Epigenetic changes in gene expression for drug-metabolizing enzymes and transporters

Pharmacotherapy

Volumn 34, Issue 2, 2014, Pages 140-150

  Kim, In Wha ^a   Han, Nayoung ^a   Burckart, Gilbert J ^b   Oh, Jung Mi ^a  

^a Seoul National University   (South Korea)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

DNA methylation; Drug metabolism; Histone modification; Personalized medicine; Pharmacoepigenetics

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; AZACITIDINE; CARRIER PROTEIN; CELL NUCLEUS RECEPTOR; CYTOCHROME P450; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; CYTOCHROME P450 24A1; CYTOCHROME P450 2A13; CYTOCHROME P450 2E1; CYTOCHROME P450 2W1; CYTOCHROME P450 3A; DRUG METABOLIZING ENZYME; DRUG TRANSPORTER PROTEIN; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; ISONIAZID; MESSENGER RNA; MICRORNA; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 8; MULTIDRUG RESISTANCE PROTEIN 1; N PHTHALOYLTRYPTOPHAN; ORGANIC ANION TRANSPORTER 3; REDUCED FOLATE CARRIER; ROMIDEPSIN; TAMOXIFEN; THEOPHYLLINE; TRICHOSTATIN A; UNCLASSIFIED DRUG; UNINDEXED DRUG; VORINOSTAT; DRUG; HISTONE;

ABCB1 GENE; ABCC1 GENE; ABCC11 GENE; ARTICLE; CANCER CELL CULTURE; CYP1A1 GENE; CYP1B1 GENE; CYP24A1 GENE; CYP2A13 GENE; CYP2E1 GENE; CYP2W1 GENE; CYP3A GENE; DNA METHYLATION; DNA SEQUENCE; DRUG ABSORPTION; DRUG DISPOSITION; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG ELIMINATION; DRUG METABOLISM; EPIGENETICS; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; PERSONALIZED MEDICINE; PHARMACOGENETICS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SLC19A1 GENE; SLC22A8 GENE; SLC29A1 GENE; ANIMAL; DRUG DESIGN; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PROCEDURES; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CYTOCHROME P-450 ENZYME SYSTEM; DNA METHYLATION; DRUG DESIGN; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONES; HUMANS; INDIVIDUALIZED MEDICINE; PHARMACEUTICAL PREPARATIONS; PHARMACOGENETICS;

EID: 84898051723     PISSN: 02770008     EISSN: None     Source Type: Journal    
DOI: 10.1002/phar.1362     Document Type: Article

References (79)

1. President's Council of Advisors on Science and Technology. Priorities for personalized medicine. September 2008. Available from http://www.ostp.gov/ galleries/PCAST/pcast-report-v2.pdf. Accessed June 19, 2009.
2. 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: 496-526.
3. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33(Suppl): 245-54.
4. Richards EJ. Inherited epigenetic variation-revisiting soft inheritance. Nat Rev Genet 2006;7: 395-401.
5. Ivanov M, Kacevska M, Ingelman-Sundberg M. Epigenomics and interindividual differences in drug response. Clin Pharmacol Ther 2012;92: 727-36.
6. Peedicayil J. Epigenetic therapy - a new development in pharmacology. Indian J Med Res 2006;123: 17-24.
7. Szyf M. Toward a Discipline of Pharmacoepigenomics. Curr Pharmacogenomics 2004;2: 357-77.
8. Jones SM, Boobis AR, Moore GE, Stanier PM. Expression of CYP2E1 during human fetal development: methylation of the CYP2E1 gene in human fetal and adult liver samples. Biochem Pharmacol 1992;43: 1876-9.
9. Duarte JD. Epigenetics primer: why the clinician should care about epigenetics. Pharmacotherapy 2013;Jul 17 [Epub ahead of print]. doi: 10.1002/phar.1325.
10. Desiderato L, Davey MW, Piper AA. Demethylation of the human MDR1 5' region accompanies activation of P-glycoprotein expression in a HL60 multidrug resistant subline. Somat Cell Mol Genet 1997;23: 391-400.
11. El-Osta A, Kantharidis P, Zalcberg JR, Wolffe AP. 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: 1844-57.
12. 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: 2025-32.
13. Kusaba H, Nakayama M, Harada T, et al. Association of 5' CpG demethylation and altered chromatin structure in the promoter region with transcriptional activation of the multidrug resistance 1 gene in human cancer cells. Eur J Biochem 1999;262: 924-32.
14. Nakayama M, Wada M, Harada T, et al. Hypomethylation status of CpG sites at the promoter region and overexpression of the human MDR1 gene in acute myeloid leukemias. Blood 1998;92: 4296-307.
15. Toyota M, Kopecky KJ, Toyota MO, Jair KW, Willman CL, Issa JP. Methylation profiling in acute myeloid leukemia. Blood 2001;97: 2823-9.
16. 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: 2217-24.
17. Shannon BA, Iacopetta BJ. Methylation of the hMLH1, p16, and MDR1 genes in colorectal carcinoma: associations with clinicopathological features. Cancer Lett 2001;167: 91-7.
18. 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: 4618-27.
19. Baker EK, Johnstone RW, Zalcberg JR, El-Osta A. Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene 2005;24: 8061-75.
20. 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: 817-24.
21. Turner JG, Gump JL, Zhang C, et al. ABCG2 expression, function, and promoter methylation in human multiple myeloma. Blood 2006;108: 3881-9.
22. 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: 5147-61.
23. Anttila S, Hakkola J, Tuominen P, et al. Methylation of cytochrome P4501A1 promoter in the lung is associated with tobacco smoking. Cancer Res 2003;63: 8623-8.
24. Okino ST, Pookot D, Li LC, et al. Epigenetic inactivation of the dioxin-responsive cytochrome P4501A1 gene in human prostate cancer. Cancer Res 2006;66: 7420-8.
25. Ghotbi R, Gomez A, Milani L, et al. Allele-specific expression and gene methylation in the control of CYP1A2 mRNA level in human livers. Pharmacogenomics J 2009;9: 208-17.
26. Hammons GJ, Yan-Sanders Y, Jin B, Blann E, Kadlubar FF, Lyn-Cook BD. Specific site methylation in the 5'-flanking region of CYP1A2 interindividual differences in human livers. Life Sci 2001;69: 839-45.
27. Tokizane T, Shiina H, Igawa M, et al. Cytochrome P450 1B1 is overexpressed and regulated by hypomethylation in prostate cancer. Clin Cancer Res 2005;11: 5793-801.
28. Tsuchiya Y, Nakajima M, Takagi S, Taniya T, Yokoi T. MicroRNA regulates the expression of human cytochrome P450 1B1. Cancer Res 2006;66: 9090-8.
29. Kalscheuer S, Zhang X, Zeng Y, Upadhyaya P. Differential expression of microRNAs in early-stage neoplastic transformation in the lungs of F344 rats chronically treated with the tobacco carcinogen 4-(methylnitrosamino)-1-(3- pyridyl)-1- butanone. Carcinogenesis 2008;29: 2394-9.
30. Onica T, Nichols K, Larin M, et al. Dexamethasone-mediated up-regulation of human CYP2A6 involves the glucocorticoid receptor and increased binding of hepatic nuclear factor 4 alpha to the proximal promoter. Mol Pharmacol 2008;73: 451-60.
31. Ling G, Wei Y, Ding X. Transcriptional regulation of human CYP2A13 expression in the respiratory tract by CCAAT/enhancer binding protein and epigenetic modulation. Mol Pharmacol 2007;71: 807-16.
32. Chung I, Karpf AR, Muindi JR, et al. Epigenetic silencing of CYP24 in tumor-derived endothelial cells contributes to selective growth inhibition by calcitriol. J Biol Chem 2007;282: 8704-14.
33. Komagata S, Nakajima M, Takagi S, Mohri T, Taniya T, Yokoi T. Human CYP24 catalyzing the inactivation of calcitriol is post-transcriptionally regulated by miR-125b. Mol Pharmacol 2009;76: 702-9.
34. 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 1996;238: 476-83.
35. Mohri T, Nakajima M, Fukami T, Takamiya M, Aoki Y, Yokoi T. Human CYP2E1 is regulated by miR-378. Biochem Pharmacol 2010;79: 1045-52.
36. Gomez A, Karlgren M, Edler D, Bernal ML, Mkrtchian S, Ingelman- Sundberg M. Expression of CYP2W1 in colon tumors: regulation by gene methylation. Pharmacogenomics 2007;8: 1315-25.
37. Karlgren M, Gomez A, Stark K, et al. Tumor-specific expression of the novel cytochrome P450 enzyme, CYP2W1. Biochem Biophys Res Commun 2006;341: 451-8.
38. Dannenberg LO, Edenberg HJ. Epigenetics of gene expression in human hepatoma cells: expression profiling the response to inhibition of DNA methylation and histone deacetylation. BMC Genomics 2006;7: 181.
39. Pan YZ, Gao W, Yu AM. MicroRNAs regulate CYP3A4 expression via direct and indirect targeting. Drug Metab Dispos 2009;37: 2112-7.
40. 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: 9674-80.
41. Xie Y, Ke S, Ouyang N, et al. Epigenetic regulation of transcriptional activity of pregnane X receptor by protein arginine methyltransferase 1. J Biol Chem 2009;284: 9199-205.
42. Assenat E, Gerbal-Chaloin S, Larrey D, et al. Interleukin 1beta inhibits CAR-induced expression of hepatic genes involved in drug and bilirubin clearance. Hepatology 2004;40: 951-60.
43. Adams BD, Furneaux H, White BA. The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptoralpha (ERalpha) and represses ERalpha messenger RNA and protein expression in breast cancer cell lines. Mol Endocrinol 2007;21: 1132-47.
44. Ronneberg JA, Tost J, Solvang HK, et al. GSTP1 promoter haplotypes affect DNA methylation levels and promoter activity in breast carcinomas. Cancer Res 2008;68: 5562-71.
45. Woodson K, O'Reilly KJ, Hanson JC, Nelson D, Walk EL, Tangrea JA. The usefulness of the detection of GSTP1 methylation in urine as a biomarker in the diagnosis of prostate cancer. J Urol 2008;179: 508-11; discussion 11-2.
46. Bovenzi V, Momparler RL. Antineoplastic action of 5-aza-2'- deoxycytidine and histone deacetylase inhibitor and their effect on the expression of retinoic acid receptor beta and estrogen receptor alpha genes in breast carcinoma cells. Cancer Chemother Pharmacol 2001;48: 71-6.
47. Kikuchi R, Kusuhara H, Hattori N, et al. Regulation of the expression of human organic anion transporter 3 by hepatocyte nuclear factor 1alpha/beta and DNA methylation. Mol Pharmacol 2006;70: 887-96.
48. Ferreri AJ, Dell'Oro S, Capello D, 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 2004;126: 657-64.
49. Wang L, Oberg AL, Asmann YW, et al. Genome-wide transcriptional profiling reveals microRNA-correlated genes and biological processes in human lymphoblastoid cell lines. PLoS ONE 2009;4:e5878.
50. 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: 299-313.
51. Candelaria M, de la Cruz-Hernandez E, Perez-Cardenas E, Trejo-Becerril C, Gutierrez-Hernandez O, Duenas-Gonzalez A. Pharmacogenetics and pharmacoepigenetics of gemcitabine. Med Oncol 2010;27: 1133-43.
52. Gagnon JF, Bernard O, Villeneuve L, Tetu B, Guillemette C. Irinotecan inactivation is modulated by epigenetic silencing of UGT1A1 in colon cancer. Clin Cancer Res 2006;12: 1850-8.
53. Nakajima M, Yokoi T. MicroRNAs from biology to future pharmacotherapy: regulation of cytochrome P450s and nuclear receptors. Pharmacol Ther 2011;131: 330-7.
54. Suter M, Abramovici A, Showalter L, et al. In utero tobacco exposure epigenetically modifies placental CYP1A1 expression. Metabolism 2010;59: 1481-90.
55. Murray GI, Taylor MC, McFadyen MC, et al. Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res 1997;57: 3026-31.
56. Lim LP, Lau NC, Garrett-Engele P, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005;433: 769-73.
57. Sharma R, Panda NK, Khullar M. Hypermethylation of carcinogen metabolism genes, CYP1A1, CYP2A13 and GSTM1 genes in head and neck cancer. Oral Dis 2010;16: 668-73.
58. Vertino PM, Yen RW, Gao J, Baylin SB. De novo methylation of CpG island sequences in human fibroblasts overexpressing DNA (cytosine-5-)- methyltransferase. Mol Cell Biol 1996;16: 4555-65.
59. Botto F, Seree E, el Khyari S, et al. Tissue-specific expression and methylation of the human CYP2E1 gene. Biochem Pharmacol 1994;48: 1095-103.
60. Ghanayem BI, Hoffler U. Investigation of xenobiotics metabolism, genotoxicity, and carcinogenicity using Cyp2e1(-/-) mice. Curr Drug Metab 2007;8: 728-49.
61. Luo W, Karpf AR, Deeb KK, et al. Epigenetic regulation of vitamin D 24-hydroxylase/CYP24A1 in human prostate cancer. Cancer Res 2010;70: 5953-62.
62. Takane H, Kobayashi D, Hirota T, et al. Haplotype-oriented genetic analysis and functional assessment of promoter variants in the MDR1 (ABCB1) gene. J Pharmacol Exp Ther 2004;311: 1179-87.
63. Dejeux E, Ronneberg 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.
64. 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: 9388-97.
65. Ling C, Groop L. Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 2009;58: 2718-25.
66. Kruh GD, Guo Y, Hopper-Borge E, Belinsky MG, Chen ZS. ABCC10, ABCC11, and ABCC12. Pflugers Arch 2007;453: 675-84.
67. Hauswald S, Duque-Afonso J, Wagner MM, et al. Histone deacetylase inhibitors induce a very broad, pleiotropic anticancer drug resistance phenotype in acute myeloid leukemia cells by modulation of multiple ABC transporter genes. Clin Cancer Res 2009;15: 3705-15.
68. To KK, Zhan Z, Bates SE. Aberrant promoter methylation of the ABCG2 gene in renal carcinoma. Mol Cell Biol 2006;26: 8572-85.
69. Youssef EM, Lotan D, Issa JP, et al. Hypermethylation of the retinoic acid receptor-beta(2) gene in head and neck carcinogenesis. Clin Cancer Res 2004;10: 1733-42.
70. 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: 4415-22.
71. Yoo CB, Cheng JC, Jones PA. Zebularine: a new drug for epigenetic therapy. Biochem Soc Trans 2004;32: 910-2.
72. Yang X, Lay F, Han H, Jones PA. Targeting DNA methylation for epigenetic therapy. Trends Pharmacol Sci 2010;31: 536-46.
73. Wu Y, Shi X, Liu Y, et al. Histone deacetylase 1 is required for Carbamazepine-induced CYP3A4 expression. J Pharm Biomed Anal 2012;58: 78-82.
74. Vanden Berghe W. Epigenetic impact of dietary polyphenols in cancer chemoprevention: Lifelong remodeling of our epigenomes. Pharmacol Res 2012;65: 565-76.
75. U.S. Food and Drug Administration Guidance for Industry: Pharmacogenomic Data Submission, 2005. Available from http://www.fda.gov/downloads/ RegulatoryInformation/Guidances/ucm126957.pdf. Accessed July 9, 2012.
76. U.S. Food and Drug Administration Guidance for Industry: Pharmacogenomic Data Submissions - Companion Guidance, 2007. Available from http://www.fda.gov/ downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm079855. pdf. Accessed July 9, 2012.
77. U.S. Food and Drug Administration Guidance for Industry and FDA Staff: Pharmacogenetic Tests and Genetic Tests for Heritable Markers, 2007. Available from http://www.fda.gov/downloads/MedicalDevices/DeviceRegulationandGuidance/ Guidance- Documents/ucm071075.pdf. Accessed July 9, 2012.
78. U.S. Food and Drug Administration Guidance for Industry: Clinical Pharmacogenomics: Premarketing Evaluation in Early Phase Clinical Studies, 2011. Available from http://www.fda. gov/downloads/Drugs/ GuidanceComplianceRegulatoryInforma tion/Guidances/UCM243702.pdf. Accessed July 9, 2012.
79. U.S. Department of Health and Human Services, Food and Drug Administration, Center for Devices and Radiological Health, Office of In Vitro Diagnostic Device Evaluation and Safety, and Division of Immunology and Hematology Devices. Multiplex tests for heritable DNA markers, mutations and expression patterns; draft Guidance for Industry and FDA reviewers, 2003. Available from http://www.fda.gov/OHRMS/DOCKETS/98fr/03d0120gdl.DOC. Accessed September 3, 2013.