559
Views
40
CrossRef citations to date
0
Altmetric
Review

ATP-binding cassette transmembrane transporters and their epigenetic control in cancer: an overview

, , , &
Pages 1419-1432 | Received 02 Mar 2016, Accepted 18 Jul 2016, Published online: 03 Aug 2016

References

  • Newman WG. Pharmacogenetics: transforming clinical medicine. J R Coll Physicians Edinb. 2012;42(3):244–247.
  • Blakey JD, Hall IP. Current progress in pharmacogenetics. Br J Clin Pharmacol. 2011;71(6):824–831.
  • Cohen JP. Overcoming regulatory and economic challenges facing pharmacogenomics. N Biotechnol. 2012;29(6):751–756.
  • Lesko LJ, Schmidt S. Individualization of drug therapy: history, present state, and opportunities for the future. Clin Pharmacol Ther. 2012;92(4):458–466.
  • Eichelbaum M, Ingelman-Sundberg M, Evans WE. Pharmacogenomics and individualized drug therapy. Annu Rev Med. 2006;57:119–137.
  • Roses AD. Pharmacogenetics and drug development: the path to safer and more effective drugs. Nat Rev Genet. 2004;5(9):645–656.
  • Peng L, Zhong X. Epigenetic regulation of drug metabolism and transport. Acta Pharm Sin B. 2015;5(2):106–112.
  • Apellaniz-Ruiz M, Gallego C, Ruiz-Pinto S, et al. Human genetics: international projects and personalized medicine. Drug Metab Pers Ther. 2016;31(1):3–8.
  • Berger SL, Kouzarides T, Shiekhattar R, et al. An operational definition of epigenetics. Genes Dev. 2009;23(7):781–783.
  • Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6–21.
  • Wang Z, Zang C, Cui K, et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell. 2009;138(5):1019–1031.
  • Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129(4):823–837.
  • Guenther MG, Levine SS, Boyer LA, et al. A chromatin landmark and transcription initiation at most promoters in human cells. Cell. 2007;130(1):77–88.
  • Rose NR, Klose RJ. Understanding the relationship between DNA methylation and histone lysine methylation. Biochim Biophys Acta. 2014;1839(12):1362–1372.
  • Cohen I, Poreba E, Kamieniarz K, et al. Histone modifiers in cancer: friends or foes? Genes Cancer. 2011;2(6):631–647.
  • Tan M, Luo H, Lee S, et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell. 2011;146(6):1016–1028.
  • Guo H, Ingolia NT, Weissman JS, et al. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010;466(7308):835–840.
  • Guttman M, Amit I, Garber M, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458(7235):223–227.
  • Hu W, Yuan B, Flygare J, et al. Long noncoding RNA-mediated anti-apoptotic activity in murine erythroid terminal differentiation. Genes Dev. 2011;25(24):2573–2578.
  • Fanini F, Fabbri M. MicroRNAs and cancer resistance: a new molecular plot. Clin Pharmacol Ther. 2016;99(5):485–493.
  • Sin TK, Wang F, Meng F, et al. Implications of MicroRNAs in the treatment of gefitinib-resistant non-small cell lung cancer. Int J Mol Sci. 2016;17(2):237.
  • Kim IW, Han N, Burckart GJ, et al. Epigenetic changes in gene expression for drug-metabolizing enzymes and transporters. Pharmacotherapy. 2014;34(2):140–150.
  • Gagnon JF, Bernard O, Villeneuve L, et al. Irinotecan inactivation is modulated by epigenetic silencing of UGT1A1 in colon cancer. Clin Cancer Res. 2006;12(6):1850–1858.
  • Woodson K, O’Reilly KJ, Hanson JC, et al. The usefulness of the detection of GSTP1 methylation in urine as a biomarker in the diagnosis of prostate cancer. J Urol. 2008;179(2):508–511.
  • Baker EK, Johnstone RW, Zalcberg JR, et al. Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene. 2005;24(54):8061–8075.
  • Turner JG, Gump JL, Zhang C, et al. ABCG2 expression, function, and promoter methylation in human multiple myeloma. Blood. 2006;108(12):3881–3889.
  • Glubb DM, Innocenti F. Mechanisms of genetic regulation in gene expression: examples from drug metabolizing enzymes and transporters. Wiley Interdiscip Rev Syst Biol Med. 2011;3(3):299–313.
  • Dean M, Rzhetsky A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001;11(7):1156–1166.
  • Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol. 1992;8:67–113.
  • Moitra K. Overcoming multidrug resistance in cancer stem cells. Biomed Res Int. 2015;2015:635745.
  • Szakacs G, Paterson JK, Ludwig JA, et al. Targeting multidrug resistance in cancer. Nat Rev Drug Discov. 2006;5(3):219–234.
  • Brambila-Tapia AJ. MDR1 (ABCB1) polymorphisms: functional effects and clinical implications. Rev Invest Clin. 2013;65(5):445–454.
  • Li YH, Wang YH, Li Y, et al. MDR1 gene polymorphisms and clinical relevance. Yi Chuan Xue Bao. 2006;33(2):93–104.
  • Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer. 2002;2(1):48–58.
  • Cordon-Cardo C, O’Brien JP, Boccia J, et al. Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumor tissues. J Histochem Cytochem. 1990;38(9):1277–1287.
  • Katayama K, Noguchi K, Sugimoto Y. Regulations of P-Glycoprotein/ABCB1/MDR1 in human cancer cells. New J Sci. 2014;2014:476974.
  • Scotto KW. Transcriptional regulation of ABC drug transporters. Oncogene. 2003;22:7496–11.
  • Lopes-Rodrigues V, Seca H, Sousa D, et al. The network of P-glycoprotein and microRNAs interactions. Int J Cancer. 2014;135(2):253–263.
  • Bakos E, Evers R, Szakacs G, et al. Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J Biol Chem. 1998;273(48):32167–32175.
  • Szakacs G, Annereau JP, Lababidi S, et al. Predicting drug sensitivity and resistance: profiling ABC transporter genes in cancer cells. Cancer Cell. 2004;6(2):129–137.
  • Hipfner DR, Deeley RG, Cole SP. Structural, mechanistic and clinical aspects of MRP1. Biochim Biophys Acta. 1999;1461(2):359–376.
  • Abbott BL. ABCG2 (BCRP) expression in normal and malignant hematopoietic cells. Hematol Oncol. 2003;21(3):115–130.
  • Ivanov M, Barragan I, Ingelman-Sundberg M. Epigenetic mechanisms of importance for drug treatment. Trends Pharmacol Sci. 2014;35(8):384–396.
  • Sim SC, Ingelman-Sundberg M. Pharmacogenomic biomarkers: new tools in current and future drug therapy. Trends Pharmacol Sci. 2011;32(2):72–81.
  • Shuldiner AR, Relling MV, Peterson JF, et al. The pharmacogenomics research network translational pharmacogenetics program: overcoming challenges of real-world implementation. Clin Pharmacol Ther. 2013;94(2):207–210.
  • Su SC, Chung WH, Hung SI. Digging up the human genome: current progress in deciphering adverse drug reactions. Biomed Res Int. 2014;2014:824343.
  • Ueda K, Pastan I, Gottesman MM. Isolation and sequence of the promoter region of the human multidrug-resistance (P-glycoprotein) gene. J Biol Chem. 1987;262(36):17432–17436.
  • Garcia-Manero G, Daniel J, Smith TL, et al. DNA methylation of multiple promoter-associated CpG islands in adult acute lymphocytic leukemia. Clin Cancer Res. 2002;8(7):2217–2224.
  • Henrique R, Oliveira AI, Costa VL, et al. Epigenetic regulation of MDR1 gene through post-translational histone modifications in prostate cancer. BMC Genomics. 2013;14:898.
  • El-Osta A, Kantharidis P, Zalcberg JR, et al. Precipitous release of methyl-CpG binding protein 2 and histone deacetylase 1 from the methylated human multidrug resistance gene (MDR1) on activation. Mol Cell Biol. 2002;22(6):1844–1857.
  • Tada Y, Wada M, Kuroiwa K, et al. MDR1 gene overexpression and altered degree of methylation at the promoter region in bladder cancer during chemotherapeutic treatment. Clin Cancer Res. 2000;6(12):4618–4627.
  • Chen KG, Wang YC, Schaner ME, et al. Genetic and epigenetic modeling of the origins of multidrug-resistant cells in a human sarcoma cell line. Cancer Res. 2005;65(20):9388–9397.
  • Huo H, Magro PG, Pietsch EC, et al. Histone methyltransferase MLL1 regulates MDR1 transcription and chemoresistance. Cancer Res. 2010;70(21):8726–8735.
  • Haenisch S, Werk AN, Cascorbi I. MicroRNAs and their relevance to ABC transporters. Br J Clin Pharmacol. 2014;77(4):587–596.
  • Rigoutsos I. New tricks for animal microRNAS: targeting of amino acid coding regions at conserved and nonconserved sites. Cancer Res. 2009;69(8):3245–3248.
  • Piriyapongsa J, Bootchai C, Ngamphiw C, et al. microPIR: an integrated database of microRNA target sites within human promoter sequences. PLoS One. 2012;7(3):e33888.
  • Griffiths-Jones S, Saini HK, van Dongen S, et al. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008;36(Databaseissue):D154- D158.
  • Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014;42(Databaseissue):D68–D73.
  • Calin GA, Sevignani C, Dumitru CD, et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA. 2004;101(9):2999–3004.
  • Toscano-Garibay JD, Aquino-Jarquin G. Regulation exerted by miRNAs in the promoter and UTR sequences: MDR1/P-gp expression as a particular case. DNA Cell Biol. 2012;31(8):1358–1364.
  • Dong Z, Ren L, Lin L, et al. Effect of microRNA-21 on multidrug resistance reversal in A549/DDP human lung cancer cells. Mol Med Rep. 2015;11(1):682–690.
  • Chen Z, Ma T, Huang C, et al. MiR-27a modulates the MDR1/P-glycoprotein expression by inhibiting FZD7/beta-catenin pathway in hepatocellular carcinoma cells. Cell Signal. 2013;25(12):2693–2701.
  • Feng DD, Zhang H, Zhang P, et al. Down-regulated miR-331-5p and miR-27a are associated with chemotherapy resistance and relapse in leukaemia. J Cell Mol Med. 2011;15(10):2164–2175.
  • Zhang Y, Qu X, Li C, et al. miR-103/107 modulates multidrug resistance in human gastric carcinoma by downregulating Cav-1. Tumour Biol. 2015;36(4):2277–2285.
  • Wu Q, Yang Z, Xia L, et al. Methylation of miR-129-5p CpG island modulates multi-drug resistance in gastric cancer by targeting ABC transporters. Oncotarget. 2014;5(22):11552–11563.
  • Zong C, Wang J, Shi TM. MicroRNA 130b enhances drug resistance in human ovarian cancer cells. Tumour Biol. 2014;35(12):12151–12156.
  • Zhu X, Li Y, Shen H, et al. miR-137 restoration sensitizes multidrug-resistant MCF-7/ADM cells to anticancer agents by targeting YB-1. Acta Biochim Biophys Sin (Shanghai). 2013;45(2):80–86.
  • Ikemura K, Yamamoto M, Miyazaki S, et al. MicroRNA-145 post-transcriptionally regulates the expression and function of P-glycoprotein in intestinal epithelial cells. Mol Pharmacol. 2013;83(2):399–405.
  • Sun KX, Jiao JW, Chen S, et al. MicroRNA-186 induces sensitivity of ovarian cancer cells to paclitaxel and cisplatin by targeting ABCB1. J Ovarian Res. 2015;8(1):80.
  • Chen J, Tian W, Cai H, et al. Down-regulation of microRNA-200c is associated with drug resistance in human breast cancer. Med Oncol. 2012;29(4):2527–2534.
  • Yang T, Zheng ZM, Li XN, et al. MiR-223 modulates multidrug resistance via downregulation of ABCB1 in hepatocellular carcinoma cells. Exp Biol Med (Maywood). 2013;238(9):1024–1032.
  • Bao L, Hazari S, Mehra S, et al. Increased expression of P-glycoprotein and doxorubicin chemoresistance of metastatic breast cancer is regulated by miR-298. Am J Pathol. 2012;180(6):2490–2503.
  • He DX, Gu XT, Jiang L, et al. A methylation-based regulatory network for microRNA 320a in chemoresistant breast cancer. Mol Pharmacol. 2014;86(5):536–547.
  • Xu Y, Ohms SJ, Li Z, et al. Changes in the expression of miR-381 and miR-495 are inversely associated with the expression of the MDR1 gene and development of multi-drug resistance. PLoS One. 2013;8(11):e82062.
  • Kovalchuk O, Filkowski J, Meservy J, 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):2152–2159.
  • Bandres E, Bitarte N, Arias F, et al. MicroRNA-451 regulates macrophage migration inhibitory factor production and proliferation of gastrointestinal cancer cells. Clin Cancer Res. 2009;15:2281–2290.
  • Shang Y, Zhang Z, Liu Z, et al. miR-508-5p regulates multidrug resistance of gastric cancer by targeting ABCB1 and ZNRD1. Oncogene. 2014;33(25):3267–3276.
  • Boyerinas B, Park SM, Murmann AE, et al. Let-7 modulates acquired resistance of ovarian cancer to Taxanes via IMP-1-mediated stabilization of multidrug resistance 1. Int J Cancer. 2012;130(8):1787–1797.
  • Zhu H, Wu H, Liu X, 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):582–588.
  • Li Z, Hu S, Wang J, et al. MiR-27a modulates MDR1/P-glycoprotein expression by targeting HIPK2 in human ovarian cancer cells. Gynecol Oncol. 2010;119(1):125–130.
  • Zhang H, Li M, Han Y, et al. Down-regulation of miR-27a might reverse multidrug resistance of esophageal squamous cell carcinoma. Dig Dis Sci. 2010;55(9):2545–2551.
  • Zhao X, Yang L, Hu J. Down-regulation of miR-27a might inhibit proliferation and drug resistance of gastric cancer cells. J Exp Clin Cancer Res. 2011;30:55.
  • Zhao X, Yang L, Hu J, et al. miR-138 might reverse multidrug resistance of leukemia cells. Leuk Res. 2010;34(8):1078–1082.
  • Tsang TY, Tang WY, Chan JY, et al. P-glycoprotein enhances radiation-induced apoptotic cell death through the regulation of miR-16 and Bcl-2 expressions in hepatocellular carcinoma cells. Apoptosis. 2011;16(5):524–535.
  • Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 2009;23(13):1494–1504.
  • Pang KC, Frith MC, Mattick JS. Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet. 2006;22(1):1–5.
  • Shi X, Sun M, Liu H, et al. Long non-coding RNAs: a new frontier in the study of human diseases. Cancer Lett. 2013;339(2):159–166.
  • Mourtada-Maarabouni M, Pickard MR, Hedge VL, et al. GAS5, a non-protein-coding RNA, controls apoptosis and is down-regulated in breast cancer. Oncogene. 2009;28(2):195–208.
  • Matouk IJ, Abbasi I, Hochberg A, et al. Highly upregulated in liver cancer non-coding RNA is overexpressed in hepatic colorectal metastasis. Eur J Gastroenterol Hepatol. 2009 Jun;21(6):688–692.
  • Wang Y, Zhang D, Wu K, et al. Long noncoding RNA MRUL promotes ABCB1 expression in multidrug-resistant gastric cancer cell sublines. Mol Cell Biol. 2014;34(17):3182–3193.
  • Cole SP. Multidrug resistance protein 1 (MRP1, ABCC1), a “multitasking” ATP-binding cassette (ABC) transporter. J Biol Chem. 2014;289(45):30880–30888.
  • Kunicka T, Soucek P. Importance of ABCC1 for cancer therapy and prognosis. Drug Metab Rev. 2014;46(3):325–342.
  • Chen M, Xue X, Wang F, et al. Expression and promoter methylation analysis of ATP-binding cassette genes in pancreatic cancer. Oncol Rep. 2012;27(1):265–269.
  • Liu H, Wu X, Huang J, et al. miR-7 modulates chemoresistance of small cell lung cancer by repressing MRP1/ABCC1. Int J Exp Pathol. 2015;96(4):240–247.
  • Ma J, Wang T, Guo R, et al. Involvement of miR-133a and miR-326 in ADM resistance of HepG2 through modulating expression of ABCC1. J Drug Target. 2015;23(6):519–524.
  • Lu L, Ju F, Zhao H, et al. MicroRNA-134 modulates resistance to doxorubicin in human breast cancer cells by downregulating ABCC1. Biotechnol Lett. 2015;37(12):2387–2394.
  • Liang Z, Wu H, Xia J, 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):817–824.
  • Pan YZ, Zhou A, Hu Z, et al. Small nucleolar RNA-derived microRNA hsa-miR-1291 modulates cellular drug disposition through direct targeting of ABC transporter ABCC1. Drug Metab Dispos. 2013;41(10):1744–1751.
  • Nakanishi T, Ross DD. Breast cancer resistance protein (BCRP/ABCG2): its role in multidrug resistance and regulation of its gene expression. Chin J Cancer. 2012;31(2):73–99.
  • To KK, Zhan Z, Bates SE. Aberrant promoter methylation of the ABCG2 gene in renal carcinoma. Mol Cell Biol. 2006;26(22):8572–8585.
  • Bram EE, Stark M, Raz S, et al. Chemotherapeutic drug-induced ABCG2 promoter demethylation as a novel mechanism of acquired multidrug resistance. Neoplasia. 2009;11(12):1359–1370.
  • Wang XK, He JH, Xu JH, et al. Afatinib enhances the efficacy of conventional chemotherapeutic agents by eradicating cancer stem-like cells. Cancer Res. 2014 Aug 15;74(16):4431–4445.
  • Moon -H-H, Kim S-H, Ku J-L. Correlation between the promoter methylation status of ATP-binding cassette sub-family G member 2 and drug sensitivity in colorectal cancer cell lines. Oncol Rep. 2016;35(1):298–306.
  • Calcagno AM, Fostel JM, To KK, et al. Single-step doxorubicin-selected cancer cells overexpress the ABCG2 drug transporter through epigenetic changes. Br J Cancer. 2008;98(9):1515–1524.
  • To KK, Polgar O, Huff LM, et al. Histone modifications at the ABCG2 promoter following treatment with histone deacetylase inhibitor mirror those in multidrug-resistant cells. Mol Cancer Res. 2008;6(1):151–164.
  • Shen WW, Zeng Z, Zhu WX, et al. MiR-142-3p functions as a tumor suppressor by targeting CD133, ABCG2, and Lgr5 in colon cancer cells. J Mol Med (Berl). 2013;91(8):989–1000.
  • 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):1374–1379.
  • Li X, Pan Y-Z, Seigel GM, et al. Breast cancer resistance protein BCRP/ABCG2 regulatory microRNAs (hsa-miR-328, -519c and -520h) and their differential expression in stem-like ABCG2+ cancer cells. Biochem Pharmacol. 2011;81(6):783–792.
  • Wang F, Xue X, Wei J, et al. hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations. Br J Cancer. 2010;103(4):567–574.
  • Liu S, Tetzlaff MT, Cui R, et al. miR-200c inhibits melanoma progression and drug resistance through down-regulation of BMI-1. Am J Pathol. 2012;181(5):1823–1835.
  • Jiao X, Zhao L, Ma M, et al. MiR-181a enhances drug sensitivity in mitoxantone-resistant breast cancer cells by targeting breast cancer resistance protein (BCRP/ABCG2). Breast Cancer Res Treat. 2013;139(3):717–730.
  • Cheng W, Liu T, Wan X, et al. MicroRNA-199a targets CD44 to suppress the tumorigenicity and multidrug resistance of ovarian cancer-initiating cells. Febs J. 2012;279(11):2047–2059.
  • Turrini E, Haenisch S, Laechelt S, et al. MicroRNA profiling in K-562 cells under imatinib treatment: influence of miR-212 and miR-328 on ABCG2 expression. Pharmacogenet Genomics. 2012;22(3):198–205.
  • Li WQ, Li YM, Tao BB, et al. Downregulation of ABCG2 expression in glioblastoma cancer stem cells with miRNA-328 may decrease their chemoresistance. Med Sci Monit. 2010;16(10):Hy27- Hy30.
  • To KK, Zhan Z, Litman T, et al. Regulation of ABCG2 expression at the 3ʹ 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):5147–5161.
  • To KK, Robey RW, Knutsen T, et al. Escape from hsa-miR-519c enables drug-resistant cells to maintain high expression of ABCG2. Mol Cancer Ther. 2009;8(10):2959–2968.
  • To KK, Leung WW, Ng SS. Exploiting a novel miR-519c-HuR-ABCG2 regulatory pathway to overcome chemoresistance in colorectal cancer. Exp Cell Res. 2015;338(2):222–231.
  • Takahashi K, Yan IK, Wood J, et al. Involvement of extracellular vesicle long noncoding RNA (linc-VLDLR) in tumor cell responses to chemotherapy. Mol Cancer Res. 2014;12(10):1377–1387.
  • Wijesekara N, Zhang LH, Kang MH, et al. miR-33a modulates ABCA1 expression, cholesterol accumulation, and insulin secretion in pancreatic islets. Diabetes. 2012;61(3):653–658.
  • Najafi-Shoushtari SH, Kristo F, Li Y, et al. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science. 2010;328(5985):1566–1569.
  • Borel F, Han R, Visser A, et al. Adenosine triphosphate-binding cassette transporter genes up-regulation in untreated hepatocellular carcinoma is mediated by cellular microRNAs. Hepatology. 2012;55(3):821–832.
  • Li X, Ji Z, Li S, et al. miR-146a-5p antagonized AGEs- and P.g-LPS-induced ABCA1 and ABCG1 dysregulation in macrophages via IRAK-1 downregulation. Inflammation. 2015;38(5):1761–1768.
  • Ramirez CM, Dávalos A, Goedeke L, et al. MicroRNA-758 regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Arterioscler Thromb Vasc Biol. 2011;31(11):2707–2714.
  • Jeon HM, Sohn YW, Oh SY, et al. ID4 imparts chemoresistance and cancer stemness to glioma cells by derepressing miR-9*-mediated suppression of SOX2. Cancer Res. 2011;71(9):3410–3421.
  • LaCroix B, Gamazon ER, Lenkala D, et al. Integrative analyses of genetic variation, epigenetic regulation, and the transcriptome to elucidate the biology of platinum sensitivity. BMC Genomics. 2014;15:292.
  • Nagiah S, Phulukdaree A, Chuturgoon A. Inverse association between microRNA-124a and ABCC4 in HepG2 cells treated with antiretroviral drugs. Xenobiotica. 2016;46(9):825–830.
  • Bartoszewski R, Brewer JW, Rab A, et al. The unfolded protein response (UPR)-activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J Biol Chem. 2011;286(48):41862–41870.
  • Wozniak M, Sztiller-Sikorska M, Czyz M. Diminution of miR-340-5p levels is responsible for increased expression of ABCB5 in melanoma cells under oxygen-deprived conditions. Exp Mol Pathol. 2015;99(3):707–716.
  • Yang G, Jiang O, Ling D, et al. MicroRNA-522 reverses drug resistance of doxorubicin-induced HT29 colon cancer cell by targeting ABCB5. Mol Med Rep. 2015;12(3):3930–3936.
  • Xu K, Liang X, Shen K, et al. miR-297 modulates multidrug resistance in human colorectal carcinoma by down-regulating MRP-2. Biochem J. 2012;446(2):291–300.
  • Haenisch S, Laechelt S, Bruckmueller H, et al. 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.
  • Gillen AE, Gosalia N, Leir SH, et al. MicroRNA regulation of expression of the cystic fibrosis transmembrane conductance regulator gene. Biochem J. 2011;438(1):25–32.
  • Li X, Li X, Liao D, et al. Elevated microRNA-23a expression enhances the chemoresistance of colorectal cancer cells with microsatellite instability to 5-fluorouracil by directly targeting ABCF1. Curr Protein Pept Sci. 2015;16(4):301–309.
  • Noguchi K, Katayama K, Sugimoto Y. Human ABC transporter ABCG2/BCRP expression in chemoresistance: basic and clinical perspectives for molecular cancer therapeutics. Pharmgenomics Pers Med. 2014;7:53–56.
  • Fletcher JI, Williams RT, Henderson MJ, et al. ABC transporters as mediators of drug resistance and contributors to cancer cell biology. Drug Resist Updates. 2016;26:1–9.
  • Leschziner GD, Andrew T, Pirmohamed M, et al. ABCB1 genotype and PGP expression, function and therapeutic drug response: a critical review and recommendations for future research. Pharmacogenomics J. 2007;7(3):154–179.
  • Hodges LM, Markova SM, Chinn LW, et al. Very important pharmacogene summary: ABCB1 (MDR1, P-glycoprotein). Pharmacogenet Genomics. 2011;21(3):152–161.
  • Komar AA. Silent SNPs: impact on gene function and phenotype. Pharmacogenomics. 2007;8(8):1075–1080.
  • Shabalina SA, Spiridonov NA, Kashina A. Sounds of silence: synonymous nucleotides as a key to biological regulation and complexity. Nucleic Acid Res. 2013;41(4):2073–2094.
  • Bruhn O, Cascorbi I. Polymorphisms of the drug transporters ABCB1, ABCG2, ABCC2 and ABCC3 and their impact on drug bioavailability and clinical relevance. Expert Opin Drug Metab Toxicol. 2014;10(10):1337–1354.
  • Mikeska T, Craig JM. DNA methylation biomarkers: cancer and beyond. Genes (Basel). 2014;5(3):821–864.
  • Pedersen SK, Symonds EL, Baker RT, et al. Evaluation of an assay for methylated BCAT1 and IKZF1 in plasma for detection of colorectal neoplasia. BMC Cancer. 2015;15:654.
  • Wen L, Li J, Guo H, et al. Genome-scale detection of hypermethylated CpG islands in circulating cell-free DNA of hepatocellular carcinoma patients. Cell Res. 2015 Dec;25(12):1376.
  • Mummaneni P, Shord SS. Epigenetics and oncology. Pharmacotherapy. 2014;34(5):495–505.
  • Mahon KL, Qu W, Devaney J, et al. Methylated glutathione S-transferase 1 (mGSTP1) is a potential plasma free DNA epigenetic marker of prognosis and response to chemotherapy in castrate-resistant prostate cancer. Br J Cancer. 2014;111(9):1802–1809.
  • Crea F, Di Paolo A, Liu HH, et al. Polycomb genes are associated with response to imatinib in chronic myeloid leukemia. Epigenomics. 2015;7(5):757–765.
  • Zhang L, Pan L, Xiang B, et al. Potential role of exosome-associated microRNA panels and in vivo environment to predict drug resistance for patients with multiple myeloma. Oncotarget. 2016;7(21):30876–30891.
  • O’Dwyer K, Maslak P. Azacitidine and the beginnings of therapeutic epigenetic modulation. Expert Opin Pharmacother. 2008;9(11):1981–1986.
  • Khan O, La Thangue NB. HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol. 2012;90(1):85–94.
  • Gray S. Epigenetic cancer therapy. Academic Press; 2015.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.