Xenobiotic transporter expression and function in the human mammary gland

Advanced Drug Delivery Reviews

Volumn 55, Issue 5, 2003, Pages 653-665

  Ito, Shinya ^a   Alcorn, Jane ^b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Biological transport; Human; Mammary gland; Milk; Nutrient transporters; Xenobiotic transporters

Indexed keywords

POLYPEPTIDES; TOXICITY;

XENOBIOTIC TRANSPORTERS;

DRUG THERAPY;

4 AMINOHIPPURIC ACID; AMINOPHENAZONE; CARBAMAZEPINE; CARNITINE; CIMETIDINE; DIPYRIDAMOLE; FURALTADONE; GLYCOPROTEIN P; HYPOXANTHINE; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; N ACETYL 4 AMINOHIPPURIC ACID; NITROFURANTOIN; OCTAMER TRANSCRIPTION FACTOR 2; OCTAMER TRANSCRIPTION FACTOR 4; PENICILLIN G; PROBENECID; PROTEIN; PROTEIN MDR3; PROTEIN OAT1; PROTEIN OAT2; PROTEIN OAT3; PROTEIN OAT4; PROTEIN OCT1; PROTEIN OCTN1; PROTEIN OCTN2; SULFACETAMIDE; TETRYLAMMONIUM; UNCLASSIFIED DRUG; VERAPAMIL;

ACTIVE TRANSPORT; ANION TRANSPORT; AREA UNDER THE CURVE; BREAST EPITHELIUM; CATION TRANSPORT; CLINICAL TRIAL; DIFFUSION; DRUG DISPOSITION; GENE EXPRESSION; HUMAN; MAMMARY GLAND FUNCTION; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOSIDE TRANSPORT; NUTRIENT SUPPLY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TRANSCYTOSIS; XENOBIOTIC METABOLISM;

EID: 0037472058     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-409X(03)00031-0     Document Type: Review

References (110)

1. Ito S. Drug therapy for breast-feeding women. N. Engl. J. Med. 343:2000;118-126.
2. Anderson P.O. Drug use during breast-feeding. Clin. Pharm. 10:1991;594-624.
3. Howard C.R., Lawrence R.A. Breast-feeding and drug exposure. Obstet. Gynecol. Clin. North Am. 25:1998;195-217.
4. J.L. McManaman, M.C. Neville, Adv. Drug. Deliv. Rev., this issue.
5. Miller G.E., Banerjee N.C., Stowe C.M. Jr. Diffusion of certain weak organic acids and bases across the bovine mammary gland membrane after systemic administration. J. Pharmacol. Exp. Ther. 157:1967;245-253.
6. Rasmussen F. Mammary excretion of sulphonamides. Acta Pharmacol. Toxicol. 15:1958;139-148.
7. Rasmussen F. Excretion of drugs by milk. Gillette J.R. Concepts in Biochemical Pharmacology. 1971;390-402 Springer, New York. Part 1.
8. Wilson J.T. Drugs in Breast Milk. 1981;15-33 ADIS Press, Australia.
9. Atkinson H.C., Begg E.J. Prediction of drug distribution into human milk from physicochemical characteristics. Clinical Pharmacokinetics. 18:1990;151-167.
10. Fleishaker J.C., Desai N., McNamara P.J. Factors affecting the milk-to-plasma drug concentration ratio in lactating women: physical interactions with protein and fat. J. Pharm. Sci. 76:1987;189-193.
11. J.C. Fleishaker, Adv. Drug. Deliv. Rev., this issue.
12. Banerjee N.C., Miller G.E., Stowe C.M. Excretion of aminopyrine and its metabolites into cows milk. Toxicol. Appl. Pharmacol. 10:1967;604-612.
13. Rasmussen F. Active mammary excretion of N4-acetylated p-aminohippuric acid. Acta Vet. Scand. 10:1969;193-194.
14. Rasmussen F. Active mammary excretion of N4-acetylated sulphanilamide. Acta Vet. Scand. 10:1969;402-403.
15. McNamara P.J., Burgio D., Yoo S.D. Pharmacokinetics of cimetidine during lactation: species differences in cimetidine transport into rat and rabbit milk. J. Pharmacol. Exp. Ther. 261:1992;918-923.
16. McNamara P.J., Meece J.A., Paxton E. Active transport of cimetidine and ranitidine into the milk of Sprague-Dawley rats. J. Pharmacol. Exp. Ther. 277:1996;1615-1621.
17. Gerk P.M., Oo C.Y., Paxton E.W., Moscow J.A., McNamara P.J. Interactions between cimetidine, nitrofurantoin, and probenecid active transport into rat milk. J. Pharmacol. Exp. Ther. 296:2001;175-180.
18. Oo C.Y., Kuhn R.J., Desai N., McNamara P.J. Active transport of cimetidine into human milk. Clin. Pharmacol. Ther. 58:1995;548-555.
19. Schadewinkel-Scherkl A.M., Rasmussen F., Merck C.C., Nielsen P., Frey H.H. Active transport of benzylpenicillin across the blood-milk barrier. Pharmacol. Toxicol. 73:1993;14-19.
20. Bito L.Z., Baroody R.A. Comparison of renal prostaglandin and p-aminohippuric acid transport processes. Am. J. Physiol. 234:1978;F80-F88.
21. Moller J.V., Sheikh M.I. Renal organic anion transport system: pharmacological, physiological, and biochemical aspects. Pharmacol. Rev. 34:1983;315-358.
22. Kari F.W., Weaver R., Neville M.C. Active transport of nitrofurantoin across the mammary epithelium in vivo. J. Pharmacol. Exp. Ther. 280:1997;664-668.
23. Gerk P.M., Kuhn R.J., McNamara P.J. Active transport of nitrofurantoin into human milk. Pharmacotherapy. 21:2001;669-675.
24. Gerk P.M., Hanson L., Neville M.C., McNamara P.J. Sodium dependence of nitrofurantoin active transport across mammary epithelia and effects of dipyridamole, nucleosides, and nucleobases. Pharm. Res. 19:2002;299-305.
25. Toddywalla V.S., Kari F.W., Neville M.C. Active transport of nitrofurantoin across a mouse mammary epithelial monolayer. J. Pharmacol. Exp. Ther. 280:1997;669-676.
26. Kwok B., Cook V., Tropea A., Ito S. The role of OCTN1 and OCTN2 in the mammary gland. Clin. Pharmacol. Ther. 69:2001;19. abstract.
27. Kekuda R., Prasad P.D., Wu X., Wang H., Fei Y.J., Leibach F.H., Ganapathy V. Cloning and functional characterization of a potential sensitive, polyspecific organic cation transporter (OCT3) most abundantly expressed in placenta. J. Biol. Chem. 273:1998;15971-15979.
28. Grundemann D., Schechinger B., Rappold G.A., Schomig E. Molecular identification of the corticosterone-sensitive extraneuronal catecholamine transporter. Nat. Neurosci. 1:1998;349-351.
29. 2) and evidence for the expression of the transporter in the brain. J. Biol. Chem. 273:1998;32776-32786.
30. Wu X., Huang W., Ganapathy M.E., Wang H., Kekuda R., Conway S.J., Leibach F.H., Ganapathy V. Structure, function, and regional distribution of the organic cation transporter OCT3 in the kidney. Am. J. Physiol. 279:2000;F449-F458.
31. Tamai I., Ohashi R., Nezu J., Yabuuchi H., Oku A., Shimane M., Sai Y., Tsuji A. Molecular and functional identification of sodium ion-dependent, high affinity human carnitine transporter OCTN2. J. Biol. Chem. 273:1998;20378-20382.
32. +-coupled transport of L-carnitine via high-affinity carnitine transporter OCTN2 and its subcellular localization in kidney. Biochim. Biophys. Acta. 1512:2001;273-284.
33. Wagner C.A., Lukewille U., Kaltenbach S., Moschen I., Broer A., Risler T., Broer S., Lang F. Functional and pharmacological characterization of human Na(+)-carnitine cotransporter hOCTN2. Am. J. Physiol. 279:2000;F584-F591.
34. Nezu J., Tamai I., Oku A., Ohashi R., Yabuuchi H., Hashimoto N., Nikaido H., Sai Y., Koizumi A., Shoji Y., Takada G., Matsuishi T., Yoshino M., Kato H., Ohura T., Tsujimoto G., Hayakawa J., Shimane M., Tsuji A. Primary systemic carnitine deficiency is caused by mutations in a gene encoding sodium ion-dependent carnitine transporter. Nat. Genet. 21:1999;91-94.
35. Grundemann D., Gorboulev V., Gambaryan S., Veyhl M., Koepsell H. Drug excretion mediated by a new prototype of polyspecific transporter. Nature. 372:1994;549-552.
36. Okuda M., Saito H., Urakami Y., Takano M., Inui K. cDNA cloning and functional expression of a novel rat kidney organic cation transporter, OCT2. Biochem. Biophys. Res. Commun. 224:1996;500-507.
37. Gorboulev V., Ulzheimer J.C., Akhoundova A., Ulzheimer-Tauber I., Karbach U., Quester S., Baumann C., Lang F., Busch A.E., Koepsell H. Cloning and characterization of two human polyspecific organic cation transporters. DNA Cell Biol. 16:1997;871-881.
38. Zhang L., Dresser M.J., Gray A.T., Yost S.C., Terashita S., Giacomini K.M. Cloning and functional expression of a human liver organic cation transporter. Mol. Pharmacol. 51:1997;913-921.
39. Grundemann D., Liebich G., Kiefer N., Koster S., Schomig E. Selective substrates for non-neuronal monoamine transporters. Mol. Pharmacol. 56:1999;1-10.
40. Tamai I., Yabuuchi H., Nezu J., Sai Y., Oku A., Shimane M., Tsuji A. Cloning and characterization of a novel human pH-dependent organic cation transporter, OCTN1. FEBS Lett. 419:1997;107-111.
41. Yabuuchi H., Tamai I., Nezu J., Sakamoto K., Oku A., Shimane M., Sai Y., Tsuji A. Novel membrane transporter OCTN1 mediates multispecific, bidirectional, and pH-dependent transport of organic cations. J. Pharmacol. Exp. Ther. 289:1999;768-773.
42. Ohashi R., Tamai I., Nezu J., Nikaido H., Hashimoto N., Oku A., Sai Y., Shimane M., Tsuji A. Molecular and physiological evidence for multifunctionality of carnitine/organic cation transporter OCTN2. Mol. Pharmacol. 59:2001;358-366.
43. Wu X., Orasad P.D., Leibach F.H., Ganapathy V. cDNA sequence, transport function, and genomic organization of human OCTN2, a new member of the organic cation transporter family. Biochem. Biophys. Res. Commun. 246:1998;589-595.
44. Ohashi R., Tamai I., Yabuuchi H., Nezu J., Oku A., Sai Y., Shimane M., Tsuji A. Na(+)-dependent carnitine transport by organic cation transporter (OCTN2): its pharmacological and toxicological relevance. J. Pharmacol. Exp. Ther. 291:1999;778-784.
45. Dhillon U., Shenton J., Cook V., Harper P.A., Watson-Macdonell J., Ito S. The expression of the human organic cation transporter hOCT1 in mammary gland. Clin. Pharmacol. Ther. 65:1999;205. abstract.
46. Alcorn J., Lu X., Moscow J.A., McNamara P.J. Transporter gene expression in lactating and non-lactating human mammary epithelial cells using real-time RT-PCR. J. Pharmacol. Exp. Ther. 303:2002;487-496.
47. 0+. J. Biol. Chem. 274:1999;23740-23745.
48. 0,+ from mouse colon expressed in HRPE cells and Xenopus oocytes. J. Physiol. 532:2001;297-304.
49. Sekine T., Watanabe N., Hosoyamada M., Kanai Y., Endou H. Expression cloning and characterization of a novel multispecific organic anion transporter. J. Biol. Chem. 272:1997;18526-18529.
50. Sweet D.H., Wolff N.A., Pritchard J.B. Expression cloning and characterization of ROAT1. J. Biol. Chem. 272:1997;30088-30095.
51. Sekine T., Cha S.H., Endou H. The multispecific organic anion transporter (OAT) family. Pflug. Arch. Eur. J. Physiol. 440:2000;337-350.
52. Bahn A., Prawitt D., Buttler D., Reid G., Enklaar T., Wolff N.A., Ebbinghaus C., Hillemann A., Schulten H.J., Gunawan B., Fuzesi L., Zabel B., Burckhardt G. Genomic structure and in vivo expression of the human organic anion transporter 1 (hOAT1) gene. Biochem. Biophys. Res. Commun. 275:2000;623-630.
53. Sugiyama D., Kusuhara H., Shitara Y., Abe T., Meier P.J., Sekine T., Endou H., Suzuki H., Sugiyama Y. Characterization of the efflux transport of 17b-estradiol-D-17b-glucuronide from the brain across the blood-brain barrier. J. Pharmacol. Exp. Ther. 298:2001;316-322.
54. Kullak-Ublick G.A., Ismair M.G., Stieger B., Landmann L., Huber R., Pizzagalli F., Fattinger K., Meier P.J., Hagenbuch B. Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver. Gastroenterology. 120:2001;525-533.
55. Kullak-Ublick G.A., Hagenbuch B., Stieger B., Schteingart C.D., Hofmann A.F., Wolkoff A.W., Meier P.J. Molecular and functional characterization of an organic anion transporting polypeptide cloned from human liver. Gastroenterology. 109:1995;1274-1282.
56. Gao B., Hagenbuch B., Kullak-Ublick G.A., Benke D., Aguzzi A., Meier P.J. Organic anion-transporting polypeptides mediate transport of opioid peptides across blood-brain barrier. J. Pharmacol. Exp. Ther. 294:2000;73-79.
57. Abe T., Kakyo M., Tokui T., Nakagomi R., Nishio T., Nakai D., Nomura H., Unno M., Suzuki M., Naitoh T., Matsuno S., Yawo H. Identification of a novel gene family encoding human liver-specific organic anion transporter LST-1. J. Biol. Chem. 274:1999;17159-17163.
58. Hsiang B., Zhu Y., Wang Z., Wu Y., Sasseville V., Yang W.-P., Kirch-Gessner T.G. A novel human hepatic organic anion transporting polypeptide (OATP2). J. Biol. Chem. 274:1999;37161-37168.
59. König J., Cui Y., Nies A.T., Keppler D. A novel human organic anion transporting polypeptide localized to the basolateral hepatocyte membrane. Am. J. Physiol. 278:2000;G156-G164.
60. König J., Cui Y., Nies A.T., Keppler D. Localization and genomic organization of a new hepatocellular organic anion transporting polypeptide. J. Biol. Chem. 275:2000;23161-23168.
61. Tamai I., Nezu J., Uchino H., Sai Y., Oku A., Shimane M., Tsuji A. Molecular identification and characterization of novel members of the human organic anion transporter (OATP) family. Biochem. Biophys. Res. Commun. 273:2000;251-260.
62. +/peptide cotransporter PEPT1: localization of PEPT1 and transport of beta-lactam antibiotics. J. Pharmacol. Exp. Ther. 281:1997;1415-1421.
63. Shen H., Smith D.E., Yang T., Huang Y.G., Schnermann J.B., Brosius F.C. III. Localization of PEPT1 and PEPT2 proton-coupled oligopeptide transporter mRNA and protein in rat kidney. Am. J. Physiol. 276:1999;F658-F665.
64. Terada T., Saito H., Mukai M., Inui K. Recognition of beta-lactam antibiotics by rat peptide transporters, PEPT1 and PEPT2, in LLC-PK1 cells. Am. J. Physiol. 273:1997;F706-F711.
65. Han H., de Vrueh R.L., Rhie J.K., Covitz K.M., Smith P.L., Lee C.P., Oh D.M., Sadee W., Amidon G.L. 5′-Amino acid esters of antiviral nucleosides, acyclovir, and AZT are absorbed by the intestinal PEPT1 peptide transporter. Pharm. Res. 15:1998;1154-1159.
66. Ganapathy M.E., Huang W., Wang H., Ganapathy V., Leibach F.H. Valacyclovir: a substrate for the intestinal and renal peptide transporters PEPT1 and PEPT2. Biochem. Biophys. Res. Commun. 246:1998;470-475.
67. Balimane P.V., Tamai I., Guo A., Nakanishi T., Kitada H., Leibach F.H., Tsuji A., Sinko P.J. Direct evidence for peptide transporter (PepT1)-mediated uptake of a non-peptide prodrug, valacyclovir. Biochem. Biophys. Res. Commun. 250:1998;246-251.
68. Temple C.S., Boyd C.A. Proton-coupled oligopeptide transport by rat renal cortical brush border membrane vesicles: a functional analysis using ACE inhibitors to determine the isoform of the transporter. Biochim. Biophys. Acta. 1373:1998;277-281.
69. Ganapathy M.E., Brandsch M., Prasad P.D., Ganapathy V., Leibach F.H. Differential recognition of beta-lactam antibiotics by intestinal and renal peptide transporters, PEPT 1 and PEPT 2. J. Biol. Chem. 20:1995;25672-25677.
70. Doring F., Walter J., Will J., Focking M., Boll M., Amasheh S., Clauss W., Daniel H. Delta-aminolevulinic acid transport by intestinal and renal peptide transporters and its physiological and clinical implications. J. Clin. Invest. 101:1998;2761-2767.
71. Groneberg D.A., Doring F., Theis S., Nickolaus M., Fischer A., Daniel H. Peptide transport in the mammary gland: expression and distribution of PEPT2 mRNA and protein. Am. J. Physiol. 282:2002;E1172-E1179.
72. Shennan D.B., Calvert D.T., Backwell F.R.C., Boyd C.A.R. Peptide aminonitrogen transport by the lactating rat mammary gland. Biochim. Biophys. Acta. 1371:1998;252-260.
73. +/nucleoside cotransporter (hCNT2) selective for purine nucleosides and uridine. Mol. Membr. Biol. 15:1998;203-211.
74. +-nucleoside cotransporter proteins (hCNT3 and mCNT3) broadly selective for purine and pyrimidine nucleosides (system cib). J. Biol. Chem. 276:2001;2914-2927.
75. +-nucleoside cotransporter (hCNT1). Am. J. Physiol. 272:(2 Pt 1):1997;C707-C714.
76. Hyde R.J., Cass C.E., Young J.D., Baldwin S.A. The ENT family of eukaryote nucleoside and nucleobase transporters: recent advances in the investigation of structure/function relationships and the identification of novel isoforms. Mol. Membr. Biol. 18:2001;53-63.
77. Yao S.Y.M., Ng A.M., Sundaram M., Cass C.E., Baldwin S.A., Young J.D. Transport of antiviral 3′-deoxy-nucleoside drugs by recombinant human and rat equilibrative, nitrobenzylthioinosine (NBMPR)-insensitive (ENT2) nucleoside transporter proteins produced in Xenopus oocytes. Mol. Membr. Biol. 18:2001;161-167.
78. Griffiths M., Beaumont N., Yao S.Y., Sundaram M., Boumah C.E., Davies A., Kwong F.Y., Coe I., Cass C.E., Young J.D., Baldwin S.A. Cloning of a human nucleoside transporter implicated in the cellular uptake of adenosine and chemotherapeutic drugs. Nat. Med. 3:1997;89-93.
79. de Koning H., Diallinas G. Nucleobase transporters. Mol. Membr. Biol. 17:2000;75-94.
80. Liang W.J., Johnson D., Jarvis S.M. Vitamin C transport systems of mammalian cells. Mol. Membr. Biol. 18:2001;87-95.
81. Wang H., Dutta B., Huang W., Devoe L.D., Leibach F.H., Ganapathy V., Prasad P.D. Human Na(+)-dependent vitamin C transporter 1 (hSVCT1): primary structure, functional characteristics and evidence for a non-functional splice variant. Biochim. Biophys. Acta. 1461:1999;1-9.
82. Daruwala R., Song J., Koh W.S., Rumsey S.C., Levine M. Cloning and functional characterization of the human sodium-dependent vitamin C transporters hSVCT1 and hSVCT2. FEBS Lett. 460:1999;480-484.
83. +-dependent L-ascorbic acid transporters. Nature. 399:1999;70-75.
84. Wang Y., Mackenzie B., Tsukaguchi H., Weremowicz S., Morton C.C., Hediger M.A. Human vitamin C (L-ascorbic acid) transporter SVCT1. Biochem. Biophys. Res. Commun. 267:2000;488-494.
85. Kartner N., Evernden-Porelle D., Bradeley G., Ling V. Detection of P-glycoprotein in multidrug resistant cell lines by monoclonal antibodies. Nature. 316:1985;820-823.
86. Gros P., Neriah Y.P., Croop J.M., Housman D D. Isolation and expression of a cDNA that confers multidrug resistance. Nature. 323:1986;728-731.
87. Dean M., Rzhetsky A., Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 11:2001;1156-1166.
88. Thiebaut F., Tsuruo T., Hamada H., Gottesman M.M., Pastan I., Willingham M.C. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc. Natl. Acad. Sci. USA. 84:1987;7735-7738.
89. Thiebaut F., Tsuruo T., Hamada H., Gottesman M.M., Pastan I., Willingham M.C. Immunohistochemical localization in normal tissues of different epitopes in the multidrug transport protein P170: evidence for localization in brain capillaries and crossreactivity of one antibody with a muscle protein. J. Histochem. Cytochem. 37:1989;159-164.
90. Sugawara I., Kataoka I., Morishita Y., Hamada H., Tsuruo T., Itoyama S., Mori S. Tissue distribution of P-glycoprotein encoded by a multidrug-resistant gene as revealed by a monoclonal antibody, MRK 16. Cancer Res. 48:1988;1926-1929.
91. Cordon-Cardo C., O'Brien J.P., Boccia J., Casals D., Bertino J.R., Melamed M.R. Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumor tissues. J. Histochem. Cytochem. 38:1990;1277-1287.
92. Cordon-Cardo C., O'Brien J.P., Casals D., Rittman-Grauer L., Biedler J.L., Melamed M.R., Bertino J.R. Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Proc. Natl. Acad. Sci. USA. 86:1989;695-698.
93. van der Valk P., van Kalken C.K., Ketelaars H., Broxterman H.J., Scheffer G., Kuiper C.M., Tsuruo T., Lankelma J., Meijer C.J., Pinedo H.M. Distribution of multi-drug resistance-associated P-glycoprotein in normal and neoplastic human tissues. Analysis with three monoclonal antibodies recognizing different epitopes of the P-glycoprotein molecule. Ann. Oncol. 1:1990;56-64.
94. Sukhai M., Yong A., Pak A., Piquette-Miller M. Decreased expression of P-glycoprotein in interleukin-1beta and interleukin-6 treated rat hepatocytes. Inflamm. Res. 50:2001;362-370.
95. Sukhai M., Yong A., Kalitsky J., Piquette-Miller M. Inflammation and interleukin-6 mediate reductions in the hepatic expression and transcription of the mdr1a and mdr1b genes. Mol. Cell. Biol. Res. Commun. 4:2000;248-256.
96. Smit J.M., Schinkel A.H., Oude Elferink R.P., Groen A.K., Wagenaar E., van Deemter L., Mol C.A., Ottenhoff R., van der Lugt N.M., van Roon M.A., van der Valk M.A., Offerhaus G.J.A., Berns A.J.M., Borst P. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell. 75:1993;451-462.
97. Cole S.P.C., Bhardwaj G., Gerlach J.H., Mackie J.E., Grant C.E., Almquist K.C., Stewart A.J., Kurz E.U., Duncan A.M.V., Deeley R.G. Overexpression of a novel transporter gene in a multidrug resistant human lung cancer cell line. Science. 258:1992;1650-1654.
98. Ishikawa T. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci. 17:1992;463-468.
99. Jedlitschky G., Leier I., Buchholz U., Center M., Keppler D. ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res. 54:1994;4833-4836.
100. Evers R., Zaman G.J.R., van Deemter L., Jansen H., Calafat J., Oomen L.C.J.M., Oude Elferink R.P.J., Borst P., Schinkel A.H. Basolateral localization and export activity of the human multidrug resistance-associated protein in polarized pig kidney cells. J. Clin. Invest. 97:1996;1211-1218.
101. Ishikawa T., Bao J., Yamane Y., Akimaru K., Frindrich K., Wright C., Kuo M.T. Coordinated induction of MRP/GS-X pump and g-glutamylcysteine synthetase by heavy metals in human leukemia cells. J. Biol. Chem. 271:1996;14981-14988.
102. Evers R., Kool M., van Deemter L., Janssen H., Calafat J., Oomen L.C., Paulusma C.C., Oude Elferink R.P.J., Baas F., Schinkel A.H., Borst P. Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J. Clin. Invest. 101:1998;1310-1319.
103. Kool M., de Haas M., Scheffer G.L., Scheper R.J., van Eijk M.J.T., Juijn J.A., Baas F., Borst P. Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res. 57:1997;3537-3547.
104. Scheffer G.L., Kool M., Heijn M., de Haas M., Pijnenborg A.C., Wijnholds J., van Helvoort A., de Jong M.C., Hooijberg J.H., Mol C.A., van der Linden M., de Vree J.M., van der Valk P., Elferink R.P., Borst P., Scheper R.J. Specific detection of multidrug resistance proteins MRP1, MRP2, MRP3, MRP5, and MDR3 P-glycoprotein with a panel of monoclonal antibodies. Cancer Res. 60:2000;5269-5277.
105. Ilias A., Urban Z., Seidl T.L., Le Saux O., Sinko E., Boyd C.D., Sarkadi B., Varadi A. Loss of ATP-dependent transport activity in Pseudoxanthoma elasticum-associated mutants of human ABCC6 (MRP6). J. Biol. Chem. 277:2002;16860-16867.
106. Schuetz J.D., Connelly M.C., Sun D., Paibir S.G., Flynn P.M., Srinivas R.V., Kumar A., Fridland A. MRP4: a previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat. Med. 5:1999;1048-1051.
107. Wijnholds J., Mol C.A., van Deemter L., de Haas M., Scheffer G.L., Baas F., Beijnen J.H., Scheper R.J., Hatse S., De Clercq E., Balzarini J., Borst P. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc. Natl. Acad. Sci. USA. 97:2000;7476-7481.
108. Gottesman M.M., Fojo T., Bates S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. (Cancer). 2:2002;48-58.
109. Bera T.K., Lee S., Salvatore G., Lee B., Pastan I. MRP8, a new member of ABC transporter superfamily, identified by EST database mining and gene prediction program, is highly expressed in breast cancer. Mol. Med. 7:2001;509-516.
110. Bera T.K., Iavarone C., Kumar V., Lee S., Pastan I. MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer. Proc. Natl. Acad. Sci. USA. 99:2002;6997-7002.