Use of an avian hepatocyte assay and the avian toxchip polymerse chain reaction array for testing prioritization of 16 organic flame retardants

Environmental Toxicology and Chemistry

Volumn 33, Issue 3, 2014, Pages 573-582

  Porter, Emily ^a   Crump, Doug ^a   Egloff, Caroline ^a   Chiu, Suzanne ^a   Kennedy, Sean W ^a,b  

^a ENVIRONMENT CANADA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Avian toxicity; Flame retardants; High throughput screening; In vitro toxicology; Transcriptomics

Indexed keywords

AVIAN TOXICITY; FLAME RETARDANTS; HIGH-THROUGHPUT SCREENING; IN VITRO TOXICOLOGY; TRANSCRIPTOMICS;

ANIMALS; BIOLOGICAL ASSAY; CELL SURVIVAL; CHARADRIIFORMES; CHICKENS; EMBRYO, NONMAMMALIAN; FLAME RETARDANTS; HEPATOCYTES; POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECIES SPECIFICITY; TRANSCRIPTOME;

EID: 84894045120     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.2469     Document Type: Article

References (54)

1. Government of Canada. Chemicals Management Plan website. [cited 2013 July 10]. Available from: http://www.chemicalsubstanceschimiques.gc.ca/plan/index-eng.php
2. Stapleton HM, Klosterhaus S, Eagle S, Fuh J, Meeker JD, Blum A, Webster TF. 2009. Detection of organophosphate flame retardants in furniture foam and U.S. house dust. Environ Sci Technol 43:7490-7495.
3. Chen D, Letcher RJ, Chu S. 2012. Determination of non-halogenated, chlorinated and brominated organophosphate flame retardants in herring gull eggs based on liquid chromatography-tandem quadrupole mass spectrometry. J Chromatogr A 1220:169-174.
4. Letcher RJ, Chen D, Chu S, Gauthier LT. 2011. Organophosphate triester flame retardant and phosphoric acid diester metabolite analysis and spatial and temporal trends in herring gulls from the North American Great Lakes. Organohalogen Compound 73:1257-1260.
5. Letcher RJ, Chen D, Backus S, McGoldrick D, Gauthier LT. 2012. Spatio-temporal trends of organophosphate flame retardants in Great Lakes herring gulls, as well as lake trout and their convergent aquatic food webs. Proceedings, SETAC North America 33rd Annual Meeting, Long Beach, CA, USA, November 11-15, 2012, p 6.
6. National Research Council. 2007. Toxicity testing in the 21st century: A vision and a strategy. The National Academies Press, Washington, DC.
7. Schmidt CW. 2009. TOX21: New dimensions of toxicity testing. Environ Health Perspect 117:A348-A353.
8. Villeneuve DL, Garcia-Reyero N. 2011. Vision and strategy: Predictive ecotoxicology in the 21st century. Environ Toxicol Chem 30:1-8.
9. Judson RS, Houck KA, Kavlock RJ, Knudsen TB, Martin MT, Mortensen HM, Reif DM, Rotroff DM, Shah I, Richard AM, Dix DJ. 2010. In vitro screening of environmental chemicals for targeted testing prioritization: The ToxCast project. Environ Health Perspect 118:485-492.
10. Su G, Zhang X, Liu H, Giesy JP, Lam MH, Lam PK, Siddiqui MA, Musarrat J, Al-Khedhairy A, Yu H. 2012. Toxicogenomic mechanisms of 6-HO-BDE-47, 6-MeO-BDE-47, and BDE-47 in E. coli. Environ Sci Technol 46:1185-1191.
11. Hickey NJ, Crump D, Jones SP, Kennedy SW. 2009. Effects of eighteen perfluoroalkyl compounds (PFCs) on mRNA expression in chicken embryo hepatocyte cultures. Toxicol Sci 111:311-320.
12. Arsenault G, Lough A, Marvin C, McAlees A, McCrindle R, MacInnis G, Pleskach K, Potter D, Riddell N, Sverko E, Tittlemier S, Tomy G. 2008. Structure characterization and thermal stabilities of the isomers of the brominated flame retardant 1, 2-dibromo-4-(1, 2-dibromoethyl)cyclohexane. Chemosphere 72:1163-1170.
13. Head JA, O'Brien J, Kennedy SW. 2006. Exposure to 3, 3', 4, 4', 5-pentachlorobiphenyl during embryonic development has a minimal effect on the cytochrome P4501A response to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in cultured chicken embryo hepatocytes. Environ Toxicol Chem 25:2981-2989.
14. Crump D, Chiu S, Kennedy SW. 2012. Effects of tris(1, 3-dichloro-2-propyl) phosphate and tris(1-chloropropyl) phosphate on cytotoxicity and mRNA expression in primary cultures of avian hepatocytes and neuronal cells. Toxicol Sci 126:140-148.
15. Head JA, Kennedy SW. 2007. Differential expression, induction, and stability of CYP1A4 and CYP1A5 mRNA in chicken and herring gull embryo hepatocytes. Comp Biochem Phys C 145:617-624.
16. Crump D, Chiu S, Egloff C, Kennedy SW. 2008. Effects of hexabromocyclododecane and polybrominated diphenyl ethers on mRNA expression in chicken (Gallus domesticus) hepatocytes. Toxicol Sci 106:479-487.
17. Crump D, Egloff C, Chiu S, Letcher RJ, Chu S, Kennedy SW. 2010. Pipping success, isomer-specific accumulation, and hepatic mRNA expression in chicken embryos exposed to HBCD. Toxicol Sci 115:492-500.
18. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108.
19. Sundkvist AM, Olofsson U, Haglund P. 2010. Organophosphorus flame retardants and plasticizers in marine and fresh water biota and in human milk. J Environ Monit 12:943-951.
20. Gauthier LT, Potter D, Hebert CE, Letcher RJ. 2009. Temporal trends and spatial distribution of non-polybrominated diphenyl ether flame retardants in the eggs of colonial populations of Great Lakes herring gulls. Environ Sci Technol 43:312-317.
21. Handschin C, Podvinec M, Stöckli J, Hoffmann K, Meyer UA. 2001. Conservation of signaling pathways of xenobiotic-sensing orphan nuclear receptors, chicken xenobiotic receptor, constitutive androstane receptor, and pregnane X receptor, from birds to humans. Mol Endocrinol 15:1571-1585.
22. Egloff C, Crump D, Chiu S, Manning G, McLaren KK, Cassone CG, Letcher RJ, Gauthier LT, Kennedy SW. 2011. In vitro and in ovo effects of four brominated flame retardants on toxicity and hepatic mRNA expression in chicken embryos. Toxicol Lett 207:25-33.
23. Farhat A, Crump D, Chiu S, Williams KL, Letcher RJ, Gauthier LT, Kennedy SW. 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.
24. Denison MS, Nagy SR. 2003. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Ann Rev Pharmacol Toxicol 43:309-334.
25. Farmahin R, Wu D, Crump D, Hervé JC, Jones SP, Hahn ME, Karchner SI, Giesy JP, Bursian SJ, Zwiernik MJ, Kennedy SW. 2012. Sequence and in vitro function of chicken, ring-necked pheasant, and Japanese quail AHR1 predict in vivo sensitivity to dioxins. Environ Sci Technol 46:2967-2975.
26. Maglich JM, Stoltz CM, Goodwin B, Hawkins-Brown D, Moore JT, Kliewer SA. 2002. Nuclear pregnane x receptor and constitutive androstane receptor regulate overlapping but distinct sets of genes involved in xenobiotic detoxification. Mol Pharmacol 62:638-646.
27. Germer S, Piersma AH, van der Ven L, Kamyschnikow A, Fery Y, Schmitz HJ, Schrenk D. 2006. Subacute effects of the brominated flame retardants hexabromocyclododecane and tetrabromobisphenol A on hepatic cytochrome P450 levels in rats. Toxicology 218:229-236.
28. Mackenzie PI, Gregory PA, Gardner-Stephen DA, Lewinsky RH, Jorgensen BR, Nishiyama T, Xie W, Radominska-Pandya A. 2003. Regulation of UDP glucuronosyltransferase genes. Curr Drug Metab 4:249-257.
29. Richardson VM, Staskal DF, Ross DG, Diliberto JJ, DeVito MJ, Birnbaum LS. 2008. Possible mechanisms of thyroid hormone disruption in mice by BDE47: a major polybrominated diphenyl ether congener. Toxicol Appl Pharmacol 226:244-250.
30. Szabo DT, Richardson VM, Ross DG, Diliberto JJ, Kodavanti PR, Birnbaum LS. 2009. Effects of perinatal PBDE exposure on hepatic phase I, phase II, phase III, and deiodinase 1 gene expression involved in thyroid hormone metabolism in male rat pups. Toxicol Sci 107:27-39.
31. van der Ven LT, Verhoef A, van de Kuil T, Slob W, Leonards PE, Visser TJ, Hamers T, Herlin M, Håkansson H, Olausson H, Piersma AH, Vos JG. 2006. A 28-day oral dose toxicity study enhanced to detect endocrine effects of hexabromocyclododecane in Wistar rats. Toxicol Sci 94:281-292.
32. Maglich JM, Watson J, McMillen PJ, Goodwin B, Willson TM, Moore JT. 2004. The nuclear receptor CAR is a regulator of thyroid hormone metabolism during caloric restriction. J Biol Chem 279:19832-19838.
33. McNabb FM. 2007. The hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction. Crit Rev Toxicol 37:163-193.
34. Cassone CG, Vongphachan V, Chiu S, Williams KL, Letcher RJ, Pelletier E, Crump D, Kennedy SW. 2012. In ovo effects of perfluorohexane sulfonate and perfluorohexanoate on pipping success, development, mRNA expression, and thyroid hormone levels in chicken embryos. Toxicol Sci 127:216-224.
35. Gould JC, Cooper KR, Scanes CG. 1999. Effects of polychlorinated biphenyls on thyroid hormones and liver type I monodeiodinase in the chick embryo. Ecotox Environ Safe 43:195-203.
36. Leonard JL, Visser TJ. 1986. Biochemistry of deiodination. In Hennemann G, ed, Thyroid Hormone Metabolism. Marcel Dekker, New York, NY, USA, pp 189-229.
37. Freeman TB, McNabb FM. 1991. Hepatic 5'-deiodinase activity of Japanese quail using reverse-T3 as substrate: Assay validation, characterization, and developmental studies. J Exp Zool 258:212-220.
38. Organization for Economic Co-operation and Development. 2006. Detailed review paper on thyroid hormone disruption assays. Series on Testing and Assessment, No. 57. Battelle, Columbus, OH, USA.
39. Scanes CG. 2009. Perspectives on the endocrinology of poultry growth and metabolism. Gen Comp Endocrinol 163:24-32.
40. LaFave LT, Augustin LB, Mariash CN. 2006. S14: Insights from knockout mice. Endocrinology 147:4044-4047.
41. Cantón RF, Peijnenburg AA, Hoogenboom RL, Piersma AH, van der Ven LT, van den Berg M, Heneweer M. 2008. Subacute effects of hexabromocyclododecane (HBCD) on hepatic gene expression profiles in rats. Toxicol Appl Pharmacol 231:267-272.
42. Achouri Y, Hegarty BD, Allanic D, Bécard D, Hainault I, Ferré P, Foufelle F. 2005. Long chain fatty acyl-CoA synthetase 5 expression is induced by insulin and glucose: Involvement of sterol regulatory element-binding protein-1c. Biochimie 87:1149-1155.
43. Soupene E, Kuypers FA. 2008. Mammalian long-chain acyl-CoA synthetases. Exp Biol Med 233:507-521.
44. O'Brien JM, Austin AJ, Williams A, Yauk CL, Crump D, Kennedy SW. 2011. Technical grade PFOS alters the expression of more transcripts in cultured chicken embryonic hepatocytes than linear PFOS. Environ Toxicol Chem 30:2846-2859.
45. Liu X, Jo A, Moon HB, 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.
46. Liu X, Ji K, Choi K. 2012. Endocrine disruption potentials of organophosphate flame retardants and related mechanisms in H295R and MVLN cell lines and in zebrafish. Aquat Toxicol 114/115:173-181.
47. Liu C, Wang Q, Liang K, Liu J, Zhou B, Zhang X, Liu H, Giesy JP, Yu H. 2013. Effects of tris(1, 3-dichloro-2-propyl) phosphate and triphenyl phosphate on receptor-associated mRNA expression in zebrafish embryos/larvae. Aquat Toxicol 128/129:147-157.
48. Andrews GK. 2000. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 59:95-104.
49. Coyle P, Philcox JC, Carey LC, Rofe AM. 2002. Metallothionein: The multipurpose protein. Cell Mol Life Sci 59:627-647.
50. Arnér ES, Holmgren A. 2000. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102-6109.
51. Collet JF, Messens J. 2010. Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 13:1205-1216.
52. Fernie KJ, Shutt JL, Mayne G, Hoffman D, Letcher RJ, Drouillard KG, Ritchie IJ. 2005. Exposure to polybrominated diphenyl ethers (PBDEs): Changes in thyroid, vitamin A, glutathione homeostasis, and oxidative stress in American kestrels (Falco sparverius). Toxicol Sci 88:375-383.
53. Dishaw LV, Powers CM, Ryde IT, Roberts SC, Seidler FJ, Slotkin TA, Stapleton HM. 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.
54. Shi H, Wang X, Luo Y, Su Y. 2005. Electron paramagnetic resonance evidence of hydroxyl radical generation and oxidative damage induced by tetrabromobisphenol A in Carassius auratus. Aquat Toxicol 74:365-371.