modulation of breast cancer resistance protein (BCRP/ABCG2) gene expression using RNA interference. Mol Cancer Ther. 2004 Dec;3(12):1577–1583.
   Google Scholar
• Ee PL, Kamalakaran S, Tonetti D, et al. Identification of a novel estrogen response element in the breast cancer resistance protein (ABCG2) gene. Cancer Res. 2004 Feb 15;64(4):1247–1251.
   Google Scholar
• Yasuda S, Kobayashi M, Itagaki S, et al. Response of the ABCG2 promoter in T47D cells and BeWo cells to sex hormone treatment. Mol Biol Rep. 2009 Sep;36(7):1889–1896.
   Google Scholar
• Zhang Y, Zhou G, Wang H, et al. Transcriptional upregulation of breast cancer resistance protein by 17beta-estradiol in ERalpha-positive MCF-7 breast cancer cells. Oncology. 2006;71(5–6):446–455.
   Google Scholar
• Imai Y, Ishikawa E, Asada S, et al. Estrogen-mediated post transcriptional down-regulation of breast cancer resistance protein/ABCG2. Cancer Res. 2005 Jan 15;65(2):596–604.
   Google Scholar
• Bukovsky A, Cekanova M, Caudle MR, et al. Expression and localization of estrogen receptor-alpha protein in normal and abnormal term placentae and stimulation of trophoblast differentiation by estradiol. Reprod Biol Endocrinol. 2003 Feb 6;1:13.
   Google Scholar
• Albrecht ED, Pepe GJ. Estrogen regulation of placental angiogenesis and fetal ovarian development during primate pregnancy. Int J Dev Biol. 2010;54(2–3):397–408.
   Google Scholar
• Bukovsky A, Caudle MR, Cekanova M, et al. Placental expression of estrogen receptor beta and its hormone binding variant–comparison with estrogen receptor alpha and a role for estrogen receptors in asymmetric division and differentiation of estrogen-dependent cells. Reprod Biol Endocrinol. 2003 Apr 15;1:36.
   Google Scholar
• Evseenko DA, Paxton JW, Keelan JA. Independent regulation of apical and basolateral drug transporter expression and function in placental trophoblasts by cytokines, steroids, and growth factors. Drug Metab Dispos. 2007 Apr;35(4):595–601.
   Google Scholar
• Wang H, Zhou L, Gupta A, et al. Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am J Physiol Endocrinol Metab. 2006 May;290(5):E798–807.
   Google Scholar
• Wang H, Unadkat JD, Mao Q. Hormonal regulation of BCRP expression in human placental BeWo cells. Pharm Res. 2008 Feb;25(2):444–452.
   Google Scholar
• Yasuda S, Itagaki S, Hirano T, et al. Effects of sex hormones on regulation of ABCG2 expression in the placental cell line BeWo. J Pharm Pharm Sci. 2006;9(1):133–139.
   Google Scholar
• Bircsak KM, Gupta V, Yuen PY, et al. Genetic and dietary regulation of glyburide efflux by the human placental breast cancer resistance protein transporter. J Pharmacol Exp Ther. 2016 Apr;357(1):103–113.
   Google Scholar
• Mathias AA, Hitti J, Unadkat JD. P-glycoprotein and breast cancer resistance protein expression in human placentae of various gestational ages. Am J Physiol Regul Integr Comp Physiol. 2005 Oct;289(4):R963–9.
   Google Scholar
• Wang H, Wu X, Hudkins K, et al. Expression of the breast cancer resistance protein (Bcrp1/Abcg2) in tissues from pregnant mice: effects of pregnancy and correlations with nuclear receptors. Am J Physiol Endocrinol Metab. 2006 Dec;291(6):E1295–304.
   Google Scholar
• Kellis JT Jr., Vickery LE. Purification and characterization of human placental aromatase cytochrome P-450. J Biol Chem. 1987 Mar 25;262(9):4413–4420.
   Google Scholar
• Stirone C, Duckles SP, Krause DN. Multiple forms of estrogen receptor-alpha in cerebral blood vessels: regulation by estrogen. Am J Physiol Endocrinol Metab. 2003 Jan;284(1):E184–92.
   Google Scholar
• Hartz AM, Madole EK, Miller DS, et al. Estrogen receptor beta signaling through phosphatase and tensin homolog/phosphoinositide 3-kinase/Akt/glycogen synthase kinase 3 down-regulates blood-brain barrier breast cancer resistance protein. J Pharmacol Exp Ther. 2010 Aug;334(2):467–476.
   Google Scholar
• Hartz AM, Mahringer A, Miller DS, et al. 17-beta-Estradiol: a powerful modulator of blood-brain barrier BCRP activity. J Cereb Blood Flow Metab. 2010 Oct;30(10):1742–1755.
   Google Scholar
• Mahringer A, Fricker G. BCRP at the blood-brain barrier: genomic regulation by 17beta-estradiol. Mol Pharm. 2010 Oct 4;7(5):1835–1847.
   Google Scholar
• Nickel S, Mahringer A. The xenoestrogens ethinylestradiol and bisphenol A regulate BCRP at the blood-brain barrier of rats. Xenobiotica. 2014 Nov;44(11):1046–1054.
   Google Scholar
• Kastner P, Krust A, Turcotte B, et al. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. Embo J. 1990 May;9(5):1603–1614.
   Google Scholar
• Dressing GE, Hagan CR, Knutson TP, et al. Progesterone receptors act as sensors for mitogenic protein kinases in breast cancer models. Endocr Relat Cancer. 2009 Jun;16(2):351–361.
   Google Scholar
• Edwards DP, Altmann M, DeMarzo A, et al. Progesterone receptor and the mechanism of action of progesterone antagonists. J Steroid Biochem Mol Biol. 1995 Jun;53(1–6):449–458.
   Google Scholar
• Wang H, Lee EW, Zhou L, et al. Progesterone receptor (PR) isoforms PRA and PRB differentially regulate expression of the breast cancer resistance protein in human placental choriocarcinoma BeWo cells. Mol Pharmacol. 2008 Mar;73(3):845–854.
   Google Scholar
• Kalabis GM, Petropoulos S, Gibb W, et al. Breast cancer resistance protein (Bcrp1/Abcg2) in mouse placenta and yolk sac: ontogeny and its regulation by progesterone. Placenta. 2007 Oct;28(10):1073–1081.
   Google Scholar
• Wu X, Zhang X, Sun L, et al. Progesterone negatively regulates BCRP in progesterone receptor-positive human breast cancer cells. Cell Physiol Biochem. 2013;32(2):344–354.
   Google Scholar
• Wu X, Zhang X, Zhang H, et al. Progesterone receptor downregulates breast cancer resistance protein expression via binding to the progesterone response element in breast cancer. Cancer Sci. 2012 May;103(5):959–967.
   Google Scholar
• Park D, Cheon M, Kim C, et al. Progesterone together with estradiol promotes luteinizing hormone beta-subunit mRNA stability in rat pituitary cells cultured in vitro. Eur J Endocrinol. 1996 Feb;134(2):236–242.
   Google Scholar
• Wu JC, Miller WL. Progesterone shortens poly(A) tails of the mRNAs for alpha and beta subunits of ovine luteinizing hormone. Biol Reprod. 1991 Aug;45(2):215–220.
   Google Scholar
• Joyeux C, Rochefort H, Chalbos D. Progestin increases gene transcription and messenger ribonucleic acid stability of fatty acid synthetase in breast cancer cells. Mol Endocrinol. 1989 Apr;3(4):681–686.
   Google Scholar
• Lan L, Vinci JM, Melendez JA, et al. Progesterone mediates decreases in uterine smooth muscle cell interleukin-1alpha by a mechanism involving decreased stability of IL-1alpha mRNA. Mol Cell Endocrinol. 1999 Sep 10;155(1–2):123–133.
   Google Scholar
• Inoue K, Creveling CR. Induction of catechol-O-methyltransferase in the luminal epithelium of rat uterus by progesterone. J Histochem Cytochem. 1991 Jun;39(6):823–828.
   Google Scholar
• Inoue K, Creveling CR. Induction of catechol-O-methyltransferase in the luminal epithelium of rat uterus by progesterone: inhibition by RU-486. Drug Metab Dispos. 1995 Mar;23(3):430–432.
   Google Scholar
• Gapter LA, Magnuson NS, Ng KY, et al. Pim-1 kinase expression during murine mammary development. Biochem Biophys Res Commun. 2006 Jul 7;345(3):989–997.
   Google Scholar
• Pasqualini JR, Cosquer-Clavreul C, Gelly C. Rapid modulation by progesterone and tamoxifen of estradiol effects on nuclear histone acetylation in the uterus of the fetal guinea pig. Biochim Biophys Acta. 1983 Jan 20;739(1):137–140.
   Google Scholar
• To KK, Zhan Z, Litman T, et al. Regulation of ABCG2 expression at the 3ʹ untranslated region of its mRNA through modulation of transcript stability and protein translation by a putative microRNA in the S1 colon cancer cell line. Mol Cell Biol. 2008 Sep;28(17):5147–5161.
   Google Scholar
• To KK, Robey RW, Knutsen T, et al. Escape from hsa-miR-519c enables drug-resistant cells to maintain high expression of ABCG2. Mol Cancer Ther. 2009 Oct;8(10):2959–2968.
   Google Scholar
• Pan YZ, Morris ME, Yu AM. MicroRNA-328 negatively regulates the expression of breast cancer resistance protein (BCRP/ABCG2) in human cancer cells. Mol Pharmacol. 2009 Jun;75(6):1374–1379.
   Google Scholar
• Wang F, Xue X, Wei J, et al. Hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations. Br J Cancer. 2010 Aug 10;103(4):567–574.
   Google Scholar
• Turner JG, Gump JL, Zhang C, et al. ABCG2 expression, function, and promoter methylation in human multiple myeloma. Blood. 2006 Dec 1;108(12):3881–3889.
   Google Scholar
• To KK, Zhan Z, Bates SE. Aberrant promoter methylation of the ABCG2 gene in renal carcinoma. Mol Cell Biol. 2006 Nov;26(22):8572–8585.
   Google Scholar
• Xie Y, Xu K, Linn DE, et al. The 44-kDa Pim-1 kinase phosphorylates BCRP/ABCG2 and thereby promotes its multimerization and drug-resistant activity in human prostate cancer cells. J Biol Chem. 2008 Feb 8;283(6):3349–3356.
   Google Scholar
• Hirai T, Fukui Y, Motojima K. PPARalpha agonists positively and negatively regulate the expression of several nutrient/drug transporters in mouse small intestine. Biol Pharm Bull. 2007 Nov;30(11):2185–2190.
   Google Scholar
• Moffit JS, Aleksunes LM, Maher JM, et al. Induction of hepatic transporters multidrug resistance-associated proteins (Mrp) 3 and 4 by clofibrate is regulated by peroxisome proliferator-activated receptor alpha. J Pharmacol Exp Ther. 2006 May;317(2):537–545.
   Google Scholar
• Muerhoff AS, Griffin KJ, Johnson EF. The peroxisome proliferator-activated receptor mediates the induction of CYP4A6, a cytochrome P450 fatty acid omega-hydroxylase, by clofibric acid. J Biol Chem. 1992 Sep 25;267(27):19051–19053.
   Google Scholar
• Hoque MT, Robillard KR, Bendayan R. Regulation of breast cancer resistant protein by peroxisome proliferator-activated receptor alpha in human brain microvessel endothelial cells. Mol Pharmacol. 2012 Apr;81(4):598–609.
   Google Scholar
• Hoque MT, Shah A, More V, et al. In vivo and ex vivo regulation of breast cancer resistant protein (Bcrp) by peroxisome proliferator-activated receptor alpha (Pparα) at the blood-brain barrier. J Neurochem. 2015 Oct 14;135:1113–1122.
   Google Scholar
• More VR, Campos CR, Evans RA, et al. PPAR-alpha, a lipid-sensing transcription factor, regulates blood-brain barrier efflux transporter expression. J Cereb Blood Flow Metab. 2017 Apr;37(4):1199–1212.
   Google Scholar
• Eldasher LM, Wen X, Little MS, et al. Hepatic and renal Bcrp transporter expression in mice treated with perfluorooctanoic acid. Toxicology. 2013 Apr 5;306:108–113.
   Google Scholar
• Szatmari I, Vamosi G, Brazda P, et al. Peroxisome proliferator-activated receptor gamma-regulated ABCG2 expression confers cytoprotection to human dendritic cells. J Biol Chem. 2006 Aug 18;281(33):23812–23823.
   Google Scholar
• Wright JA, Haslam IS, Coleman T, et al. Breast cancer resistance protein BCRP (ABCG2)-mediated transepithelial nitrofurantoin secretion and its regulation in human intestinal epithelial (Caco-2) layers. Eur J Pharmacol. 2011 Dec 15;672(1–3):70–76.
   Google Scholar
• Lin Y, Bircsak KM, Gorczyca L, et al. Regulation of the placental BCRP transporter by PPAR gamma. J Biochem Mol Toxicol. 2017 May;31(5).
   Google Scholar
• Yamamoto Y, Moore R, Goldsworthy TL, et al. The orphan nuclear receptor constitutive active/androstane receptor is essential for liver tumor promotion by phenobarbital in mice. Cancer Res. 2004 Oct 15;64(20):7197–7200.
   Google Scholar
• Yang H, Wang H. Signaling control of the constitutive androstane receptor (CAR). Protein Cell. 2014 Feb;5(2):113–123.
   Google Scholar
• Phillips JM, Yamamoto Y, Negishi M, et al. Orphan nuclear receptor constitutive active/androstane receptor-mediated alterations in DNA methylation during phenobarbital promotion of liver tumorigenesis. Toxicol Sci. 2007 Mar;96(1):72–82.
   Google Scholar
• Huang W, Zhang J, Washington M, et al. Xenobiotic stress induces hepatomegaly and liver tumors via the nuclear receptor constitutive androstane receptor. Mol Endocrinol. 2005 Jun;19(6):1646–1653.
   Google Scholar
• Benoki S, Yoshinari K, Chikada T, et al. Transactivation of ABCG2 through a novel cis-element in the distal promoter by constitutive androstane receptor but not pregnane X receptor in human hepatocytes. Arch Biochem Biophys. 2012 Jan 15;517(2):123–130.
   Google Scholar
• Lemmen J, Tozakidis IE, Bele P, et al. Constitutive androstane receptor upregulates Abcb1 and Abcg2 at the blood-brain barrier after CITCO activation. Brain Res. 2013 Mar 21;1501:68–80.
   Google Scholar
• Wang X, Sykes DB, Miller DS. Constitutive androstane receptor-mediated up-regulation of ATP-driven xenobiotic efflux transporters at the blood-brain barrier. Mol Pharmacol. 2010 Sep;78(3):376–383.
   Google Scholar
• Jigorel E, Le Vee M, Boursier-Neyret C, et al. Differential regulation of sinusoidal and canalicular hepatic drug transporter expression by xenobiotics activating drug-sensing receptors in primary human hepatocytes. Drug Metab Dispos. 2006 Oct;34(10):1756–1763.
   Google Scholar
• Jouan E, Le Vee M, Denizot C, et al. drug transporter expression and activity in human hepatoma HuH-7 cells. Pharmaceutics. 2016 Dec 28;9(1):3.
   Google Scholar
• Kliewer SA, Goodwin B, Willson TM. The nuclear pregnane X receptor: a key regulator of xenobiotic metabolism. Endocr Rev. 2002 Oct;23(5):687–702.
   Google Scholar
• Lemmen J, Tozakidis IE, Galla HJ. Pregnane X receptor upregulates ABC-transporter Abcg2 and Abcb1 at the blood-brain barrier. Brain Res. 2013 Jan 23;1491:1–13.
   Google Scholar
• Timsit YE, Negishi M. CAR and PXR: the xenobiotic-sensing receptors. Steroids. 2007 Mar;72(3):231–246.
   Google Scholar
• Whyte-Allman SK, Hoque MT, Jenabian MA, et al. Xenobiotic nuclear receptors pregnane X receptor and constitutive androstane receptor regulate antiretroviral drug efflux transporters at the blood-testis barrier. J Pharmacol Exp Ther. 2017 Dec;363(3):324–335.
   Google Scholar
• Gahir SS, Piquette-Miller M. Gestational and pregnane X receptor-mediated regulation of placental ATP-binding cassette drug transporters in mice. Drug Metab Dispos. 2011 Mar;39(3):465–471.
   Google Scholar
• Oscarson M, Zanger UM, Rifki OF, et al. Transcriptional profiling of genes induced in the livers of patients treated with carbamazepine. Clin Pharmacol Ther. 2006 Nov;80(5):440–456.
   Google Scholar
• Anapolsky A, Teng S, Dixit S, et al. The role of pregnane X receptor in 2-acetylaminofluorene-mediated induction of drug transport and -metabolizing enzymes in mice. Drug Metab Dispos. 2006 Mar;34(3):405–409.
   Google Scholar
• Han Y, Sugiyama Y. Expression and regulation of breast cancer resistance protein and multidrug resistance associated protein 2 in BALB/c mice. Biol Pharm Bull. 2006 May;29(5):1032–1035.
   Google Scholar
• Teng S, Piquette-Miller M. The involvement of the pregnane X receptor in hepatic gene regulation during inflammation in mice. J Pharmacol Exp Ther. 2005 Feb;312(2):841–848.
   Google Scholar
• Naspinski C, Gu X, Zhou GD, et al. Pregnane X receptor protects HepG2 cells from BaP-induced DNA damage. Toxicol Sci. 2008 Jul;104(1):67–73.
   Google Scholar
• Qiao EQ, Yang HJ. Effect of pregnane X receptor expression on drug resistance in breast cancer. Oncol Lett. 2014 Apr;7(4):1191–1196.
   Google Scholar
• Dauchy S, Miller F, Couraud PO, et al. Expression and transcriptional regulation of ABC transporters and cytochromes P450 in hCMEC/D3 human cerebral microvascular endothelial cells. Biochem Pharmacol. 2009 Mar 1;77(5):897–909.
   Google Scholar
• Deng L, Lin-Lee YC, Claret FX, et al. 2-acetylaminofluorene up-regulates rat mdr1b expression through generating reactive oxygen species that activate NF-kappa B pathway. J Biol Chem. 2001 Jan 5;276(1):413–420.
   Google Scholar
• Granberg L, Ostergren A, Brandt I, et al. CYP1A1 and CYP1B1 in blood-brain interfaces: CYP1A1-dependent bioactivation of 7,12-dimethylbenz(a)anthracene in endothelial cells. Drug Metab Dispos. 2003 Mar;31(3):259–265.
   Google Scholar
• Kawajiri K, Fujii-Kuriyama Y. Cytochrome P450 gene regulation and physiological functions mediated by the aryl hydrocarbon receptor. Arch Biochem Biophys. 2007 Aug 15;464(2):207–212.
   Google Scholar
• Petrulis JR, Perdew GH. The role of chaperone proteins in the aryl hydrocarbon receptor core complex. Chem Biol Interact. 2002 Sep 20;141(1–2):25–40.
   Google Scholar
• Bradfield CA, Glover E, Poland A. Purification and N-terminal amino acid sequence of the Ah receptor from the C57BL/6J mouse. Mol Pharmacol. 1991 Jan;39(1):13–19.
   Google Scholar
• Kafafi SA, Afeefy HY, Ali AH, et al. Binding of polychlorinated biphenyls to the aryl hydrocarbon receptor. Environ Health Perspect. 1993 Oct;101(5):422–428.
   Google Scholar
• Ebert B, Seidel A, Lampen A. Identification of BCRP as transporter of benzo[a]pyrene conjugates metabolically formed in Caco-2 cells and its induction by Ah-receptor agonists. Carcinogenesis. 2005 Oct;26(10):1754–1763.
   Google Scholar
• Tan KP, Wang B, Yang M, et al. Aryl hydrocarbon receptor is a transcriptional activator of the human breast cancer resistance protein (BCRP/ABCG2). Mol Pharmacol. 2010 Aug;78(2):175–185.
   Google Scholar
• Tompkins LM, Li H, Li L, et al. A novel xenobiotic responsive element regulated by aryl hydrocarbon receptor is involved in the induction of BCRP/ABCG2 in LS174T cells. Biochem Pharmacol. 2010 Dec 01;80(11):1754–1761.
   Google Scholar
• Sayyed K, Vee ML, Abdel-Razzak Z, et al. Alteration of human hepatic drug transporter activity and expression by cigarette smoke condensate. Toxicology. 2016 Jul 1;363–364:58–71.
   Google Scholar
• Stejskalova L, Vecerova L, Perez LM, et al. Aryl hydrocarbon receptor and aryl hydrocarbon nuclear translocator expression in human and rat placentas and transcription activity in human trophoblast cultures. Toxicol Sci. 2011 Sep;123(1):26–36.
   Google Scholar
• Neradugomma NK, Liao MZ, Mao Q. Buprenorphine, Norbuprenorphine, R-Methadone, and S-Methadone upregulate BCRP/ABCG2 expression by activating aryl hydrocarbon receptor in human placental trophoblasts. Mol Pharmacol. 2017 Mar;91(3):237–249.
   Google Scholar
• Wang X, Hawkins BT, Miller DS. Aryl hydrocarbon receptor-mediated up-regulation of ATP-driven xenobiotic efflux transporters at the blood-brain barrier. Faseb J. 2011 Feb;25(2):644–652.
   Google Scholar
• Campos CR, Schroter C, Wang X, et al. ABC transporter function and regulation at the blood-spinal cord barrier. J Cereb Blood Flow Metab. 2012 Aug;32(8):1559–1566.
   Google Scholar
• Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007;47:89–116.
   Google Scholar
• Morito N, Yoh K, Itoh K, et al. Nrf2 regulates the sensitivity of death receptor signals by affecting intracellular glutathione levels. Oncogene. 2003 Dec 18;22(58):9275–9281.
   Google Scholar
• Rangasamy T, Cho CY, Thimmulappa RK, et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest. 2004 Nov;114(9):1248–1259.
   Google Scholar
• Hagiya Y, Adachi T, Ogura S, et al. Nrf2-dependent induction of human ABC transporter ABCG2 and heme oxygenase-1 in HepG2 cells by photoactivation of porphyrins: biochemical implications for cancer cell response to photodynamic therapy. J Exp Ther Oncol. 2008;7(2):153–167.
   Google Scholar
• Singh A, Wu H, Zhang P, et al. Expression of ABCG2 (BCRP) is regulated by Nrf2 in cancer cells that confers side population and chemoresistance phenotype. Mol Cancer Ther. 2010 Aug;9(8):2365–2376.
   Google Scholar
• Adachi T, Nakagawa H, Chung I, et al. Nrf2-dependent and -independent induction of ABC transporters ABCC1, ABCC2, and ABCG2 in HepG2 cells under oxidative stress. J Exp Ther Oncol. 2007;6(4):335–348.
   Google Scholar
• Choi BH, Ryu DY, Ryoo IG, et al. NFE2L2/NRF2 silencing-inducible miR-206 targets c-MET/EGFR and suppresses BCRP/ABCG2 in cancer cells. Oncotarget. 2017 Dec 5;8(63):107188–107205.
   Google Scholar
• Ryoo IG, Kim G, Choi BH, et al. Involvement of NRF2 signaling in doxorubicin resistance of cancer stem cell-enriched colonospheres. Biomol Ther (Seoul). 2016 Sep 1;24(5):482–488.
   Google Scholar
• Choi BH, Ryoo IG, Kang HC, et al. The sensitivity of cancer cells to pheophorbide a-based photodynamic therapy is enhanced by Nrf2 silencing. PLoS One. 2014;9(9):e107158.
   Google Scholar
• Jeong HS, Ryoo IG, Kwak MK. Regulation of the expression of renal drug transporters in KEAP1-knockdown human tubular cells. Toxicol In Vitro. 2015 Aug;29(5):884–892.
   Google Scholar
• Wang X, Campos CR, Peart JC, et al. Nrf2 upregulates ATP binding cassette transporter expression and activity at the blood-brain and blood-spinal cord barriers. J Neurosci. 2014 Jun 18;34(25):8585–8593.
   Google Scholar
• Li X, Pan YZ, Seigel GM, et al. Breast cancer resistance protein BCRP/ABCG2 regulatory microRNAs (hsa-miR-328, −519c and −520h) and their differential expression in stem-like ABCG2+ cancer cells. Biochem Pharmacol. 2011 Mar 15;81(6):783–792.
   Google Scholar
• Nakagawa H, Wakabayashi-Nakao K, Tamura A, et al. Disruption of N-linked glycosylation enhances ubiquitin-mediated proteasomal degradation of the human ATP-binding cassette transporter ABCG2. Febs J. 2009 Dec;276(24):7237–7252.
   Google Scholar
• Draheim V, Reichel A, Weitschies W, et al. N-glycosylation of ABC transporters is associated with functional activity in sandwich-cultured rat hepatocytes. Eur J Pharm Sci. 2010 Oct 9;41(2):201–209.
   Google Scholar
• Szilagyi JT, Vetrano AM, Laskin JD, et al. Localization of the placental BCRP/ABCG2 transporter to lipid rafts: role for cholesterol in mediating efflux activity. Placenta. 2017;55:29–36.
   Google Scholar
• Liu Y, Yin Y, Sheng Q, et al. Association of ABCC2-24C>T polymorphism with high-dose methotrexate plasma concentrations and toxicities in childhood acute lymphoblastic leukemia. PLoS One. 2014;9(1):e82681.
   Google Scholar
• Choi YH, Yu AM. ABC transporters in multidrug resistance and pharmacokinetics, and strategies for drug development. Curr Pharm Des. 2014;20(5):793–807.
   Google Scholar
• Chen S, Wang H, Li Z, et al. Interaction of WBP2 with ERalpha increases doxorubicin resistance of breast cancer cells by modulating MDR1 transcription. Br J Cancer. 2018 May 1;119:182–192.
   Google Scholar
• Shi JF, Yang N, Ding HJ, et al. ERalpha directly activated the MDR1 transcription to increase paclitaxel-resistance of ERalpha-positive breast cancer cells in vitro and in vivo. Int J Biochem Cell Biol. 2014;53:35–45.
   Google Scholar
• Coles LD, Lee IJ, Voulalas PJ, et al. Estradiol and progesterone-mediated regulation of P-gp in P-gp overexpressing cells (NCI-ADR-RES) and placental cells (JAR). Mol Pharm. 2009 Nov-Dec;6(6):1816–1825.
   Google Scholar
• Kim WY, Benet LZ. P-glycoprotein (P-gp/MDR1)-mediated efflux of sex-steroid hormones and modulation of P-gp expression in vitro. Pharm Res. 2004 Jul;21(7):1284–1293.
   Google Scholar
• Zampieri L, Bianchi P, Ruff P, et al. Differential modulation by estradiol of P-glycoprotein drug resistance protein expression in cultured MCF7 and T47D breast cancer cells. Anticancer Res. 2002 Jul-Aug;22(4):2253–2259.
   Google Scholar
• Edavana VK, Penney RB, Yao-Borengasser A, et al. Fulvestrant up regulates UGT1A4 and MRPs through ERalpha and c-Myb pathways: a possible primary drug disposition mechanism. Springerplus. 2013;2:620.
   Google Scholar
• Zhang H, Jing X, Wu X, et al. Suppression of multidrug resistance by rosiglitazone treatment in human ovarian cancer cells through downregulation of FZD1 and MDR1 genes. Anticancer Drugs. 2015 Aug;26(7):706–715.
   Google Scholar
• Konieczna A, Novakova V, Medalova J, et al. Thiazolidinediones regulate the level of ABC transporters expression on lung cancer cells. Klin Onkol. 2015;28(6):431–438.
   Google Scholar
• Manceau S, Giraud C, Decleves X, et al. Lack of P-glycoprotein induction by rifampicin and phenobarbital in human lymphocytes. Int J Pharm. 2010 Aug 16;395(1–2):98–103.
   Google Scholar
• Wang L, Ma L, Lin Y, et al. Leflunomide increases hepatic exposure to methotrexate and its metabolite by differentially regulating multidrug resistance-associated protein Mrp2/3/4 transporters via peroxisome proliferator-activated receptor alpha activation. Mol Pharmacol. 2018 Jun;93(6):563–574.
   Google Scholar
• Maher JM, Aleksunes LM, Dieter MZ, et al. Nrf2- and PPAR alpha-mediated regulation of hepatic Mrp transporters after exposure to perfluorooctanoic acid and perfluorodecanoic acid. Toxicol Sci. 2008 Dec;106(2):319–328.
   Google Scholar
• Alexander RL, Bates DJ, Wright MW, et al. Modulation of nitrated lipid signaling by multidrug resistance protein 1 (MRP1): glutathione conjugation and MRP1-mediated efflux inhibit nitrolinoleic acid-induced, PPARgamma-dependent transcription activation. Biochemistry. 2006 Jun 27;45(25):7889–7896.
   Google Scholar
• Maher JM, Cheng X, Slitt AL, et al. Induction of the multidrug resistance-associated protein family of transporters by chemical activators of receptor-mediated pathways in mouse liver. Drug Metab Dispos. 2005 Jul;33(7):956–962.
   Google Scholar
• Olinga P, Elferink MG, Draaisma AL, et al. Coordinated induction of drug transporters and phase I and II metabolism in human liver slices. Eur J Pharm Sci. 2008 Apr 23;33(4–5):380–389.
   Google Scholar
• Kullak-Ublick GA, Becker MB. Regulation of drug and bile salt transporters in liver and intestine. Drug Metab Rev. 2003 Nov;35(4):305–317.
   Google Scholar
• Lu Y, Yan Y, Wang XF. Antiepileptic drug-induced multidrug resistance P-glycoprotein overexpression in astrocytes cultured from rat brains. Chin Med J (Engl). 2004 Nov;117(11):1682–1686.
   Google Scholar
• Merino G, Alvarez AI, Pulido MM, et al. Breast cancer resistance protein (BCRP/ABCG2) transports fluoroquinolone antibiotics and affects their oral availability, pharmacokinetics, and milk secretion. Drug Metab Dispos. 2006 Apr;34(4):690–695.
   Google Scholar
• van Hoppe S, Sparidans RW, Wagenaar E, et al. Breast cancer resistance protein (BCRP/ABCG2) and P-glycoprotein (P-gp/ABCB1) transport afatinib and restrict its oral availability and brain accumulation. Pharmacol Res. 2017;120:43–50.
   Google Scholar
• Durmus S, Sparidans RW, van Esch A, et al. Breast cancer resistance protein (BCRP/ABCG2) and P-glycoprotein (P-GP/ABCB1) restrict oral availability and brain accumulation of the PARP inhibitor rucaparib (AG-014699). Pharm Res. 2015 Jan;32(1):37–46.
   Google Scholar
• Durmus S, Sparidans RW, Wagenaar E, et al. Oral availability and brain penetration of the B-RAFV600E inhibitor vemurafenib can be enhanced by the P-GLYCOprotein (ABCB1) and breast cancer resistance protein (ABCG2) inhibitor elacridar. Mol Pharm. 2012 Nov 5;9(11):3236–3245.
   Google Scholar
• Vlaming ML, van Esch A, van de Steeg E, et al. Impact of abcc2 [multidrug resistance-associated protein (MRP) 2], abcc3 (MRP3), and abcg2 (breast cancer resistance protein) on the oral pharmacokinetics of methotrexate and its main metabolite 7-hydroxymethotrexate. Drug Metab Dispos. 2011 Aug;39(8):1338–1344.
   Google Scholar
• Prueksaritanont T, Chu X, Gibson C, et al. Drug-drug interaction studies: regulatory guidance and an industry perspective. Aaps J. 2013 Jul;15(3):629–645.
   Google Scholar
• Simonson SG, Raza A, Martin PD, et al. Rosuvastatin pharmacokinetics in heart transplant recipients administered an antirejection regimen including cyclosporine. Clin Pharmacol Ther. 2004 Aug;76(2):167–177.
   Google Scholar
• Kusuhara H, Furuie H, Inano A, et al. Pharmacokinetic interaction study of sulphasalazine in healthy subjects and the impact of curcumin as an in vivo inhibitor of BCRP. Br J Pharmacol. 2012 Jul;166(6):1793–1803.
   Google Scholar
• Pham PA, la Porte CJ, Lee LS, et al. Differential effects of tipranavir plus ritonavir on atorvastatin or rosuvastatin pharmacokinetics in healthy volunteers. Antimicrob Agents Chemother. 2009 Oct;53(10):4385–4392.
   Google Scholar
• Chen YJ, Huang WC, Wei YL, et al. Elevated BCRP/ABCG2 expression confers acquired resistance to gefitinib in wild-type EGFR-expressing cells. PLoS One. 2011;6(6):e21428.
   Google Scholar
• Washio I, Nakanishi T, Ishiguro N, et al. Impact of breast cancer resistance protein expression on the in vitro efficacy of anticancer drugs in pancreatic cancer cell lines. Drug Metab Dispos. 2018 Mar;46(3):214–222.
   Google Scholar
• Badolo L, Jensen B, Sall C, et al. Evaluation of 309 molecules as inducers of CYP3A4, CYP2B6, CYP1A2, OATP1B1, OCT1, MDR1, MRP2, MRP3 and BCRP in cryopreserved human hepatocytes in sandwich culture. Xenobiotica. 2015 Feb;45(2):177–187.
   Google Scholar
• Liu L, Zhou L, Hu S, et al. Down-regulation of ABCG2 and ABCB4 transporters in the placenta of rats exposed to cadmium. Oncotarget. 2016 Jun 21;7(25):38154–38163.
   Google Scholar
• Kummu M, Sieppi E, Wallin K, et al. Cadmium inhibits ABCG2 transporter function in BeWo choriocarcinoma cells and MCF-7 cells overexpressing ABCG2. Placenta. 2012 Oct;33(10):859–865.
   Google Scholar
• Rigalli JP, Scholz PN, Tocchetti GN, et al. The phytoestrogens daidzein and equol inhibit the drug transporter BCRP/ABCG2 in breast cancer cells: potential chemosensitizing effect. Eur J Nutr. 2019 Feb;58(1):139–150.
   Google Scholar