Expression variability of absorption, distribution, metabolism, excretion-related microRNAs in human liver: Influence of nongenetic factors and association with gene expression

Drug Metabolism and Disposition

Volumn 41, Issue 10, 2013, Pages 1752-1762

  Rieger, Jessica K ^a   Klein, Kathrin ^a   Winter, Stefan ^a   Zanger, Ulrich M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; CYTOCHROME P450 1A1; CYTOCHROME P450 2A6; CYTOCHROME P450 2C19; CYTOCHROME P450 2E1; MICRORNA; MICRORNA 10A; MICRORNA 122; MICRORNA 130B; MICRORNA 132; MICRORNA 142 3P; MICRORNA 148A; MICRORNA 15A; MICRORNA 185; MICRORNA 200A; MICRORNA 200B; MICRORNA 200C; MICRORNA 21; MICRORNA 22; MICRORNA 27B; MICRORNA 31; MICRORNA 34A; MICRORNA 539; MICRORNA LET 7G; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADME GENE; ADULT; AGE DISTRIBUTION; AGED; ARTICLE; BINDING SITE; CHOLESTASIS; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; INFLAMMATION; LIVER; MALE; PATHOPHYSIOLOGY; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION;

3' UNTRANSLATED REGIONS; ABSORPTION; AGED; C-REACTIVE PROTEIN; CYTOCHROME P-450 ENZYME SYSTEM; FEMALE; GENE EXPRESSION; HUMANS; LIVER; MALE; METABOLIC DETOXICATION, DRUG; MICRORNAS; TISSUE DISTRIBUTION;

EID: 84884679763     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.113.052126     Document Type: Article

References (60)

1. Abba M, Mudduluru G, and Allgayer H (2012) MicroRNAs in cancer: small molecules, big chances. Anticancer Agents Med Chem 12:733-743.
2. Barad O, Meiri E, Avniel A, Aharonov R, Barzilai A, Bentwich I, Einav U, Gilad S, Hurban P, and Karov Y, et al. (2004) MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Res 14:2486-2494. (Pubitemid 40012232)
3. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215-233.
4. Baskerville S and Bartel DP (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11:241-247. (Pubitemid 40270816)
5. Braconi C, Huang N, and Patel T (2010) MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology 51:881-890.
6. Burk O, Arnold KA, Nussler AK, Schaeffeler E, Efimova E, Avery BA, Avery MA, Fromm MF, and Eichelbaum M (2005) Antimalarial artemisinin drugs induce cytochrome P450 and MDR1 expression by activation of xenosensors pregnane X receptor and constitutive androstane receptor. Mol Pharmacol 67:1954-1965. (Pubitemid 41007777)
7. Dimmeler S and Nicotera P (2013) MicroRNAs in age-related diseases. EMBO Mol Med 5:180-190.
8. Feidt DM, Klein K, Hofmann U, Riedmaier S, Knobeloch D, Thasler WE, Weiss TS, Schwab M, and Zanger UM (2010) Profiling induction of cytochrome p450 enzyme activity by statins using a new liquid chromatography-tandem mass spectrometry cocktail assay in human hepatocytes. Drug Metab Dispos 38:1589-1597.
9. Friedman RC, Farh KK-H, Burge CB, and Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92-105.
10. Gomes AM, Winter S, Klein K, Turpeinen M, Schaeffeler E, Schwab M, and Zanger UM (2009) Pharmacogenomics of human liver cytochrome P450 oxidoreductase: multifactorial analysis and impact on microsomal drug oxidation. Pharmacogenomics 10:579-599.
11. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, and Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34 (Database issue):D140-D144.
12. Gusachenko ON, Zenkova MA, and Vlassov VV (2013) Nucleic acids in exosomes: disease markers and intercellular communication molecules. Biochemistry (Mosc) 78:1-7.
13. Habano W, Gamo T, Terashima J, Sugai T, Otsuka K, Wakabayashi G, and Ozawa S (2011) Involvement of promoter methylation in the regulation of Pregnane X receptor in colon cancer cells. BMC Cancer 11:81.
14. Haberl M, Anwald B, Klein K, Weil R, Fuss C, Gepdiremen A, Zanger UM, Meyer UA, and Wojnowski L (2005) Three haplotypes associated with CYP2A6 phenotypes in Caucasians. Pharmacogenet Genomics 15:609-624. (Pubitemid 41113334)
15. Hofmann MH, Blievernicht JK, Klein K, Saussele T, Schaeffeler E, Schwab M, and Zanger UM (2008) Aberrant splicing caused by single nucleotide polymorphism c.516G>T [Q172H], a marker of CYP2B6*6, is responsible for decreased expression and activity of CYP2B6 in liver. J Pharmacol Exp Ther 325:284-292. (Pubitemid 351439175)
16. Ingelman-Sundberg M, Sim SC, Gomez A, and Rodriguez-Antona C (2007) Influence of cytochrome P450 polymorphisms on drug therapies: pharmacogenetic, pharmacoepigenetic and clinical aspects. Pharmacol Ther 116:496-526. (Pubitemid 350116943)
17. Ito T, Yagi S, and Yamakuchi M (2010) MicroRNA-34a regulation of endothelial senescence. Biochem Biophys Res Commun 398:735-740.
18. Jiang J, Gusev Y, Aderca I, Mettler TA, Nagorney DM, Brackett DJ, Roberts LR, and Schmittgen TD (2008) Association of MicroRNA expression in hepatocellular carcinomas with hepatitis infection, cirrhosis, and patient survival. Clin Cancer Res 14:419-427. (Pubitemid 351226109)
19. Kacevska M, Ivanov M, Wyss A, Kasela S, Milani L, Rane A, and Ingelman-Sundberg M (2012) DNA methylation dynamics in the hepatic CYP3A4 gene promoter. Biochimie 94:2338-2344.
20. Kida K, Nakajima M, Mohri T, Oda Y, Takagi S, Fukami T, and Yokoi T (2011) PPARα is regulated by miR-21 and miR-27b in human liver. Pharm Res 28:2467-2476.
21. Klein K, Thomas M, Winter S, Nussler AK, Niemi M, Schwab M, and Zanger UM (2012) PPARA: a novel genetic determinant of CYP3A4 in vitro and in vivo. Clin Pharmacol Ther 91:1044-1052.
22. Klein K, Winter S, Turpeinen M, Schwab M, and Zanger UM (2010). Pathway-targeted pharmacogenomics of CYP1A2 in human liver. Front Pharmacol 1:129.
23. Kumar P, Luo Y, Tudela C, Alexander JM, and Mendelson CR (2013) The c-Myc-regulated microRNA-17-92 (miR-17-92) and miR-106a-363 clusters target hCYP19A1 and hGCM1 to inhibit human trophoblast differentiation. Mol Cell Biol 33:1782-1796.
24. Kumarswamy R, Volkmann I, and Thum T (2011) Regulation and function of miRNA-21 in health and disease. RNA Biol 8:706-713.
25. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, and Tuschl T (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12:735-739. (Pubitemid 34455427)
26. Lakner AM, Steuerwald NM, Walling TL, Ghosh S, Li T, McKillop IH, Russo MW, Bonkovsky HL, and Schrum LW (2012) Inhibitory effects of microRNA 19b in hepatic stellate cell-mediated fibrogenesis. Hepatology 56:300-310.
27. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, and Landthaler M, et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401-1414. (Pubitemid 46970709)
28. Lang T, Klein K, Fischer J, Nüssler AK, Neuhaus P, Hofmann U, Eichelbaum M, Schwab M, and Zanger UM (2001) Extensive genetic polymorphism in the human CYP2B6 gene with impact on expression and function in human liver. Pharmacogenetics 11:399-415. (Pubitemid 32656581)
29. Lee J and Kemper JK (2010) Controlling SIRT1 expression by microRNAs in health and metabolic disease. Aging (Albany, NY Online) 2:527-534.
30. Li N, Muthusamy S, Liang R, Sarojini H, and Wang E (2011) Increased expression of miR-34a and miR-93 in rat liver during aging, and their impact on the expression of Mgst1 and Sirt1. Mech Ageing Dev 132:75-85.
31. Lv M, Zhang X, Jia H, Li D, Zhang B, Zhang H, Hong M, Jiang T, Jiang Q, and Lu J, et al. (2012) An oncogenic role of miR-142-3p in human T-cell acute lymphoblastic leukemia (TALL) by targeting glucocorticoid receptor-a and cAMP/PKA pathways. Leukemia 26:769-777.
32. Maes OC, Sarojini H, and Wang E (2009) Stepwise up-regulation of microRNA expression levels from replicating to reversible and irreversible growth arrest states in WI-38 human fibroblasts. J Cell Physiol 221:109-119.
33. Mohri T, Nakajima M, Fukami T, Takamiya M, Aoki Y, and Yokoi T (2010) Human CYP2E1 is regulated by miR-378. Biochem Pharmacol 79:1045-1052.
34. Morgan ET (2009) Impact of infectious and inflammatory disease on cytochrome P450-mediated drug metabolism and pharmacokinetics. Clin Pharmacol Ther 85:434-438.
35. Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H, Okanoue T, and Shimotohno K (2006) Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene 25:2537-2545.
36. Nies AT, Koepsell H, Winter S, Burk O, Klein K, Kerb R, Zanger UM, Keppler D, Schwab M, and Schaeffeler E (2009) Expression of organic cation transporters OCT1 (SLC22A1) and OCT3 (SLC22A3) is affected by genetic factors and cholestasis in human liver. Hepatology 50:1227-1240.
37. Nies AT, Niemi M, Burk O, Winter S, Zanger UM, Stieger B, Schwab M, and Schaeffeler E (2013) Genetics is a major determinant of expression of the human hepatic uptake transporter OATP1B1, but not of OATP1B3 and OATP2B1. Genome Med 5:1.
38. Oda Y, Nakajima M, Mohri T, Takamiya M, Aoki Y, Fukami T, and Yokoi T (2012) Aryl hydrocarbon receptor nuclear translocator in human liver is regulated by miR-24. Toxicol Appl Pharmacol 260:222-231.
39. Pan Y-Z, Gao W, and Yu A-M (2009) MicroRNAs regulate CYP3A4 expression via direct and indirect targeting. Drug Metab Dispos 37:2112-2117.
40. Petrocca F, Vecchione A, and Croce CM (2008) Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res 68:8191-8194.
41. Plant N (2007) The human cytochrome P450 sub-family: transcriptional regulation, interindividual variation and interaction networks. Biochim Biophys Acta 1770:478-488.
42. Ramamoorthy A, Li L, Gaedigk A, Bradford LD, Benson EA, Flockhart DA, and Skaar TC (2012) In silico and in vitro identification of microRNAs that regulate hepatic nuclear factor 4α expression. Drug Metab Dispos 40:726-733.
43. Ramamoorthy A and Skaar TC (2011) In silico identification of microRNAs predicted to regulate the drug metabolizing cytochrome P450 genes. Drug Metab Lett 5:126-131.
44. Rieger JK, Bodan DA, and Zanger UM (2011) MIRNA-DISTILLER: A Stand-Alone Application to Compile microRNA Data from Databases. Front Genet 2:39.
45. Schröder A, Klein K, Winter S, Schwab M, Bonin M, Zell A, and Zanger UM (2013) Genomics of ADME gene expression: mapping expression quantitative trait loci relevant for absorption, distribution, metabolism and excretion of drugs in human liver. Pharmacogenomics J 13:12-20.
46. Strum JC, Johnson JH, Ward J, Xie H, Feild J, Hester A, Alford A, and Waters KM (2009) MicroRNA 132 regulates nutritional stress-induced chemokine production through repression of SirT1. Mol Endocrinol 23:1876-1884.
47. Takagi S, Nakajima M, Kida K, Yamaura Y, Fukami T, and Yokoi T (2010) MicroRNAs regulate human hepatocyte nuclear factor 4alpha, modulating the expression of metabolic enzymes and cell cycle. J Biol Chem 285:4415-4422.
48. Takagi S, Nakajima M, Mohri T, and Yokoi T (2008) Post-transcriptional regulation of human pregnane X receptor by micro-RNA affects the expression of cytochrome P450 3A4. J Biol Chem 283:9674-9680.
49. Thomas M, Burk O, Klumpp B, Kandel BA, Damm G, Weiss TS, Klein K, Schwab M, and Zanger UM (2013) Direct transcriptional regulation of human hepatic cytochrome P450 3A4 (CYP3A4) by peroxisome proliferator-activated receptor alpha (PPARa). Mol Pharmacol 83:709-718.
50. Toscano C, Klein K, Blievernicht J, Schaeffeler E, Saussele T, Raimundo S, Eichelbaum M, Schwab M, and Zanger UM (2006) Impaired expression of CYP2D6 in intermediate metabolizers carrying the*41 allele caused by the intronic SNP 2988G′A: evidence for modulation of splicing events. Pharmacogenet Genomics 16:755-766. (Pubitemid 44454870)
51. Tsuchiya Y, Nakajima M, Takagi S, Taniya T, and Yokoi T (2006) MicroRNA regulates the expression of human cytochrome P450 1B1. Cancer Res 66:9090-9098. (Pubitemid 44521128)
52. Wang X (2008) miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA 14:1012-1017.
53. Wei Z, Chen M, Zhang Y, Wang X, Jiang S, Wang Y, Wu X, Qin S, He L, and Zhang L, et al. (2013) No correlation of hsa-miR-148a with expression of PXR or CYP3A4 in human livers from Chinese Han population. PLoS ONE 8:e59141.
54. Wolbold R, Klein K, Burk O, Nüssler AK, Neuhaus P, Eichelbaum M, Schwab M, and Zanger UM (2003) Sex is a major determinant of CYP3A4 expression in human liver. Hepatology 38:978-988. (Pubitemid 37221681)
55. Yamaura Y, Nakajima M, Takagi S, Fukami T, Tsuneyama K, and Yokoi T (2012) Plasma microRNA profiles in rat models of hepatocellular injury, cholestasis, and steatosis. PLoS ONE 7:e30250.
56. Yang X, Zhang B, Molony C, Chudin E, Hao K, Zhu J, Gaedigk A, Suver C, Zhong H, and Leeder JS, et al. (2010) Systematic genetic and genomic analysis of cytochrome P450 enzyme activities in human liver. Genome Res 20:1020-1036.
57. Yokoi T and Nakajima M (2013) microRNAs as mediators of drug toxicity. Annu Rev Pharmacol Toxicol 53:377-400.
58. Zanger UM, Fischer J, Raimundo S, Stüven T, Evert BO, Schwab M, and Eichelbaum M (2001) Comprehensive analysis of the genetic factors determining expression and function of hepatic CYP2D6. Pharmacogenetics 11:573-585. (Pubitemid 32953583)
59. Zanger UM and Schwab M (2013) Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol Ther 138:103-141.
60. Zhang Y, Klein K, Sugathan A, Nassery N, Dombkowski A, Zanger UM, and Waxman DJ (2011) Transcriptional profiling of human liver identifies sex-biased genes associated with polygenic dyslipidemia and coronary artery disease. PLoS ONE 6:e23506.