Developmental exposure to organophosphate flame retardants elicits overt toxicity and alters behavior in early life stage zebrafish (danio rerio)

Toxicological Sciences

Volumn 142, Issue 2, 2014, Pages 445-454

  Dishaw, Laura V ^a   Hunter, Deborah L ^b   Padnos, Beth ^b   Padilla, Stephanie ^b   Stapleton, Heather M ^a  

^a DUKE UNIVERSITY   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Development; Flame retardant; Neurotoxicity; Organophosphate; TDCPP; Zebrafish

Indexed keywords

CHLORPYRIFOS; FLAME RETARDANT; ORGANOPHOSPHATE PESTICIDE; TRIS (1 CHLORO 2 PROPYL) PHOSPHATE; TRIS (1,3 DICHLORO 2 PROPYL) PHOSPHATE; TRIS (2 CHLOROETHYL) PHOSPHATE; TRIS (2,3 DIBROMOPROPYL) PHOSPHATE; UNCLASSIFIED DRUG; ORGANOPHOSPHATE;

ADULT; ANIMAL BEHAVIOR; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; COMPARATIVE STUDY; CONTROLLED STUDY; DEATH; EMBRYO; ENVIRONMENTAL EXPOSURE; HATCHING; HYDROPHOBICITY; NONHUMAN; STANDARD; SWIMMING; TERATOGENESIS; TISSUE HOMOGENATE; ZEBRA FISH; ABNORMALITIES, DRUG-INDUCED; ANIMAL; ANIMAL EMBRYO; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; EMBRYO DEVELOPMENT; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVOUS SYSTEM; PSYCHOLOGY; SURVIVAL;

DANIO RERIO;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FLAME RETARDANTS; MOLECULAR STRUCTURE; NERVOUS SYSTEM; ORGANOPHOSPHATES; SURVIVAL ANALYSIS; SWIMMING; ZEBRAFISH;

EID: 84922430830     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu194     Document Type: Article

References (42)

1. Ahmed, A. E., Jacob, S., Soliman, S., Ahmed, N., Osman, K., Loh, J. P., and Romero, N. (1993). Whole-body autoradiographic disposition, elimination and placental transport of [14C]tri-ocresyl phosphate in mice. J. Appl. Toxicol. 13, 259-267.
2. Barceló, D., Porte, C., Cid, J., and Albaigés, J. (1990). Determination of organophosphorus compounds in Mediterranean coastal waters and biota samples using gas chromatography with nitrogen-phosphorus and chemical ionization mass spectrometric detection. Int. J. Environ. Anal. Chem. 38, 199-209.
3. Behra, M., Cousin, X., Bertrand, C., Vonesch, J.-L., Biellmann, D., Chatonnet, A., and Strähle, U. (2002). Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo. Nat. Neurosci. 5, 111-118.
4. Behra, M., Etard, C., Cousin, X., and Strähle, U. (2004). The use of zebrafish mutants to identify secondary target effects of acetylcholine esterase inhibitors. Toxicol. Sci. 77, 325-333.
5. Blum, A., and Ames, B. N. (1977). Flame-retardant additives as possible cancer hazards. Science 195, 17-23.
6. Blum, A., Gold, M. D., Ames, B. N., Jones, F. R., Hett, E. A., Dougherty, R. C., Horning, E. C., Dzidic, I., Carroll, D. I., Stillwell, R. N., et al. (1978). Children absorb tris-BP flame retardant from sleepwear: urine contains the mutagenic metabolite, 2,3-dibromopropanol. Science 201, 1020-1023.
7. Bondy, S. C., and Campbell, A. (2005). Developmental neurotoxicology. J. Neurosci. Res. 81, 605-612.
8. Butt, C. M., Congleton, J., Hoffman, K., Fang, M., and Stapleton, H. M. (2014). Metabolites of organophosphate flame retardants and 2-ethylhexyl tetrabromobenzoate in urine from paired mothers and toddlers. Environ. Sci. Technol. 48, 10432-10438.
9. De Esch, C., Slieker, R., Wolterbeek, A., Woutersen, R., and De Groot, D. (2012). Zebrafish as potential model for developmental neurotoxicity testing: a mini review. Neurotoxicol. Teratol. 34, 545-553.
10. Dishaw, L. V., Powers, C. M., Ryde, I. T., Roberts, S. C., Seidler, F. J., Slotkin, T. A., and Stapleton, H. M. (2011). Is the PentaBDE replacement, tris (1,3-dichloro-2-propyl) phosphate (TDCPP), a developmental neurotoxicant? Studies in PC12 cells. Toxicol. Appl. Pharmacol. 256, 281-289.
11. Eaton, D. L., Daroff, R. B., Autrup, H., Bridges, J., Buffler, P., Costa, L. G., Coyle, J., McKhann, G., Mobley, W. C., Nadel, L., et al. (2008). Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit. Rev. Toxicol., 38(Suppl. 2), 1-125.
12. Eddins, D., Cerutti, D., Williams, P., Linney, E., and Levin, E. D. (2010). Zebrafish provide a sensitivemodel of persisting neurobehavioral effects of developmental chlorpyrifos exposure: comparison with nicotine and pilocarpine effects and relationship to dopamine deficits. Neurotoxicol. Teratol. 32, 99-108.
13. Eldefrawi, A. T., Mansour, N. a, Brattsten, L. B., Ahrens, V. D., and Lisk, D. J. (1977). Further toxicologic studies with commercial and candidate flame retardant chemicals. Part II. Bull. Environ. Contam. Toxicol. 17, 720-726.
14. European Union. (2008). Risk Assessment Report: Tris [2-chloro-1-(chloromethyl)ethyl] Phosphate (TDCP), p. 274. European Chemicals Agency.
15. Farhat, A., Crump, D., Chiu, S., Williams, K. L., Letcher, R. J., Gauthier, L. T., and Kennedy, S. W. (2013). In Ovo effects of two organophosphate flame retardants-TCPP and TDCPP-on pipping success, development, mRNA expression, and thyroid hormone levels in chicken embryos. Toxicol. Sci.134, 92-102.
16. Frederiksen, M., Vorkamp, K., Thomsen, M., and Knudsen, L. E. (2009). Human internal and external exposure to PBDEs-a review of levels and sources. Int. J. Hyg. Environ. Health 212, 109-134.
17. Freudenthal, R., and Henrich, R. (2000). Chronic toxicity and carcinogenic potential of tris-(1, 3-dichloro-2-propyl) phosphate in Sprague-Dawley rat. Int. J. Toxicol. 19, 119-125.
18. Gold, M. D., Blum, a, and Ames, B. N. (1978). Another flame retardant, tris-(1,3-dichloro-2-propyl)-phosphate, and its expected metabolites are mutagens. Science 200, 785-787.
19. Goldstone, J. V., McArthur, A. G., Kubota, A., Zanette, J., Parente, T., Jönsson, M. E., Nelson, D. R., and Stegeman, J. J. (2010). Identification and developmental expression of the full complement of Cytochrome P450 genes in Zebrafish. BMC Genomics 11, 643.
20. Harley, K. G., Marks, A. R., Chevrier, J., Bradman, A., Sjödin, A., and Eskenazi, B. (2010). PBDE concentrations in women's serum and fecundability. Environ. Health Perspect. 118, 699-704.
21. Herbstman, J. B., Sjödin, A., Kurzon, M., Lederman, S. a, Jones, R. S., Rauh, V., Needham, L. L., Tang, D., Niedzwiecki, M., Wang, R. Y., et al. (2010). Prenatal exposure to PBDEs and neurodevelopment. Environ. Health Perspect. 118, 712-719.
22. Küster, E. (2005). Cholin-and carboxylesterase activities in developing zebrafish embryos (Danio rerio) and their potential use for insecticide hazard assessment. Aquat. Toxicol. 75, 76-85.
23. Lauder, J. M., and Schambra, U. B. (1999). Morphogenetic roles of acetylcholine. 107, 65-69.
24. Liu, X., Ji, K., Jo, A., Moon, H.-B., and Choi, K. (2013). Effects of TDCPP or TPP on gene transcriptions and hormones of HPG axis, and their consequences on reproduction in adult zebrafish (Danio rerio). Aquat. Toxicol. 134-135, 104-111.
25. Matthews, H., Eustis, S., and Haseman, J. (1993). Toxicity and carcinogenicity of chronic exposure to tris (2-chloroethyl) phosphate. Fundam. Appl. Toxicol. 20, 477-485.
26. McGee, S. P., Cooper, E. M., Stapleton, H. M., and Volz, D. C. (2012). Early zebrafish embryogenesis is susceptible to developmental TDCPP exposure. Environ. Health Perspect. 120, 1585-1591.
27. Meeker, J. D., Cooper, E. M., Stapleton, H. M., and Hauser, R. (2013). Urinary metabolites of organophosphate flame retardants: temporal variability and correlations with house dust concentrations. Environ. Health Perspect. 121, 580-585.
28. Meeker, J. D., Johnson, P. I., Camann, D., and Hauser, R. (2009). Polybrominated diphenyl ether (PBDE) concentrations in house dust are related to hormone levels in men. Sci. Total Environ. 407, 3425-3429.
29. Meeker, J. D., and Stapleton, H. M. (2010). House dust concentrations of organophosphate flame retardants in relation to hormone levels and semen quality parameters. Environ. Health Perspect. 118, 318-323.
30. NTP. (2011). Tris(2,3-dibromopropyl) phosphate. Rep. Carcinog. 12, 428-429.
31. Padilla, S., Hunter, D. L., Padnos, B., Frady, S., and MacPhail, R. C. (2011). Assessing locomotor activity in larval zebrafish: Influence of extrinsic and intrinsic variables. Neurotoxicol. Teratol. 33, 624-630.
32. Shaw, S. D., Blum, A., Weber, R., Kannan, K., Rich, D., Lucas, D., Koshland, C. P., Dobraca, D., Hanson, S., and Birnbaum, L. S. (2010). Halogenated flame retardants: do the fire safety benefits justify the risks? Rev. Environ. Health 25, 261-305.
33. Sledge, D., Yen, J., Morton, T., Dishaw, L., Petro, A., Donerly, S., Linney, E., and Levin, E. D. (2011). Critical duration of exposure for developmental chlorpyrifos-induced neurobehavioral toxicity. Neurotoxicol. Teratol. 33, 742-751.
34. Slotkin, T. A., and Seidler, F. J. (2007). Comparative developmental neurotoxicity of organophosphates in vivo: transcriptional responses of pathways for brain cell development, cell signaling, cytotoxicity and neurotransmitter systems. Brain Res. Bull. 72, 232-274.
35. Slotkin, T. A, Seidler, F. J. F., and Fumagalli, F. (2008). Targeting of neurotrophic factors, their receptors, and signaling pathways in the developmental neurotoxicity of organophosphates in vivo and in vitro. Brain Res. Bull. 76, 424-438.
36. Stapleton, H. M., Klosterhaus, S., Eagle, S., Fuh, J., Meeker, J. D., Blum, A., and Webster, T. F. (2009). Detection of organophosphate flame retardants in furniture foam and U.S. house dust. Environ. Sci. Technol. 43, 7490-7495.
37. Stapleton, H. M., Klosterhaus, S., Keller, A., Ferguson, P. L., Van, S., Cooper, E., Webster, T. F., Blum, A., and van Bergen, S. (2011). Identification of flame retardants in polyurethane foam collected from baby products. Environ. Sci. Technol. 45, 5323-5331.
38. Stapleton, H. M., Sharma, S., Getzinger, G., Ferguson, P. L., Gabriel, M., Webster, T. F., and Blum, A. (2012). Novel and high volume use flame retardants in US couches reflective of the 2005 PentaBDE phase out. Environ. Sci. Technol. 46, 13432-13439.
39. Sundkvist, A. M., Olofsson, U., and Haglund, P. (2010). Organophosphorus flame retardants and plasticizers in marine and fresh water biota and in human milk. J. Environ. Monit. 12, 943-951.
40. US EPA. (2008). Child-Specific Exposure Factors Handbook (Final Report), p. 687. U.S. Environmental Protection Agency,Washington, D.C. Van der Veen, I., and de Boer, J. (2012). Phosphorus flame retardants: properties, production, environmental occurrence, toxicity and analysis. Chemosphere 88, 1119-1153.
41. Wang, Q., Liang, K., Liu, J., Yang, L., Guo, Y., Liu, C., and Zhou, B. (2013). Exposure of zebrafish embryos/larvae to TDCPP alters concentrations of thyroid hormones and transcriptions of genes involved in the hypothalamic-pituitary-thyroid axis. Aquat. Toxicol. 126, 207-213.
42. Yen, J., Donerly, S., Levin, E. D., and Linney, E. A. (2011). Differential acetylcholinesterase inhibition of chlorpyrifos, diazinon and parathion in larval zebrafish. Neurotoxicol. Teratol. 33, 735-741.