DNA methylation of ADME genes

Clinical Pharmacology and Therapeutics

Volumn 99, Issue 5, 2016, Pages 512-527

  Fisel, P ^a,b   Schaeffeler, E ^a,b   Schwab, M ^a,b,c  

^a DR MARGARETE FISCHER BOSCH INSTITUTE OF CLINICAL PHARMACOLOGY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER G1; ACYLTRANSFERASE; ARYLDIALKYLPHOSPHATASE 1; BREAST CANCER RESISTANCE PROTEIN; CONCENTRATIVE NUCLEOSIDE TRANSPORTER 1; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; CYTOCHROME P450 2C19; CYTOCHROME P450 2D6; CYTOCHROME P450 2E1; CYTOCHROME P450 3A4; DNA; GLUCURONOSYLTRANSFERASE 1A1; GLUTATHIONE PEROXIDASE 3; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE A4; GLUTATHIONE TRANSFERASE M5; GLUTATHIONE TRANSFERASE P1; GLUTATHIONE TRANSFERASE T1; MONOCARBOXYLATE TRANSPORTER 4; MULTIDRUG RESISTANCE PROTEIN 1; ORGANIC CATION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 2; ORGANIC CATION TRANSPORTER 3; PREGNANE X RECEPTOR; REDUCED FOLATE CARRIER; SEROTONIN TRANSPORTER; SULFOTRANSFERASE 1A1; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR; DRUG; HISTONE; MICRORNA;

5' UNTRANSLATED REGION; ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; BLADDER CANCER; BREAST CANCER; CANCER RESISTANCE; CANCER SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; COLON CANCER; COLORECTAL CANCER; CPG ISLAND; DEPRESSION; DNA METHYLATION; DRUG ABSORPTION; DRUG DISTRIBUTION; DRUG EXCRETION; DRUG METABOLISM; DRUG RESPONSE; DRUG UPTAKE; ENDOMETRIUM CANCER; ENHANCER REGION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; HUMAN; INSULIN RESISTANCE; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; MENTAL DISEASE; METABOLIC DISORDER; PERSONALIZED MEDICINE; PHARMACOGENETICS; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; REVIEW; TRANSCRIPTION INITIATION SITE; ADVERSE DRUG REACTION; ANIMAL; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHARMACOKINETICS;

ANIMALS; DNA METHYLATION; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONES; HUMANS; MICRORNAS; PHARMACEUTICAL PREPARATIONS; PHARMACOKINETICS; PRECISION MEDICINE;

EID: 84975709046     PISSN: 00099236     EISSN: 15326535     Source Type: Journal    
DOI: 10.1002/cpt.343     Document Type: Review

References (75)

1. Meyer U.A., Zanger U.M., & Schwab M. Omics and drug response. Annu. Rev. Pharmacol. Toxicol. 53, 475-502 (2013).
2. Ehmann F., et al. Pharmacogenomic information in drug labels: European Medicines Agency perspective. Pharmacogenomics J. 15(3), 201-210 (2015).
3. Holliday R. Epigenetics: a historical overview. Epigenetics 1(2), 76-80 (2006).
4. Goldberg A.D., Allis C.D., & Bernstein E. Epigenetics: a landscape takes shape. Cell 128(4), 635-638 (2007).
5. Jones P.A., & Baylin S.B. The epigenomics of cancer. Cell 128(4), 683-692 (2007).
6. Kacevska M., Ivanov M., & Ingelman-Sundberg M. Perspectives on epigenetics and its relevance to adverse drug reactions. Clin. Pharmacol. Ther. 89(6), 902-907 (2011).
7. Kacevska M., Ivanov M., & Ingelman-Sundberg M. Epigeneticdependent regulation of drug transport and metabolism: an update. Pharmacogenomics 13(12), 1373-1385 (2012).
8. Feinberg A.P. Phenotypic plasticity and the epigenetics of human disease. Nature 447(7143), 433-440 (2007).
9. Szyf M. Nongenetic inheritance and transgenerational epigenetics. Trends Mol. Med. 21(2), 134-144 (2015).
10. Fraga M.F., et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. U. S. A. 102(30), 10604-10609 (2005).
11. Talens R.P., et al. Epigenetic variation during the adult lifespan: cross-sectional and longitudinal data on monozygotic twin pairs. Aging Cell. 11(4), 694-703 (2012).
12. Stevens J.C., et al. Developmental expression of the major human hepatic CYP3A enzymes. J. Pharmacol. Exp. Ther. 307(2), 573-582 (2003).
13. Brouwer K.L., et al. Human ontogeny of drug transporters: review and recommendations of the Pediatric Transporter Working Group. Clin. Pharmacol. Ther. 98(3), 266-287 (2015).
14. Mooij M.G., et al. Development of human membrane transporters: drug disposition and pharmacogenetics. Clin. Pharmacokinet. (2015); e-pub ahead of print.
15. Bonder M.J., et al. Genetic and epigenetic regulation of gene expression in fetal and adult human livers. BMC Genomics 15, 860 (2014).
16. Seripa D., Panza F., Daragjati J., Paroni G., & Pilotto A. Measuring pharmacogenetics in special groups: geriatrics. Expert Opin. Drug Metab. Toxicol. 11(7), 1073-1088 (2015).
17. Branco M.R., Ficz G., & Reik W. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet. 13(1), 7-13 (2012).
18. Li W., & Liu M. Distribution of 5-hydroxymethylcytosine in different human tissues. J. Nucleic Acids 2011, 870726 (2011).
19. Ivanov M., et al. Ontogeny, distribution and potential roles of 5-hydroxymethylcytosine in human liver function. Genome Biol. 14(8), R83 (2013).
20. Xiong J., et al. DNA hydroxymethylation age of human blood determined by capillary hydrophilic-interaction liquid chromatography/ mass spectrometry. Clin. Epigenetics 7(1), 72 (2015).
21. Song C.X., Yi C., & He C. Mapping recently identified nucleotide variants in the genome and transcriptome. Nat. Biotechnol. 30(11), 1107-1116 (2012).
22. Zanger U.M., & Schwab M. Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol. Ther. 138(1), 103-141 (2013).
23. Habano W., et al Involvement of promoter methylation in the regulation of Pregnane X receptor in colon cancer cells BMC Cancer 11 81 2011).
24. Kacevska M., et al. DNA methylation dynamics in the hepatic CYP3A4 gene promoter. Biochimie. 94(11), 2338-2344 (2012).
25. Okino S.T., et al. Epigenetic inactivation of the dioxin-responsive cytochrome P4501A1 gene in human prostate cancer. Cancer Res. 66(15), 7420-7428 (2006).
26. Anttila S., et al. Methylation of cytochrome P4501A1 promoter in the lung is associated with tobacco smoking. Cancer Res. 63(24), 8623-8628 (2003).
27. Tekpli X., Zienolddiny S., Skaug V., Stangeland L., Haugen A., & Mollerup S. DNA methylation of the CYP1A1 enhancer is associated with smoking-induced genetic alterations in human lung. Int. J. Cancer 131(7), 1509-1516 (2012).
28. He L., et al. Involvement of cytochrome P450 1A1 and glutathione S-Transferase P1 polymorphisms and promoter hypermethylation in the progression of anti-Tuberculosis drug-induced liver injury: a casecontrol study. PLoS One 10(3), e0119481 (2015).
29. Tokizane T., et al. Cytochrome P450 1B1 is overexpressed and regulated by hypomethylation in prostate cancer. Clin. Cancer Res. 11(16), 5793-5801 (2005).
30. Widschwendter M., et al. Association of breast cancer DNA methylation profiles with hormone receptor status and response to tamoxifen. Cancer Res. 64(11), 3807-3813 (2004).
31. DiNardo C.D., et al. Impact of aberrant DNA methylation patterns including CYP1B1 methylation in adolescents and young adults with acute lymphocytic leukemia. Am. J. Hematol. 88(9), 784-789 (2013).
32. Jones S.M., Boobis A.R., Moore G.E., & Stanier P.M. Expression of CYP2E1 during human fetal development: methylation of the CYP2E1 gene in human fetal and adult liver samples. Biochem. Pharmacol. 43(8), 1876-1879 (1992).
33. Vieira I., Sonnier M., & Cresteil T. Developmental expression of CYP2E1 in the human liver. Hypermethylation control of gene expression during the neonatal period. Eur. J. Biochem. 238(2), 476-483 (1996).
34. Kaut O., Schmitt I., & Wullner U. Genome-scale methylation analysis of Parkinson?s disease patients? brains reveals DNA hypomethylation and increased mRNA expression of cytochrome P450 2E1. Neurogenetics 13(1), 87-91 (2012).
35. Stenstedt K., Hallstrom M., Johansson I., Ingelman-Sundberg M., Ragnhammar P., & Edler D. The expression of CYP2W1: a prognostic marker in colon cancer. Anticancer Res. 32(9), 3869-3874 (2012).
36. Travica S., et al. Colon cancer-specific cytochrome P450 2W1 converts duocarmycin analogues into potent tumor cytotoxins. Clin. Cancer Res. 19(11), 2952-2961 (2013).
37. Gomez A., Karlgren M., Edler D., Bernal M.L., Mkrtchian S., & Ingelman-Sundberg M. Expression of CYP2W1 in colon tumors: regulation by gene methylation. Pharmacogenomics 8(10), 1315-1325 (2007).
38. Choong E., et al. Developmental regulation and induction of cytochrome P450 2W1, an enzyme expressed in colon tumors. PLoS One 10(4), e0122820 (2015).
39. Chen B., Rao X., House M.G., Nephew K.P., Cullen K.J., & Guo Z. GPx3 promoter hypermethylation is a frequent event in human cancer and is associated with tumorigenesis and chemotherapy response. Cancer Lett. 309(1), 37-45 (2011).
40. Gagnon J.F., Bernard O., Villeneuve L., Tetu B., & Guillemette C. Irinotecan inactivation is modulated by epigenetic silencing of UGT1A1 in colon cancer. Clin. Cancer Res. 12(6), 1850-1858 (2006).
41. Oda S., Fukami T., Yokoi T., & Nakajima M. Epigenetic regulation is a crucial factor in the repression of UGT1A1 expression in the human kidney. Drug Metab. Dispos. 41(10), 1738-1743 (2013).
42. Bieche I., Girault I., Urbain E., Tozlu S., & Lidereau R. Relationship between intratumoral expression of genes coding for xenobioticmetabolizing enzymes and benefit from adjuvant tamoxifen in estrogen receptor alpha-positive postmenopausal breast carcinoma. Breast Cancer Res. 6(3), R252-R263 (2004).
43. Kim S.J., et al. Methylation patterns of genes coding for drugmetabolizing enzymes in tamoxifen-resistant breast cancer tissues. J. Mol. Med. (Berl). 88(11), 1123-1131 (2010).
44. Kim S.J., et al. Promoter hypomethylation of the N-Acetyltransferase 1 gene in breast cancer. Oncol. Rep. 19(3), 663-668 (2008).
45. Habano W., Kawamura K., Iizuka N., Terashima J., Sugai T., & Ozawa S. Analysis of DNA methylation landscape reveals the roles of DNA methylation in the regulation of drug metabolizing enzymes. Clin. Epigenetics 7, 105 (2015).
46. Petersen A.K., et al. Epigenetics meets metabolomics: an epigenome-wide association study with blood serum metabolic traits. Hum. Mol. Genet. 23(2), 534-545 (2014).
47. How K.A., Nielsen H.M., & Tost J. DNA methylation based biomarkers: practical considerations and applications. Biochimie. 94(11), 2314-2337 (2012).
48. Comerford K.M., Wallace T.J., Karhausen J., Louis N.A., Montalto M.C., & Colgan S.P. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 62(12), 3387-3394 (2002).
49. Baker E.K., & El-Osta A. MDR1, chemotherapy and chromatin remodeling. Cancer Biol. Ther. 3(9), 819-824 (2004).
50. Dejeux E., et al. DNA methylation profiling in doxorubicin treated primary locally advanced breast tumours identifies novel genes associated with survival and treatment response. Mol. Cancer 9, 68 (2010).
51. Bram E.E., Stark M., Raz S., & Assaraf Y.G. Chemotherapeutic drug-induced ABCG2 promoter demethylation as a novel mechanism of acquired multidrug resistance. Neoplasia. 11(12), 1359-1370 (2009).
52. Worm J., Kirkin A.F., Dzhandzhugazyan K.N., & Guldberg P. Methylation-dependent silencing of the reduced folate carrier gene in inherently methotrexate-resistant human breast cancer cells. J. Biol. Chem. 276(43), 39990-40000 (2001).
53. Ferreri A.J., et al. Aberrant methylation in the promoter region of the reduced folate carrier gene is a potential mechanism of resistance to methotrexate in primary central nervous system lymphomas. Br. J. Haematol. 126(5), 657-664 (2004).
54. Nies A.T., Koepsell H., Damme K., & Schwab M. Organic cation transporters (OCTs, MATEs), in vitro and in vivo evidence for the importance in drug therapy. Handb. Exp. Pharmacol. 201 105-167 2011).
55. Nies A.T., et al. Expression of organic cation transporters OCT1 (SLC22A1) and OCT3 (SLC22A3) is affected by genetic factors and cholestasis in human liver. Hepatology 50(4), 1227-1240 (2009).
56. Aoki M., et al. Kidney-specific expression of human organic cation transporter 2 OCT2/SLC22A2) is regulated by DNA methylation. Am. J. Physiol. Renal Physiol. 295(1), F165-F170 (2008).
57. Schaeffeler E., et al. DNA methylation is associated with downregulation of the organic cation transporter OCT1 (SLC22A1) in human hepatocellular carcinoma. Genome Med. 3(12), 82 (2011).
58. Lin R., et al. Long-Term cisplatin exposure promotes methylation of the OCT1 gene in human esophageal cancer cells. Dig. Dis. Sci. 58(3), 694-698 (2013).
59. Chen L., et al. Genetic and epigenetic regulation of the organic cation transporter 3, SLC22A3. Pharmacogenomics J. 13(2), 110-120 (2013).
60. Fisel P., et al. DNA methylation of the SLC16A3 promoter regulates expression of the human lactate transporter MCT4 in renal cancer with consequences for clinical outcome. Clin. Cancer Res. 19(18), 5170-5181 (2013).
61. Fisel P., et al. MCT4 surpasses the prognostic relevance of the ancillary protein CD147 in clear cell renal cell carcinoma. Oncotarget. 6(31), 30615-30627 (2015).
62. Misawa A., et al. Methylation-Associated silencing of the nuclear receptor 1I2 gene in advanced-Type neuroblastomas, identified by bacterial artificial chromosome array-based methylated CpG island amplification. Cancer Res. 65(22), 10233-10242 (2005).
63. Pancione M., et al. Epigenetic silencing of peroxisome proliferatoractivated receptor gamma is a biomarker for colorectal cancer progression and adverse patients? outcome. PLoS One 5(12), e14229 (2010).
64. Marik R., et al. DNA methylation-related vitamin D receptor insensitivity in breast cancer. Cancer Biol. Ther. 10(1), 44-53 (2010).
65. Varley K.E., et al. Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res. 23(3), 555-567 (2013).
66. Zhao J., Goldberg J., Bremner J.D., & Vaccarino V. Association between promoter methylation of serotonin transporter gene and depressive symptoms: a monozygotic twin study. Psychosom. Med. 75(6), 523-529 (2013).
67. Domschke K., et al. Serotonin transporter gene hypomethylation predicts impaired antidepressant treatment response. Int. J. Neuropsychopharmacol. 17(8), 1167-1176 (2014).
68. Hidalgo B., et al. Epigenome-wide association study of fasting measures of glucose, insulin, and HOMA-IR in the Genetics of Lipid Lowering Drugs and Diet Network study. Diabetes 63(2), 801-807 (2014).
69. Ivanov M., Kals M., Kacevska M., Metspalu A., Ingelman-Sundberg M., & Milani L. In-solution hybrid capture of bisulfiteconverted DNA for targeted bisulfite sequencing of 174 ADME genes. Nucleic Acids Res. 41(6), e72 (2013).
70. Li X.Y., et al. Blockade of DNA methylation enhances the therapeutic effect of gefitinib in non-small cell lung cancer cells. Oncol. Rep. 29(5), 1975-1982 (2013).
71. Rius M., et al. Human concentrative nucleoside transporter 1-mediated uptake of 5-Azacytidine enhances DNA demethylation. Mol. Cancer Ther. 8(1), 225-231 (2009).
72. Cox D.B., Platt R.J., & Zhang F. Therapeutic genome editing: prospects and challenges. Nat. Med. 21(2), 121-131 (2015).
73. Ivanov M., & Barragan I., Ingelman-Sundberg M. Epigenetic mechanisms of importance for drug treatment. Trends Pharmacol. Sci. 35(8), 384-396 (2014).
74. Malumbres M. miRNAs and cancer: an epigenetics view. Mol. Aspects Med. 34(4), 863-874 (2013).
75. Fisel P., Renner O., Nies A.T., Schwab M., & Schaeffeler E. Solute carrier transporter and drug-related nephrotoxicity: the impact of proximal tubule cell models for preclinical research. Expert Opin. Drug Metab. Toxicol. 10(3), 395-408 (2014).