Assessment of ABCG2-mediated transport of xenobiotics across the blood-milk barrier of dairy animals using a new MDCKII in vitro model

Archives of Toxicology

Volumn 87, Issue 9, 2013, Pages 1671-1682

  Wassermann, Louise ^a   Halwachs, Sandra ^a   Baumann, Daniela ^a   Schaefer, Ingo ^a   Seibel, Peter ^a   Honscha, Walther ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

ABCG2 BCRP; Blood milk barrier; Dairy animals; Drugs; MDCKII cells; Transport

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; ENROFLOXACIN; SALICYLATE SODIUM;

ANIMAL CELL; ARTICLE; BLOOD MILK BARRIER; CELL MEMBRANE PERMEABILITY; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IN VITRO STUDY; MDCK CELL; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSPORT KINETICS; XENOBIOTIC METABOLISM;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CATTLE; CELL MEMBRANE PERMEABILITY; CELL POLARITY; DOGS; DRUG RESIDUES; FEMALE; FOOD CONTAMINATION; GOATS; MADIN DARBY CANINE KIDNEY CELLS; MAMMARY GLANDS, ANIMAL; MATERNAL-FETAL EXCHANGE; MEMBRANE TRANSPORT MODULATORS; MILK; MODELS, BIOLOGICAL; PREGNANCY; RECOMBINANT PROTEINS; SPECIES SPECIFICITY; XENOBIOTICS;

EID: 84883519817     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-013-1066-9     Document Type: Article

References (37)

1. Allen JD, van Loevezijn A, Lakhai JM, van der Valk M, van Tellingen O, Reid G, Schellens JH, Koomen GJ, Schinkel AH (2002) Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol Cancer Ther 1:417-425
2. Alvarez AI, Real R, Pérez M, Mendoza G, Prieto JG, Merino G (2010) Modulation of the activity of ABC transporters (P-glycoprotein, MRP2, BCRP) by flavonoids and drug response. J Pharm Sci 99:598-617
3. Braun A, Hämmerle S, Suda K, Rothen-Rutishauser B, Günthert M, Krämer SD, Wunderli-Allenspach H (2000) Cell cultures as tools in biopharmacy. Eur J Pharm Sci 11:S51-S60
4. Cho MJ, Thompson DP, Cramer CT, Vidmar TJ, Scieszka JF (1989) The Madin Darby canine kidney (MDCK) epithelial cell monolayer as a model cellular transport barrier. Pharm Res 6:71-77 (Pubitemid 19060827)
5. Deli MA (2007) Blood-brain barrier models. In: Lajtha A, Reith MEA (eds) Handbook of neurochemistry and molecular neurobiology, neural membrane and transport, 3rd edn. Springer, New York, pp 29-55
6. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK, Ross DD (1998) A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 95:15665-15670 (Pubitemid 29018757)
7. Enokizono J, Kusuhara H, Sugiyama Y (2007) Effect of breast cancer resistance protein (Bcrp/Abcg2) on the disposition of phytoestrogens. Mol Pharmacol 72:967-975 (Pubitemid 47481419)
8. Gallo P, Fabbrocino S, Vinci F, Fiori M, Danese V, Serpe L (2008) Confirmatory identification of sixteen non-steroidal anti-inflammatory drug residues in raw milk by liquid chromatography coupled with ion trap mass spectrometry. Rapid Commun Mass Spectrom 22:841-854 (Pubitemid 351442558)
9. Garberg P, Ball M, Borg N, Cecchelli R, Fenart L, Hurst RD, Lindmark T, Mabondzo A, Nilsson JE, Raub TJ, Stanimirovic D, Terasaki T, Oberg JO, Osterberg T (2005) In vitro models for the blood-brain barrier. Toxicol In Vitro 19:299-334 (Pubitemid 40248750)
10. González-Lobato L, Real R, Prieto JG, Alvarez AI, Merino G (2010) Differential inhibition of murine Bcrp1/Abcg2 and human BCRP/ABCG2 by the mycotoxin fumitremorgin C. Eur J Pharmacol 644:41-48
11. Halwachs S, Schaefer I, Seibel P, Honscha W (2011) Antiepileptic drugs reduce the efficacy of methotrexate chemotherapy through accelerated degradation of the reduced folate carrier by the ubiquitin-proteasome pathway. Chemotherapy 57:345-356
12. Halwachs S, Wassermann L, Lindner S, Zizzadoro C, Honscha W (2013) The fungicide prochloraz and environmental pollutant dioxin induce the ABCG2 transporter in bovine mammary epithelial cells by the arylhydrocarbon receptor signaling pathway. Toxicol Sci 131:491-501
13. Hegedus C, Szakács G, Homolya L, Orbán TI, Telbisz A, Jani M, Sarkadi B (2009) Ins and outs of the ABCG2 multidrug transporter: an update on in vitro functional assays. Adv Drug Deliv Rev 61:47-56
14. Irvine JD, Takahashi L, Lockhart K, Cheong J, Tolan JW, Selick HE, Grove JR (1999) MDCK (Madin-Darby canine kidney) cells: a tool for membrane permeability screening. J Pharm Sci 88:28-33 (Pubitemid 29037364)
15. Jonker JW, Merino G, Musters S, van Herwaarden AE, Bolscher E, Wagenaar E, Mesman E, Dale TC, Schinkel AH (2005) The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat Med 11:127-129 (Pubitemid 40321346)
16. Kaartinen L, Salonen M, Alli L, Pyörälä S (1995) Pharmacokinetics of enrofloxacin after single intravenous, intramuscular and subcutaneous injections in lactating cows. J Vet Pharmacol Ther 18:357-362
17. Kneuer C, Honscha KU, Honscha W (2005) Rat reduced-folate carrier-1 is localized basolaterally in MDCK kidney epithelial cells and contributes to the secretory transport of methotrexate and fluoresceinated methotrexate. Cell Tissue Res 320:517-524 (Pubitemid 40884153)
18. Krishnamurthy P, Schuetz JD (2006) Role of ABCG2/BCRP in biology and medicine. Annu Rev Pharmacol Toxicol 46:381-410 (Pubitemid 43271195)
19. Larger P, Altamura M, Catalioto RM, Giuliani S, Maggi CA, Valenti C, Triolo A (2002) Simultaneous LC-MS/MS Determination of Reference Pharmaceuticals as a method for the characterization of the Caco-2 cell monolayer absorption properties. Anal Chem 74:5273-5281 (Pubitemid 35215356)
20. Lindner S, Halwachs S, Wassermann L, Honscha W (2013) Expression and subcellular localization of efflux transporter ABCG2/BCRP in important tissue barriers of lactating dairy cows, sheep and goats. J Vet Pharmacol Ther (in press)
21. Litman T, Brangi M, Hudson E, Fetsch P, Abati A, Ross DD, Miyake K, Resau JH, Bates SE (2000) The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). J Cell Sci 113:2011-2021 (Pubitemid 30386505)
22. Maubach J, Bracke ME, Heyerick A, Depypere HT, Serreyn RF, Mareel MM, De Keukeleire D (2003) Quantitation of soy-derived phytoestrogens in human breast tissue and biological fluids by high-performance liquid chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 784:137-144 (Pubitemid 36009350)
23. Merino G, Alvarez AI, Pulido MM, Molina AJ, Schinkel AH, Prieto JG (2006) Breast cancer resistance protein (BCRP/ABCG2) transports fluoroquinolone antibiotics and affects their oral availability, pharmacokinetics, and milk secretion. Drug Metab Dispos 34:690-695
24. Pavek P, Merino G, Wagenaar E, Bolscher E, Novotna M, Jonker JW, Schinkel AH (2005) Human breast cancer resistance protein: interactions with steroid drugs, hormones, the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo(4,5-b) pyridine, and transport of cimetidine. J Pharmacol Exp Ther 312:144-152 (Pubitemid 40096463)
25. Polishchuk R, Di Pentima A, Lippincott-Schwartz J (2004) Delivery of raft-associated, GPI-anchored proteins to the apical surface of polarized MDCK cells by a transcytotic pathway. Nat Cell Biol 6:297-307 (Pubitemid 38584819)
26. Poller B, Wagenaar E, Tang SC, Schinkel AH (2011) Double-transduced MDCKII cells to study human P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) interplay in drug transport across the blood-brain barrier. Mol Pharm 8:571-582
27. Pulido MM, Molina AJ, Merino G, Mendoza G, Prieto JG, Alvarez AI (2006) Interaction of enrofloxacin with breast cancer resistance protein (BCRP/ABCG2): influence of flavonoids and role in milk secretion in sheep. J Vet Pharmacol Ther 29:279-287 (Pubitemid 43995435)
28. Rabindran SK, Ross DD, Doyle LA (2000) Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein. Cancer Res 60:47-50 (Pubitemid 30058728)
29. Real R, Egido E, Pérez M, González-Lobato L, Barrera B, Prieto JG, Alvarez AI, Merino G (2011) Involvement of breast cancer resistance protein (BCRP/ABCG2) in the secretion of danofloxacin into milk: interaction with ivermectin. J Vet Pharmacol Ther 34:313-321
30. Rothen-Rutishauser B, Krämer SD, Braun A, Günthert M, Wunderli-Allenspach H (1998) MDCK cell cultures as an epithelial in vitro model: cytoskeleton and tight junctions as indicators for the definition of age-related stages by confocal microscopy. Pharm Res 15:964-971 (Pubitemid 28356908)
31. Subramanian VS, Marchant JS, Said HM (2008) Apical membrane targeting and trafficking of the human proton-coupled transporter in polarized epithelia. Am J Physiol Cell Physiol 294:C233-C240
32. van Herwaarden AE, Schinkel AH (2006) The function of breast cancer resistance protein in epithelial barriers, stem cells and milk secretion of drugs and xenotoxins. Trends Pharmacol Sci 27:10-16 (Pubitemid 43063119)
33. van Herwaarden AE, Jonker JW, Wagenaar E, Brinkhuis RF, Schellens JH, Beijnen JH, Schinkel AH (2003) The breast cancer resistance protein (Bcrp1/Abcg2) restricts exposure to the dietary carcinogen 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine. Cancer Res 63:6447-6452 (Pubitemid 37255195)
34. Wang Q, Strab R, Kardos P, Ferguson C, Li J, Owen A, Hidalgo IJ (2007) Application and limitation of inhibitors in drug-transporter interaction studies. Int J Pharm 356:12-18
35. Wassermann L, Halwachs S, Lindner S, Honscha KU, Honscha W (2013) Determination of functional ABCG2 activity and assessment of drug-ABCG2 interactions in dairy animals using a novel MDCKII in vitro model. J Pharm Sci 102:772-784
36. Xia CQ, Liu N, Yang D, Miwa G, Gan LS (2005) Expression, localization, and functional characteristics of breast cancer resistance protein in Caco-2 cells. Drug Metab Dispos 33:637-643 (Pubitemid 40593877)
37. Zhao X, Lacasse P (2008) Mammary tissue damage during bovine mastitis: causes and control. J Anim Sci 86:57-65