ATP-binding cassette transporters in reproduction: A new frontier

Human Reproduction Update

Volumn 22, Issue 2, 2016, Pages 164-181

  Bloise, E ^a,b   Ortiga Carvalho, T M ^a   Reis, F M ^b   Lye, S J ^c,d,e   Gibb, W ^f   Matthews, S G ^c,d,e  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e MOUNT SINAI HOSPITAL   (Canada)

^f UNIVERSITY OF OTTAWA   (Canada)

Author keywords

ABC transporters; Breast cancer related protein; Decidua; Fetal membranes; Multidrug resistance associated proteins; Myometrium; Ovary; P glycoprotein; Placenta; Testes

Indexed keywords

ABC TRANSPORTER; BREAST CANCER RESISTANCE PROTEIN; LIPID; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1;

DECIDUA; EMBRYO DEVELOPMENT; EMBRYO SEGMENTATION; FETUS MEMBRANE; HUMAN; MOTHER FETUS RELATIONSHIP; OVARY; PLACENTA; PREGNANCY; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN FUNCTION; REPRODUCTION; REVIEW; TESTIS; UTERUS; ANIMAL; BLASTOCYST; FEMALE; GENETICS; METABOLISM; PHYSIOLOGY; TISSUE DISTRIBUTION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BLASTOCYST; EMBRYONIC DEVELOPMENT; FEMALE; HUMANS; PLACENTA; PREGNANCY; REPRODUCTION; TISSUE DISTRIBUTION;

EID: 84959872204     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmv049     Document Type: Review

References (194)

1. Agassandian M, Mathur SN, Zhou J, Field FJ, Mallampalli RK. Oxysterols trigger ABCA1-mediated basolateral surfactant efflux. Am J Respir Cell Mol Biol 2004; 31:227-233.
2. Alam SM, Konno T, Dai G, Lu L, Wang D, Dunmore JH, Godwin AR, Soares MJ. A uterine decidual cell cytokine ensures pregnancy-dependent adaptations to a physiological stressor. Development 2007;134:407-415.
3. Albrecht C, Soumian S, Tetlow N, Patel P, Sullivan MH, Lakasing L, Nicolaides K, Williamson C. Placental ABCA1 expression is reduced in primary antiphospholipid syndrome compared to pre-eclampsia and controls. Placenta 2007;28:701-708.
4. Albrecht C, Nikitina L, Wenger F, Baumann M, Surbek D, Korner M. Localisation of ABCA1 in first trimester and term placental tissues. Placenta 2010;31: 741-742.
5. Augustine LM, Markelewicz RJ Jr, Boekelheide K, Cherrington NJ. Xenobiotic and endobiotic transporter mRNA expression in the blood-testis barrier. Drug Metab Dispos 2005;33:182-189.
6. Axiotis CA,Guarch R, Merino MJ, Laporte N,NeumannRD. P-glycoprotein expression is increased in human secretory and gestational endometrium. Lab Invest 1991; 65:577-581.
7. Aye IL, Paxton JW, Evseenko DA, Keelan JA. Expression, localisation and activity of ATP-binding cassette (ABC) family of drug transporters in human amnion membranes. Placenta 2007;28:868-877.
8. AyeIL, SinghAT,KeelanJA. Transport of lipidsbyABCproteins: interactions andimplications for cellular toxicity, viability and function. Chem Biol Interact 2009; 180:327-339.
9. Aye IL, Waddell BJ, Mark PJ, Keelan JA. Placental ABCA1 and ABCG1 transporters efflux cholesterol and protect trophoblasts from oxysterol induced toxicity. Biochim Biophys Acta 2010;1801:1013-1024.
10. Aye IL, Keelan JA. Placental ABC transporters, cellular toxicity and stress in pregnancy. Chem Biol Interact 2013;203:456-466.
11. Azzaroli F, Mennone A, Feletti V, Simoni P, Baglivo E, Montagnani M, Rizzo N, Pelusi G, DE Aloysio D, Lodato F et al. Clinical trial: modulation of human placental multidrug resistance proteins in cholestasis of pregnancy by ursodeoxycholic acid. Aliment Pharmacol Ther 2007;26:1139-1146.
12. Baardman ME, Kerstjens-FrederikseWS,Berger RM, BakkerMK,Hofstra RM, Plosch T. The role of maternal-fetal cholesterol transport in early fetal life: current insights. Biol Reprod 2013;88:24.
13. Baello S, Iqbal M, Bloise E, Javam M, GibbW, Matthews SG. TGF-beta1 regulation of multidrug resistance P-glycoprotein in the developing male blood-brain barrier. Endocrinology 2014;155:475-484.
14. Barnes KM, Dickstein B, Cutler GB Jr, Fojo T, Bates SE. Steroid treatment, accumulation, and antagonism of P-glycoprotein in multidrug-resistant cells. Biochemistry 1996;35:4820-4827.
15. Bart J, Groen HJ, van der Graaf WT, Hollema H, Hendrikse NH, Vaalburg W, Sleijfer DT, de Vries EG. An oncological view on the blood-testis barrier. Lancet Oncol 2002;3:357-363.
16. Bart J, Hollema H, Groen HJ, de Vries EG, Hendrikse NH, Sleijfer DT,Wegman TD, Vaalburg W, van der Graaf WT. The distribution of drug-efflux pumps, P-gp, BCRP, MRP1 and MRP2, in the normal blood-testis barrier and in primary testicular tumours. Eur J Cancer 2004;40:2064-2070.
17. Baumann M, Korner M, Huang X,Wenger F, Surbek D, Albrecht C. Placental ABCA1 and ABCG1expression in gestational disease: pre-eclampsia affectsABCA1levels in syncytiotrophoblasts. Placenta 2013;34:1079-1086.
18. Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G. Comparative aspects of implantation. Reproduction 2009;138:195-209.
19. Bellamy WT. P-glycoproteins and multidrug resistance. Annu Rev Pharmacol Toxicol 1996;36:161-183.
20. Bellarosa C, Bortolussi G, Tiribelli C. The role of ABC transporters in protecting cells from bilirubin toxicity. Curr Pharm Des 2009;15:2884-2892.
21. Bhattacharjee J, Ietta F, Giacomello E, Bechi N, Romagnoli R, Fava A, Paulesu L. Expression and localization of ATP-binding cassette transporter A1 (ABCA1) in first trimester and term human placenta. Placenta 2010;31:423-430.
22. Bleier BS, Nocera AL, Iqbal H, Hoang JD, Feldman RE, Han X. P-glycoprotein functions as an immunomodulator in healthy human primary nasal epithelial cells. Int Forum Allergy Rhinol 2013;3:433-438.
23. Bloise E, Torricelli M, Novembri R, Borges LE, Carrarelli P, Reis FM, Petraglia F. Heat-killed Lactobacillus rhamnosus GG modulates urocortin and cytokine release in primary trophoblast cells. Placenta 2010;31:867-872.
24. Bloise E, Lin W, Liu X, Simbulan R, Kolahi KS, Petraglia F, Maltepe E, Donjacour A, Rinaudo P. Impaired placental nutrient transport in mice generated by in vitro fertilization. Endocrinology 2012;153:3457-3467.
25. Bloise E, Bhuiyan M, Audette MC, Petropoulos S, Javam M, Gibb W, Matthews SG. Prenatal endotoxemia and placental drug transport in the mouse: placental size-specific effects. PLoS One 2013;8:e65728.
26. Bloise E, Feuer SK, Rinaudo PF. Comparative intrauterine development and placental function of ART concepti: implications for human reproductive medicine and animal breeding. Hum Reprod Update 2014;20:822-839.
27. Borst P, deWolf C, van deWetering K. Multidrug resistance-associated proteins 3, 4, and 5. Pflugers Arch 2007;453:661-673.
28. Brown KA, Dore M, Lussier JG, Sirois J. Human chorionic gonadotropin-dependent up-regulation of genes responsible for estrogen sulfoconjugation and export in granulosa cells of luteinizing preovulatory follicles. Endocrinology 2006;147:4222-4233.
29. Burton GJ, Woods AW, Jauniaux E, Kingdom JC. Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 2009;30:473-482.
30. Camus M, Delomenie C, Didier N, Faye A, Gil S, Dauge MC, Mabondzo A, Farinotti R. Increased expression of MDR1 mRNAs and P-glycoprotein in placentas from HIV-1 infected women. Placenta 2006;27:699-706.
31. Cao C, Pressman EK, Cooper EM, Guillet R, Westerman M, O'Brien KO. Placental heme receptor LRP1 correlates with the heme exporter FLVCR1 and neonatal iron status. Reproduction 2014;148:295-302.
32. Cartwright JE, Fraser R, Leslie K,Wallace AE, James JL. Remodelling at the maternal-fetal interface: relevance to human pregnancy disorders. Reproduction 2010; 140:803-813.
33. ChaddhaV, Viero S, Huppertz B, Kingdom J. Developmental biology of the placenta and the origins of placental insufficiency. Semin Fetal Neonatal Med 2004;9:357-369.
34. Challis JRG, Matthews SG, GibbW, Lye SJ. Endocrine and paracrine regulation of birth at term and preterm. Endocr Rev 2000;21:514-550.
35. Chapman K, Holmes M, Seckl J. 11beta-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. Physiol Rev 2013;93:1139-1206.
36. Cho E, Montgomery RB, Mostaghel EA. Minireview: SLCO and ABC transporters: a role for steroid transport in prostate cancer progression. Endocrinology 2014; 155:4124-4132.
37. Christiansen-Weber TA, Voland JR,WuY, Ngo K, Roland BL, Nguyen S, Peterson PA, Fung-Leung WP. Functional loss of ABCA1 in mice causes severe placental malformation, aberrant lipid distribution, and kidney glomerulonephritis as well as high-density lipoprotein cholesterol deficiency. Am J Pathol 2000;157:1017-1029.
38. Ciarmela P, Islam MS, Reis FM, Gray PC, Bloise E, Petraglia F, ValeW, Castellucci M. Growth factors and myometrium: biological effects in uterine fibroid and possible clinical implications. Hum Reprod Update 2011;17:772-790.
39. Coles LD, Lee IJ, Voulalas PJ, Eddington ND. Estradiol and progesterone-mediated regulation of P-gp in P-gp overexpressing cells (NCI-ADR-RES) and placental cells (JAR). Mol Pharm 2009;6:1816-1825.
40. Conti N, Torricelli M, Voltolini C, Vannuccini S, Clifton VL, Bloise E, Petraglia F. Term histologic chorioamnionitis: a heterogeneous condition. Eur J Obstet Gynecol Reprod Biol 2015;188:34-38.
41. Cordon-Cardo C, O'Brien JP, Casals D, Rittman-Grauer L, Biedler JL, Melamed MR, Bertino JR. Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Proc Natl Acad Sci USA 1989;86:695-698.
42. Dankers AC, Sweep FC, Pertijs JC, Verweij V, van den Heuvel JJ, Koenderink JB, Russel FG, Masereeuw R. Localization of breast cancer resistance protein (Bcrp) in endocrine organs and inhibition of its transport activity by steroid hormones. Cell Tissue Res 2012;349:551-563.
43. Dankers AC, Roelofs MJ, Piersma AH, Sweep FC, Russel FG, van den Berg M, van Duursen MB, Masereeuw R. Endocrine disruptors differentially target ATP-binding cassette transporters in the blood-testis barrier and affect Leydig cell testosterone secretion in vitro. Toxicol Sci 2013;136:382-391.
44. deWaartDR, PaulusmaCC, Kunne C,Oude Elferink RP. Multidrug resistance associated protein 2 mediates transport of prostaglandin E2. Liver Int 2006; 26:362-368.
45. Dean M, Annilo T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 2005;6:123-142.
46. Desforges M, Sibley CP. Placental nutrient supply and fetal growth. Int J Dev Biol 2010; 54:377-390.
47. Desuzinges-Mandon E, Arnaud O, Martinez L, Huche F, Di Pietro A, Falson P. ABCG2 transports and transfers heme to albumin through its large extracellular loop. J Biol Chem 2010;285:33123-33133.
48. Devoto L, Kohen P, Vega M, Castro O, Gonzalez RR, Retamales I, Carvallo P, Christenson LK, Strauss JF. Control of human luteal steroidogenesis. Mol Cell Endocrinol 2002;186:137-141.
49. Dilworth MR, Sibley CP. Review: Transport across the placenta of mice and women. Placenta 2013;34(Suppl):S34-S39.
50. Dowling O, Chatterjee PK, Gupta M, Tam Tam HB, Xue X, Lewis D, Rochelson B, Metz CN. Magnesium sulfate reduces bacterial LPS-induced inflammation at the maternal-fetal interface. Placenta 2012;33:392-398.
51. Drouineaud V, Sagot P,Garrido C, Logette E,Deckert V,Gambert P, Jimenez C, Staels B, Lagrost L, Masson D. Inhibition of progesterone production in human luteinized granulosa cells treated with LXR agonists. Mol Hum Reprod 2007;13:373-379.
52. Dube E, Ethier-Chiasson M, Lafond J. Modulation of cholesterol transport by insulin-treated gestational diabetes mellitus in human full-term placenta. Biol Reprod 2013;88:16.
53. Elbling L, Berger W, Rehberger A, Waldhor T, Micksche M. P-glycoprotein regulates chemosensitivity in earlydevelopmental stagesof themouse.FASEBJ1993;7:1499-1506.
54. Ericsson A, Hamark B, Powell TL, Jansson T. Glucose transporter isoform 4 is expressed in the syncytiotrophoblast of first trimester human placenta. Hum Reprod 2005;20:521-530.
55. Evseenko DA, Murthi P, Paxton JW, Reid G, Emerald BS, Mohankumar KM, Lobie PE, Brennecke SP, Kalionis B, Keelan JA. The ABC transporter BCRP/ABCG2 is a placental survival factor, and its expression is reduced in idiopathic human fetal growth restriction. FASEB J 2007a; 21:3592-3605.
56. 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 2007b; 35:595-601.
57. FarkeC, Viturro E, Meyer HH,Albrecht C. Identification of the bovine cholesterol efflux regulatory protein ABCA1 and its expression in various tissues. J Anim Sci 2006; 84:2887-2894.
58. Folkers GFEPCRMHKG. Transporters as Drug Carriers: Structure, Function, Substrates. Wiley-VCH, 2009.
59. Fukuda H, Arai M, Soh T, Yamauchi N, Hattori MA. Progesterone regulation of the expression and function of multidrug resistance type I in porcine granulosa cells. Reprod Toxicol 2006;22:62-68.
60. Fukuda H, He PJ, Yokota K, Soh T, Yamauchi N, Hattori MA. Progesterone-dependent and -independent expression of the multidrug resistance type I gene in porcine granulosa cells. Mol Cell Biochem 2007;298:179-186.
61. George AM, Jones PM. Perspectives on the structure-function of ABC transporters: the Switch and Constant Contact models. Prog Biophys Mol Biol 2012; 109:95-107.
62. Gibb W. The role of prostaglandins in human parturition. Ann Med 1998;30: 235-241.
63. GibbW, Sun M. Localization of prostaglandin H synthase type 2 protein and mRNA in term human fetal membranes and decidua. J Endocrinol 1996;150:497-503.
64. Gil S, Saura R, Forestier F, Farinotti R. P-glycoprotein expression of the human placenta during pregnancy. Placenta 2005;26:268-270.
65. Gori I, Rodriguez Y, Pellegrini C, Achtari C, Hornung D, Chardonnens E, Wunder D, Fiche M, Canny GO. Augmented epithelial multidrug resistance-associated protein 4 expression in peritoneal endometriosis: regulation by lipoxin A(4). Fertil Steril 2013;99:1965-1973 e1962.
66. Hauguel-de Mouzon S, Guerre-Millo M. The placenta cytokine network and inflammatory signals. Placenta 2006;27:794-798.
67. Helguera G, Eghbali M, Sforza D, MinosyanTY, Toro L, Stefani E. Changes in global gene expression in rat myometrium in transition from late pregnancy to parturition. Physiol Genomics 2009; 36:89-97.
68. Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992; 8:67-113.
69. Hodyl NA, Stark MJ, Butler M, Clifton VL. Placental P-glycoprotein is unaffected by timing of antenatal glucocorticoid therapy but reduced in SGA preterm infants. Placenta 2013;34:325-330.
70. HonoratM, Falson P, Terreux R, Di Pietro A, Dumontet C, Payen L. Multidrug resistance ABC transporter structure predictions by homology modeling approaches. Curr Drug Metab 2011; 12:268-277.
71. Hutson JR, Koren G, Matthews SG. Placental P-glycoprotein and breast cancer resistance protein: influence of polymorphisms on fetal drug exposure and physiology. Placenta 2010;31:351-357.
72. Ietta F, Bechi N,RomagnoliR,Bhattacharjee J, RealacciM, Di Vito M, Ferretti C, Paulesu L. 17{beta}-Estradiol modulates the macrophage migration inhibitory factor secretory pathway by regulating ABCA1 expression in human first-trimester placenta. Am J Physiol Endocrinol Metab 2010;298:E411-E418.
73. Ikonen E. Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol 2008;9:125-138.
74. Iqbal M, Gibb W, Matthews SG. Corticosteroid regulation of P-glycoprotein in the developing blood-brain barrier. Endocrinology 2011;152:1067-1079.
75. IqbalM, Ho HL, Petropoulos S,Moisiadis VG, GibbW,Matthews SG. Pro-inflammatory cytokine regulation of P-glycoprotein in the developing blood-brain barrier. PLoS One 2012;7:e43022.
76. Jaffer S, Shynlova O, Lye S. Mammalian target of rapamycin is activated in associationwith myometrial proliferation during pregnancy. Endocrinology 2009; 150:4672-4680.
77. Javam M, Audette MC, Iqbal M, Bloise E, GibbW, Matthews SG. Effect of oxygen on multidrug resistance in term human placenta. Placenta 2014;35:324-330.
78. Jin H, Audus KL. Effect of bisphenolAon drug efflux inBeWo, a human trophoblast-like cell line. Placenta 2005;26(Suppl A):S96-S103.
79. Kajihara T, Brosens JJ, Ishihara O. The role of FOXO1 in the decidual transformation of the endometrium and early pregnancy. Med Mol Morphol 2013;46:61-68.
80. Kalabis GM, Kostaki A, Andrews MH, Petropoulos S, GibbW, Matthews SG. Multidrug resistance phosphoglycoprotein (ABCB1) in the mouse placenta: fetal protection. Biol Reprod 2005;73:591-597.
81. Kalabis GM, Petropoulos S, Gibb W, Matthews SG. Breast cancer resistance protein (Bcrp1/Abcg2) in mouse placenta and yolk sac: ontogeny and its regulation by progesterone. Placenta 2007;28:1073-1081.
82. Kalabis GM, Petropoulos S, Gibb W, Matthews SG. Multidrug resistance phosphoglycoprotein (ABCB1) expression in the guinea pig placenta: developmental changes and regulation by betamethasone. Can J Physiol Pharmacol 2009;87:973-978.
83. Kaludjerovic J, Ward WE. The interplay between estrogen and fetal adrenal cortex. J Nutr Metab 2012;2012:837901.
84. Kapoor A, Petropoulos S, Matthews SG. Fetal programming of hypothalamic-pituitaryadrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Res Rev 2008;57:586-595.
85. Keppler D. The roles of MRP2, MRP3, OATP1B1, and OATP1B3 in conjugated hyperbilirubinemia. Drug Metab Dispos 2014;42:561-565.
86. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD. Cytokines, prostaglandins and parturition-a review. Placenta 2003;24(Suppl A):S33-S46.
87. Keelan JA, Aye IL, Mark PJ, Waddell BJ. ABCA1 and placental cholesterol efflux. Placenta 2011;32:708-709; author reply 710-701.
88. Klaassen CD, Aleksunes LM. Xenobiotic, bile acid, and cholesterol transporters: function and regulation. Pharmacol Rev 2010;62:1-96.
89. Klein DM, Wright SH, Cherrington NJ. Localization of multidrug resistance-associated proteins along the blood-testis barrier in rat, macaque, and human testis. Drug Metab Dispos 2014;42:89-93.
90. Koga K, Mor G. Expression and function of toll-like receptors at the maternal-fetal interface. Reprod Sci 2008;15:231-242.
91. KooijG,MizeeMR, vanHorssen J, ReijerkerkA,WitteME,Drexhage JA, van der Pol SM, van Het Hof B, Scheffer G, Scheper R et al. Adenosine triphosphate-binding cassette transporters mediate chemokine (C-C motif) ligand 2 secretion from reactive astrocytes: relevance to multiple sclerosis pathogenesis. Brain 2011;134:555-570; author reply 710-701.
92. Kooij G, Kroon J, Paul D, Reijerkerk A, Geerts D, van der Pol SM, van Het Hof B, Drexhage JA, van Vliet SJ, Hekking LH et al. P-glycoprotein regulates trafficking of CD8(+) T cells to the brain parenchyma. Acta Neuropathol 2014;127:699-711.
93. Krisher RL, Heuberger AL, Paczkowski M, Stevens J, Pospisil C, Prather RS, Sturmey RG, Herrick JR, Schoolcraft WB. Applying metabolomic analyses to the practice of embryology: physiology, development and assisted reproductive technology. Reprod Fertil Dev 2015;27:602-620.
94. Krishnamurthy P, Ross DD, Nakanishi T, Bailey-Dell K, Zhou S, Mercer KE, Sarkadi B, Sorrentino BP, Schuetz JD. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 2004;279:24218-24225.
95. Kunjachan S, Rychlik B, Storm G, Kiessling F, Lammers T. Multidrug resistance: physiological principles and nanomedical solutions. Adv Drug Deliv Rev 2013; 65:1852-1865.
96. Lacroix-Pepin N, Danyod G, Krishnaswamy N, Mondal S, Rong PM, Chapdelaine P, Fortier MA. The multidrug resistance-associated protein 4 (MRP4) appears as a functional carrier of prostaglandins regulated by oxytocin in the bovine endometrium. Endocrinology 2011;152:4993-5004.
97. Lager S, Powell TL. Regulation of nutrient transport across the placenta. J Pregnancy 2012;2012:179827.
98. LangmannT,MauererR,ZahnA,MoehleC,ProbstM,StremmelW, Schmitz G. Real-time reverse transcription-PCR expression profiling of the complete human ATP-binding cassette transporter superfamily in various tissues. Clin Chem 2003; 49:230-238.
99. Lankas GR, Wise LD, Cartwright ME, Pippert T, Umbenhauer DR. Placental P-glycoprotein deficiency enhances susceptibility to chemically induced birth defects in mice. Reprod Toxicol 1998;12:457-463.
100. Lee GY, Croop JM, Anderson E. Multidrug resistance gene expression correlates with progesterone production in dehydroepiandrosterone-induced polycystic and equine chorionic gonadotropin-stimulated ovaries of prepubertal rats. Biol Reprod 1998;58:330-337.
101. Lemos C, Kathmann I, Giovannetti E, Dekker H, Scheffer GL, Calhau C, Jansen G, Peters GJ. Folate deprivation induces BCRP (ABCG2) expression and mitoxantrone resistance in Caco-2 cells. Int J Cancer 2008;123:1712-1720.
102. Lin ZP, Zhu YL, Johnson DR, Rice KP, Nottoli T, Hains BC, McGrath J,Waxman SG, Sartorelli AC. Disruption of cAMP and prostaglandin E2 transport by multidrug resistance protein 4 deficiency alters cAMP-mediated signaling and nociceptive response. Mol Pharmacol 2008;73:243-251.
103. Long Y, Li Q, Li J, Cui Z. Molecular analysis, developmental function and heavy metal-induced expression of ABCC5 in zebrafish. Comp Biochem Physiol B Biochem Mol Biol 2011;158:46-55.
104. Lye P, Bloise E, Dunk C, Javam M, GibbW, Lye SJ, Matthews SG. Effect of oxygen on multidrug resistance in the first trimester human placenta. Placenta 2013;34: 817-823.
105. Lye P, Bloise E, Javam M, Gibb W, Lye SJ, Matthews SG. Impact of bacterial and viral challenge on multidrug resistance in first- and third-trimester human placenta. Am J Pathol 2015;185:1666-1675.
106. Macias H, Hinck L. Mammary gland development. Wiley Interdiscip Rev Dev Biol 2012; 1:533-557.
107. Macias RI, Marin JJ, Serrano MA. Excretion of biliary compounds during intrauterine life. World J Gastroenterol 2009;15:817-828.
108. Maher JM, Slitt AL, Cherrington NJ, Cheng X, Klaassen CD. Tissue distribution and hepatic and renal ontogeny of the multidrug resistance-associated protein (Mrp) family in mice. Drug Metab Dispos 2005;33:947-955.
109. Manceau S, Giraud C, Decleves X, Scherrmann JM, Artiguebieille F, Goffinet F, Chappuy H, Vinot C, Treluyer JM. ABC drug transporter and nuclear receptor expression in human cytotrophoblasts: influence of spontaneous syncytialization and induction by glucocorticoids. Placenta 2012;33:927-932.
110. Mark PJ, Augustus S, Lewis JL, Hewitt DP, Waddell BJ. Changes in the placental glucocorticoid barrier during rat pregnancy: impact on placental corticosterone levels and regulation by progesterone. Biol Reprod 2009;80:1209-1215.
111. Marquez B, Van Bambeke F. ABC multidrug transporters: target formodulation of drug pharmacokinetics and drug-drug interactions. Curr Drug Targets 2011;12:600-620.
112. MasonCW, Buhimschi IA, Buhimschi CS, DongY,WeinerCP, SwaanPW. ATP-binding cassette transporter expression in human placenta as a function of pregnancy condition. Drug Metab Dispos 2011; 39:1000-1007.
113. Mason C, Lee GT, Dong Y, Zhou H, He L, Weiner CP. Effect of Prostaglandin E2 on Multidrug Resistance Transporters In Human Placental Cells. Drug Metab Dispos 2014;42:2077-2086.
114. 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;289:R963-R969.
115. Mazur CS, Marchitti SA, DimovaM, Kenneke JF, Lumen A, Fisher J. Human and ratABC transporter efflux of bisphenol a and bisphenol a glucuronide: interspecies comparison and implications for pharmacokinetic assessment. Toxicol Sci 2012; 128:317-325.
116. MeyerZuSchwabedissenHE,GrubeM,HeydrichB,LinnemannK, FuschC,KroemerHK, Jedlitschky G. 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 2005a; 166:39-48.
117. Meyer Zu Schwabedissen HE, Jedlitschky G, Gratz M, Haenisch S, Linnemann K, Fusch C, Cascorbi I, Kroemer HK. Variable expression of MRP2 (ABCC2) in human placenta: influence of gestational age and cellular differentiation. Drug Metab Dispos 2005b; 33:896-904.
118. Mitchell MD, Simpson KL, Keelan JA. Paradoxical proinflammatory actions of interleukin-10 in human amnion: potential roles in term and preterm labour. J Clin Endocrinol Metab 2004;89:4149-4152.
119. Mizutani T, Masuda M, Nakai E, Furumiya K, Togawa H, Nakamura Y, Kawai Y, Nakahira K, Shinkai S, Takahashi K. Genuine functions of P-glycoprotein (ABCB1). Curr Drug Metab 2008;9:167-174.
120. Moisiadis VG, Matthews SG. Glucocorticoids and fetal programming part 1: outcomes. Nat Rev Endocrinol 2014a; 10:391-402.
121. Moisiadis VG, Matthews SG. Glucocorticoids and fetal programming part 2: mechanisms. Nat Rev Endocrinol 2014b; 10:403-411.
122. Morgan JA, Cheepala SB,WangY,NealeG, Adachi M, NachagariD, Leggas M,ZhaoW, BoydK,Venkataramanan R et al.Deregulated hepatic metabolismexacerbates impaired testosterone production in Mrp4-deficient mice. J Biol Chem2012;287:14456-14466.
123. Mori M, Kasa S, Isozaki Y, Kamori T, Yamaguchi S, Ueda S, Kuwano T, Eguchi M, Isayama K, Nishimura S et al. Improvement of the cellular quality of cryopreserved bovine blastocysts accompanied by enhancement of the ATP-binding cassette sub-family B member 1 expression. Reprod Toxicol 2013;35:17-24.
124. Mouzat K, Prod'homme M, Volle DH, Sion B, Dechelotte P, Gauthier K, Vanacker JM, Lobaccaro JM. Oxysterol nuclear receptor LXRbeta regulates cholesterol homeostasis and contractile function in mouse uterus. J Biol Chem 2007;282:4693-4701.
125. Myatt L, Sun K. Role of fetal membranes in signaling of fetal maturation and parturition. Int J Dev Biol 2010;54:545-553.
126. Mylona P, Hoyland JA, Sibley CP. Sites of mRNA expression of the cystic fibrosis (CF) and multidrug resistance (MDR1) genes in the human placenta of early pregnancy: no evidence for complementary expression. Placenta 1999;20:493-496.
127. NagashigeM,Ushigome F, KoyabuN,Hirata K, Kawabuchi M,Hirakawa T, Satoh S, Tsukimori K, Nakano H, Uchiumi T et al. Basal membrane localization of MRP1 in human placental trophoblast. Placenta 2003;24:951-958.
128. Nies AT, Keppler D. The apical conjugate efflux pump ABCC2 (MRP2). Pflugers Arch 2007;453:643-659.
129. Nikitina L,Wenger F, Baumann M, Surbek D, Korner M, Albrecht C. Expression and localization pattern of ABCA1 in diverse human placental primary cells and tissues. Placenta 2011;32:420-430.
130. Nishimura M, Naito S. Tissue-specific mRNA expression profiles of human ATP-binding cassette and solute carrier transporter superfamilies. Drug Metab Pharmacokinet 2005;20:452-477.
131. Novembri R, Torricelli M, Bloise E, Conti N, Galeazzi LR, Severi FM, Petraglia F. Effects of urocortin 2 and urocortin 3 on IL-10 and TNF-alpha expression and secretion from human trophoblast explants. Placenta 2011;32:969-974.
132. Oram JF, Vaughan AM. ATP-Binding cassette cholesterol transporters and cardiovascular disease. Circ Res 2006;99:1031-1043.
133. Pappas JJ, Petropoulos S, Suderman M, Iqbal M, Moisiadis V, Turecki G, Matthews SG, Szyf M. The multidrug resistance 1 gene Abcb1 in brain and placenta: comparative analysis in human and guinea pig. PLoS One 2014;9:e111135.
134. Pavek P,Cerveny L, Svecova L,BryschM, Libra A, VrzalR,NachtigalP, Staud F,Ulrichova J, Fendrich Z et al. Examination of Glucocorticoid receptor alpha-mediated transcriptional regulation of P-glycoprotein, CYP3A4, and CYP2C9 genes in placental trophoblast cell lines. Placenta 2007;28:1004-1011.
135. Pawlik A, Baskiewicz-Masiuk M, Machalinski B, Safranow K, Gawronska-Szklarz B. Involvement of P-glycoprotein in the release of cytokines from peripheral blood mononuclear cells treated with methotrexate and dexamethasone. J Pharm Pharmacol 2005;57:1421-1425.
136. Petropoulos S, Kalabis GM, Gibb W, Matthews SG. Functional changes of mouse placental multidrug resistance phosphoglycoprotein (ABCB1) with advancing gestation and regulation by progesterone. Reprod Sci 2007;14:321-328.
137. Petropoulos S, Gibb W, Matthews SG. Developmental expression of multidrug resistance phosphoglycoprotein (P-gp) in the mouse fetal brain and glucocorticoid regulation. Brain Res 2010a; 1357:9-18.
138. Petropoulos S, Gibb W, Matthews SG. Effect of glucocorticoids on regulation of placental multidrug resistance phosphoglycoprotein (P-gp) in the mouse. Placenta 2010b; 31:803-810.
139. Petrovic V, Piquette-Miller M. Impact of polyinosinic/polycytidylic acid on placental and hepatobiliary drug transporters in pregnant rats. Drug Met ab Dispos 2010;38:1760-1766.
140. Petrovic V, Wang JH, Piquette-Miller M. Effect of endotoxin on the expression of placental drug transporters and glyburide disposition in pregnant rats. Drug Metab Dispos 2008;36:1944-1950.
141. Plosch T, Gellhaus A, van Straten EM,Wolf N, Huijkman NC, Schmidt M, Dunk CE, Kuipers F, Winterhager E. The liver X receptor (LXR) and its target gene ABCA1 are regulated upon low oxygen in human trophoblast cells: a reason for alterations in preeclampsia? Placenta 2010; 31:910-918.
142. Pringle KG, Kind KL, Sferruzzi-Perri AN, Thompson JG, Roberts CT. Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy. Hum Reprod Update 2010;16:415-431.
143. Prouillac C, Videmann B, Mazallon M, Lecoeur S. Induction of cells differentiation and ABC transporters expression by a myco-estrogen, zearalenone, in human choriocarcinoma cell line (BeWo). Toxicology 2009;263:100-107.
144. Puttabyatappa M, Vandevoort CA, Chaffin CL. hCG-induced down-regulation of PPARgamma and liver X receptors promotes periovulatory progesterone synthesis by macaque granulosa cells. Endocrinology 2010;151:5865-5872.
145. Qian X,ChengYH, Mruk DD,ChengCY. Breast cancer resistance protein (Bcrp) and the testis-an unexpected turn of events. Asian J Androl 2013;15:455-460.
146. Ramakrishnan U, Imhoff-Kunsch B, Martorell R. Maternal nutrition interventions to improve maternal, newborn, and child health outcomes. Nestle Nutr Inst Workshop Ser 2014;78:71-80.
147. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, Fisher SJ. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest 2004;114:744-754.
148. Reid G, Wielinga P, Zelcer N, van der Heijden I, Kuil A, de Haas M, Wijnholds J, Borst P. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc Natl Acad Sci USA 2003;100:9244-9249.
149. Rius M, Thon WF, Keppler D, Nies AT. Prostanoid transport by multidrug resistance protein 4 (MRP4/ABCC4) localized in tissues of the human urogenital tract. J Urol 2005;174:2409-2414.
150. Robillard KR, Hoque T, Bendayan R. Expression of ATP-binding cassette membrane transporters in rodent and human sertoli cells: relevance to the permeability of antiretroviral therapy at the blood-testis barrier. J Pharmacol Exp Ther 2012; 340:96-108.
151. Ruiz JL, Fernandes LR, Levy D, Bydlowski SP. Interrelationship between ATP-binding cassette transporters and oxysterols. Biochem Pharmacol 2013;86:80-88.
152. Sawicki WT, Kujawa M, Jankowska-Steifer E, Mystkowska ET, Hyc A, Kowalewski C. Temporal/spatial expression and efflux activity of ABC transporter, P-glycoprotein/Abcb1 isoforms and Bcrp/Abcg2 during early murine development. Gene Expr Patterns 2006;6:738-746.
153. Schinkel AH, Jonker JW. Mammalian drug efflux transporters of the ATP-binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 2003;55:3-29.
154. Schinkel AH, Mol CA, Wagenaar E, van Deemter L, Smit JJ, Borst P. Multidrug resistance and the role of P-glycoprotein knockout mice. Eur J Cancer 1995; 31A:1295-1298.
155. Selva DM, Hirsch-Reinshagen V, Burgess B, Zhou S, Chan J, McIsaac S, Hayden MR, Hammond GL, Vogl AW,Wellington CL. The ATP-binding cassette transporter 1 mediates lipid efflux from Sertoli cells and influences male fertility. J Lipid Res 2004; 45:1040-1050.
156. Seo H, Choi Y, Shim J, YooI, Ka H. Prostaglandin transportersABCC4andSLCO2A1in the uterine endometrium and conceptus during pregnancy in pigs. Biol Reprod 2014; 90:100.
157. Serrano-Sanchez M, Tanfin Z, Leiber D. Signaling pathways involved in sphingosine kinase activation and sphingosine-1-phosphate release in rat myometrium in late pregnancy: role in the induction of cyclooxygenase 2. Endocrinology 2008; 149:4669-4679.
158. Sharom FJ. The P-glycoprotein multidrug transporter. Essays Biochem 2011; 50:161-178.
159. Sharom FJ. Complex interplay between the P-glycoprotein multidrug efflux pump and the membrane: its role in modulating protein function. Front Oncol 2014;4:41.
160. Sibley CP, Brownbill P, Dilworth M, Glazier JD. Review: adaptation in placental nutrient supply to meet fetal growth demand: implications for programming. Placenta 2010; 31(Suppl):S70-S74.
161. Sivils JC, Gonzalez I, Bain LJ. Mice lacking Mrp1 have reduced testicular steroid hormone levels and alterations in steroid biosynthetic enzymes. Gen Comp Endocrinol 2010; 167:51-59.
162. Smith AJ, van Helvoort A, van Meer G, Szabo K, Welker E, Szakacs G, Varadi A, Sarkadi B, Borst P. MDR3 P-glycoprotein, a phosphatidylcholine translocase, transports several cytotoxic drugs and directly interacts with drugs as judged by interference with nucleotide trapping. J Biol Chem 2000;275:23530-23539.
163. Sodani K, Patel A, Kathawala RJ, Chen ZS. Multidrug resistance associated proteins in multidrug resistance. Chin J Cancer 2012;31:58-72.
164. St-Pierre MV, Serrano MA, Macias RI, Dubs U, Hoechli M, Lauper U, Meier PJ, Marin JJ. Expression of members of the multidrug resistance protein family in human term placenta. Am J Physiol Regul Integr Comp Physiol 2000;279:R1495-R1503.
165. Staud F, Cerveny L, Ceckova M. Pharmacotherapy in pregnancy; effect of ABC and SLC transporters on drug transport across the placenta and fetal drug exposure. J Drug Target 2012;20:736-763.
166. Stefulj J, Panzenboeck U, Becker T, Hirschmugl B, Schweinzer C, Lang I, Marsche G, Sadjak A, Lang U, Desoye G et al. Human endothelial cells of the placental barrier efficiently deliver cholesterol to the fetal circulation via ABCA1 and ABCG1. Circ Res 2009;104:600-608.
167. Stewart PA, Beliveau R, Rogers KA. Cellular localization of P-glycoprotein in brain versus gonadal capillaries. J Histochem Cytochem 1996;44:679-685.
168. Sun M, Kingdom J, Baczyk D, Lye SJ, Matthews SG, Gibb W. Expression of the multidrug resistance P-glycoprotein, (ABCB1 glycoprotein) in the human placenta decreases with advancing gestation. Placenta 2006;27:602-609.
169. Tanfin Z, Serrano-Sanchez M, Leiber D. ATP-binding cassette ABCC1 is involved in the release of sphingosine 1-phosphate from rat uterine leiomyoma ELT3 cells and late pregnant rat myometrium. Cell Signal 2011; 23:1997-2004.
170. Tarling EJ, Edwards PA. ATP-binding cassette transporter G1 (ABCG1) is an intracellular sterol transporter. Proc Natl Acad Sci USA 2011;108:19719-19724.
171. Tarling EJ, de Aguiar VallimTQ,Edwards PA. Role ofABCtransporters in lipid transport and human disease. Trends Endocrinol Metab 2013; 24:342-350.
172. Torricelli M, Voltolini C, Bloise E, Biliotti G, Giovannelli A, De Bonis M, Imperatore A, Petraglia F. Urocortin increases IL-4 and IL-10 secretion and reverses LPS-induced TNF-alpha release from human trophoblast primary cells. Am J Reprod Immunol 2009;62:224-231.
173. Vahakangas K, Myllynen P. Drug transporters in the human blood-placental barrier. Br J Pharmacol 2009;158:665-678.
174. van de Ven R, Oerlemans R, van der Heijden JW, Scheffer GL, de Gruijl TD, Jansen G, Scheper RJ. ABC drug transporters and immunity: novel therapeutic targets in autoimmunity and cancer. J Leukoc Biol 2009;86:1075-1087.
175. Van Sinderen M, Menkhorst E, Winship A, Cuman C, Dimitriadis E. Preimplantation human blastocyst-endometrial interactions: the role of inflammatory mediators. Am J Reprod Immunol 2013;69:427-440.
176. Vigano P, Mangioni S, Pompei F, Chiodo I. Maternal-conceptus cross talk-a review. Placenta 2003;24(Suppl B):S56-S61.
177. Vilella F, Ramirez L, Berlanga O, Martinez S, Alama P, Meseguer M, Pellicer A, Simon C. PGE2 and PGF2alpha concentrations in human endometrial fluid as biomarkers for embryonic implantation. J Clin Endocrinol Metab 2013;98:4123-4132.
178. Volpicelli ER, Lezcano C, Zhan Q, Girouard SD, Kindelberger DW, Frank MH, Frank NY, Crum CP, Murphy GF. The multidrug-resistance transporter ABCB5 is expressed in human placenta. Int J Gynecol Pathol 2014;33:45-51.
179. WangYH, Li Y, Yang SL, Yang L. Classification of substrates and inhibitors of P-glycoprotein using unsupervised machine learning approach. J Chem Inf Model 2005;45:750-757.
180. Wang H, Zhou L, Gupta A, Vethanayagam RR, Zhang Y, Unadkat JD, Mao Q. Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am J Physiol Endocrinol Metab 2006;290:E798-E807.
181. Wang H, Lee EW, Zhou L, Leung PC, Ross DD, Unadkat JD, Mao Q. 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;73:845-854.
182. Waterkotte B, Hambruch N, Doring B, Geyer J, Tinneberg HR, Pfarrer C. P-glycoprotein is functionally expressed in the placenta-derived bovine caruncular epithelial cell line 1 (BCEC-1). Placenta 2011;32:146-152.
183. Wenzel JJ, Piehler A, Kaminski WE. ABC A-subclass proteins: gatekeepers of cellular phospho- and sphingolipid transport. Front Biosci 2007;12:3177-3193.
184. Wielinga P, Hooijberg JH, Gunnarsdottir S, Kathmann I, Reid G, Zelcer N, van der Born K, de Haas M, van der Heijden I, Kaspers G et al. The human multidrug resistance protein MRP5 transports folates and can mediate cellular resistance against antifolates. Cancer Res 2005;65:4425-4430.
185. Wilcox CB, Feddes GO, Willett-Brozick JE, Hsu LC, DeLoia JA, Baysal BE. Coordinate up-regulation of TMEM97 and cholesterol biosynthesis genes in normal ovarian surface epithelial cells treated with progesterone: implications for pathogenesis of ovarian cancer. BMC Cancer 2007;7:223.
186. Wood CE. Estrogen in the fetus. Adv Exp Med Biol 2014;814:217-228.
187. Xia CQ, Smith PG. Drug efflux transporters and multidrug resistance in acute leukemia: therapeutic impact and novel approaches to mediation. Mol Pharmacol 2012; 82:1008-1021.
188. Yabuuchi H, Takayanagi S, Yoshinaga K, Taniguchi N, Aburatani H, Ishikawa T. ABCC13, an unusual truncated ABC transporter, is highly expressed in fetal human liver. Biochem Biophys Res Commun 2002;299:410-417.
189. Yasuda S, Itagaki S, Hirano T, Iseki K. Effects of sex hormones on regulation of ABCG2 expression in the placental cell line BeWo. J Pharm Pharm Sci 2006;9:133-139.
190. Yates CR, Chang C, Kearbey JD, Yasuda K, Schuetz EG, Miller DD, Dalton JT, Swaan PW. Structural determinants of P-glycoprotein-mediated transport of glucocorticoids. Pharm Res 2003;20:1794-1803.
191. Yeboah D, Sun M, Kingdom J, Baczyk D, Lye SJ, Matthews SG, Gibb W. Expression of breast cancer resistance protein (BCRP/ABCG2) in human placenta throughout gestation and at term before and after labor. Can J Physiol Pharmacol 2006; 84:1251-1258.
192. Yeboah D, Kalabis GM, Sun M, Ou RC, Matthews SG, Gibb W. Expression and localisation of breast cancer resistance protein (BCRP) in human fetal membranes and decidua and the influence of labour at term. Reprod Fertil Dev 2008;20:328-334.
193. Yoshino Y, Yuan B, Kaise T, Takeichi M, Tanaka S, Hirano T, Kroetz DL, Toyoda H. Contribution of aquaporin 9 and multidrug resistance-associated protein 2 to differential sensitivity to arsenite between primary cultured chorion and amnion cells prepared from human fetal membranes. Toxicol Appl Pharmacol 2011; 257:198-208.
194. Zhou SF,Wang LL, Di YM, Xue CC, DuanW, Li CG, Li Y. Substrates and inhibitors of human multidrug resistance associated proteins and the implications in drug development. Curr Med Chem 2008;15:1981-2039.