Assessment of the developmental neurotoxicity of compounds by measuring locomotor activity in zebrafish embryos and larvae

Neurotoxicology and Teratology

Volumn 37, Issue , 2013, Pages 44-56

  Selderslaghs, Ingrid W T ^a,b   Hooyberghs, Jef ^a,c   Blust, Ronny ^b   Witters, Hilda E ^a  

^a FLEMISH INSTITUTE FOR TECHNOLOGICAL RESEARCH VITO   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c HASSELT UNIVERSITY   (Belgium)

Author keywords

Developmental neurotoxicity; Locomotor activity; Screening; Zebrafish

Indexed keywords

3,3' IMINODIPROPIONITRILE; 4,4' ISOPROPYLIDENEDIPHENOL; ACRYLAMIDE; CHLORPROMAZINE; METHYLMERCURY; OMEPRAZOLE; PARACETAMOL; PROPYLTHIOURACIL; SACCHARIN; THIAMAZOLE;

ANIMAL EMBRYO; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL SCREENING; DEVELOPMENTAL TOXICITY; DEVELOPMENTAL, AGE AND GROWTH PARAMETERS; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO SPONTANEOUS TAIL COILING; EVOLUTIONARY HOMOLOGY; HAZARD ASSESSMENT; IN VIVO STUDY; LARVAL DEVELOPMENT; LOCOMOTION; MAMMAL; NERVOUS SYSTEM DEVELOPMENT; NEUROTOXICITY; NONHUMAN; PERFORMANCE MEASUREMENT SYSTEM; PREDICTIVE VALUE; PRIORITY JOURNAL; SPECIES COMPARISON; SWIMMING; TERATOGEN TESTING; TERATOGENICITY; ZEBRA FISH;

ANIMAL USE ALTERNATIVES; ANIMALS; DATA INTERPRETATION, STATISTICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, NONMAMMALIAN; HAZARDOUS SUBSTANCES; LARVA; MOTOR ACTIVITY; NEUROTOXICITY SYNDROMES; SWIMMING; TOXICITY TESTS; ZEBRAFISH;

ANIMALIA; DANIO RERIO; MAMMALIA;

EID: 84875793321     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2013.01.003     Document Type: Article

References (73)

1. Axelstad M., Hansen P.R., Boberg J., Bonnichsen M., Nellemann C., Lund S.P., et al. Developmental neurotoxicity of propylthiouracil (PTU) in rats: relationship between transient hypothyroxinemia during development and long-lasting behavioural and functional changes. Toxicol Appl Pharmacol 2008, 232:1-13.
2. Barone S., Das K.P., Lassiter T.L., White L.D. Vulnerable processes of nervous system development: a review of markers and methods. Neurotoxicology 2000, 21:15-36.
3. Bjorling-Poulsen M., Andersen H.R., Grandjean P. Potential developmental neurotoxicity of pesticides used in Europe. Environ Health 2008, 7:50.
4. Boulet S.L., Boyle C.A., Schieve L.A. Health care use and health and functional impact of developmental disabilities among US children, 1997-2005. Arch Pediatr Adolesc Med 2009, 163:19-26.
5. Breier J.M., Radio N.M., Mundy W.R., Shafer T.J. Development of a high-throughput screening assay for chemical effects on proliferation and viability of immortalized human neural progenitor cells. Toxicol Sci 2008, 105:119-133.
6. Brosset C., Lord E. Methylmercury in ambient air. Method of determination and some measurements results. Water Air Soil Pollut 1995, 82:739-750.
7. Brown N.A. Selection of test chemicals for the ECVAM international validation study on in vitro embryotoxicity tests. European Centre for the Validation of Alternative Methods. Altern Lab Anim 2002, 30:177-198.
8. Buss R.R., Drapeau P. Synaptic drive to motoneurons during fictive swimming in the developing zebrafish. J Neurophysiol 2001, 86:197-210.
9. Chapin R.E., Adams J., Boekelheide K., Gray L.E., Hayward S.W., Lees P.S., et al. NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Res B Dev Reprod Toxicol 2008, 83:157-395.
10. Coecke S., Goldberg A.M., Allen S., Buzanska L., Calamandrei G., Crofton K., et al. Workgroup report: incorporating in vitro alternative methods for developmental neurotoxicity into international hazard and risk assessment strategies. Environ Health Perspect 2007, 115:924-931.
11. Committee on the toxicological effects of methylmercury National Research Council, toxicological effects of methylmercury 2000, National Academy Press, Washington DC.
12. Crofton K.M., Peele D.B., Stanton M.E. Developmental neurotoxicity following neonatal exposure to 3,3'-iminodipropionitrile in the rat. Neurotoxicol Teratol 1993, 15:117-129.
13. 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.
14. Drapeau P., Saint-Amant L., Buss R.R., Chong M., McDearmid J.R., Brustein E. Development of the locomotor network in zebrafish. Prog Neurobiol 2002, 68:85-111.
15. Dubovicky M., Kovacovsky P., Ujhazy E., Navarova J., Brucknerova I., Mach M. Evaluation of developmental neurotoxicity: some important issues focused on neurobehavioral development. Interdiscip Toxicol 2008, 1:206-210.
16. Eisen J.S. Developmental neurobiology of the zebrafish. J Neurosci 1991, 11:311-317.
17. Fleischer M. Testing costs and testing capacity according to the REACH requirements - results of a survey of independent and corporate GLP laboratories in the EU and Switzerland. J Bus Chem 2007, 4:96-114.
18. Franco J.L., Teixeira A., Meotti F.C., Ribas C.M., Stringari J., Garcia Pomblum S.C., et al. Cerebellar thiol status and motor deficit after lactational exposure to methylmercury. Environ Res 2006, 102:22-28.
19. Gao Y., Ding Y., Shi R., Tian Y. Effects of methylmercury on postnatal neurobehavioral development in mice. Neurotoxicol Teratol 2008, 30:462-467.
20. Grandjean P., Landrigan P.J. Developmental neurotoxicity of industrial chemicals. Lancet 2006, 368:2167-2178.
21. Gustafson A.L., Stedman D.B., Ball J., Hillegass J.M., Flood A., Zhang C.X., et al. Inter-laboratory assessment of a harmonized zebrafish developmental toxicology assay - progress report on phase I. Reprod Toxicol 2012, 33:155-164.
22. Hannah R.S., Parkinson D., Spira A.W., Roth S.H. The effect of chlorpromazine on monoamine levels in the rat cerebellum and hippocampus: a developmental study. Neurosci Lett 1987, 79:133-137.
23. Hass U. The need for developmental neurotoxicity studies in risk assessment for developmental toxicity. Reprod Toxicol 2006, 22:148.
24. Henck J.W., Frahm D.T., Anderson J.A. Validation of automated behavioral test systems. Neurotoxicol Teratol 1996, 18:189-197.
25. Henn K., Braunbeck T. Dechorionation as a tool to improve the fish embryo toxicity test (FET) with the zebrafish (Danio rerio). Comp Biochem Physiol C Toxicol Pharmacol 2011, 153:91-98.
26. Hill A., Mesens N., Steemans M., Xu J.J., Aleo M.D. Comparisons between in vitro whole cell imaging and in vivo zebrafish-based approaches for identifying potential human hepatotoxicants earlier in pharmaceutical development. Drug Metab Rev 2012, 44:127-140.
27. Irons T.D., Macphail R.C., Hunter D.L., Padilla S. Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicol Teratol 2010, 32:84-90.
28. Kobayashi K., Tsuji R., Yoshioka T., Kushida M., Yabushita S., Sasaki M., et al. Effects of hypothyroidism induced by perinatal exposure to PTU on rat behavior and synaptic gene expression. Toxicology 2005, 212:135-147.
29. 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.
30. Lefebvre J.L., Ono F., Puglielli C., Seidner G., Franzini-Armstrong C., Brehm P., et al. Increased neuromuscular activity causes axonal defects and muscular degeneration. Development 2004, 131:2605-2618.
31. Lein P., Silbergeld E., Locke P., Goldberg A.M. In vitro and other alternative approaches to developmental neurotoxicity testing (DNT). Environ Toxicol Pharmacol 2005, 19:735-744.
32. Lein P., Locke P., Goldberg A. Meeting report: alternatives for developmental neurotoxicity testing. Environ Health Perspect 2007, 115:764-768.
33. Lo W.Y., Friedman J.M. Teratogenicity of recently introduced medications in human pregnancy. Obstet Gynecol 2002, 100:465-473.
34. M.J., Robertson R.T., Peter C.P., Bokelman D.L. Effects of prenatal exposure to chlorpromazine on postnatal development and behavior of rats. Toxicol Appl Pharmacol 1980, 53:541-549.
35. Makris S., Raffaelle K., Sette W., Seed J. A retrospective analysis of twelve developmental neurotoxicity studies http://wwwmindfullyorg/Pesticide/Developmental-Neurotoxicity-EPA12nov98htm.
36. Makris S.L., Raffaele K., Allen S., Bowers W.J., Hass U., Alleva E., et al. A retrospective performance assessment of the developmental neurotoxicity study in support of OECD test guideline 426. Environ Health Perspect 2009, 117:17-25.
37. Melancon E., Liu D.W., Westerfield M., Eisen J.S. Pathfinding by identified zebrafish motoneurons in the absence of muscle pioneers. J Neurosci 1997, 17:7796-7804.
38. Menelaou E., Husbands E.E., Pollet R.G., Coutts C.A., Ali D.W., Svoboda K.R. Embryonic motor activity and implications for regulating motoneuron axonal pathfinding in zebrafish. Eur J Neurosci 2008, 28:1080-1096.
39. Middaugh L.D., Dow-Edwards D., Li A.A., Sandler J.D., Seed J., Sheets L.P., et al. Neurobehavioral assessment: a survey of use and value in safety assessment studies. Toxicol Sci 2003, 76:250-261.
40. Miodovnik A. Environmental neurotoxicants and developing brain. Mt Sinai J Med 2011, 78:58-77.
41. Miyagawa K., Narita M., Narita M., Akama H., Suzuki T. Memory impairment associated with a dysfunction of the hippocampal cholinergic system induced by prenatal and neonatal exposures to bisphenol-A. Neurosci Lett 2007, 418:236-241.
42. OECD OECD guidelines for the testing of chemicals. No 203: fish, acute toxicity test 1992.
43. OECD OECD guidelines for the testing of chemicals. No. 422: combined repeated dose toxicity study with the reproduction/developmental toxicity screening test 1996.
44. OECD OECD guidelines for the testing of chemicals: no. 414: prenatal developmental toxicity study 2001.
45. OECD OECD guideline for testing of chemicals. No. 426: developmental neurotoxicity study 2008.
46. Peterson R.T., Nass R., Boyd W.A., Freedman J.H., Dong K., Narahashi T. Use of non-mammalian alternative models for neurotoxicological study. Neurotoxicology 2008, 29:546-555.
47. Pineda R.H., Svoboda K.R., Wright M.A., Taylor A.D., Novak A.E., Gamse J.T., et al. Knockdown of Nav1.6a Na+ channels affects zebrafish motoneuron development. Development 2006, 133:3827-3836.
48. Radio N.M., Breier J.M., Shafer T.J., Mundy W.R. Assessment of chemical effects on neurite outgrowth in PC12 cells using high content screening. Toxicol Sci 2008, 105:106-118.
49. Reiter L. An introduction to neurobehavioral toxicology. Environ Health Perspect 1978, 26:5-7.
50. Rice S.A., Millan D.P., West J.A. The behavioral effects of perinatal methimazole administration in Swiss Webster mice. Fundam Appl Toxicol 1987, 8:531-540.
51. Richter C.A., Birnbaum L.S., Farabollini F., Newbold R.R., Rubin B.S., Talsness C.E., et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 2007, 24:199-224.
52. Rihel J., Prober D.A., Arvanites A., Lam K., Zimmerman S., Jang S., et al. Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 2010, 327:348-351.
53. Rovida C., Hartung T. Re-evaluation of animal numbers and costs for in vivo tests to accomplish REACH legislation requirements for chemicals - a report by the transatlantic think tank for toxicology (t(4)). ALTEX 2009, 26:187-208.
54. Rowland J., Makris S.L., Raffaele K., Schumacher K., Scarano L. A retrospective review of the use of the developmental neurotoxicity study in pesticide risk assessments. Toxicologist 2007, 96:369.
55. Saint-Amant L. Development of motor networks in zebrafish embryos. Zebrafish 2006, 3:173-190.
56. Saint-Amant L., Drapeau P. Motoneuron activity patterns related to the earliest behavior of the zebrafish embryo. J Neurosci 2000, 20:3964-3972.
57. Sanes D.H., Reh T.A., Harris W.A. Development of the nervous system 2005, Academic Press, San Diego, [Edition].
58. Schreiber R., Altenburger R., Paschke A., Schuurmann G., Kuster E. A novel in vitro system for the determination of bioconcentration factors and the internal dose in zebrafish (Danio rerio) eggs. Chemosphere 2009, 77:928-933.
59. 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.
60. Selderslaghs I.W., Hooyberghs J., De Coen W., Witters H.E. Locomotor activity in zebrafish embryos: a new method to assess developmental neurotoxicity. Neurotoxicol Teratol 2010, 32:460-471.
61. Selderslaghs I.W., Blust R., Witters H.E. Feasibility study of the zebrafish assay as an alternative method to screen for developmental toxicity and embryotoxicity using a training set of 27 compounds. Reprod Toxicol 2011, 33:142-154.
62. Smith L.E., Carvan M.J., Dellinger J.A., Ghorai J.K., White D.B., Williams F.E., et al. Developmental selenomethionine and methylmercury exposures affect zebrafish learning. Neurotoxicol Teratol 2010, 32:246-255.
63. Strahle U., Scholz S., Geisler R., Greiner P., Hollert H., Rastegar S., 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 2011, 33:128-132.
64. Sukardi H., Chng H.T., Chan E.C., Gong Z., Lam S.H. Zebrafish for drug toxicity screening: bridging the in vitro cell-based models and in vivo mammalian models. Expert Opin Drug Metab Toxicol 2011, 7:579-589.
65. Tierney K.B. Behavioural assessments of neurotoxic effects and neurodegeneration in zebrafish. Biochim Biophys Acta 2011, 1812:381-389.
66. Tilson H.A. Developmental neurotoxicology of endocrine disruptors and pesticides: identification of information gaps and research needs. Environ Health Perspect 1998, 106(Suppl. 3):807-811.
67. 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.
68. Tropepe V., Sive H.L. Can zebrafish be used as a model to study the neurodevelopmental causes of autism?. Genes Brain Behav 2003, 2:268-281.
69. U.S.EPA Health effects test guidelines OPPTS 870.6300 developmental neurotoxicity study 1998.
70. Weber D.N., Connaughton V.P., Dellinger J.A., Klemer D., Udvadia A., Carvan M.J. Selenomethionine reduces visual deficits due to developmental methylmercury exposures. Physiol Behav 2008, 93:250-260.
71. Werboff J., Dembicki E.L. Toxic effects of tranquilizers administered to gravid rats. J Neuropsychiatr 1962, 4:87-91.
72. Wise L.D., Gordon L.R., Soper K.A., Duchai D.M., Morrissey R.E. Developmental neurotoxicity evaluation of acrylamide in Sprague-Dawley rats. Neurotoxicol Teratol 1995, 17:189-198.
73. Zoeller R.T., Crofton K.M. Mode of action: developmental thyroid hormone insufficiency-neurological abnormalities resulting from exposure to propylthiouracil. Crit Rev Toxicol 2005, 35:771-781.