The classification of motor neuron defects in the zebrafish embryo toxicity test (ZFET) as an animal alternative approach to assess developmental neurotoxicity

Neurotoxicology and Teratology

Volumn 34, Issue 4, 2012, Pages 413-424

  Muth Köhne, Elke ^a   Wichmann, Arne ^a,b   Delov, Vera ^a,b   Fenske, Martina ^a  

^a FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Developmental neurotoxicity; Motor neuron development; Non animal alternative; Zebrafish embryo toxicity test

Indexed keywords

3,4 DICHLOROANILINE; ALCOHOL; CARTAP; DISULFIRAM; NEUROTOXIN; NICOTINE; THIOCYCLAM; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONGENITAL MALFORMATION; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; EMBRYOTOXICITY; IMMUNOHISTOCHEMISTRY; MOTONEURON; MOTOR NEURON DISEASE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TOXICITY TESTING; ZEBRA FISH;

ANIMAL USE ALTERNATIVES; ANIMALS; DISEASE MODELS, ANIMAL; EMBRYO, NONMAMMALIAN; FEMALE; MALE; MOTOR NEURON DISEASE; NEUROTOXICITY SYNDROMES; NEUROTOXINS; TOXICITY TESTS; ZEBRAFISH;

ANIMALIA; DANIO RERIO; RODENTIA; VERTEBRATA;

EID: 84862140847     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2012.04.006     Document Type: Article

References (58)

1. Anderson C., Bartlett S.J., Gansner J.M., Wilson D., He L., Gitlin J.D., et al. Chemical genetics suggests a critical role for lysyl oxidase in zebrafish notochord morphogenesis. Mol Biosyst 2007, 3:51-59.
2. Bedoux G., Roig B., Thomas O., Dupont V., Le Bot B. Occurrence and toxicity of antimicrobial triclosan and by-products in the environment. Environ Sci Pollut Res Int 2011, 10.1007/s11356-011-0632-z.
3. Brannen K.C., Panzica-Kelly J.M., Danberry T.L., Augustine-Rauch K.A. Development of a zebrafish embryo teratogenicity assay and quantitative prediction model. Birth Defects Res B Dev Reprod Toxicol 2010, 89:66-77.
4. Braunbeck T., Boettcher M., Hollert H., Kosmehl T., Lammer E., Leist E., et al. Towards an alternative for the acute fish LC(50) test in chemical assessment: the fish embryo toxicity test goes multi-species - an update. ALTEX 2005, 22:87-102.
5. Carrel T.L., McWhorter M.L., Workman E., Zhang H., Wolstencroft E.C., Lorson C., et al. Survival motor neuron function in motor axons is independent of functions required for small nuclear ribonucleoprotein biogenesis. J Neurosci 2006, 26:11014-11022.
6. Chiba S., Saji Y., Takeo Y., Yui T., Aramaki Y. Nereistoxin and its derivatives their neuromuscular blocking and convulsive actions. Jpn J Pharmacol 1967, 17:491-492.
7. Crofton K.M., Mundy W.R., Lein P.J., Bal-Price A., Coecke S., Seiler A.E., et al. Developmental neurotoxicity testing: recommendations for developing alternative methods for the screening and prioritization of chemicals. ALTEX 2011, 28:9-15.
8. DIN38415-6 German standard methods for the examination of water, waste water and sludge - subanimal testing (group T) - part 6: toxicity to fish: determination of the non-acute-poisonous effect of waste water to fish eggs by dilution limits (T 6) 2003.
9. Durham H.D., Dahrouge S., Cashman N.R. Evaluation of the spinal cord neuron X neuroblastoma hybrid cell line NSC-34 as a model for neurotoxicity testing. Neurotoxicology 1993, 14:387-395.
10. Eisen J.S., Pike S.H., Debu B. The growth cones of identified motoneurons in embryonic zebrafish select appropriate pathways in the absence of specific cellular interactions. Neuron 1989, 2:1097-1104.
11. EU 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.
12. Fan C.Y., Cowden J., Simmons S.O., Padilla S., Ramabhadran R. Gene expression changes in developing zebrafish as potential markers for rapid developmental neurotoxicity screening. Neurotoxicol Teratol 2010, 32:91-98.
13. Filosto M., Tentorio M., Broglio L., Buzio S., Lazzarini C., Pasolini M.P., et al. Disulfiram neuropathy: two cases of distal axonopathy. Clin Toxicol (Phila) 2008, 46:314-316.
14. Fleming A. Zebrafish as an alternative model organism for disease modelling and drug discovery: implications for the 3Rs. NC3Rs, National Centre for the Replacement, refinement and reduction of animals in research 2007.
15. Gansner J.M., Mendelsohn B.A., Hultman K.A., Johnson S.L., Gitlin J.D. Essential role of lysyl oxidases in notochord development. Dev Biol 2007, 307:202-213.
16. Haendel M.A., Tilton F., Bailey G.S., Tanguay R.L. Developmental toxicity of the dithiocarbamate pesticide sodium metam in zebrafish. Toxicol Sci 2004, 81:390-400.
17. Harry G.J., Billingsley M., Bruinink A., Campbell I.L., Classen W., Dorman D.C., et al. In vitro techniques for the assessment of neurotoxicity. Environ Health Perspect 1998, 106(Suppl. 1):131-158.
18. Harry G.J., Tiffany-Castiglioni E. Evaluation of neurotoxic potential by use of in vitro systems. Expert Opin Drug Metab Toxicol 2005, 1:701-713.
19. Hinther A., Bromba C.M., Wulff J.E., Helbing C.C. Effects of triclocarban, triclosan, and methyl triclosan on thyroid hormone action and stress in frog and mammalian culture systems. Environ Sci Technol 2011, 45:5395-5402.
20. Karamanakos P.N., Pappas P., Stephanou P., Marselos M. Differentiation of disulfiram effects on central catecholamines and hepatic ethanol metabolism. Pharmacol Toxicol 2001, 88:106-110.
21. Kimmel C.B., Warga R.M., Kane D.A. Cell cycles and clonal strings during formation of the zebrafish central nervous system. Development 1994, 120:265-276.
22. Kokel D., Bryan J., Laggner C., White R., Cheung C.Y., Mateus R., et al. Rapid behavior-based identification of neuroactive small molecules in the zebrafish. Nat Chem Biol 2010, 6:231-237.
23. Kuegler P.B., Zimmer B., Waldmann T., Baudis B., Ilmjarv S., Hescheler J., et al. Markers of murine embryonic and neural stem cells, neurons and astrocytes: reference points for developmental neurotoxicity testing. ALTEX 2010, 27:17-42.
24. 2+ released via IP3 receptors is required for furrow deepening during cytokinesis in zebrafish embryos. Int J Dev Biol 2003, 47:411-421.
25. Luo J. GSK3beta in ethanol neurotoxicity. Mol Neurobiol 2009, 40:108-121.
26. Mendelsohn B.A., Yin C., Johnson S.L., Wilm T.P., Solnica-Krezel L., Gitlin J.D. Atp7a determines a hierarchy of copper metabolism essential for notochord development. Cell Metab 2006, 4:155-162.
27. Myers P.Z., Eisen J.S., Westerfield M. Development and axonal outgrowth of identified motoneurons in the zebrafish. J Neurosci 1986, 6:2278-2289.
28. Nagata K., Iwanaga Y., Shono T., Narahashi T. Modulation of the neuronal nicotinic acetylcholine receptor channel by imidacloprid and cartap. Pestic Biochem Physiol 1997, 59:119-128.
29. Nagel R. DarT: the embryo test with the zebrafish Danio rerio-a general model in ecotoxicology and toxicology. ALTEX 2002, 19(Suppl. 1):38-48.
30. Noraberg J. Organotypic brain slice cultures: an efficient and reliable method for neurotoxicological screening and mechanistic studies. Altern Lab Anim 2004, 32:329-337.
31. OECD Test guideline 426. OECD test guideline 426: developmental neurotoxicity study 2007.
32. Ott H., Diekmann H., Stuermer C.A., Bastmeyer M. Function of neurolin (DM-GRASP/SC-1) in guidance of motor axons during zebrafish development. Dev Biol 2001, 235:86-97.
33. Parng C., Roy N.M., Ton C., Lin Y., McGrath P. Neurotoxicity assessment using zebrafish. J Pharmacol Toxicol Methods 2007, 55:103-112.
34. Pike S.H., Melancon E.F., Eisen J.S. Pathfinding by zebrafish motoneurons in the absence of normal pioneer axons. Development 1992, 114:825-831.
35. Richter R., Otto D., Mengs H.-J. Insecticide compounds, acting on the acetylcholine receptor of the insect nervous system. Chemistry of plant protection 2: degradation of pesticides, desiccation and defoliation, ACh-receptors as targets 1989, 157-195. Springer-Verlag, Berlin, Heidelberg. G. Haug, H. Hoffmann (Eds.).
36. Ring A., Tanso R., Noraberg J. The use of organotypic hippocampal slice cultures to evaluate protection by non-competitive NMDA receptor antagonists against excitotoxicity. Altern Lab Anim 2010, 38:71-82.
37. Sakai M., Sato Y. Metabolic conversion of the nereistoxin-related compounds into nereistoxin as a factor of their insecticidal action. Insecticides 1972, vol. I:455-467. Gordon and Breach Science Publishers.
38. Sattelle D.B., Harrow I.D., David J.A., Pelhate M., Callec J.J. Nereistoxin: actions on a CNS acetylcholine receptor/ion channel in the cockroach Periplaneta americana. J Exp Biol 1985, 118:37-52.
39. Scholz S., Fischer S., Gundel U., Kuster E., Luckenbach T., Voelker D. The zebrafish embryo model in environmental risk assessment-applications beyond acute toxicity testing. Environ Sci Pollut Res Int 2008, 15:394-404.
40. 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.
41. Shastry P., Basu A., Rajadhyaksha M.S. Neuroblastoma cell lines-a versatile in vitro model in neurobiology. Int J Neurosci 2001, 108:109-126.
42. Spengler B.A., Ross R.A., Biedler J.L. Differential drug sensitivity of human neuroblastoma cells. Cancer Treat Rep 1986, 70:959-965.
43. Stoppini L., Buchs P.A., Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 1991, 37:173-182.
44. Sylvain N.J., Brewster D.L., Ali D.W. Embryonic ethanol exposure alters synaptic properties at zebrafish neuromuscular junctions. Neurotoxicol Teratol 2011, 33(2):313-321.
45. Sylvain N.J., Brewster D.L., Ali D.W. Zebrafish embryos exposed to alcohol undergo abnormal development of motor neurons and muscle fibers. Neurotoxicol Teratol 2010, 32:472-480.
46. Thomas L.T., Welsh L., Galvez F., Svoboda K.R. Acute nicotine exposure and modulation of a spinal motor circuit in embryonic zebrafish. Toxicol Appl Pharmacol 2009, 239:1-12.
47. Tilton F., La Du J.K., Vue M., Alzarban N., Tanguay R.L. Dithiocarbamates have a common toxic effect on zebrafish body axis formation. Toxicol Appl Pharmacol 2006, 216:55-68.
48. Tilton F., Tanguay R.L. Exposure to sodium metam during zebrafish somitogenesis results in early transcriptional indicators of the ensuing neuronal and muscular dysfunction. Toxicol Sci 2008, 106:103-112.
49. Ton C., Lin Y., Willett C. Zebrafish as a model for developmental neurotoxicity testing. Birth Defects Res A Clin Mol Teratol 2006, 76:553-567.
50. Tonkin E.G., Valentine H.L., Zimmerman L.J., Valentine W.M. Parenteral N, N-diethyldithiocarbamate produces segmental demyelination in the rat that is not dependent on cysteine carbamylation. Toxicol Appl Pharmacol 2003, 189:139-150.
51. Trevarrow B., Marks D.L., Kimmel C.B. Organization of hindbrain segments in the zebrafish embryo. Neuron 1990, 4:669-679.
52. van Boxtel A.L., Kamstra J.H., Fluitsma D.M., Legler J. Dithiocarbamates are teratogenic to developing zebrafish through inhibition of lysyl oxidase activity. Toxicol Appl Pharmacol 2010, 244:156-161.
53. 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.
54. Welsh L., Tanguay R.L., Svoboda K.R. Uncoupling nicotine mediated motoneuron axonal pathfinding errors and muscle degeneration in zebrafish. Toxicol Appl Pharmacol 2009, 237:29-40.
55. Westerfield M. The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio), vol 4 2000, University of Oregon Press, Eugene.
56. Yamada T., Pfaff S.L., Edlund T., Jessell T.M. Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 1993, 73:673-686.
57. Zeller J., Schneider V., Malayaman S., Higashijima S., Okamoto H., Gui J., et al. Migration of zebrafish spinal motor nerves into the periphery requires multiple myotome-derived cues. Dev Biol 2002, 252:241-256.
58. Zhou S., Dong Q., Li S., Guo J., Wang X., Zhu G. Developmental toxicity of cartap on zebrafish embryos. Aquat Toxicol 2009, 95:339-346.