Pharmacoepigenetics: an element of personalized therapy?

References

• Kim IW, Han N, Burckart GJ, et al. Epigenetic changes in gene expression for drug-metabolizing enzymes and transporters. Pharmacotherapy. 2014;34:140–150.
   PubMed Web of Science ®Google Scholar
• Tollefsbol T. Epigenetics of personalised medicine. In: Tollefsbol T editors. Personalized epigenetics. London: 1st. Academic Press, 2015. p. 4–12. Print Book ISBN:9780124201354.
   Google Scholar
• Paluszczak P, Baer-Dubowska W. Epigenetic diagnostics of cancer–the application of DNA methylation markers. J Appl Genet. 2006;47:365–375.
   PubMed Web of Science ®Google Scholar
• Ivanov M, Barragan I, Ingelman-Sundberg M. Epigenetic mechanisms of importance for drug treatment. Trends Pharmacol Sci. 2014;35:384–396.
   PubMed Web of Science ®Google Scholar
• Bannister AJ1, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–395.
   PubMed Web of Science ®Google Scholar
• Iorio MV, Piovan C, Croce CM. Interplay between microRNAs and the epigenetic machinery: an intricate network. Biochim Biophys Acta. 2010;1799:694–701.
   PubMed Web of Science ®Google Scholar
• Penn NW, Suwalski R, O’Riley C, et al. The presence of 5-hydroxymethylcytosine in animal deoxyribonucleic acid. Biochem J. 1972;126:781–790.
   PubMed Web of Science ®Google Scholar
• Ivanov M, Kals M, Kacevska M, et al. Ontogeny, distribution and potential roles of 5-hydroxymethylcytosine in human liver function. Genome Biol. 2013;14:R83.
   PubMed Web of Science ®Google Scholar
• Ingelman-Sundberg M, Cascorbi I. Pharmacogenomic or -epigenomic biomarkers in drug treatment - two sides of the same medal? Clin Pharmacol Ther. 2016;99:478–480.
   PubMed Web of Science ®Google Scholar
• Heyn H, Méndez-González J, Esteller M. Epigenetic profiling joins personalized cancer medicine. Expert Rev Mol Diagn. 2013;13:473–479.
   PubMed Web of Science ®Google Scholar
• Fisel P, Schaeffeler E, Schwab M. DNA Methylation of ADME Genes. Clin Pharmacol Ther. 2016;99:512–527.
   PubMed Web of Science ®Google Scholar
• Pera B, Cerchietti L. Personalized epigenetic therapy-chemosensitivity testing. Epigenetic Cancer Therapy Gray S.G (Ed.). London: Academic Press, 2015. DOI:10.1016/B978-0-12-800206-3.00028-8
   Google Scholar
• Clark SJ, Melki J. DNA methylation and gene silencing in cancer: which is the guilty party? Oncogene. 2002;21:5380–5387.
   PubMed Web of Science ®Google Scholar
• Tang X, Chen S. Epigenetic regulation of cytochrome P450 enzymes and clinical implication. Curr Drug Metab. 2015;16:86–96.
   PubMed Web of Science ®Google Scholar
• Miyajima A, Furihata T, Chiba K. Functional analysis of GC Box and its CpG methylation in the regulation of CYP1A2 gene expression. Drug Metab Pharmacokinet. 2009;24:269–276.
   PubMed Web of Science ®Google Scholar
• Habano W, Kawamura K, Iizuka N, et al. Analysis of DNA methylation landscape reveals the roles of DNA methylation in the regulation of drug metabolizing enzymes. Clin Epigenetics. 2015;7:105.
   PubMed Web of Science ®Google Scholar
• Kacevska M, Ivanov M, Wyss A, et al. DNA methylation dynamics in the hepatic CYP3A4 gene promoter. Biochimie. 2012;94:2338–2344.
   PubMed Web of Science ®Google Scholar
• Takagi S, Nakajima M, Mohri T, et al. Post-transcriptional regulation of human pregnane X receptor by micro-RNA affects the expression ofcytochrome P450 3A4. J Biol Chem. 2008;283:9674–9680.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Zhao LJ, Xu X, et al. DNA methylation levels of CYP2R1 and CYP24A1 predict vitamin D response variation. J Steroid Biochem Mol Biol. 2014;144:207–214.
   PubMed Web of Science ®Google Scholar
• Penaloza CG1, Estevez B, Han DM, et al. Sex-dependent regulation of cytochrome P450 family members Cyp1a1, Cyp2e1, and Cyp7b1 by methylation of DNA. FASEB J. 2014;28:966–977.
   PubMed Web of Science ®Google Scholar
• Tekpli X, Zienolddiny S, Skaug V, et al. DNA methylation of the CYP1A1 enhancer is associated with smoking-induced genetic alterations in human lung. Int J Cancer. 2012;131:1509–1516.
   PubMed Web of Science ®Google Scholar
• DiNardo CD, Gharibyan V, Yang H, et al. Impact of aberrant DNA methylation patterns including CYP1B1 methylation in adolescents and young adults with acute lymphocytic leukemia. Am J Hematol. 2013;88:784–789.
   PubMed Web of Science ®Google Scholar
• Olsson M, Gustafsson O, Skogastierna C, et al. Regulation and expression of human CYP7B1 in prostate: overexpression of CYP7B1 during progression of prostatic adenocarcinoma. Prostate. 2007;67:1439–1446.
   PubMed Web of Science ®Google Scholar
• Huang YW, Jansen RA, Fabbri E, et al. Identification of candidate epigenetic biomarkers for ovarian cancer detection. Oncol Rep. 2009;22:853–861.
   PubMed Web of Science ®Google Scholar
• Gonzalgo ML, Pavlovich CP, Lee SM, et al. Prostate cancer detection by GSTP1 methylation analysis of postbiopsy urine specimens. Clin Cancer Res. 2003;9:2673–2677.
   PubMed Web of Science ®Google Scholar
• Gagnon JF, Bernard O, Villeneuve L, et al. Irinotecan inactivation is modulated by epigenetic silencing of UGT1A1 in colon cancer. Clin Cancer Res. 2006;12:1850–1858.
   PubMed Web of Science ®Google Scholar
• Kwon MS, Kim SJ, Lee SY, et al. Epigenetic silencing of the sulfotransferase 1A1 gene by hypermethylation in breast tissue. Oncol Rep. 2006;15:27–32.
   PubMed Web of Science ®Google Scholar
• Kim SJ, Kang HS, Jung SY, et al. Methylation patterns of genes coding for drug-metabolizing enzymes in tamoxifen-resistant breast cancer tissues. J Mol Med. 2010;88:1123–1131.
   PubMed Web of Science ®Google Scholar
• Baer-Dubowska W, Majchrzak-Celińska A, Cichocki M. Pharmocoepigenetics: a new approach to predicting individual drug responses and targeting new drugs. Pharmacol Rep. 2011;63:293–304.
   PubMed Web of Science ®Google Scholar
• Ramamoorthy A, Skaar TC. In silico identification of microRNAs predicted to regulate the drug metabolizing cytochrome P450 genes. Drug Metab Lett. 2011;5:126–131.
   PubMedGoogle Scholar
• Tsuchiya Y, Nakajima M, Takagi S, et al. MicroRNA regulates the expression of human cytochrome P450 1B1. Cancer Res. 2006;66:9090–9098.
   PubMed Web of Science ®Google Scholar
• Wei Z, Jiang S, Zhang Y, et al. The effect of microRNAs in the regulation of human CYP3A4: a systematic study using a mathematical model. Sci Rep. 2014;4:4283.
   PubMed Web of Science ®Google Scholar
• Zhang SY, Surapureddi S, Coulter S, et al. Human CYP2C8 is post-transcriptionally regulated by microRNAs 103 and 107 in human liver. Mol Pharmacol. 2012;82:529–540.
   PubMed Web of Science ®Google Scholar
• Rieger JK, Klein K, Winter S, et al. Expression variability of absorption, distribution, metabolism, excretion-related microRNAs in human liver: influence of nongenetic factors and association with gene expression. Drug Metab Dispos. 2013;41:1752–1762.
   PubMed Web of Science ®Google Scholar
• Kantharidis P, El-Osta A, deSilva M, et al. Altered methylation of the human MDR1 promoter is associated with acquired multidrug resistance. Clin Cancer Res. 1997;3:2025–2032.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ye P, Xing H, Lou F, et al. Histone deacetylase 2 regulates doxorubicin (Dox) sensitivity of colorectal cancer cells by targeting ABCB1 transcription. Cancer Chemother Pharmacol. 2016;77:613–621.
   PubMed Web of Science ®Google Scholar
• Baker EK, Johnstone RW, Zalcberg JR, et al. Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene. 2005;24:8061–8075.
   PubMed Web of Science ®Google Scholar
• Bram EE, Stark M, Raz S, et al. Chemotherapeutic drug-induced ABCG2 promoter demethylation as a novel mechanism of acquired multidrug resistance. Neoplasia. 2009;11:1359–1370.
   PubMed Web of Science ®Google Scholar
• 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;76:582–588.
   PubMed Web of Science ®Google Scholar
• 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;41:1744–1751.
   PubMed Web of Science ®Google Scholar
• Park JY, Helm JF, Zheng W, et al. Silencing of the candidate tumor suppressor gene solute carrier family 5 member 8 (SLC5A8) in human pancreatic cancer. Pancreas. 2008;36:e32–9.
   PubMed Web of Science ®Google Scholar
• Lin R, Li X, Li J, et al. Long-term cisplatin exposure promotes methylation of the OCT1 gene in human esophageal cancer cells. Dig Dis Sci. 2013;58:694–698.
   PubMed Web of Science ®Google Scholar
• Schaeffeler E, Hellerbrand C, Nies AT, et al. DNA methylation is associated with downregulation of the organic cation transporter OCT1 (SLC22A1) in human hepatocellular carcinoma. Genome Med. 2011;3:82.
   PubMed Web of Science ®Google Scholar
• Svoboda M, Riha J, Wlcek K, et al. Organic anion transporting polypeptides (OATPs): regulation of expression and function. Curr Drug Metab. 2011;12:139–153.
   PubMed Web of Science ®Google Scholar
• Rawłuszko-Wieczorek AA, Horst N, Horbacka K, et al. Effect of DNA methylation profile on OATP3A1 and OATP4A1 transcript levels in colorectal cancer. Biomed Pharmacother. 2015;74:233–242.
   PubMed Web of Science ®Google Scholar
• Ichihara S, Kikuchi R, Kusuhara H, et al. DNA methylation profiles of organic anion transporting polypeptide 1B3 in cancer cell lines. Pharm Res. 2010;27:510–516.
   PubMed Web of Science ®Google Scholar
• Dalmasso G, Nguyen HT, Yan Y, et al. MicroRNA-92b regulates expression of the oligopeptide transporter PepT1 in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2011;300:G52–9.
   PubMed Web of Science ®Google Scholar
• Li KK, Pang JC, Ching AK, et al. miR-124 is frequently down-regulated in medulloblastoma and is a negative regulator of SLC16A1. Hum Pathol. 2009;40:1234–1243.
   PubMed Web of Science ®Google Scholar
• Huang Z, Zhang S, Shen Y, et al. Influence of MDR1 methylation on the curative effect of interventional embolism chemotherapy for cervical cancer. Ther Clin Risk Manag. 2016;12:217–223.
   PubMed Web of Science ®Google Scholar
• 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;119:125–130.
   PubMed Web of Science ®Google Scholar
• 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;8:80.
   PubMed Web of Science ®Google Scholar
• Wu DD, Li XS, Meng XN, et al. MicroRNA-873 mediates multidrug resistance in ovarian cancer cells by targeting ABCB1. Tumour Biol. 2016 [cited Feb 5]. DOI: 10.1007/s13277-016-4944-y
   Web of Science ®Google Scholar
• Shang Y, Zhang Z, Liu Z, et al. miR-508-5p regulates multidrug resistance of gastric cancer by targeting ABCB1 and ZNRD1. Oncogene. 2014;33:3267–3276.
   PubMed Web of Science ®Google Scholar
• 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;96:240–247.
   PubMed Web of Science ®Google Scholar
• 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;80:314–320.
   PubMed Web of Science ®Google Scholar
• Moon HH, Kim SH, Ku JL. 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;35:298–306.
   PubMed Web of Science ®Google Scholar
• 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;6:151–164.
   PubMed Web of Science ®Google Scholar
• 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;75:1374–1379.
   PubMed Web of Science ®Google Scholar
• Dai X, Chen X, Chen Q, et al. MicroRNA-193a-3p reduces intestinal inflammation in response to microbiota via down-regulation of colonic pepT1. J Biol Chem. 2015;290:16099–16115.
   PubMed Web of Science ®Google Scholar
• Ikehata M, Ueda K, Iwakawa S. Different involvement of DNA methylation and histone deacetylation in the expression of solute-carrier transporters in 4 colon cancer cell lines. Biol Pharm Bull. 2012;35:301–307.
   PubMed Web of Science ®Google Scholar
• Jiang Q, Yuan H, Xing X, et al. Methylation of adrenergic β1 receptor is a potential epigenetic mechanism controlling antihypertensive response to metoprolol. Indian J Biochem Biophys. 2011;48:301–307.
   PubMed Web of Science ®Google Scholar
• Liu H, Xing X, Huang L, et al. The expression level of myocardial β1-adrenergic receptor affects metoprolol antihypertensive effects: a novel mechanism for interindividual difference. Med Hypotheses. 2013;81:71–72.
   PubMed Web of Science ®Google Scholar
• Rivière G, Lienhard D, Andrieu T, et al. Epigenetic regulation of somatic angiotensin-converting enzyme by DNA methylation and histone acetylation. Epigenetics. 2011;6:478–489.
   PubMed Web of Science ®Google Scholar
• Benevolenskaya EV, Islam AB, Ahsan H3, et al. DNA methylation and hormone receptor status in breast cancer. Clin Epigenetics. 2016;8:17.
   PubMed Web of Science ®Google Scholar
• Ye XM, Zhu HY, Bai WD, et al. Epigenetic silencing of miR-375 induces trastuzumab resistance in HER2-positive breast cancer by targeting IGF1R. BMC Cancer. 2014;14:134.
   PubMed Web of Science ®Google Scholar
• Kim JY, Hwang J, Lee SH, et al. Decreased efficacy of drugs targeting the vascular endothelial growth factor pathway by the epigenetic silencing of FLT1 in renal cancer cells. Clin Epigenetics. 2015;7:99.
   PubMed Web of Science ®Google Scholar
• Esteller M, Garcia-Foncillas J, Andion E, et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med. 2000;343:1350–1354.
   PubMed Web of Science ®Google Scholar
• Wirsching HG, Galanis E, Weller M. Glioblastoma. Handb Clin Neurol. 2016;134:381–397.
   PubMedGoogle Scholar
• Esteller M, Hamilton SR, Burger PC, et al. Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res. 1999;59:793–797.
   PubMed Web of Science ®Google Scholar
• Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet. 2012;13:679–692.
   PubMed Web of Science ®Google Scholar
• Fornaro L, Vivaldi C, Caparello C, et al. Pharmacoepigenetics in gastrointestinal tumors: MGMT methylation and beyond. Front Biosci (Elite Ed). 2016;8:170–180.
   PubMedGoogle Scholar
• Zeller C, Dai W, Steele NL, et al. Candidate DNA methylation drivers of acquired cisplatin resistance in ovarian cancer identified by methylome and expression profiling. Oncogene. 2012;31:4567–4576.
   PubMed Web of Science ®Google Scholar
• Chen HY, Shao CJ, Chen FR, et al. Role of ERCC1 promoter hypermethylation in drug resistance to cisplatin in human gliomas. Int J Cancer. 2010;126:1944–1954.
   PubMed Web of Science ®Google Scholar
• Shen L, Kondo Y, Ahmed S, et al. Drug sensitivity prediction by CpG island methylation profile in the NCI-60 cancer cell line panel. Cancer Res. 2007;67:11335–11343.
   PubMed Web of Science ®Google Scholar
• Soengas MS, Capodieci P, Polsky D, et al. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature. 2001;409:207–211.
   PubMed Web of Science ®Google Scholar
• Dejeux E, Rønneberg JA, Solvang H, et al. DNA methylation profiling in doxorubicin treated primary locally advanced breast tumours identifies novel genes associated with survival and treatment response. Mol Cancer. 2010;9:68.
   PubMed Web of Science ®Google Scholar
• Chen B, Rao X, House MG, et al. GPx3 promoter hypermethylation is a frequent event in human cancer and is associated with tumorigenesis and chemotherapy response. Cancer Lett. 2011;309:37–45.
   PubMed Web of Science ®Google Scholar
• Iorns E, Turner NC, Elliott R, et al. Identification of CDK10 as an important determinant of resistance to endocrine therapy for breast cancer. Cancer Cell. 2008;13:91–104.
   PubMed Web of Science ®Google Scholar
• Maier S, Nimmrich I, Koenig T, et al. DNA-methylation of the homeodomain transcription factor PITX2 reliably predicts risk of distant disease recurrence in tamoxifen-treated, node-negative breast cancer patients–Technical and clinical validation in a multi-centre setting in collaboration with the European Organisation for Research and Treatment of Cancer (EORTC) pathobiology group. Eur J Cancer. 2007;43:1679–1686.
   PubMed Web of Science ®Google Scholar
• Zhu J, Wang Y, Duan J, et al. DNA Methylation status of Wnt antagonist SFRP5 can predict the response to the EGFR-tyrosine kinase inhibitor therapy in non-small cell lung cancer. J Exp Clin Cancer Res. 2012;31:80.
   PubMed Web of Science ®Google Scholar
• Salazar F, Molina MA, Sanchez-Ronco M, et al. First-line therapy and methylation status of CHFR in serum influence outcome to chemotherapy versus EGFR tyrosine kinase inhibitors as second-line therapy in stage IV non-small-cell lung cancer patients. Lung Cancer. 2011;72:84–91.
   PubMed Web of Science ®Google Scholar
• Hughes LA, Melotte V, de Schrijver J, et al. The CpG island methylator phenotype: what’s in a name? Cancer Res. 2013 Oct 1;73(19):5858–5868.
   PubMed Web of Science ®Google Scholar
• Noushmehr H, Weisenberger DJ, Diefes K, et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell. 2010;17:510–522.
   PubMed Web of Science ®Google Scholar
• Fang F, Turcan S, Rimner A, et al. Breast cancer methylomes establish an epigenomic foundation for metastasis. Sci Transl Med. 2011;3:75ra25.
   PubMed Web of Science ®Google Scholar
• Majchrzak-Celińska A, Paluszczak J, Kleszcz R, et al. Detection of MGMT, RASSF1A, p15INK4B, and p14ARF promoter methylation in circulating tumor-derived DNA of central nervous system cancer patients. J Appl Genet. 2013;54:335–344.
   PubMed Web of Science ®Google Scholar
• Bertoli G, Cava C, Castiglioni I. MicroRNAs as biomarkers for diagnosis, prognosis and theranostics in prostate cancer. Int J Mol Sci. 2016;17:pii: E421. DOI:10.3390/ijms17030421
   PubMed Web of Science ®Google Scholar
• Peedicayil J. Pharmacoepigenetics and pharmacoepigenomics. Pharmacogenomics. 2008;9:1785–1786.
   PubMed Web of Science ®Google Scholar
• Roboz GJ. Epigenetic targeting and personalized approaches for AML. Hematology Am Soc Hematol Educ Program. 2014;2014:44–51.
   PubMedGoogle Scholar
• Babu E, Ramachandran S, CoothanKandaswamy V, et al. Role of SLC5A8, a plasma membrane transporter and a tumor suppressor, in the antitumor activity of dichloroacetate. Oncogene. 2011;30:4026–4037.
   PubMed Web of Science ®Google Scholar
• Mottamal M, Zheng S, Huang TL, et al. Histone deacetylase inhibitors in clinical studies as templates for new anticancer agents. Molecules. 2015;20:3898–3941.
   PubMed Web of Science ®Google Scholar
• West AC, Johnstone RW. New and emerging HDAC inhibitors for cancer treatment. J Clin Invest. 2014;124:30–39.
   PubMed Web of Science ®Google Scholar
• Malmquist NA, Moss TA, Mecheri S, et al. Small-molecule histone methyltransferase inhibitors display rapid antimalarial activity against all blood stage forms in Plasmodium falciparum. Proc Natl Acad Sci U S A. 2012;109:16708–16713.
   PubMed Web of Science ®Google Scholar
• Salarinia R, Sahebkar A, Mirzaei HR, et al. Epi-drugs and Epi-miRs: moving beyond current cancer therapies. Curr Cancer Drug Targets. 2016;16:773–788.
   PubMed Web of Science ®Google Scholar
• Zhao J, Tao Y, Zhou Y, et al. MicroRNA-7: a promising new target in cancer therapy. Cancer Cell Int. 2015;15:103.
   PubMed Web of Science ®Google Scholar
• Nadim WD, Simion V, Bénédetti H, et al. MicroRNAs in neurocognitive dysfunctions: new molecular targets for pharmacological treatments? Curr Neuropharmacol. 2016. [cited July 8];PMID: 27396304.[Epub ahead of print].
   Google Scholar
• Broderick JA, Zamore PD. MicroRNA therapeutics. Gene Ther. 2011;18:1104–1110.
   PubMed Web of Science ®Google Scholar
• Turcan S, Rohle D, Goenka A, et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature. 2012;483(7390):479–483.
   PubMed Web of Science ®Google Scholar
• Ivanov M, Kals M, Kacevska M, et al. In-solution hybrid capture of bisulfite-converted DNA for targeted bisulfite sequencing of 174 ADME genes. Nucleic Acids Res. 2013;41:e72. DOI:10.1093/nar/gks1467
   PubMed Web of Science ®Google Scholar
• Smith N, Nucera C. Personalized therapy in patients with anaplastic thyroid cancer: targeting genetic and epigenetic alterations. J Clin Endocrinol Metab. 2015;100:35–42.
   PubMed Web of Science ®Google Scholar