Humanizing the zebrafish liver shifts drug metabolic profiles and improves pharmacokinetics of CYP3A4 substrates

Archives of Toxicology

Volumn 91, Issue 3, 2017, Pages 1187-1197

  Poon, Kar Lai ^a   Wang, Xingang ^a   Ng, Ashley S ^a   Goh, Wei Huang ^a   McGinnis, Claudia ^b   Fowler, Stephen ^b   Carney, Tom J ^a,c   Wang, Haishan ^a   Ingham, Phillip W ^a,c  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

CYP3A4; Humanized; Liver; Microsomes; Midazolam; Toxicity; Zebrafish

Indexed keywords

ACETYLSALICYLIC ACID; AMIODARONE; CARBAMAZEPINE; CHLORPROMAZINE; CYCLOPHOSPHAMIDE; CYTOCHROME P450 3A4; DESIPRAMINE; DEXTROMETHORPHAN; DICLOFENAC; ETHOXYRESORUFIN; INDOMETACIN; ISONIAZID; KETOCONAZOLE; MIDAZOLAM; NEFAZODONE; PARACETAMOL; PIOGLITAZONE; TROGLITAZONE; CYP3A4 PROTEIN, HUMAN; CYTOCHROME P450 3A; DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; AQUEOUS SOLUTION; ARTICLE; CONTROLLED STUDY; DRUG ABSORPTION; DRUG CLEARANCE; DRUG METABOLISM; DRUG RESPONSE; DRUG SOLUBILITY; DRUG UPTAKE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMANIZED ZEBRAFISH; LC50; LIPOPHILICITY; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; LIVER; LIVER MICROSOME; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TOXICITY ASSAY; TRANSGENIC ZEBRAFISH; WILD TYPE; ANIMAL; CHEMICAL PHENOMENA; CHEMISTRY; DRUG EFFECTS; DRUG INACTIVATION; GENETICS; HUMAN; MASS SPECTROMETRY; METABOLISM; PHARMACOKINETICS; PROCEDURES; SOLUBILITY; TOXICITY TESTING; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOCHROME P-450 CYP3A; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INACTIVATION, METABOLIC; LIVER; MASS SPECTROMETRY; PHARMACEUTICAL PREPARATIONS; PHARMACOKINETICS; SOLUBILITY; TOXICITY TESTS; ZEBRAFISH;

EID: 84982839351     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-016-1789-5     Document Type: Article

References (42)

1. Alderton W, Berghmans S, Butler P et al (2010) Accumulation and metabolism of drugs and CYP probe substrates in zebrafish larvae. Xenobiotica 40(8):547–557
2. Chang CT, Chung HY, Su HT, Tseng HP, Tzou WS, Hu CH (2013) Regulation of zebrafish CYP3A65 transcription by AHR2. Toxicol Appl Pharmacol 270(2):174–184
3. Cheung C, Gonzalez FJ (2008) Humanized mouse lines and their application for prediction of human drug metabolism and toxicological risk assessment. J Pharmacol Exp Ther 327(2):288–299
4. Cheung C, Ma X, Krausz KW et al (2005a) Differential metabolism of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in mice humanized for CYP1A1 and CYP1A2. Chem Res Toxicol 18(9):1471–1478
5. Cheung C, Yu AM, Ward JM et al (2005b) The cyp2e1-humanized transgenic mouse: role of cyp2e1 in acetaminophen hepatotoxicity. Drug Metab Dispos 33(3):449–457
6. Chng HT, Ho HK, Yap CW, Lam SH, Chan ECY (2012) An investigation of the bioactivation potential and metabolism profile of zebrafish versus human. J Biomol Screen 17(7):974–986
7. Corchero J, Granvil CP, Akiyama TE et al (2001) The CYP2D6 humanized mouse: effect of the human CYP2D6 transgene and HNF4alpha on the disposition of debrisoquine in the mouse. Mol Pharmacol 60(6):1260–1267
8. Dalvie D, Obach RS, Kang P et al (2009) Assessment of three human in vitro systems in the generation of major human excretory and circulating metabolites. Chem Res Toxicol 22(2):357–368
9. Dragin N, Uno S, Wang B, Dalton TP, Nebert DW (2007) Generation of ‘humanized’ hCYP1A1_1A2_Cyp1a1/1a2(−/−) mouse line. Biochem Biophys Res Commun 359(3):635–642
10. Goldstone JV, McArthur AG, Kubota A et al (2010) Identification and developmental expression of the full complement of Cytochrome P450 genes in zebrafish. BMC Genom 11(1):643
11. Granvil CP, Yu AM, Elizondo G et al (2003) Expression of the human CYP3A4 gene in the small intestine of transgenic mice: in vitro metabolism and pharmacokinetics of midazolam. Drug Metab Dispos 31(5):548–558
12. Guengerich FP (2011) Mechanisms of drug toxicity and relevance to pharmaceutical development. Drug Metab Pharmacokinet 26(1):3–14
13. Gustafson AL, Stedman DB, Ball J et al (2012) Inter-laboratory assessment of a harmonized zebrafish developmental toxicology assay—progress report on phase I. Reprod Toxicol 33(2):155–164
14. Hasegawa M, Kapelyukh Y, Tahara H et al (2011) Quantitative prediction of human pregnane X receptor and cytochrome P450 3A4 mediated drug-drug interaction in a novel multiple humanized mouse line. Mol Pharmacol 80(3):518–528
15. Her GM, Yeh YH, Wu JL (2003) 435-bp liver regulatory sequence in the liver fatty acid binding protein (L-FABP) gene is sufficient to modulate liver regional expression in transgenic zebrafish. Dev Dyn 227(3):347–356
16. Hesse RG, Kouklis GK, Ahituv N, Pomerantz JH (2015) The human ARF tumor suppressor senses blastema activity and suppresses epimorphic tissue regeneration. Elife 4:e07702
17. Jomaa B, Hermsen SA, Kessels MY et al (2014) Developmental toxicity of thyroid-active compounds in a zebrafish embryotoxicity test. ALTEX 31(3):303–317
18. Jones HS, Trollope HT, Hutchinson TH, Panter GH, Chipman JK (2012) Metabolism of ibuprofen in zebrafish larvae. Xenobiotica 42(11):1069–1075
19. Katoh M, Tateno C, Yoshizato K, Yokoi T (2008) Chimeric mice with humanized liver. Toxicology 246(1):9–17
20. Klieber S, Hugla S, Ngo R et al (2008) Contribution of the N-glucuronidation pathway to the overall in vitro metabolic clearance of midazolam in humans. Drug Metab Dispos 36(5):851–862
21. Kwan KM, Fujimoto E, Grabher C et al (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236(11):3088–3099
22. Li Y, Ross-Viola JS, Shay NF, Moore DD, Ricketts ML (2009) Human CYP3A4 and murine Cyp3A11 are regulated by equol and genistein via the pregnane X receptor in a species-specific manner. J Nutr 139(5):898–904
23. Lofgren S, Baldwin RM, Hiratsuka M et al (2008) Generation of mice transgenic for human CYP2C18 and CYP2C19: characterization of the sexually dimorphic gene and enzyme expression. Drug Metab Dispos 36(5):955–962
24. North TE, Babu IR, Vedder LM et al (2010) PGE2-regulated wnt signaling and N-acetylcysteine are synergistically hepatoprotective in zebrafish acetaminophen injury. Proc Natl Acad Sci USA 107(40):17315–17320
25. Ouellet D, Bramson C, Roman D et al (2007) Effects of three cytochrome P450 inhibitors, ketoconazole, fluconazole, and paroxetine, on the pharmacokinetics of lasofoxifene. Br J Clin Pharmacol 63(1):59–66
26. Pang SC, Wang HP, Li KY, Zhu ZY, Kang JX, Sun YH (2014) Double transgenesis of humanized fat1 and fat2 genes promotes omega-3 polyunsaturated fatty acids synthesis in a zebrafish model. Mar Biotechnol 16(5):580–593
27. Raldua D, Pina B (2014) In vivo zebrafish assays for analyzing drug toxicity. Expert Opin Drug Metab Toxicol 10(5):685–697
28. Scheer N, Roland Wolf C (2013) Xenobiotic receptor humanized mice and their utility. Drug Metab Rev 45(1):110–121
29. Scheer N, Wolf CR (2014) Genetically humanized mouse models of drug metabolizing enzymes and transporters and their applications. Xenobiotica 44(2):96–108
30. Schubert S, Keddig N, Hanel R, Kammann U (2014) Microinjection into zebrafish embryos (Danio rerio)—a useful tool in aquatic toxicity testing? Environ Sci Eur 26(1):1–8
31. Scornaienchi ML, Thornton C, Willett KL, Wilson JY (2010) Cytochrome P450-mediated 17β-estradiol metabolism in zebrafish (Danio rerio). J Endocrinol 206(3):317–325
32. Seo K-A, Bae SK, Choi Y-K, Choi CS, Liu K-H, Shin J-G (2010) Metabolism of 1′- and 4-hydroxymidazolam by glucuronide conjugation is largely mediated by UDP-glucuronosyltransferases 1A4, 2B4, and 2B7. Drug Metab Dispos 38(11):2007–2013
33. Shayeganpour A, El-Kadi AOS, Brocks DR (2006) Determination of the enzyme(s) involved in the metabolism of amiodarone in liver and intestine of rat: the contribution of cytochrome P450 3A isoforms. Drug Metab Dispos 34(1):43–50
34. Tseng HP, Hseu TH, Buhler DR, Wang WD, Hu CH (2005) Constitutive and xenobiotics-induced expression of a novel CYP3A gene from zebrafish larva. Toxicol Appl Pharmacol 205(3):247–258
35. van Herwaarden AE, Smit JW, Sparidans RW et al (2005) Midazolam and cyclosporin a metabolism in transgenic mice with liver-specific expression of human CYP3A4. Drug metabolism and disposition: the biological fate of chemicals 33(7):892–895
36. van Herwaarden AE, Wagenaar E, van der Kruijssen CM et al (2007) Knockout of cytochrome P450 3A yields new mouse models for understanding xenobiotic metabolism. J Clin Invest 117(11):3583–3592
37. Walsky RL, Obach RS (2004) Validated assays for human cytochrome P450 activities. Drug Metab Dispos 32(6):647–660
38. Williams PA, Cosme J, Vinkovic DM et al (2004) Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science 305(5684):683–686
39. Xie W, Barwick JL, Downes M et al (2000) Humanized xenobiotic response in mice expressing nuclear receptor SXR. Nature 406(6794):435–439
40. Zanger UM, Schwab M (2013) Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol Ther 138(1):103–141
41. Zhang F, Qin W, Zhang JP, Hu CQ (2015) Antibiotic toxicity and absorption in zebrafish using liquid chromatography-tandem mass spectrometry. PLoS ONE 10(5):e0124805
42. Zhu B, Bush D, Doss GA, Vincent SH, Franklin RB, Xu S (2008) Characterization of 1′-hydroxymidazolam glucuronidation in human liver microsomes. Drug Metab Dispos 36(2):331–338