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Review Articles

Regulation of human UDP-glycosyltransferase (UGT) genes by miRNAs

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Pages 120-140 | Received 12 Dec 2021, Accepted 25 Feb 2022, Published online: 11 Mar 2022

References

  • Abel Y, Rederstorff M. 2021. Gene reporter assays to study miRNA function. Methods Mol Biol. 2300:119–131.
  • Agarwal V, Bell GW, Nam JW, Bartel DP. 2015. Predicting effective microRNA target sites in mammalian mRNAs. Elife. 4:5.
  • Alarcon CR, Lee H, Goodarzi H, Halberg N, Tavazoie SF. 2015. N6-methyladenosine marks primary microRNAs for processing. Nature. 519(7544):482–485.
  • Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. 2008. The impact of microRNAs on protein output. Nature. 455(7209):64–71.
  • Barbier O, Belanger A. 2008. Inactivation of androgens by UDP-glucuronosyltransferases in the human prostate. Best Pract Res Clin Endocrinol Metab. 22(2):259–270.
  • Barbier O, Trottier J, Kaeding J, Caron P, Verreault M. 2009. Lipid-activated transcription factors control bile acid glucuronidation. Mol Cell Biochem. 326(1–2):3–8.
  • Basu NK, Kole L, Basu M, Chakraborty K, Mitra PS, Owens IS. 2008. The major chemical-detoxifying system of UDP-glucuronosyltransferases requires regulated phosphorylation supported by protein kinase C. J Biol Chem. 283(34):23048–23061.
  • Basu NK, Kovarova M, Garza A, Kubota S, Saha T, Mitra PS, Banerjee R, Rivera J, Owens IS. 2005. Phosphorylation of a UDP-glucuronosyltransferase regulates substrate specificity. Proc Natl Acad Sci USA. 102(18):6285–6290.
  • Beitzinger M, Peters L, Zhu JY, Kremmer E, Meister G. 2007. Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol. 4(2):76–84.
  • Belanger A, Pelletier G, Labrie F, Barbier O, Chouinard S. 2003. Inactivation of androgens by UDP-glucuronosyltransferase enzymes in humans. Trends Endocrinol Metab. 14(10):473–479.
  • Bosio A, Binczek E, Le Beau MM, Fernald AA, Stoffel W. 1996. The human gene CGT encoding the UDP-galactose ceramide galactosyl transferase (cerebroside synthase): cloning, characterization, and assignment to human chromosome 4, band q26. Genomics. 34(1):69–75.
  • Bottini S, Pratella D, Grandjean V, Repetto E, Trabucchi M. 2018. Recent computational developments on CLIP-seq data analysis and microRNA targeting implications. Brief Bioinform. 19(6):1290–1301.
  • Bushey RT, Lazarus P. 2012. Identification and functional characterization of a novel UDP-glucuronosyltransferase 2A1 splice variant: potential importance in tobacco-related cancer susceptibility. J Pharmacol Exp Ther. 343(3):712–724.
  • Bushey RT, Chen G, Blevins-Primeau AS, Krzeminski J, Amin S, Lazarus P. 2011. Characterization of UDP-glucuronosyltransferase 2A1 (UGT2A1) variants and their potential role in tobacco carcinogenesis. Pharmacogenet Genomics. 21(2):55–65.
  • Bushey RT, Dluzen DF, Lazarus P. 2013. Importance of UDP-glucuronosyltransferases 2A2 and 2A3 in tobacco carcinogen metabolism. Drug Metab Dispos. 41(1):170–179.
  • Cao Q, Chen X, Wu X, Liao R, Huang P, Tan Y, Wang L, Ren G, Huang J, Dong C. 2018. Inhibition of UGT8 suppresses basal-like breast cancer progression by attenuating sulfatide-αVβ5 axis. J Exp Med. 215(6):1679–1692.
  • Catalanotto C, Cogoni C, Zardo G. 2016. MicroRNA in control of gene expression: an overview of nuclear functions. Int J Mol Sci. 17(10):1712.
  • Chanawong A, Hu DG, Meech R, Mackenzie PI, McKinnon RA. 2015. Induction of UDP-glucuronosyltransferase 2B15 gene expression by the major active metabolites of tamoxifen, 4-hydroxytamoxifen and endoxifen, in breast cancer cells. Drug Metab Dispos. 43(6):889–897.
  • Chanawong A, Mackenzie PI, McKinnon RA, Hu DG, Meech R. 2017. Exemestane and Its Active Metabolite 17-Hydroexemestane Induce UDP-Glucuronosyltransferase (UGT) 2B17 Expression in Breast Cancer Cells. J Pharmacol Exp Ther. 361(3):482–491.
  • Chen G, Blevins-Primeau AS, Dellinger RW, Muscat JE, Lazarus P. 2007. Glucuronidation of nicotine and cotinine by UGT2B10: loss of function by the UGT2B10 Codon 67 (Asp > Tyr) polymorphism. Cancer Res. 67(19):9024–9029.
  • Chen G, Dellinger RW, Sun D, Spratt TE, Lazarus P. 2008. Glucuronidation of tobacco-specific nitrosamines by UGT2B10. Drug Metab Dispos. 36(5):824–830.
  • Chen K, Song F, Calin GA, Wei Q, Hao X, Zhang W. 2008. Polymorphisms in microRNA targets: a gold mine for molecular epidemiology. Carcinogenesis. 29(7):1306–1311.
  • Chipman LB, Pasquinelli AE. 2019. miRNA targeting: growing beyond the seed. Trends Genet. 35(3):215–222.
  • Chouinard S, Yueh MF, Tukey RH, Giton F, Fiet J, Pelletier G, Barbier O, Belanger A. 2008. Inactivation by UDP-glucuronosyltransferase enzymes: the end of androgen signaling. J Steroid Biochem Mol Biol. 109(3–5):247–253.
  • Court MH, Freytsis M, Wang X, Peter I, Guillemette C, Hazarika S, Duan SX, Greenblatt DJ, Lee WM. 2013. The UDP-glucuronosyltransferase (UGT) 1A polymorphism c.2042C > G (rs8330) is associated with increased human liver acetaminophen glucuronidation, increased UGT1A exon 5a/5b splice variant mRNA ratio, and decreased risk of unintentional acetaminophen-induced acute liver failure. J Pharmacol Exp Ther. 345(2):297–307.
  • Court MH, Zhang X, Ding X, Yee KK, Hesse LM, Finel M. 2012. Quantitative distribution of mRNAs encoding the 19 human UDP-glucuronosyltransferase enzymes in 26 adult and 3 fetal tissues. Xenobiotica. 42(3):266–277.
  • Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. 2004. Processing of primary microRNAs by the Microprocessor complex. Nature. 432(7014):231–235.
  • Dluzen DF, Lazarus P. 2015. MicroRNA regulation of the major drug-metabolizing enzymes and related transcription factors. Drug Metab Rev. 47(3):320–334.
  • Dluzen DF, Sun D, Salzberg AC, Jones N, Bushey RT, Robertson GP, Lazarus P. 2014. Regulation of UDP-glucuronosyltransferase 1A1 expression and activity by microRNA 491-3p. J Pharmacol Exp Ther. 348(3):465–477.
  • Dluzen DF, Sutliff AK, Chen G, Watson CJ, Ishmael FT, Lazarus P. 2016. Regulation of UGT2B expression and activity by miR-216b-5p in liver cancer cell lines. J Pharmacol Exp Ther. 359(1):182–193.
  • Doench JG, Petersen CP, Sharp PA. 2003. siRNAs can function as miRNAs. Genes Dev. 17(4):438–442.
  • Douglas SR, Shenoda BB, Qureshi RA, Sacan A, Alexander GM, Perreault M, Barrett JE, Aradillas-Lopez E, Schwartzman RJ, Ajit SK. 2015. Analgesic response to intravenous ketamine is linked to a circulating microrna signature in female patients with complex regional pain syndrome. J Pain. 16(9):814–824.
  • Easow G, Teleman AA, Cohen SM. 2007. Isolation of microRNA targets by miRNP immunopurification. RNA. 13(8):1198–1204.
  • Eichhorn SW, Guo H, McGeary SE, Rodriguez-Mias RA, Shin C, Baek D, Hsu S-H, Ghoshal K, Villén J, Bartel DP. 2014. mRNA destabilization is the dominant effect of mammalian microRNAs by the time substantial repression ensues. Mol Cell. 56(1):104–115.
  • Elton TS, Yalowich JC. 2015. Experimental procedures to identify and validate specific mRNA targets of miRNAs. Excli J. 14:758–790.
  • Fehlmann T, Sahay S, Keller A, Backes C. 2019. A review of databases predicting the effects of SNPs in miRNA genes or miRNA-binding sites. Brief Bioinform. 20(3):1011–1020.
  • Ge Y, Chen S, Mu W, Ba Q, Li J, Chen P, Wang X, Wang H. 2019. Epigenetic regulation of UDP-Glucuronosyltransferase by microRNA-200a/-183: implications for responses to sorafenib treatment in patients with hepatocellular carcinoma. Cancer Lett. 454:14–25.
  • Gebert LFR, MacRae IJ. 2019. Regulation of microRNA function in animals. Nat Rev Mol Cell Biol. 20(1):21–37.
  • Girard H, Levesque E, Bellemare J, Journault K, Caillier B, Guillemette C. 2007. Genetic diversity at the UGT1 locus is amplified by a novel 3′ alternative splicing mechanism leading to nine additional UGT1A proteins that act as regulators of glucuronidation activity. Pharmacogenet Genomics. 17(12):1077–1089.
  • Girard-Bock C, Benoit-Biancamano MO, Villeneuve L, Desjardins S, Guillemette C. 2016. A rare UGT2B7 variant creates a novel N-glycosylation site at codon 121 with impaired enzyme activity. Drug Metab Dispos. 44(12):1867–1871.
  • Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. 2006. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34(Database issue):D140–144.
  • Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. 2007. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell. 27(1):91–105.
  • Guo H, Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 466(7308):835–840.
  • Guo ZW, Xie C, Yang JR, Li JH, Yang JH, Zheng L. 2015. MtiBase: a database for decoding microRNA target sites located within CDS and 5′UTR regions from CLIP-Seq and expression profile datasets. Database. 2015:bav102.
  • Haas U, Sczakiel G, Laufer SD. 2012. MicroRNA-mediated regulation of gene expression is affected by disease-associated SNPs within the 3′-UTR via altered RNA structure. RNA Biol. 9(6):924–937.
  • Helwak A, Kudla G, Dudnakova T, Tollervey D. 2013. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell. 153(3):654–665.
  • Hijazi Y, Boulieu R. 2002. Contribution of CYP3A4, CYP2B6, and CYP2C9 isoforms to N-demethylation of ketamine in human liver microsomes. Drug Metab Dispos. 30(7):853–858.
  • Honke K, Tsuda M, Koyota S, Wada Y, Iida-Tanaka N, Ishizuka I, Nakayama J, Taniguchi N. 2001. Molecular cloning and characterization of a human beta-Gal-3′-sulfotransferase that acts on both type 1 and type 2 (Gal beta 1-3/1-4GlcNAc-R) oligosaccharides. J Biol Chem. 276(1):267–274.
  • Hu DG, Hulin JA, Wijayakumara DD, McKinnon RA, Mackenzie PI, Meech R. 2018. Intergenic splicing between four adjacent UGT genes (2B15, 2B29P2, 2B17, 2B29P1) gives rise to variant UGT proteins that inhibit glucuronidation via protein-protein interactions. Mol Pharmacol. 94(3):938–952.
  • Hu DG, Hulin JU, Nair PC, Haines AZ, McKinnon RA, Mackenzie PI, Meech R. 2019. The UGTome: the expanding diversity of UDP glycosyltransferases and its impact on small molecule metabolism. Pharmacol Ther. 204:107414.
  • Hu DG, Mackenzie PI, Hulin JA, McKinnon RA, Meech R. 2021a. Circular RNAs of UDP-Glycosyltransferase (UGT) genes expand the complexity and diversity of the UGT transcriptome. Mol Pharmacol. 99(6):488–503.
  • Hu DG, Marri S, Mackenzie PI, Hulin JA, McKinnon RA, Meech R. 2021b. The expression profiles and deregulation of UDP-glycosyltransferase (UGT) genes in human cancers and their association with clinical outcomes. Cancers. 13(17):4491.
  • Hu DG, Meech R, McKinnon RA, Mackenzie PI. 2014. Transcriptional regulation of human UDP-glucuronosyltransferase genes. Drug Metab Rev. 46(4):421–458.
  • Huang Y, Shen XJ, Zou Q, Wang SP, Tang SM, Zhang GZ. 2011. Biological functions of microRNAs: a review. J Physiol Biochem. 67(1):129–139.
  • Jonas S, Izaurralde E. 2015. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet. 16(7):421–433.
  • Kaivosaari S, Finel M, Koskinen M. 2011. N-glucuronidation of drugs and other xenobiotics by human and animal UDP-glucuronosyltransferases. Xenobiotica. 41(8):652–669.
  • Kaivosaari S, Toivonen P, Hesse LM, Koskinen M, Court MH, Finel M. 2007. Nicotine glucuronidation and the human UDP-glucuronosyltransferase UGT2B10. Mol Pharmacol. 72(3):761–768.
  • Kozomara A, Griffiths-Jones S. 2014. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42(Database issue):D68–73.
  • Kozomara A, Birgaoanu M, Griffiths-Jones S. 2019. miRBase: from microRNA sequences to function. Nucleic Acids Res. 47(D1):D155–D162.
  • Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, et al. 2005. Combinatorial microRNA target predictions. Nat Genet. 37(5):495–500.
  • Kuhn DE, Martin MM, Feldman DS, Terry AV, Jr., Nuovo GJ, Elton TS. 2008. Experimental validation of miRNA targets. Methods. 44(1):47–54.
  • Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 120(1):15–20.
  • Li CH, To KF, Tong JH, Xiao Z, Xia T, Lai PB, Chow SC, Zhu YX, Chan SL, Marquez VE, et al. 2013. Enhancer of zeste homolog 2 silences microRNA-218 in human pancreatic ductal adenocarcinoma cells by inducing formation of heterochromatin. Gastroenterology. 144(5):1086–1097. e1089.
  • Li Y, Kowdley KV. 2012. MicroRNAs in common human diseases. Genomics Proteomics Bioinformatics. 10(5):246–253.
  • Liu B, Shyr Y, Cai J, Liu Q. 2018. Interplay between miRNAs and host genes and their role in cancer. Brief Funct Genomics. 18(4):255–266.
  • Liu C, Mallick B, Long D, Rennie WA, Wolenc A, Carmack CS, Ding Y. 2013. CLIP-based prediction of mammalian microRNA binding sites. Nucleic Acids Res. 41(14):e138.
  • Liu W, Wang X. 2019. Prediction of functional microRNA targets by integrative modeling of microRNA binding and target expression data. Genome Biol. 20(1):18.
  • Loeb GB, Khan AA, Canner D, Hiatt JB, Shendure J, Darnell RB, Leslie CS, Rudensky AY. 2012. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol Cell. 48(5):760–770.
  • Loureiro AI, Bonifacio MJ, Fernandes-Lopes C, Almeida L, Wright LC, Soares-Da-Silva P. 2006. Human metabolism of nebicapone (BIA 3-202), a novel catechol-o-methyltransferase inhibitor: characterization of in vitro glucuronidation. Drug Metab Dispos. 34(11):1856–1862.
  • Mackenzie PI, Bock KW, Burchell B, Guillemette C, Ikushiro S, Iyanagi T, Miners JO, Owens IS, Nebert DW. 2005. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet Genomics. 15(10):677–685.
  • Mackenzie PI, Hu DG, Gardner-Stephen DA. 2010. The regulation of UDP-glucuronosyltransferase genes by tissue-specific and ligand-activated transcription factors. Drug Metab Rev. 42(1):99–109.
  • Mackenzie PI, Owens IS, Burchell B, Bock KW, Bairoch A, Belanger A, Fournel-Gigleux S, Green M, Hum DW, Iyanagi T, et al. 1997. The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics. 7(4):255–269.
  • Margaillan G, Levesque E, Guillemette C. 2016. Epigenetic regulation of steroid inactivating UDP-glucuronosyltransferases by microRNAs in prostate cancer. J Steroid Biochem Mol Biol. 155:85–93.
  • Martin HC, Wani S, Steptoe AL, Krishnan K, Nones K, Nourbakhsh E, Vlassov A, Grimmond SM, Cloonan N. 2014. Imperfect centered miRNA binding sites are common and can mediate repression of target mRNAs. Genome Biol. 15(3):R51.
  • Meech R, Hu DG, McKinnon RA, Mubarokah SN, Haines AZ, Nair PC, Rowland A, Mackenzie PI. 2019. The UDP-glycosyltransferase (UGT) superfamily: new members, new functions, and novel paradigms. Physiol Rev. 99(2):1153–1222.
  • Meech R, Mubarokah N, Shivasami A, Rogers A, Nair PC, Hu DG, McKinnon RA, Mackenzie PI. 2015. A novel function for UDP glycosyltransferase 8: galactosidation of bile acids. Mol Pharmacol. 87(3):442–450.
  • Menard V, Collin P, Margaillan G, Guillemette C. 2013. Modulation of the UGT2B7 enzyme activity by C-terminally truncated proteins derived from alternative splicing. Drug Metab Dispos. 41(12):2197–2205.
  • Menard V, Eap O, Roberge J, Harvey M, Levesque E, Guillemette C. 2011. Transcriptional diversity at the UGT2B7 locus is dictated by extensive pre-mRNA splicing mechanisms that give rise to multiple mRNA splice variants. Pharmacogenet Genomics. 21(10):631–641.
  • Meng CL, Zhao W, Zhong DN. 2021. Epigenetics and microRNAs in UGT1As. Hum Genomics. 15(1):30.
  • Mitra PS, Basu NK, Basu M, Chakraborty S, Saha T, Owens IS. 2011. Regulated phosphorylation of a major UDP-glucuronosyltransferase isozyme by tyrosine kinases dictates endogenous substrate selection for detoxification. J Biol Chem. 286(2):1639–1648.
  • Mittal N, Zavolan M. 2014. Seq and CLIP through the miRNA world. Genome Biol. 15(1):202.
  • Moszynska A, Gebert M, Collawn JF, Bartoszewski R. 2017. SNPs in microRNA target sites and their potential role in human disease. Open Biol. 7(4):170019.
  • Nakajima M, Koga T, Sakai H, Yamanaka H, Fujiwara R, Yokoi T. 2010. N-Glycosylation plays a role in protein folding of human UGT1A9. Biochem Pharmacol. 79(8):1165–1172.
  • Nakamura A, Nakajima M, Yamanaka H, Fujiwara R, Yokoi T. 2008. Expression of UGT1A and UGT2B mRNA in human normal tissues and various cell lines. Drug Metab Dispos. 36(8):1461–1464.
  • Nazarov PV, Kreis S. 2021. Integrative approaches for analysis of mRNA and microRNA high-throughput data. Comput Struct Biotechnol J. 19:1154–1162.
  • O'Brien J, Hayder H, Zayed Y, Peng C. 2018. Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol. 9:402.
  • Ohno A, Saito Y, Hanioka N, Jinno H, Saeki M, Ando M, Ozawa S, Sawada J. 2004. Involvement of human hepatic UGT1A1, UGT2B4, and UGT2B7 in the glucuronidation of carvedilol. Drug Metab Dispos. 32(2):235–239.
  • Ohno S, Nakajin S. 2009. Determination of mRNA expression of human UDP-glucuronosyltransferases and application for localization in various human tissues by real-time reverse transcriptase-polymerase chain reaction. Drug Metab Dispos. 37(1):32–40.
  • Okada C, Yamashita E, Lee SJ, Shibata S, Katahira J, Nakagawa A, Yoneda Y, Tsukihara T. 2009. A high-resolution structure of the pre-microRNA nuclear export machinery. Science. 326(5957):1275–1279.
  • Owczarek TB, Suchanski J, Pula B, Kmiecik AM, Chadalski M, Jethon A, Dziegiel P, Ugorski M. 2013. Galactosylceramide affects tumorigenic and metastatic properties of breast cancer cells as an anti-apoptotic molecule. PLoS One. 8(12):e84191.
  • Papageorgiou I, Court MH. 2017a. Identification and validation of microRNAs directly regulating the UDP-glucuronosyltransferase 1A subfamily enzymes by a functional genomics approach. Biochem Pharmacol. 137:93–106.
  • Papageorgiou I, Court MH. 2017b. Identification and validation of the microRNA response elements in the 3'-untranslated region of the UDP glucuronosyltransferase (UGT) 2B7 and 2B15 genes by a functional genomics approach. Biochem Pharmacol. 146:199–213.
  • Paulusch S, Kalthoff S, Landerer S, Jansen C, Schierwagen R, Klein S, Trebicka J, Strassburg CP. 2021. Regulation of uridine diphosphate-glucuronosyltransferase 1A expression by miRNA-214-5p and miRNA-486-3p. Epigenomics. 13(4):271–283.
  • Peng Y, Croce CM. 2016. The role of MicroRNAs in human cancer. Signal Transduct Target Ther. 1:15004.
  • Radominska-Pandya A, Little JM, Pandya JT, Tephly TR, King CD, Barone GW, Raufman JP. 1998. UDP-glucuronosyltransferases in human intestinal mucosa. Biochim Biophys Acta. 1394(2–3):199–208.
  • Raungrut P, Uchaipichat V, Elliot DJ, Janchawee B, Somogyi AA, Miners JO. 2010. In vitro-in vivo extrapolation predicts drug-drug interactions arising from inhibition of codeine glucuronidation by dextropropoxyphene, fluconazole, ketoconazole, and methadone in humans. J Pharmacol Exp Ther. 334(2):609–618.
  • Riolo G, Cantara S, Marzocchi C, Ricci C. 2020. miRNA targets: from prediction tools to experimental validation. Methods Protoc. 4(1):1.
  • Rojo Arias JE, Busskamp V. 2019. Challenges in microRNAs’ targetome prediction and validation. Neural Regen Res. 14(10):1672–1677.
  • Rukov JL, Shomron N. 2011. MicroRNA pharmacogenomics: post-transcriptional regulation of drug response. Trends Mol Med. 17(8):412–423.
  • Saetrom P, Heale BS, Snove O, Jr., Aagaard L, Alluin J, Rossi JJ. 2007. Distance constraints between microRNA target sites dictate efficacy and cooperativity. Nucleic Acids Res. 35(7):2333–2342.
  • Saliminejad K, Khorram Khorshid HR, Soleymani Fard S, Ghaffari SH. 2019. An overview of microRNAs: biology, functions, therapeutics, and analysis methods. J Cell Physiol. 234(5):5451–5465.
  • Schmitz U, Lai X, Winter F, Wolkenhauer O, Vera J, Gupta SK. 2014. Cooperative gene regulation by microRNA pairs and their identification using a computational workflow. Nucleic Acids Res. 42(12):7539–7552.
  • Schwartzman RJ, Alexander GM, Grothusen JR. 2011. The use of ketamine in complex regional pain syndrome: possible mechanisms. Expert Rev Neurother. 11(5):719–734.
  • Sethupathy P, Collins FS. 2008. MicroRNA target site polymorphisms and human disease. Trends Genet. 24(10):489–497.
  • Sevignani C, Calin GA, Siracusa LD, Croce CM. 2006. Mammalian microRNAs: a small world for fine-tuning gene expression. Mamm Genome. 17(3):189–202.
  • Shenoda BB, Ramanathan S, Ajit SK. 2017. In vitro validation of miRNA-mediated gene expression linked to drug metabolism. Curr Protoc Pharmacol. 79:9 26 21–29 26 15.
  • Shin C, Nam JW, Farh KK, Chiang HR, Shkumatava A, Bartel DP. 2010. Expanding the microRNA targeting code: functional sites with centered pairing. Mol Cell. 38(6):789–802.
  • Sutliff AK, Shi J, Watson CJW, Hunt MS, Chen G, Zhu HJ, Lazarus P. 2019a. Potential regulation of UGT2B10 and UGT2B7 by miR-485-5p in human liver. Mol Pharmacol. 96(6):674–682.
  • Sutliff AK, Watson CJW, Chen G, Lazarus P. 2019b. Regulation of UGT2A1 by miR-196a-5p and miR-196b-5p. J Pharmacol Exp Ther. 369(2):234–243.
  • Tan SM, Kirchner R, Jin J, Hofmann O, McReynolds L, Hide W, Lieberman J. 2014. Sequencing of captive target transcripts identifies the network of regulated genes and functions of primate-specific miR-522. Cell Rep. 8(4):1225–1239.
  • Tatsumi N, Tokumitsu S, Nakano M, Fukami T, Nakajima M. 2018. miR-141-3p commonly regulates human UGT1A isoforms via different mechanisms. Drug Metab Pharmacokinet. 33(4):203–210.
  • Tourancheau A, Margaillan G, Rouleau M, Gilbert I, Villeneuve L, Levesque E, Droit A, Guillemette C. 2016. Unravelling the transcriptomic landscape of the major phase II UDP-glucuronosyltransferase drug metabolizing pathway using targeted RNA sequencing. Pharmacogenomics J. 16(1):60–70.
  • Tourancheau A, Rouleau M, Guauque-Olarte S, Villeneuve L, Gilbert I, Droit A, Guillemette C. 2018. Quantitative profiling of the UGT transcriptome in human drug-metabolizing tissues. Pharmacogenomics J. 18(2):251–261.
  • Turfus SC, Parkin MC, Cowan DA, Halket JM, Smith NW, Braithwaite RA, Elliot SP, Steventon GB, Kicman AT. 2009. Use of human microsomes and deuterated substrates: an alternative approach for the identification of novel metabolites of ketamine by mass spectrometry. Drug Metab Dispos. 37(8):1769–1778.
  • Turgeon D, Carrier JS, Levesque E, Hum DW, Belanger A. 2001. Relative enzymatic activity, protein stability, and tissue distribution of human steroid-metabolizing UGT2B subfamily members. Endocrinology. 142(2):778–787.
  • Uchaipichat V, Raungrut P, Chau N, Janchawee B, Evans AM, Miners JO. 2011. Effects of ketamine on human UDP-glucuronosyltransferases in vitro predict potential drug-drug interactions arising from ketamine inhibition of codeine and morphine glucuronidation. Drug Metab Dispos. 39(8):1324–1328.
  • Uchaipichat V, Suthisisang C, Miners JO. 2013. The glucuronidation of R- and S-lorazepam: human liver microsomal kinetics, UDP-glucuronosyltransferase enzyme selectivity, and inhibition by drugs. Drug Metab Dispos. 41(6):1273–1284.
  • Wang P, Nie YL, Wang SJ, Yang LL, Yang WH, Li JF, Li XT, Zhang LR. 2018. Regulation of UGT1A expression by miR-298 in human livers from the Han Chinese population and in human cell lines. Epigenomics. 10(1):43–57.
  • Wijayakumara DD, Hu DG, Meech R, McKinnon RA, Mackenzie PI. 2015. Regulation of human UGT2B15 and UGT2B17 by miR-376c in prostate cancer cell lines. J Pharmacol Exp Ther. 354(3):417–425.
  • Wijayakumara DD, Mackenzie PI, McKinnon RA, Hu DG, Meech R. 2017. Regulation of UDP-glucuronosyltransferases UGT2B4 and UGT2B7 by MicroRNAs in liver cancer cells. J Pharmacol Exp Ther. 361(3):386–397.
  • Wijayakumara DD, Mackenzie PI, McKinnon RA, Hu DG, Meech R. 2018. Regulation of UDP-glucuronosyltransferase 2B15 by miR-331-5p in prostate cancer cells involves canonical and noncanonical target sites. J Pharmacol Exp Ther. 365(1):48–59.
  • Williams JA, Hyland R, Jones BC, Smith DA, Hurst S, Goosen TC, Peterkin V, Koup JR, Ball SE. 2004. Drug-drug interactions for UDP-glucuronosyltransferase substrates: a pharmacokinetic explanation for typically observed low exposure (AUCi/AUC) ratios. Drug Metab Dispos. 32(11):1201–1208.
  • Wu L, Fan J, Belasco JG. 2006. MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci USA. 103(11):4034–4039.
  • Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W. 2004. Single processing center models for human Dicer and bacterial RNase III. Cell. 118(1):57–68.
  • Zhong X, Heinicke F, Rayner S. 2019. miRBaseMiner, a tool for investigating miRBase content. RNA Biol. 16(11):1534–1546.
  • Zhou D, Guo J, Linnenbach AJ, Booth-Genthe CL, Grimm SW. 2010. Role of human UGT2B10 in N-glucuronidation of tricyclic antidepressants, amitriptyline, imipramine, clomipramine, and trimipramine. Drug Metab Dispos. 38(5):863–870.
  • Zhu AZ, Zhou Q, Cox LS, Ahluwalia JS, Benowitz NL, Tyndale RF. 2013. Variation in trans-3′-hydroxycotinine glucuronidation does not alter the nicotine metabolite ratio or nicotine intake. PLoS One. 8(8):e70938.

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