In vitro biotransformation of two human CYP3A probe substrates and their inhibition during early zebrafish development

International Journal of Molecular Sciences

Volumn 18, Issue 1, 2017, Pages

  Verbueken, Evy ^a   Alsop, Derek ^b   Saad, Moayad A ^a   Pype, Casper ^a   van Peer, Els M ^a   Casteleyn, Christophe R ^a   Van Ginneken, Chris J ^a   Wilson, Joanna ^b   Van Cruchten, Steven J ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Activity; And biotransformation; Cytochrome P450; Development; Embryo; In vitro; Zebrafish

Indexed keywords

CYTOCHROME P450 1A2; CYTOCHROME P450 2B6; CYTOCHROME P450 2C8; CYTOCHROME P450 2D6; CYTOCHROME P450 3A; CYTOCHROME P450 3A4; KETOCONAZOLE; RESORUFIN; 7-METHOXYRESORUFIN; LUCIFERIN; MOLECULAR PROBE; OXAZINE DERIVATIVE;

ADULT; AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOTRANSFORMATION; CENTRIFUGATION; CONTROLLED STUDY; ENVIRONMENTAL CHANGE; FEMALE; FERTILIZATION; FLUORESCENCE; GENE EXPRESSION; IN VITRO STUDY; LIMIT OF DETECTION; LIMIT OF QUANTITATION; LIVER MICROSOME; NONHUMAN; ORGANOGENESIS; PROCESS OPTIMIZATION; PROTEIN EXPRESSION; TEMPERATURE; TERATOGENICITY; ZEBRA FISH; ANIMAL; DRUG EFFECTS; EMBRYO DEVELOPMENT; EMBRYOLOGY; ENZYME SPECIFICITY; GENETIC RECOMBINATION; GENETICS; HUMAN; METABOLISM; MOLECULAR PROBE; NONMAMMALIAN EMBRYO;

ANIMALS; BIOTRANSFORMATION; CYTOCHROME P-450 CYP3A; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; FIREFLY LUCIFERIN; HUMANS; KETOCONAZOLE; MICROSOMES, LIVER; MOLECULAR PROBES; OXAZINES; RECOMBINATION, GENETIC; SUBSTRATE SPECIFICITY; ZEBRAFISH;

EID: 85010723481     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18010217     Document Type: Article

References (52)

1. Barros, T.P.; Alderton, W.K.; Reynolds, H.M.; Roach, A.G.; Berghmans, S. Zebrafish: An emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery. Br. J. Pharmacol. 2008, 154, 1400–1413.
2. Kari, G.; Rodeck, U.; Dicker, A.P. Zebrafish: An emerging model system for human disease and drug discovery. Clin. Pharmacol. Ther. 2007, 82, 70–80.
3. Lammer, E.; Carr, G.J.; Wendler, K.; Rawlings, J.M.; Belanger, S.E.; Braunbeck, T. Is the fish embryo toxicity test (FET) with the zebrafish (Danio rerio) a potential alternative for the fish acute toxicity test? Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2009, 149, 196–209.
4. McGrath, P.; Li, C.Q. Zebrafish: A predictive model for assessing drug-induced toxicity. Drug Discov. Today 2008, 13, 394–401.
5. Westerfield, M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Brachydanio Rerio), 5th ed.; M.Westerfield: Eugene, OR, USA, 1993; pp. 1.1, 2.1–2.8.
6. Kimmel, C.B.; Ballard, W.W.; Kimmel, S.R.; Ullmann, B.; Schilling, T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203, 253–310.
7. Food and Drug Administration. Code of Federal Regulations Title 21. Available online: https://www. accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr=314.108 (accessed on 19 September 2016).
8. European Union. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Off. J. Eur. Union 2010, 276, 33–79.
9. Strahle, U.; Scholz, S.; Geisler, R.; Greiner, P.; Hollert, H.; Rastegar, S.; Schumacher, A.; Selderslaghs, I.; Weiss, C.;Witters, H.; et al. Zebrafish embryos as an alternative to animal experiments—A commentary on the definition of the onset of protected life stages in animal welfare regulations. Reprod. Toxicol. 2012, 33, 128–132.
10. Hines, R.N.; McCarver, D.G. The ontogeny of human drug-metabolizing enzymes: Phase I oxidative enzymes. J. Pharmacol. Exp. Ther. 2002, 300, 355–360.
11. De Wildt, S.N.; Kearns, G.L.; Leeder, J.S.; van den Anker, J.N. Glucuronidation in humans. Pharmacogenetic and developmental aspects. Clin. Pharmacokinet. 1999, 36, 439–452.
12. Weigt, S.; Huebler, N.; Strecker, R.; Braunbeck, T.; Broschard, T.H. Zebrafish (Danio rerio) embryos as a model for testing proteratogens. Toxicology 2011, 281, 25–36.
13. Chang, G.W.; Kam, P.C. The physiological and pharmacological roles of cytochrome P450 isoenzymes. Anaesthesia 1999, 54, 42–50.
14. Guengerich, F.P. Cytochrome P450s and other enzymes in drug metabolism and toxicity. AAPS J. 2006, 8, E101–E111.
15. Martignoni, M.; Groothuis, G.M.M.; de Kanter, R. Species differences between mouse, rat, dog, monkey and human CYP–mediated drug metabolism, inhibition and induction. Expert Opin. Drug Metab. Toxicol. 2006, 2, 875–894.
16. Zanger, U.M.; Schwab, M. Cytochrome P450 enzymes in drug metabolism: Regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol. Ther. 2013, 138, 103–141.
17. Goldstone, J.V.; McArthur, A.G.; Kubota, A.; Zanette, J.; Parente, T.; Jonsson, M.E.; Nelson, D.R.; Stegeman, J.J. Identification and developmental expression of the full complement of Cytochrome P450 genes in Zebrafish. BMC Genom. 2010, 11, 643.
18. McArthur, A.G.; Hegelund, T.; Cox, R.L.; Stegeman, J.J.; Liljenberg, M.; Olsson, U.; Sundberg, P.; Celander, M.C. Phylogenetic analysis of the cytochrome P450 3 (CYP3) gene family. J. Mol. Evol. 2003, 57, 200–211.
19. Yan, J.; Cai, Z. Molecular evolution and functional divergence of the cytochrome P450 3 (CYP3) Family in Actinopterygii (ray-finned fish). PLoS ONE 2010, 5, e14276.
20. Braunig, J.; Schiwy, S.; Broedel, O.; Muller, Y.; Frohme, M.; Hollert, H.; Keiter, S.H. Time–dependent expression and activity of cytochrome P450 1s in early life–stages of the zebrafish (Danio rerio). Environ. Sci. Pollut. Res. Int. 2015, 22, 16319–16328.
21. Chng, H.T.; Ho, H.K.; Yap, C.W.; Lam, S.H.; Chan, E.C. An investigation of the bioactivation potential and metabolism profile of Zebrafish versus human. J. Biomol. Screen. 2012, 17, 974–986.
22. Corley-Smith, G.E.; Su, H.T.; Wang-Buhler, J.L.; Tseng, H.P.; Hu, C.H.; Hoang, T.; Chung, W.G.; Buhler, D.R. CYP3C1, the first member of a new cytochrome P450 subfamily found in zebrafish (Danio rerio). Biochem. Biophys. Res. Commun. 2006, 340, 1039–1046.
23. Creusot, N.; Brion, F.; Piccini, B.; Budzinski, H.; Porcher, J.M.; Ait-Aissa, S. BFCOD activity in fish cell lines and zebrafish embryos and its modulation by chemical ligands of human aryl hydrocarbon and nuclear receptors. Environ. Sci. Pollut. Res. Int. 2015, 22, 16393–16404.
24. He, Q.; Liu, K.; Wang, S.; Hou, H.; Yuan, Y.; Wang, X. Toxicity induced by emodin on zebrafish embryos. Drug Chem. Toxicol. 2012, 35, 149–154.
25. Jones, H.S.; Panter, G.H.; Hutchinson, T.H.; Chipman, J.K. Oxidative and conjugative xenobiotic metabolism in zebrafish larvae in vivo. Zebrafish 2010, 7, 23–30.
26. Li, X.; Ma, J.; Fang, Q.; Li, Y. Transcription alterations of microRNAs, cytochrome P4501A1 and 3A65, and AhR and PXR in the liver of zebrafish exposed to crude microcystins. Toxicon 2013, 73, 17–22.
27. Liu, H.; Nie, F.H.; Lin, H.Y.; Ma, Y.; Ju, X.H.; Chen, J.J.; Gooneratne, R. Developmental toxicity, EROD, and CYP1A mRNA expression in zebrafish embryos exposed to dioxin–like PCB126. Environ. Toxicol. 2016, 31, 201–210.
28. Mattingly, C.J.; Toscano, W.A. Posttranscriptional silencing of cytochrome P4501A1 (CYP1A1) during zebrafish (Danio rerio) development. Dev. Dyn. 2001, 222, 645–654.
29. Otte, J.C.; Schmidt, A.D.; Hollert, H.; Braunbeck, T. Spatio–temporal development of CYP1 activity in early life–stages of zebrafish (Danio rerio). Aquat. Toxicol. 2010, 100, 38–50.
30. Saad, M.; Verbueken, E.; Pype, C.; Casteleyn, C.; Van Ginneken, C.; Maes, L.; Cos, P.; Van Cruchten, S. In vitro CYP1A activity in the zebrafish: Temporal but low metabolite levels during organogenesis and lack of gender differences in the adult stage. Reprod. Toxicol. 2016, 64, 50–56.
31. Schiwy, S.; Braunig, J.; Alert, H.; Hollert, H.; Keiter, S.H. A novel contact assay for testing aryl hydrocarbon receptor (AhR)-mediated toxicity of chemicals and whole sediments in zebrafish (Danio rerio) embryos. Environ. Sci. Pollut. Res. Int. 2015, 22, 16305–16318.
32. Scornaienchi, M.L.; Thornton, C.; Willett, K.L.; Wilson, J.Y. Cytochrome P450-mediated 17-estradiol metabolism in zebrafish (Danio rerio). J. Endocrinol. 2010, 206, 317–325.
33. Scornaienchi, M.L.; Thornton, C.;Willett, K.L.;Wilson, J.Y. Functional differences in the cytochrome P450 1 family enzymes from zebrafish (Danio rerio) using heterologously expressed proteins. Arch. Biochem. Biophys. 2010, 502, 17–22.
34. Shaya, L.; Dejong, C.; Wilson, J.Y. Expression patterns of cytochrome P450 3B and 3C genes in model fish species. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2014, 166, 115–125.
35. Tseng, H.P.; Hseu, T.H.; Buhler, D. R.; Wang,W. D.; Hu, C. H. Constitutive and xenobiotics-induced expression of a novel CYP3A gene from zebrafish larva. Toxicol. Appl. Pharmacol. 2005, 205, 247–258.
36. Doshi, U.; Li, A.P. Luciferin IPA-based higher throughput human hepatocyte screening assays for CYP3A4 inhibition and induction. J. Biomol. Screen. 2011, 16, 903–909.
37. Meisenheimer, P.L.; Uyeda, H.T.; Ma, D.; Sobol, M.; McDougall, M.G.; Corona, C.; Simpson, D.; Klaubert, D.H.; Cali, J.J. Proluciferin acetals as bioluminogenic substrates for cytochrome P450 activity and probes for CYP3A inhibition. Drug Metab. Disp. 2011, 39, 2403–2410.
38. Greenblatt, D.J.; Zhao, Y.; Venkatakrishnan, K.; Duan, S.X.; Harmatz, J.S.; Parent, S.J.; Court, M.H.; von Moltke, L.L. Mechanism of cytochrome P450–3A inhibition by ketoconazole. J. Pharm. Pharmacol. 2011, 63, 214–221.
39. Walsky, R.L.; Obach, R.S.; Hyland, R.; Kang, P.; Zhou, S.; West, M.; Geoghegan, K.F.; Helal, C.J.; Walker, G.S.; Goosen, T.C.; et al. Selective mechanism-based inactivation of CYP3A4 by CYP3cide (PF-04981517) and its utility as an in vitro tool for delineating the relative roles of CYP3A4 versus CYP3A5 in the metabolism of drugs. Drug Metab. Dispos. 2012, 40, 1686–1697.
40. Hewitt, N.J.; Lechon, M.J.G.; Houston, J.B.; Hallifax, D.; Brown, H.S.; Maurel, P.; Kenna, J.G.; Gustavsson, L.; Lohmann, C.; Skonberg, C.; et al. Primary hepatocytes: Current understanding of the regulation of metabolic enzymes and transporter proteins, and pharmaceutical practice for the use of hepatocytes in metabolism, enzyme induction, transporter, clearance, and hepatotoxicity studies. Drug Metab. Rev. 2007, 39, 159–234.
41. Xue, L.; Zgoda, V.G.; Arison, B.; Correia, M.A. Structure-function relationships of rat liver CYP3A9 to its human liver orthologs: Site–directed active site mutagenesis to a progesterone dihydroxylase. Arch. Biochem. Biophys. 2003, 409, 113–126.
42. Eagling, V.A.; Tjia, J.F.; Back, D.J. Differential selectivity of cytochrome P450 inhibitors against probe substrates in human and rat liver microsomes. Br. J. Clin. Pharmacol. 1998, 45, 107–114.
43. Hegelund, T.; Ottosson, K.; Radinger, M.; Tomberg, P.; Celander, M.C. Effects of the antifungal imidazole ketoconazole on CYP1A and CYP3A in rainbow trout and killifish. Environ. Toxicol. Chem. 2004, 23, 1326–1334.
44. Cohen, L.H.; Remley, M.J.; Raunig, D.; Vaz, A.D. In vitro drug interactions of cytochrome p450: An evaluation of fluorogenic to conventional substrates. Drug Metab. Dispos. 2003, 31, 1005–1015.
45. Zlokarnik, G.; Volak, L.P.; Andrew, M.M.; Tran, C.; Drysdale, T.; Shah, U.; Cleveland, T.; Makings, L.R. Validation of Fluorogenic Vivid™Probe Substrates for Analysis of CYP450-Drug Interactions. In Proceedings of the 10th North American ISSX Meeting, Indianapolis, IN, USA, 24–28 October 2000.
46. Field, H.A.; Ober, E.A.; Roeser, T.; Stainier, D.Y. Formation of the digestive system in zebrafish. I. Liver morphogenesis. Dev. Biol. 2003, 253, 279–290.
47. Ober, E.A.; Field, H.A.; Stainier, D.Y. From endoderm formation to liver and pancreas development in zebrafish. Mech. Dev. 2003, 120, 5–18.
48. Ng, A.N.; de Jong-Curtain, T.A.; Mawdsley, D.J.; White, S.J.; Shin, J.; Appel, B.; Dong, P.D.; Stainier, D.Y.; Heath, J.K. Formation of the digestive system in zebrafish: III. Intestinal epithelium morphogenesis. Dev. Biol. 2005, 286, 114–135.
49. Alderton, W.; Berghmans, S.; Butler, P.; Chassaing, H.; Fleming, A.; Golder, Z.; Richards, F.; Gardner, I. Accumulation and metabolism of drugs and CYP probe substrates in zebrafish larvae. Xenobiotica 2010, 40, 547–557.
50. European Union. Commission Recommendation of 18 June 2007 on guidelines for the accomodation and care of animals used for experimental and other scientific purposes (2007/526/EC). Off. J. Eur. Union 2007, 197, 89.
51. Hill, J.R. In vitro Drug Metabolism Using Liver Microsomes. In Current Protocols in Pharmacology; Enna, S.J., Williams, M., Eds.; JohnWiley & Sons, Inc.: New York, NY, USA, 2003; Volume 2, pp. 7.8.1–7.8.11.
52. Sengul, U. Comparing determination methods of detection and quantification limits for aflatoxin analysis in hazelnut. J. Food Drug Anal. 2016, 24, 56–62.