Breast cancer resistance protein BCRP/ABCG2 regulatory microRNAs (hsa-miR-328, -519c and -520h) and their differential expression in stem-like ABCG2+ cancer cells

Biochemical Pharmacology

Volumn 81, Issue 6, 2011, Pages 783-792

  Li, Xin ^a,b   Pan, Yu Zhuo ^a   Seigel, Gail M ^a,c   Hu, Zi Hua ^d   Huang, Min ^b   Yu, Ai Ming ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c SUNY EYE INSTITUTE   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

BCRP ABCG2; Breast cancer; Drug disposition; Epigenetic; Gene regulation; miRNA; Multidrug resistance; Retinoblastoma; Stem cell

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; HSA MICRORNA 328; LUCIFERASE; MESSENGER RNA; MICRORNA; MICRORNA 519C; MICRORNA 520H; MITOXANTRONE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BREAST CANCER; CANCER CELL; CELL STRAIN MCF 7; CONTROLLED STUDY; DIFFERENTIAL DISPLAY; DNA RESPONSIVE ELEMENT; DOWN REGULATION; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOMAGNETIC SEPARATION; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINOBLASTOMA; RNA DEGRADATION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; UPREGULATION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; LUCIFERASES, RENILLA; MICRORNAS; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS;

EID: 79951943718     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.12.018     Document Type: Article

References (47)

1. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136(2):215-33.
2. Ambros V. The functions of animal microRNAs. Nature 2004;431(7006):350-5. (Pubitemid 39265675)
3. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009;19(1):92-105.
4. Yu AM. Role of microRNAs in the regulation of drug metabolism and disposition. Expert Opin Drug Metab Toxicol 2009;5(12):1513-28.
5. Yu AM. Small interfering RNA in drug metabolism and transport. Curr Drug Metab 2007;8(7):700-8.
6. Ingelman-Sundberg M, Sim SC, Gomez A, Rodriguez-Antona C. Influence of cytochrome P450 polymorphisms on drug therapies: pharmacogenetic, pharmacoepigenetic and clinical aspects. Pharmacol Ther 2007;116(3):496-526. (Pubitemid 350116943)
7. Choudhuri S, Cui Y, Klaassen CD. Molecular targets of epigenetic regulation and effectors of environmental influences. Toxicol Appl Pharmacol 2010;245(3): 378-93.
8. Gomez A, Ingelman-Sundberg M. Epigenetic and microRNA-dependent control of cytochrome P450 expression: a gap between DNA and protein. Pharmacogenomics 2009;10(7):1067-76.
9. Tsuchiya Y, Nakajima M, Takagi S, Taniya T, Yokoi T. MicroRNA regulates the expression of human cytochrome P450 1B1. Cancer Res 2006;66(18):9090-8. (Pubitemid 44521128)
10. Pan YZ, Gao W, Yu AM. MicroRNAs regulate CYP3A4 expression via direct and indirect targeting. Drug Metab Dispos 2009;37(10):2112-7.
11. 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;75(6):1374-9.
12. Kovalchuk O, Filkowski J, Meservy J, Ilnytskyy Y, Tryndyak VP, Chekhun VF, et al. Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol Cancer Ther 2008;7(7): 2152-9.
13. Zhu H, Wu H, Liu X, Evans BR, Medina DJ, Liu CG, et al. Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells. Biochem Pharmacol 2008;76(5):582-8.
14. To KK, Robey RW, Knutsen T, Zhan Z, Ried T, Bates SE. Escape from hsa-miR- 519c enables drug-resistant cells to maintain high expression of ABCG2. Mol Cancer Ther 2009;8(10):2959-68.
15. To KK, Zhan Z, Litman T, Bates SE. Regulation of ABCG2 expression at the 3′ 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;28(17):5147-61.
16. Liang Z, Wu H, Xia J, Li Y, Zhang Y, Huang K, et al. Involvement of miR-326 in chemotherapy resistance of breast cancer through modulating expression of multidrug resistance-associated protein 1. Biochem Pharmacol 2010;79(6): 817-24.
17. Mohri T, Nakajima M, Fukami T, Takamiya M, Aoki Y, Yokoi T. Human CYP2E1 is regulated by miR-378. Biochem Pharmacol 2010;79(7):1045-52.
18. Wang F, Xue X, Wei J, An Y, Yao J, Cai H, et al. hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations. Br J Cancer 2010;103(4):567-74.
19. Guo L, Liu Y, Bai Y, Sun Y, Xiao F, Guo Y. Gene expression profiling of drug-resistant small cell lung cancer cells by combining microRNA and cDNA expression analysis. Eur J Cancer 2010;46(9):1692-702.
20. Takagi S, Nakajima M, Mohri T, Yokoi T. Post-transcriptional regulation of human pregnane X receptor by micro-RNA affects the expression of cytochrome P450 3A4. J Biol Chem 2008;283(15):9674-80.
21. Ji J, Zhang J, Huang G, Qian J, Wang X, Mei S. Over-expressed microRNA-27a and 27b influence fat accumulation and cell proliferation during rat hepatic stellate cell activation. FEBS Lett 2009;583(4):759-66.
22. Takagi S, Nakajima M, Kida K, Yamaura Y, Fukami T, Yokoi T. MicroRNAs regulate human hepatocyte nuclear factor 4alpha, modulating the expression of metabolic enzymes and cell cycle. J Biol Chem 2010;285(7):4415-22.
23. Krishnamurthy P, Schuetz JD. Role of ABCG2/BCRP in biology and medicine. Annu Rev Pharmacol Toxicol 2006;46:381-410. (Pubitemid 43271195)
24. van Herwaarden AE, Schinkel AH. The function of breast cancer resistance protein in epithelial barriers, stem cells and milk secretion of drugs and xenotoxins. Trends Pharmacol Sci 2006;27(1):10-6. (Pubitemid 43063119)
25. Ross DD, Yang W, Abruzzo LV, Dalton WS, Schneider E, Lage H, et al. Atypical multidrug resistance: breast cancer resistance protein messenger RNA expression in mitoxantrone-selected cell lines. J Natl Cancer Inst 1999;91(5): 429-33. (Pubitemid 29128278)
26. Volk EL, Farley KM,Wu Y, Li F, Robey RW, Schneider E. Overexpression of wild-type breast cancer resistance protein mediates methotrexate resistance. Cancer Res 2002;62(17):5035-40. (Pubitemid 34984431)
27. Knutsen T, Rao VK, Ried T, Mickley L, Schneider E, Miyake K, et al. Amplification of 4q21-q22 and the MXR gene in independently derived mitoxantrone-resistant cell lines. Genes Chromosomes Cancer 2000;27(1):110-6.
28. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 2001;7(9):1028-34. (Pubitemid 32937383)
29. Kim M, Turnquist H, Jackson J, Sgagias M, Yan Y, Gong M, et al. The multidrug resistance transporter ABCG2 (breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietic stem cells. Clin Cancer Res 2002;8(1):22-8. (Pubitemid 34101455)
30. Scharenberg CW, Harkey MA, Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 2002;99(2):507-12. (Pubitemid 34533085)
31. Liao R, Sun J, Zhang L, Lou G, Chen M, Zhou D, et al. MicroRNAs play a role in the development of human hematopoietic stem cells. J Cell Biochem 2008;104(3): 805-17. (Pubitemid 351830831)
32. Apati A, Orban TI, Varga N, Nemeth A, Schamberger A, Krizsik V, et al. High level functional expression of the ABCG2 multidrug transporter in undifferentiated human embryonic stem cells. Biochim Biophys Acta 2008;1778(12): 2700-9.
33. Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB. Proliferating cells express mRNAs with shortened 30 untranslated regions and fewer microRNA target sites. Science 2008;320(5883):1643-7. (Pubitemid 351931255)
34. Mayr C, Bartel DP. Widespread shortening of 30UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 2009;138(4):673-84.
35. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005;120(1):15-20. (Pubitemid 40094598)
36. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. The role of site accessibility in microRNA target recognition. Nat Genet 2007;39(10):1278-84. (Pubitemid 47482690)
37. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 2006;34(Database issue):D140-4.
38. Miranda KC, Huynh T, Tay Y, Ang YS, Tam WL, Thomson AM, et al. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 2006;126(6):1203-17. (Pubitemid 44380294)
39. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005;33(20):e179.
40. Robey RW, Honjo Y, van de Laar A, Miyake K, Regis JT, Litman T, et al. A functional assay for detection of the mitoxantrone resistance protein, MXR (ABCG2). Biochim Biophys Acta 2001;1512(2):171-82. (Pubitemid 32530764)
41. Zhou XF, Yang X, Wang Q, Coburn RA, Morris ME. Effects of dihydropyridines and pyridines on multidrug resistance mediated by breast cancer resistance protein: in vitro and in vivo studies. Drug Metab Dispos 2005;33(8):1220-8. (Pubitemid 41043766)
42. Merino G, Real R, Baro MF, Gonzalez-Lobato L, Prieto JG, Alvarez AI, et al. Natural allelic variants of bovine ATP-binding cassette transporter ABCG2: increased activity of the Ser581 variant and development of tools for the discovery of new ABCG2 inhibitors. Drug Metab Dispos 2009;37(1):5-9.
43. Young IT. Proof without prejudice: use of the Kolmogorov-Smirnov test for the analysis of histograms from flow systems and other sources. J Histochem Cytochem 1977;25(7):935-41. (Pubitemid 8170725)
44. Garcia-Escarp M, Martinez-Munoz V, Sales-Pardo I, Barquinero J, Domingo JC, Marin P, et al. Flow cytometry-based approach to ABCG2 function suggests that the transporter differentially handles the influx and efflux of drugs. Cytometry A 2004;62(2):129-38. (Pubitemid 39579243)
45. Seigel GM, Hackam AS, Ganguly A, Mandell LM, Gonzalez-Fernandez F. Human embryonic and neuronal stem cell markers in retinoblastoma. Mol Vis 2007;13:823-32. (Pubitemid 46908324)
46. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414(6859):105-11. (Pubitemid 33041634)
47. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 2007;43(5):935-46. (Pubitemid 46366698)