Regulation of expression and activity of multidrug resistance proteins MRP2 and MDR1 by estrogenic compounds in Caco-2 cells. Role in prevention of xenobiotic-induced cytotoxicity

Toxicology

Volumn 320, Issue 1, 2014, Pages 46-55

  Arias, Agostina ^a   Rigalli, Juan Pablo ^a   Villanueva, Silvina S M ^a   Ruiz, María L ^a   Luquita, Marcelo G ^a   Perdomo, Virginia G ^a   Vore, Mary ^b   Catania, Viviana A ^a   Mottino, Aldo D ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Estrogen receptor; Ethynylestradiol; Genistein; MDR1; MRP2

Indexed keywords

1 CHLORO 2,4 DINITROBENZENE; BREAST CANCER RESISTANCE PROTEIN; ETHINYLESTRADIOL; GENISTEIN; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 1; XENOBIOTIC AGENT;

ARTICLE; CELL DEATH; CELL PROTECTION; CELL STRAIN CACO 2; CHEMICAL INJURY; CYTOTOXICITY; CYTOTOXICITY ASSAY; ESTROGEN ACTIVITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; INGESTION; INTESTINE EPITHELIUM; INTESTINE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; UPREGULATION;

ESTROGEN RECEPTOR; ETHYNYLESTRADIOL; GENISTEIN; MDR1; MRP2;

ATP-BINDING CASSETTE TRANSPORTERS; CACO-2 CELLS; DINITROCHLOROBENZENE; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGEN ANTAGONISTS; ESTROGEN RECEPTOR BETA; ETHINYL ESTRADIOL; GENE EXPRESSION REGULATION; GENISTEIN; HUMANS; INTESTINAL MUCOSA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; P-GLYCOPROTEIN; PARAQUAT; RNA, MESSENGER; SOYBEANS; UP-REGULATION; XENOBIOTICS;

EID: 84902967582     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2014.03.007     Document Type: Article

References (61)

1. Arias A., Villanueva S.S., Ruiz M.L., Luquita M.G., Veggi L.M., Pellegrino J.M., Vore M., Catania V.A., Mottino A.D. Regulation of expression and activity of rat intestinal multidrug resistance-associated protein 2 by cholestatic estrogens. Drug Metab. Dispos. 2009, 37(6):1277-1285.
2. Bakos E., Evers R., Sinko E., Varadi A., Borst P., Sarkadi B. Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol. 2000, 57(4):760-768.
3. Barone M., Lofano K., De Tullio N., Licinio R., Albano F., Di Leo A. Dietary, endocrine, and metabolic factors in the development of colorectal cancer. J. Gastrointest. Cancer. 2012, 43(1):13-19.
4. Bjornstrom L., Sjoberg M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol. Endocrinol. 2005, 19(4):833-842.
5. Chan L.M., Lowes S., Hirst B.H. The ABCs of drug transport in intestine and liver: efflux proteins limiting drug absorption and bioavailability. Eur. J. Pharm. Sci. 2004, 21(1):25-51.
6. Chan Y.Y., Kalpana S., Chang W.C., Chen B.K. Expression of aryl hydrocarbon receptor nuclear translocator enhances cisplatin resistance by upregulating MDR1 expression in cancer cells. Mol. Pharmacol. 2013, 84(4):591-602.
7. Di Leo A., Messa C., Cavallini A., Linsalata M. Estrogens and colorectal cancer. Curr. Drug Targets Immune Endocr. Metabol. Disord. 2001, 1(1):1-12.
8. Diah S.K., Smitherman P.K., Townsend A.J., Morrow C.S. Detoxification of 1-chloro-2,4-dinitrobenzene in MCF7 breast cancer cells expressing glutathione S-transferase P 1-1 and/or multidrug resistance protein 1. Toxicol. Appl. Pharmacol. 1999, 157(2):85-93.
9. Dietrich C.G., Geier A., Oude Elferink R.P. ABC of oral bioavailability: transporters as gatekeepers in the gut. Gut 2003, 52(12):1788-1795.
10. Ebert B., Seidel A., Lampen A. Phytochemicals induce breast cancer resistance protein in Caco-2 cells and enhance the transport of benzo[a]pyrene-3-sulfate. Toxicol. Sci. 2007, 96(2):227-236.
11. Edvardsson K., Nguyen-Vu T., Kalasekar S.M., Ponten F., Gustafsson J.A., Williams C. Estrogen receptor beta expression induces changes in the microRNA pool in human colon cancer cells. Carcinogenesis 2013, 34(7):1431-1441.
12. Englund G., Rorsman F., Ronnblom A., Rönnblom A., Karlbom U., Lazorova L., Grasjö J., Kindmark A., Artursson P. Regional levels of drug transporters along the human intestinal tract: co-expression of ABC and SLC transporters and comparison with Caco-2 cells. Eur. J. Pharm. Sci. 2006, 29(3-4):269-277.
13. Enokizono J., Kusuhara H., Sugiyama Y. Regional expression and activity of breast cancer resistance protein (Bcrp/Abcg2) in mouse intestine: overlapping distribution with sulfotransferases. Drug Metab. Dispos. 2007, 35(6):922-928.
14. García F., Kierbel A., Larocca M.C., Gradilone S.A., Splinter P., LaRusso N.F., Marinelli R.A. The water channel aquaporin-8 is mainly intracellular in rat hepatocytes, and its plasma membrane insertion is stimulated by cyclic AMP. J. Biol. Chem. 2001, 276(15):12147-12152.
15. Gerk P.M., Vore M. Regulation of expression of the multidrug resistanceassociated protein 2 (MRP2) and its role in drug disposition. J. Pharmacol. Exp. Ther. 2002, 302:407-415.
16. Goldzieher J.W., Stanczyk F.Z. Oral contraceptives and individual variability of circulating levels of ethinyl estradiol and progestins. Contraception 2008, 78(1):4-9.
17. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpiridine. Anal. Biochem. 1980, 106:207-212.
18. Guo J.Y., Li X., Browning J.D., Rottinghaus G.E., Lubahn D.B., Constantinou A., Bennink M., MacDonald R.S. Dietary soy isoflavones and estrone protect ovariectomized ER alpha KO and wild-type mice from carcinogen-induced colon cancer. J. Nutr. 2004, 134(1):179-182.
19. Gutmann H., Hruz P., Zimmermann C., Beglinger C., Drewe J. Distribution of breast cancer resistance protein (BCRP/ABCG2) mRNA expression along the human GI tract. Biochem. Pharmacol. 2005, 70(5):695-699.
20. Haenisch S., Laechelt S., Bruckmueller H., Werk A., Noack A., Bruhn O., Remmler C., Cascorbi I. Down-regulation of ATP-binding cassette C2 protein expression in HepG2 cells after rifampicin treatment is mediated by MicroRNA-379. Mol. Pharmacol. 2011, 80(2):314-320.
21. Hammond G.L., Lahteenmaki P.L., Lahteenmaki P., Luukkainen T. Distribution and percentages of non-protein bound contraceptive steroids in human serum. J. Steroid Biochem. 1982, 17(4):375-380.
22. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., Tujague M., Strom A., Treuter E., Warner M., Gustafsson J.A. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 2007, 87(3):905-931.
23. Hua P., Tsai W.J., Kuo S.M. Estrogen response element-independent regulation of gene expression by genistein in intestinal cells. Biochim. Biophys. Acta 2003, 1627(2-3):63-70.
24. Ikeguchi M., Teeter L.D., Eckersberg T., Ganapathi R., Kuo M.T. Structural and functional analyses of the promoter of the murine multidrug resistance gene mdr3/mdr1a reveal a negative element containing the AP-1 binding site. DNA Cell Biol. 1991, 10(9):639-649.
25. Imai Y., Ishikawa E., Asada S., Sugimoto Y. Estrogen-mediated post transcriptional down-regulation of breast cancer resistance protein/ABCG2. Cancer Res. 2005, 65(2):596-604.
26. Jacobs M.N., Nolan G.T., Hood S.R. Lignans, bacteriocides and organochlorine compounds activate the human pregnane X receptor (PXR). Toxicol. Appl. Pharmacol. 2005, 209(2):123-133.
27. Johnson D.R., Klaassen C.D. Regulation of rat multidrug resistance protein 2 by classes of prototypical microsomal enzyme inducers that activate distinct transcription pathways. Toxicol. Sci. 2002, 67:182-189.
28. Kamath A.V., Darling I.M., Morris M.E. Choline uptake in human intestinal Caco-2 cells is carrier-mediated. J. Nutr. 2003, 133(8):2607-2611.
29. Katzenellenbogen B.S., Montano M.M., Ediger T.R., Sun J., Ekena K., Lazennec G., Martini P.G., McInerney E.M., Delage-Mourroux R., Weis K., Katzenellenbogen J.A. Estrogen receptors: selective ligands, partners, and distinctive pharmacology. Recent Prog. Horm. Res. 2000, 55:163-193. (discussion 194-5).
30. Konstantinopoulos P.A., Kominea A., Vandoros G., Sykiotis G.P., Andricopoulos P., Varakis I., Sotiropoulou-Bonikou G., Papavassiliou A.G. Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour's dedifferentiation. Eur. J. Cancer 2003, 39(9):1251-1258.
31. Kota B.P., Tran V.H., Allen J., Bebawy M., Roufogalis B.D. Characterization of PXR mediated P-glycoprotein regulation in intestinal LS174T cells. Pharmacol. Res. 2010, 62(5):426-431.
32. Leslie E.M., Ghibellini G., Nezasa K., Brouwer K.L. Biotransformation and transport of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) in bile duct-cannulated wild-type and Mrp2/Abcc2-deficient (TR-) Wistar rats. Carcinogenesis 2007, 28(12):2650-2656.
33. Levin E.R. Integration of the extranuclear and nuclear actions of estrogen. Mol. Endocrinol. 2005, 19(8):1951-1959.
34. Li L.C., Yeh C.C., Nojima D., Dahiya R. Cloning and characterization of human estrogen receptor beta promoter. Biochem. Biophys. Res. Commun. 2000, 275(2). 682-9,10.
35. Marguerite V., Beri-Dexheimer M., Ortiou S., Gueant J.L., Merten M. Cobalamin potentiates vinblastine cytotoxicity through downregulation of mdr-1 gene expression in HepG2 cells. Cell Physiol. Biochem. 2007, 20(6):967-976.
36. Marino M., Galluzzo P., Ascenzi P. Estrogen signaling multiple pathways to impact gene transcription. Curr. Genomics 2006, 7(8):497-508.
37. Miao Z.H., Ding J. Transcription factor c-Jun activation represses mdr-1 gene expression. Cancer Res. 2003, 63(15):4527-4532.
38. Minhas H.S., Thornalley P.J. Reduced glutathione esters antidotes to toxicity. Cytotoxicity induced by hydrogen peroxide, 1-chloro-2,4-dinitrobenzene, and menadione in murine P388D1 macrophages in vitro. J. Biochem. Toxicol. 1995, 10(5):245-250.
39. Mnif W., Pascussi J.M., Pillon A., Escande A., Bartegi A., Nicolas J.C., Cavaillès V., Duchesne M.J., Balaguer P. Estrogens and antiestrogens activate hPXR. Toxicol. Lett. 2007, 170(1):19-29.
40. Mottino A.D., Hoffman T., Jennes L., Cao J., Vore M. Expression of multidrug resistance-associated protein 2 in small intestine from pregnant and postpartum rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 280(6):G1261-G1273.
41. Mottino A.D., Hoffman T., Jennes L., Vore M. Expression and localization of multidrug resistant protein mrp2 in rat small intestine. J. Pharmacol. Exp. Ther. 2000, 293(3):717-723.
42. Nagao M., Saitoh H., Zhang W.D., Iseki K., Yamada Y., Takatori T., Miyazaki K. Transport characteristics of paraquat across rat intestinal brush-border membrane. Arch. Toxicol. 1993, 67(4):262-267.
43. Oseni T., Patel R., Pyle J., Jordan V.C. Selective estrogen receptor modulators and phytoestrogens. Planta Med. 2008, 74(13):1656-1665.
44. Penny J.I., Campbell F.C. Active transport of benzo[a]pyrene in apical membrane vesicles from normal human intestinal epithelium. Biochim. Biophys. Acta 1994, 1226(2):232-236.
45. Press B., Di Grandi D. Permeability for intestinal absorption: Caco-2 assay and related issues. Curr. Drug Metab. 2008, 9(9):893-900.
46. Rigalli J.P., Ruiz M.L., Perdomo V.G., Villanueva S.S., Mottino A.D., Catania V.A. Pregnane X receptor mediates the induction of P-glycoprotein by spironolactone in HepG2 cells. Toxicology 2011, 285(1-2):18-24.
47. Robertson J.F. Faslodex (ICI 182, 780), a novel estrogen receptor downregulator - future possibilities in breast cancer. J. Steroid Biochem. Mol. Biol. 2001, 79(1-5):209-212.
48. Ruiz M.L., Villanueva S.S., Luquita M.G., Sánchez-Pozzi E.J., Crocenzi F.A., Pellegrino J.M., Ochoa J.E., Vore M., Mottino A.D., Catania V.A. Mechanisms involved in spironolactone-induced choleresis in the rat. Role of multidrug resistance-associated protein 2. Biochem. Pharmacol. 2005, 69(3):531-539.
49. Sane R.S., Buckley D.J., Buckley A.R., Nallani S.C., Desai P.B. Role of human pregnane X receptor in tamoxifen- and 4-hydroxytamoxifen-mediated CYP3A4 induction in primary human hepatocytes and LS174T cells. Drug Metab. Dispos. 2008, 36(5):946-954.
50. Schinkel A.H., Jonker J.W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv. Drug Deliv. Rev. 2003, 55(1):3-29.
51. Setchell K.D., Cassidy A. Dietary isoflavones: biological effects and relevance to human health. J. Nutr. 1999, 129(3):758S-767S.
52. Silva R., Carmo H., Dinis-Oliveira R., Cordeiro-da-Silva A., Lima S.C., Carvalho F., Bastos M.de L., Remião F. In vitro study of P-glycoprotein induction as an antidotal pathway to prevent cytotoxicity in Caco-2 cells. Arch. Toxicol. 2011, 85(4):315-326.
53. Takano M., Yumoto R., Murakami T. Expression and function of efflux drug transporters in the intestine. Pharmacol. Ther. 2006, 109(1-2):137-161.
54. Tateishi Y., Kawabe Y., Chiba T., Murata S., Ichikawa K., Murayama A., Tanaka K., Baba T., Kato S., Yanagisawa J. Ligand-dependent switching of ubiquitin-proteasome pathways for estrogen receptor. EMBO J. 2004, 23(24):4813-4823.
55. Tiong C.T., Chen C., Zhang S.J., Li J., Soshilov A., Denison M.S., Lee L.S., Tam V.H., Wong S.P., Xu H.E., Yong E.L. A novel prenylflavone restricts breast cancer cell growth through AhR-mediated destabilization of ERalpha protein. Carcinogenesis 2012, 33(5):1089-1097.
56. Townsend A.J., Fields W.R., Haynes R.L., Doss A.J., Li Y., Doehmer J., Morrow C.S. Chemoprotective functions of glutathione S-transferases in cell lines induced to express specific isozymes by stable transfection. Chem. Biol. Interact. 1998, 111-112:389-407.
57. Vermeulen M.A., de Jong J., Vaessen M.J., van Leeuwen P.A., Houdijk A.P. Glutamate reduces experimental intestinal hyperpermeability and facilitates glutamine support of gut integrity. World J. Gastroenterol. 2011, 17(12):1569-1573.
58. Videmann B., Tep J., Cavret S., Lecoeur S. Epithelial transport of deoxynivalenol: involvement of human P-glycoprotein (ABCB1) and multidrug resistance-associated protein 2 (ABCC2). Food Chem. Toxicol. 2007, 45(10):1938-1947.
59. Wang T.T., Sathyamoorthy N., Phang J.M. Molecular effects of genistein on estrogen receptor mediated pathways. Carcinogenesis 1996, 17(2):271-275.
60. Weige C.C., Allred K.F., Allred C.D. Estradiol alters cell growth in nonmalignant colonocytes and reduces the formation of preneoplastic lesions in the colon. Cancer Res. 2009, 69(23):9118-9124.
61. Zhao L., O'Neill K., Brinton R.D. Estrogenic agonist activity of ICI 182,780 (Faslodex) in hippocampal neurons: implications for basic science understanding of estrogen signaling and development of estrogen modulators with a dual therapeutic profile. J. Pharmacol. Exp. Ther. 2006, 319(3):1124-1132.