Zebrafish teratogenicity test with metabolic activation (mDarT): Effects of phase I activation of acetaminophen on zebrafish Danio rerio embryos

Toxicology

Volumn 275, Issue 1-3, 2010, Pages 36-49

  Weigt, Stefan ^a,b   Huebler, Nicole ^a   Braunbeck, Thomas ^b   von Landenberg, Friedrich ^a   Broschard, Thomas H ^a  

^a Merck Serono GmbH   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Acetaminophen; Biotransformation; Cyclophosphamide; Detoxification; Teratogenicity; Zebrafish

Indexed keywords

CYCLOPHOSPHAMIDE; CYTOCHROME P450; CYTOCHROME P450 2E1; DNA; ELECTROPHILE; GLUTATHIONE; ISONIAZID; N ACETYL 1,4 BENZOQUINONE IMINE; PARACETAMOL; RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; DNA BINDING; DRUG ACTIVATION; EMBRYO; EMBRYO CULTURE; EMBRYO DEVELOPMENT; EMBRYOTOXICITY; ENZYME ACTIVATION; FEMALE; GLUCURONIDATION; IN VITRO STUDY; IN VIVO STUDY; LETHALITY; LIVER MICROSOME; LIVER MICROSOME METABOLISM; MALE; METABOLIC ACTIVATION; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; SULFATION; TERATOGENICITY; ZEBRA FISH;

ACETAMINOPHEN; ANIMALS; BIOTRANSFORMATION; DRUG EVALUATION, PRECLINICAL; FEMALE; MALE; PREGNANCY; ZEBRAFISH;

DANIO RERIO; MAMMALIA; RATTUS;

EID: 77954819352     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2010.05.012     Document Type: Article

References (84)

1. Antkiewicz D.S., Burns C.G., Carney S.A., Peterson R.E., Heideman W. Heart malformation is an early response to TCDD in embryonic zebrafish. Toxicol. Sci. 2005, 84:368-377.
2. Bachmann, J., 2002. Entwicklung und Erprobung eines Teratogenitäts-Screening Testes mit Embryonen des Zebrabärblings Danio rerio. Ph.D. Thesis, Technical University Dresden, Germany.
3. Balu N., Gamcsik M.P., Colvin M.E., Colvin M.O., Dolan M.E., Ludeman S.M. Modified guanines representing O6-alkylation by the cyclophosphamide metabolites acrolein and chloroacetaldehyde: synthesis, stability, and ab initio studies. Chem. Res. Toxicol. 2002, 15(3):380-387.
4. Black R.A., Hill D.A. Over-the-counter medications in pregnancy. Am. Fam. Physician 2003, 67:2517-2523.
5. Busquet F., Nagel R., von Landenberg F., Mueller S.O., Huebler N., Broschard T.H. Development of a new screening assay to identify proteratogenic substances using zebrafish Danio rerio embryo combined with an exogenous mammalian metabolic activation system (mDarT). Toxicol. Sci. 2008, 104(1):177-188.
6. Byer A.J., Trayler T.R., Semmer J.R. Acetaminophen overdose in the third trimester of pregnancy. JAMA 1982, 247:3114-3115.
7. Chakraborty C., Hsu C.H., Wen Z.H., Lin C.S., Agoramoorthy G. Zebrafish: a complete animal model for in vivo drug discovery and development. Curr. Drug Metab. 2009, 10:116-124.
8. Chauret N., Gauthier A., Nicoll-Griffith D.A. Effects of common organic solvents on in vitro cytochrome P450-mediated metabolic activities in human liver microsomes. Drug Metab. Dispos. 1998, 26(1):1-5.
9. Chen W., Koenigs L.L., Thompson S.J., Peter R.M., Rettie A.E., Trager W.F., Nelson S.D. Oxidation of acetaminophen to its toxic quinone imine and nontoxic catechol metabolites by Baculovirus-expressed and purified human cytochromes P450 2E1 and 2A6. Chem. Res. Toxicol. 1998, 11(4):295-301.
10. Colvin M., Brundrett R.B., Kan M.-N.N., Jardine I., Fenselau C. Alkylating properties of phosphoramide mustard. Cancer Res. 1976, 36:1121-1126.
11. Dai G., He L., Chou N., Wan Y.-J.Y. Acetaminophen metabolism does not contribute to gender difference in its hepatotoxicity in mouse. Toxicol. Sci. 2006, 92(1):33-41.
12. David A., Pancharatna K. Effects of acetaminophen (paracetamol) in the embryonic development of zebrafish, Danio rerio. J. Appl. Toxicol. 2009, 597-602.
13. Dirven H.A.A.M., van Ommen B., van Bladeren P.J. Involvement of human glutathione S-transferase isoenzymes in the conjugation of cyclophosphamide metabolites with glutathione. Cancer Res. 1994, 54(1):6215-6220.
14. Dirven H.A.A.M., Megens L., Oudshoorn M.J., Dingemanse M.A., van Ommen B., van Bladeren P.J. Glutathione conjugation of the cytostatic drug ifosfamide and the role of human glutathione S-transferases. Chem. Res. Toxicol. 1995, 8(7):979-986.
15. Fantel A.G. Culture of whole rodent embryos in teratogen screening. Teratog. Carcinog. Mutagen. 1982, 2:231-242.
16. Fantel A.G., Greenaway J.C., Juchau M.R., Shepard T.H. Teratogenic bioactivation of cyclophosphamide in vitro. Life Sci. 1979, 25:67-72.
17. Flint O.P. In vitro tests for teratogens: desirable endpoints, test batteries and current status of the micromass teratogen test. Reprod. Toxicol. 1993, 7(Suppl. 1):103-111.
18. Friedman J.M., Polifka J.E. Teratogenic Effects of Drugs-A Resource for Clinicians (TERIS) 2000, The Johns Hopkins University Press, Baltimore and London. 2nd ed.
19. Gardiner C.S., Reed D.J. Synthesis of glutathion in the preimplantation mouse embryo. Arch. Biochem. Biophys. 1995, 318:30-36.
20. Gerlinger P., Clavert J. Action de la cyclophosphamide injectée à des lapines en gestation sur les gonades embryonnaires. C.R. Hebd. Séances Acad. Sci. 1964, 258:2899-2901.
21. Gibson J.D., Pumford N.R., Samokyszyn V.M., Hinson J.A. Mechanism of acetaminophen-induced hepatotoxicity: covalent binding versus oxidative stress. Chem. Res. Toxicol. 1996, 9(3):580-585.
22. Gonzalez F.J., Yu A.-M. Cytochrome P450 and xenobiotic receptor humanized mice. Annu. Rev. Pharmacol. Toxicol. 2006, 46:41-64.
23. Gut I., Danielová V., Holubová J., Souček P., Klučková H. Cytotoxicity of cyclophosphamide, paclitaxel, and docetaxel for tumor cell lines in vitro: effects of concentration, time and cytochrome P450-catalysed metabolism. Arch. Toxicol. 2000, 74:437-446.
24. Gyamlani G.G., Parikh C.R. Acetaminophen toxicity: suicidal vs accidental. Crit. Care 2002, 6:155-159.
25. Hackenberger I., von Kreybig T. Comparative teratologic studies in mouse and rat. Arzneimittelforschung 1965, 15:1456-1460.
26. Haibach H., Akhter J.E., Muscato M.S., Cary P.L., Hoffmann M.F. Acetaminophen overdose with fetal demise. Am. J. Clin. Pathol. 1984, 82:240-242.
27. Hales B.F. Comparison of the mutagenicity and teratogenicity of cyclophosphamide and its active metabolites, 4-hydroxycyclophosphamide, phosphoramide mustard, and acrolein. Cancer Res. 1982, 42:3016-3021.
28. Harris C., Stark K.L., Luchtel D.L., Juchau M.R. Abnormal neurulation induced by 7-hydroxy-2-acetylaminofluorene and acetaminophen: evidence for catechol metabolites as proximate dysmorphogens. Toxicol. Appl. Pharmacol. 1989, 101:432-446.
29. Hazai E., Vereczkey L., Monostory K. Reduction of toxic metabolite formation of acetaminophen. Biochem. Biophys. Res. Commun. 2002, 291:1089-1094.
30. Hill A.J., Teraoka H., Heideman W., Peterson R.E. Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol. Sci. 2005, 86(1):6-19.
31. Hoffmann K.J., Axworthy D.B., Baillie T.A. Mechanistic studies on the metabolic activation of acetaminophen in vivo. Chem. Res. Toxicol. 1990, 3(3):204-211.
32. Jaeschke H., Bajt M.L. Intracellular signalling mechanisms of acetaminophen induced liver cell death. Toxicol. Sci. 2006, 89:31-41.
33. 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.
34. Lee S.S., Buters J.T., Pineau T., Fernandez-Salguero P., Gonzalez F.J. Role of CYP2E1 in the hepatotoxicity of acetaminophen. J. Biol. Chem. 1996, 271:12063-12067.
35. Lee S.K., Bista S.R., Jeong H., Kim D.H., Kang M.J., Jahng Y., Jeong T.C. The effects of rutaecarpine on the pharmacokinetics of acetaminophen in rats. Arch. Pharm. Res. 2007, 30(12):1628-1634.
36. Lewerenz V., Hanelt S., Nastevska C., El-Bahay C., Rohrdanz E., Kahl R. Antioxidants protect primary rat hepatocyte cultures against acetaminophen-induced DNA strand breaks but not against acetaminophen-induced cytotoxicity. Toxicology 2003, 191:179-187.
37. Loucks E., Carvan M.J. Strain-dependent effects of developmental ethanol exposure in zebrafish. Neurotoxicol. Teratol. 2004, 26:745-755.
38. Lubec G. Paracetamol hepatotoxicity. Padiatr. Padol. Pediatr. Padol. 1990, 25(1):39-41.
39. Lupp A., Tralls M., Fuchs U., Klinger W. Transplantation of fetal liver tissue suspensions into the spleens of adult syngenic rats: effects of different cytotoxins on cytochrome P450 mediated monooxygenase functions and on oxidative state. Exp. Toxicol. Pathol. 2000, 52:529-538.
40. Lupp A., Karge E., Danz M., Deufel T., Oelschläger H., Klinger W. Single and chronic administration of ciprofibrate or of ciprofibrate-glycinate in male Fischer 344 rats: comparison of the effects on morphological and biochemical parameters in liver and blood. Eur. J. Drug Metab. Pharmacokinet. 2005, 30:203-218.
41. Lupp A., Karge E., Deufel T., Oelschläger H., Fleck C. Ciprofibrate, clofibric acid and respective glycinate derivatives: effects of a four-week treatment on male lean and obese Zucker rats. Arzneimittelforschung 2008, 58:225-241.
42. Manyike P.T., Kharasch E.D., Kalhorn T.F. Contribution of CYP2E1 and CYP3A to acetaminophen reactive metabolite formation. Clin. Pharmacol. Ther. 2000, 67:275-282.
43. Marschall H.U., Wagner M., Zollner G., Trauner M. Clinical hepatotoxicity. Regulation and treatment with inducers of transport and cofactors. Mol. Pharm. 2007, 4(6):895-910.
44. Mason R.P., Fischer V. Free radicals of acetaminophen: their subsequent reactions and toxicological significance. Fed. Proc. 1986, 45:2493-2499.
45. McGrath P., Li C.Q. Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov. Today 2008, 13:394-401.
46. Mirkes P.E., Brown N.A., Kajbaf M., Lamb J.H., Farmer P.B., Naylor S. Identification of cyclophosphamide-DNA adducts in rat embryos exposed in vitro to 4-hydroperoxycyclophosphamide. Chem. Res. Toxicol. 1992, 5(3):382-385.
47. Murphy M.L. Teratogenic effects in rats of growth inhibiting chemicals, including studies on thalidomide. Clin. Proc. Child. Dist. Columbia 1962, 18:307-322.
48. Nagel R. DarT: the embryo test with the zebrafish Danio rerio-a general model in ecotoxicology and toxicology. ALTEX 2002, 19:38-48.
49. Nakagiri R., Oda H., Kamiya T. Small scale rat hepatocyte primary culture with applications for screening hepatoprotective substances. Biosci. Biotechnol. Biochem. 2003, 67:1629-1635.
50. New D.A. Whole-embryo culture and the study of mammalian embryos during organogenesis. Biol. Rev. Camb. Philos. Soc. 1978, 53:81-122.
51. Organization for Economic Cooperation and Development OECD Draft Proposal for A New Guideline, 1st Version 2006, Guideline for the Testing of Chemicals. Fish Embryo Toxicity, FET Test, Available at: http://www.oecd.org/dataoecd/39/59/36817070.pdf.
52. Piersma A.H. Validation of alternative methods for developmental toxicity testing. Toxicol. Lett. 2004, 149:147-153.
53. Poloyac S.M., Tortorici M.A., Przychodzin D.I., Reynolds R.B., Wen X., Frye R.F., Zemaitis M.A. The effect of isoniazid on CYP2E1- and CYP4A-mediated hydroxylation of arachidonic acid in the rat liver and kidney. Drug Metab. Disp. 2004, 32(7):727-733.
54. Popp R.A., Sessions C., Owens S. Effects of acetaminophen in mice. Environ. Mutagen. 1979, 1:117.
55. Posadas I., Vellecco V., Santos P., Prieto-Lloret J., Cena V. Acetaminophen potentiates staurosporine-induced death in a human neuroblastoma cell line. Br. J. Pharmacol. 2007, 150:577-585.
56. Reel J.R., Lawton A.D., Lamb J.C. Reproductive toxicity evaluation of acetaminophen in Swiss CD-1 mice using a continuous breeding protocol. Fundam. Appl. Toxicol. 1992, 18:233-239.
57. Reimers M.J., Flockton A.R., Tanguay R.L. Ethanol- and acetaldehyde-mediated developmental toxicity in zebrafish. Neurotoxicol. Teratol. 2004, 26:769-781.
58. Riggs B.S., Bronstein A.C., Kulig K., Archer P.G., Rumack B.H. Acute acetaminophen overdose during pregnancy. Obstet. Gynecol. 1989, 74(2):247-253.
59. Roberts I., Robinson M.J., Mughal M.Z., Ratcliffe J.G., Prescott L.F. Paracetamol metabolites in the neonate following maternal overdose. Br. J. Clin. Pharmacol. 1984, 18:201-206.
60. Rogers L.K., Moorthy B., Smith C.V. Acetaminophen binds to mouse hepatic and renal DNA at human therapeutic doses. Chem. Res. Toxicol. 1997, 10(4):470-476.
61. Ryan D.E., Koop D.R., Thomas P.E., Coon M.J., Levin W. Evidence that isoniazid and ethanol induce the same microsomal cytochrome P-450 in rat liver, an isozyme homologous to rabbit liver cytochrome P-450 isozyme 3A. Arch. Biochem. Biophys. 1986, 246(2):633-644.
62. Schardein J.L., Macina O.T. Human Developmental Toxicants: Aspects of Toxicology and Chemistry 2007, CRC Press, Taylor & Francis Group. 1st ed.
63. Selderslaghs I.W., Van Rompay A.R., De Coen W., Witters H.E. Development of a screening assay to identify teratogenic and embryotoxic chemicals using the zebrafish embryo. Reprod. Toxicol. 2009, 28:308-320.
64. Sessink P.J.M., Vaes W.H.J., van den Broek P.H.H., de Roos J.H.C., Noordhoek J., Bos R.P. Influence of Aroclor 1254, phenobarbital, β-naphthoflavone, and ethanol pretreatment on the biotransformation of cyclophosphamide in male and female rats. Toxicology 1996, 112:141-150.
65. Shen C., Zhang G., Qiu H., Meng Q. Acetaminophen-induced hepatotoxicity of gel entrapped rat hepatocytes in hollow fibers. Chem. Biol. Interact. 2006, 162:53-61.
66. Sinclair J.F., Szakacs J.G., Wood S.G., Walton H.S., Bement J.L., Gonzalez F.J., Jeffery E.H., Wrighton S.A., Bement W.J., Sinclair P.R. Short-term treatment with alcohols causes hepatic steatosis and enhances acetaminophen hepatotoxicity in CYP2E1 (-I-) mice. Toxicol. Appl. Pharmacol. 2000, 168:114-122.
67. Spielmann H., Pohl I., Döring B., Liebsch M., Moldenhauer F. The embryonic stem cell test, an in vitro embryotoxicity test using two permanent mouse cell lines: 3T3 fibroblast and embryonic stem cells. In Vitro Toxicol. 1997, 10(1):119-127.
68. Spielmann H., Seiler A., Bremer S., Hareng L., Hartung T., Ahr H., Faustman E., Haas U., Moffat G.J., Nau H., Vanparys P., Piersma A., Sintes J.R., Stuart J. The practical application of three validated in vitro embryotoxicity tests. The report and recommendations of an ECVAM/ZEBET workshop, ECVAM workshop 57. Altern. Lab. Anim. 2006, 34:527-538.
69. Springer J.B., Chang Y.H., Koo K.I., Colvin O.M., Colvin M.E., Dolan M.E., Delaney S.M., Flowers J.L., Ludeman S.M. 1,3- vs 1,5-intramolecular alkylation reactions in isophosphoramide and phosphoramide mustards. Chem. Res. Toxicol. 2004, 17(9):1217-1226.
70. Stark K.L., Harris C., Juchau M.R. Modulation of the embryotoxicity and cytotoxicity elicited by 7-hydroxy-2-acetylaminofluorene and acetaminophen via deacetylation. Toxicol. Appl. Pharmacol. 1989, 97:548-560.
71. Stark K.L., Harris C., Juchau M.R. Influence of electrophilic character and glutathione depletion on chemical dysmorphogenesis in cultured rat embryos. Biochem. Pharmacol. 1989, 38(16):2685-2692.
72. Stark K.L., Lee Q.P., Namkung M.J., Harris C., Juchau M.R. Dysmorphogenesis elicited by microinjected acetaminophen analogues and metabolites in rat embryos cultured in vitro. J. Pharmacol. Exp. Ther. 1990, 255(1):74-82.
73. Stern S.T., Bruno M.K., Hennig G.E., Horton R.A., Roberts J.C., Cohen S.D. Contribution of acetaminophen-cysteine to acetaminophen nephrotoxicity in CD-1 mice. I. Enhancement of acetaminophen nephrotoxicity by acetaminophen-cysteine. Toxicol. Appl. Pharmacol. 2005, 202:151-159.
74. Tan S.C., New L.S., Chan E.C.Y. Prevention of acetaminophen (APAP)-induced hepatotoxicity by leflunomide via inhibition of APAP biotransformation to N-acetyl-p-benzoquinone imine. Toxicol. Lett. 2008, 180:174-181.
75. Terneus M.V., Kiningham K.K., Carpenter A.B., Sullivan S.B., Valentovic M.A. Comparison of S-adenosyl-l-methionine and N-acetylcysteine protective effects on acetaminophen hepatic toxicity. J. Pharmacol. Exp. Ther. 2007, 320:99-107.
76. Ton C., Lin Y., Willett C. Zebrafish as a model for developmental neurotoxicity testing. Birth Defects Res. A: Clin. Mol. Teratol. 2006, 176:553-567.
77. Torkelson A.R., LaBudde J.A., Weikel J.H. The metabolic fate of cyclophosphamide. Drug. Metab. Rev. 1974, 3:131-165.
78. Webster W.S., Brown-Woodman P.D.C., Richtie H.E. A review of the contribution of whole embryo culture to the determination of hazard and risk in teratogenicity testing. Int. J. Dev. Biol. 1997, 41:329-335.
79. Weeks B.S., Gamache P., Klein N.W., Hinson J.A., Bruno M., Khairallah E. Acetaminophen toxicity to cultured rat embryos. Teratog. Carcinog. Mutagen. 1990, 10:361-371.
80. Wells P.G., Bhuller Y., Chen C.S., Jeng W., Kasapinovic S., Kennedy J.C., Kim P.M., Laposa R.R., McCallum G.P., Nicol C.J., Parman T., Wiley M.J., Wong A.W. Molecular and biochemical mechanisms in teratogenesis involving reactive oxygen species. Toxicol. Appl. Pharmacol. 2005, 207:S354-366.
81. Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish, Danio rerio 2000, University of Oregon Press, Eugene. 4th ed.
82. Yang L., Ho N.Y., Alshut R., Legradi J., Weiss C., Reischl M., Mikut R., Liebel U., Müller F., Strähle U. Zebrafish embryos as models for embryotoxic and teratological effects of chemicals. Reprod. Toxicol. 2009, 28:245-253.
83. Yoon M.Y., Kim S.J., Lee B.-H., Chung J.-H., Kim Y.C. Effects of dimethylsulfoxide on metabolism and toxicity of acetaminophen in mice. Biol. Pharm. Bull. 2006, 29(8):1618-1624.
84. Zhao J., Krafft N., Terlouw G.D.C., Bechter R. A model combining the whole embryo culture with human liver S-9 fraction for human teratogenic prediction. Toxicol. In Vitro 1993, 7:827-831.