Fish embryo toxicity test: Identification of compounds with weak toxicity and analysis of behavioral effects to improve prediction of acute toxicity for neurotoxic compounds

Environmental Science and Technology

Volumn 49, Issue 11, 2015, Pages 7002-7011

  Klüver, Nils ^a   König, Maria ^a   Ortmann, Julia ^a   Massei, Riccardo ^a   Paschke, Albrecht ^a   Kühne, Ralph ^a   Scholz, Stefan ^a  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FISH; INSECTICIDES; TESTING;

CONCENTRATION ANALYSIS; CORRELATION ANALYSIS; EXPERIMENTAL ANALYSIS; FISH TOXICITY TESTS; NEUROTOXIC COMPOUNDS; PREDICTIVE CAPACITY; QUANTITATIVE PREDICTION; SYSTEMATIC ANALYSIS;

TOXICITY;

ALDICARB; AZINPHOS METHYL; CYANAZINE; DIELDRIN; DIQUAT; ENDOSULFAN; FENVALERATE; NEUROTOXIN; PICLORAM;

BEHAVIORAL RESPONSE; EMBRYO; FISH; PREDICTION; TOXIC SUBSTANCE; TOXICITY TEST;

ACUTE TOXICITY; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; EMBRYO MORTALITY; EMBRYONIC AND FETAL FUNCTIONS; EMBRYOTOXICITY; FISH; LC50; LOCOMOTION; MOVEMENT (PHYSIOLOGY); NEUROTOXICITY; NONHUMAN; ORGANISATION FOR ECONOMIC CO-OPERATION AND DEVELOPMENT; PREDICTIVE VALUE; TOXICITY TESTING; TOXICOKINETICS; ANALYSIS; ANIMAL; BIOASSAY; DRUG EFFECTS; EMBRYOLOGY; ENVIRONMENTAL EXPOSURE; LD50; MOTOR ACTIVITY; REGRESSION ANALYSIS; TIME; ZEBRA FISH;

DANIO RERIO;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL ASSAY; ENVIRONMENTAL EXPOSURE; LETHAL DOSE 50; MOTOR ACTIVITY; NEUROTOXINS; REGRESSION ANALYSIS; TIME FACTORS; TOXICITY TESTS, ACUTE; ZEBRAFISH;

EID: 84930635209     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b01910     Document Type: Article

References (52)

1. Scholz, S.; Sela, E.; Blaha, L.; Braunbeck, T.; Galay-Burgos, M.; Garcia-Franco, M.; Guinea, J.; Klüver, N.; Schirmer, K.; Tanneberger, K.; Tobor-Kaplon, M.; Witters, H.; Belanger, S.; Benfenati, E.; Creton, S.; Cronin, M. T.; Egqgen, R. I.; Embry, M.; Ekman, D.; Gourmelon, A.; Halder, M.; Hardy, B.; Hartung, T.; Hubesch, B.; Jungmann, D.; Lampi, M. A.; Lee, L.; Leonard, M.; Küster, E.; Lillicrap, A.; Luckenbach, T.; Murk, A. J.; Navas, J. M.; Peijnenburg, W.; Repetto, G.; Salinas, E.; Schüürmann, G.; Spielmann, H.; Tollefsen, K. E.; Walter-Rohde, S.; Whale, G.; Wheeler, J. R.; Winter, M. J. A European perspective on alternatives to animal testing for environmental hazard identification and risk assessment Regul. Toxicol. Pharmacol. 2013, 67 (3) 506-530
2. OECD. OECD guideline for testing of chemicals. Test No. 203: Acute fish test; Organization for Economic Cooperation and Development: Paris, France, 1992.
3. Braunbeck, T.; Böttcher, M.; Hollert, H.; Kosmehl, T.; Lammer, E.; Leist, E.; Rudolf, M.; Seitz, N. 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 (2) 87-102
4. Nagel, R. DarT: The embryo test with the zebrafish Danio rerio-A general model in ecotoxicology and toxicology ALTEX 2002, 19 (Suppl 1/02) 38-48
5. Rufli, H. Introduction of moribund category to OECD fish acute test and its effect on suffering and LC50 values Environ. Toxicol. Chem. 2012, 31 (5) 1107-1112
6. Rufli, H.; Springer, T. A. Can we reduce the number of fish in the OECD acute toxicity test? Environ. Toxicol. Chem. 2011, 30 (4) 1006-1011
7. OECD. Guideline No. 126: Short guidance on the threshold approach for acute fish toxicity; Organization for Economic Cooperation and Development: Paris, France, 2010.
8. Belanger, S. E.; Rawlings, J. M.; Carr, G. J. Use of fish embryo toxicity tests for the prediction of acute fish toxicity to chemicals Environ. Toxicol. Chem. 2013, 32 (8) 1768-1783
9. Knöbel, M.; Busser, F. J.; Rico-Rico, A.; Kramer, N. I.; Hermens, J. L.; Hafner, C.; Tanneberger, K.; Schirmer, K.; Scholz, S. Predicting adult fish acute lethality with the zebrafish embryo: Relevance of test duration, endpoints, compound properties, and exposure concentration analysis Environ. Sci. Technol. 2012, 46 (17) 9690-9700
10. 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 (2) 196-209
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, L 2010, L 276, 33-79
12. EU Commission Implementing Decision 2012/707/EU establishing a common format for the submission of the information pursuant to Directive 2010/63/EU of the European Parliament and of the Council on the protection of animals used for scientific purposes Off. J. Eur. Union L 2012, L 320, 33-50
13. OECD. OECD guideline for testing of chemicals. Test No. 236: Fish embryo acute toxicity (FET) test; Organization for Economic Cooperation and Development: Paris, France, 2013.
14. Busquet, F.; Strecker, R.; Rawlings, J. M.; Belanger, S. E.; Braunbeck, T.; Carr, G. J.; Cenijn, P.; Fochtman, P.; Gourmelon, A.; Hubler, N.; Kleensang, A.; Knobel, M.; Kussatz, C.; Legler, J.; Lillicrap, A.; Martinez-Jeronimo, F.; Polleichtner, C.; Rzodeczko, H.; Salinas, E.; Schneider, K. E.; Scholz, S.; van den Brandhof, E. J.; van der Ven, L. T.; Walter-Rohde, S.; Weigt, S.; Witters, H.; Halder, M. OECD validation study to assess intra- and inter-laboratory reproducibility of the zebrafish embryo toxicity test for acute aquatic toxicity testing Regul. Toxicol. Pharmacol. 2014, 69 (3) 496-511
15. Strahle, U.; Scholz, S.; Geisler, R.; Greiner, P.; Hollert, H.; Rastegar, S.; Schumacher, A.; Selderslaghs, I.; Weiss, C.; Witters, H.; Braunbeck, T. 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 (2) 128-132
16. Sobanska, M. A.; Cesnaitis, R.; Sobanski, T.; Versonnen, B.; Bonnomet, V.; Tarazona, J. V.; De Coen, W. Analysis of the ecotoxicity data submitted within the framework of the REACH Regulation. Part 1. General overview and data availability for the first registration deadline Sci. Total Environ. 2014, 470-471, 1225-1232
17. Klüver, N.; Ortmann, J.; Paschke, H.; Renner, P.; Ritter, A. P.; Scholz, S. Transient overexpression of adh8a increases allyl alcohol toxicity in zebrafish embryos PLoS One 2014, 9 (3 e90619
18. Van Leeuwen, C. J.; Griffioen, P. S.; Vergouw, W. H. A.; Maas-Diepeveen, J. L. Differences in susceptibility of early life stages of rainbow trout (Salmo gairdneri) to environmental pollutants Aquat. Toxicol. 1985, 7 (1-2) 59-78
19. Berghmans, S.; Butler, P.; Goldsmith, P.; Waldron, G.; Gardner, I.; Golder, Z.; Richards, F. M.; Kimber, G.; Roach, A.; Alderton, W.; Fleming, A. Zebrafish based assays for the assessment of cardiac, visual and gut function - Potential safety screens for early drug discovery J. Pharmacol. Toxicol. Methods 2008, 58 (1) 59-68
20. Scholz, S.; Ortmann, J.; Klüver, N.; Léonard, M. Extensive review of fish embryo acute toxicities for the prediction of GHS acute systemic toxicity categories Regul. Toxicol. Pharmacol. 2014, 69 (3) 572-579
21. Gobas, F. A.; Zhang, X. Measuring bioconcentration factors and rate constants of chemicals in aquatic organisms under conditions of variable water concentrations and short exposure time Chemosphere 1992, 25 (12) 1961-1971
22. US EPA. Estimation Programs Interface Suite for Microsoft Windows, v. 4.11; U. S. Environ. Prot. Agency, Washington, DC, USA, 2014.
23. Stanley, K. A.; Curtis, L. R.; Simonich, S. L.; Tanguay, R. L. Endosulfan I and endosulfan sulfate disrupts zebrafish embryonic development Aquat. Toxicol. 2009, 95 (4) 355-361
24. Tarazona, J. V.; Sobanska, M. A.; Cesnaitis, R.; Sobanski, T.; Bonnomet, V.; Versonnen, B.; De Coen, W. Analysis of the ecotoxicity data submitted within the framework of the REACH Regulation. Part 2. Experimental aquatic toxicity assays Sci. Total Environ. 2014, 472, 137-145
25. Hrovat, M.; Segner, H.; Jeram, S. Variability of in vivo fish acute toxicity data Regul. Toxicol. Pharmacol. 2009, 54 (3) 294-300
26. Raimondo, S.; Vivian, D. N.; Barron, M. G. Standardizing acute toxicity data for use in ecotoxicology models: Influence of test type, life stage, and concentration reporting Ecotoxicology 2009, 18 (7) 918-928
27. Creton, R. The calcium pump of the endoplasmic reticulum plays a role in midline signaling during early zebrafish development Brain Res. 2004, 151 (1-2) 33-41
28. Cheng, J.; Flahaut, E.; Cheng, S. H. Effect of carbon nanotubes on developing zebrafish (Danio rerio) embryos Environ. Toxicol. Chem. 2007, 26 (4) 708-716
29. Vijverberg, H. P.; vanden Bercken, J. Neurotoxicological effects and the mode of action of pyrethroid insecticides Crit. Rev. Toxicol. 1990, 21 (2) 105-126
30. Tu, W.; Lu, B.; Niu, L.; Xu, C.; Lin, C.; Liu, W. Dynamics of uptake and elimination of pyrethroid insecticides in zebrafish (Danio rerio) eleutheroembryos Ecotoxicol. Environ. Saf. 2014, 107, 186-191
31. Bradbury, S. P.; Carlson, R. W.; Henry, T. R.; Padilla, S.; Cowden, J. Toxic responses of the fish nervous system. In The toxicology of fishes; Taylor & Francis, Boca Raton, FL, 2008; pp 417-456.
32. Russom, C. L.; LaLone, C. A.; Villeneuve, D. L.; Ankley, G. T. Development of an adverse outcome pathway for acetylcholinesterase inhibition leading to acute mortality Environ. Toxicol. Chem. 2014, 33 (10) 2157-2169
33. Jacob, E.; Drexel, M.; Schwerte, T.; Pelster, B. Influence of hypoxia and of hypoxemia on the development of cardiac activity in zebrafish larvae Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 283 (4) R911-R917
34. 2 uptake in developing zebrafish, Danio rerio J. Exp. Biol. 2002, 205 (12) 1787-1794
35. Ducharme, N. A.; Peterson, L. E.; Benfenati, E.; Reif, D.; McCollum, C. W.; Gustafsson, J. A.; Bondesson, M. Meta-analysis of toxicity and teratogenicity of 133 chemicals from zebrafish developmental toxicity studies Reprod. Toxicol. 2013, 41, 98-108
36. Novak, A. E.; Taylor, A. D.; Pineda, R. H.; Lasda, E. L.; Wright, M. A.; Ribera, A. B. Embryonic and larval expression of zebrafish voltage-gated sodium channel α-subunit genes Dev. Dyn. 2006, 235 (7) 1962-1973
37. Teixido, E.; Pique, E.; Gomez-Catalan, J.; Llobet, J. Assessment of developmental delay in the zebrafish embryo teratogenicity assay Toxicol. in Vitro 2013, 27 (1) 469-478
38. Baxendale, S.; Holdsworth, C. J.; Santoscoy, P. L. M.; Harrison, M. R.; Fox, J.; Parkin, C. A.; Ingham, P. W.; Cunliffe, V. T. Identification of compounds with anti-convulsant properties in a zebrafish model of epileptic seizures Dis. Models & Mech. 2012, 5 (6) 773-784
39. 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 Genomics 2010, 11, 643
40. Weigt, S.; Huebler, N.; Strecker, R.; Braunbeck, T.; Broschard, T. H. Zebrafish (Danio rerio) embryos as a model for testing proteratogens Toxicology 2011, 281 (1-3) 25-36
41. 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 (8) 547-557
42. Carlsson, G.; Patring, J.; Kreuger, J.; Norrgren, L.; Oskarsson, A. Toxicity of 15 veterinary pharmaceuticals in zebrafish (Danio rerio) embryos Aquat. Toxicol. 2013, 126, 30-41
43. Kühnert, A.; Vogs, C.; Altenburger, R.; Küster, E. The internal concentration of organic substances in fish embryos - A toxicokinetic approach Environ. Toxicol. Chem. 2013, 32 (8) 1819-1827
44. Guo, J.-X.; Wu, J. J. Q.; Wright, J. B.; Lushington, G. H. Mechanistic insight into acetylcholinesterase inhibition and acute toxicity of organophosphorus compounds: A molecular modeling study Chem. Res. Toxicol. 2006, 19 (2) 209-216
45. Kuster, E.; Altenburger, R. Suborganismic and organismic effects of aldicarb and its metabolite aldicarb-sulfoxide to the zebrafish embryo (Danio rerio) Chemosphere 2007, 68 (4) 751-760
46. Kokel, D.; Bryan, J.; Laggner, C.; White, R.; Cheung, C. Y. J.; Mateus, R.; Healey, D.; Kim, S.; Werdich, A. A.; Haggarty, S. J. Rapid behavior-based identification of neuroactive small molecules in the zebrafish Nat. Chem. Biol. 2010, 6 (3) 231-237
47. Selderslaghs, I. W.; Hooyberghs, J.; Blust, R.; Witters, H. E. Assessment of the developmental neurotoxicity of compounds by measuring locomotor activity in zebrafish embryos and larvae Neurotoxicol. Teratol. 2013, 37, 44-56
48. 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 (4) 460-471
49. Prosch, S.; Voss, S. Interaction of glyphosate with photosystem II inhibitor herbicides as a selection tool for roundup ready events. Patent WO2006121902 A3, 2006.
50. Savaldi-Goldstein, S.; Baiga, T. J.; Pojer, F.; Dabi, T.; Butterfield, C.; Parry, G.; Santner, A.; Dharmasiri, N.; Tao, Y.; Estelle, M.; Noel, J. P.; Chory, J. New auxin analogs with growth-promoting effects in intact plants reveal a chemical strategy to improve hormone delivery Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (39) 15190-15195
51. Dodge, A.; Harris, N. The mode of action of paraquat and diquat Biochem. J. 1970, 118, 43P-44P
52. Zhao, X.; Salgado, V. L.; Yeh, J. Z.; Narahashi, T. Differential actions of fipronil and dieldrin insecticides on GABA-gated chloride channels in cockroach neurons J. Pharmacol. Exp. Ther. 2003, 306 (3) 914-924