Developmental exposure to the organophosphorus flame retardant tris(1,3-dichloro-2-propyl) phosphate: Estrogenic activity, endocrine disruption and reproductive effects on zebrafish

Aquatic Toxicology

Volumn 160, Issue , 2015, Pages 163-171

  Wang, Qiangwei ^a,b   Lam, James C W ^c   Han, Jian ^c   Wang, Xianfeng ^a   Guo, Yongyong ^a   Lam, Paul K S ^c   Zhou, Bingsheng ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c CITY UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Bioconcentration; Endocrine disruption; Organophosphate flame retardant; Reproduction; Steroid hormone; TDCPP; Zebrafish

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; 3BETA HYDROXY DELTA5 STEROID DEHYDROGENASE; ACTIVIN RECEPTOR 2; AROMATASE; CYTOCHROME P450 17; ESTROGEN RECEPTOR BETA; FLAME RETARDANT; FOLLITROPIN BETA SUBUNIT; GONADORELIN; LUTEINIZING HORMONE BETA SUBUNIT; LUTEINIZING HORMONE RECEPTOR; MESSENGER RNA; ORGANOPHOSPHORUS COMPOUND; SEX HORMONE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; THYROTROPIN RECEPTOR; TRIS [1,3 DICHLORO 2 PROPYL]PHOSPHATE; UNCLASSIFIED DRUG; VITELLOGENIN; ENDOCRINE DISRUPTOR; ORGANOPHOSPHATE; TRIS(2,3-DIBROMOPROPYL)PHOSPHATE; WATER POLLUTANT;

BIOACCUMULATION; CONCENTRATION (COMPOSITION); CYPRINID; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; FECUNDITY; HISTOLOGY; HORMONE; ORGANOPHOSPHATE; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENDOCRINE DISEASE; ENVIRONMENTAL EXPOSURE; ESTROGEN ACTIVITY; FEMALE; GAMETOGENESIS; GENETIC TRANSCRIPTION; GONAD DEVELOPMENT; HISTOPATHOLOGY; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LIVER; MALE; NONHUMAN; OOCYTE MATURATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTIVE TOXICITY; SEMEN ABNORMALITY; STEROIDOGENESIS; SURVIVAL RATE; UPREGULATION; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; BLOOD; CHEMISTRY; DRUG EFFECTS; ENDOCRINE SYSTEM; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; GONAD; HYPOPHYSIS; HYPOTHALAMUS; METABOLISM; TOXICITY; WATER POLLUTANT;

DANIO RERIO;

ANIMALS; EMBRYO, NONMAMMALIAN; ENDOCRINE DISRUPTORS; ENDOCRINE SYSTEM; FEMALE; FERTILITY; FLAME RETARDANTS; GENE EXPRESSION REGULATION; GONADAL STEROID HORMONES; GONADS; HYPOTHALAMUS; LIVER; MALE; ORGANOPHOSPHATES; PITUITARY GLAND; VITELLOGENINS; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 84921831636     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2015.01.014     Document Type: Article

References (57)

1. Andersson E., Nijenhuis W., Male R., Swanson P., Bogerd J., Taranger G.L., Schulz R.W. Pharmacological characterization: localization and quantification of expression of gonadotropin receptors in Atlantic salmon (Salmo salar L.) ovaries. Gen. Comp. Endocrinol. 2009, 163:329-339.
2. Ankley G.T., Jensen K.M., Durhan E.J., Makynen E.A., Butterworth B.C., Kahl M.D., Villeneuve D.L., Linnum A., Gray L.E., Cardon M. Effects of two fungicides with multiple modes of action on reproductive endocrine function in the fathead minnow (Pimephales promelas). Toxicol. Sci. 2005, 86:300-308.
3. Barni M.F., Gonzalez M., Miglioranza K.S. Assessment of persistent organic pollutants accumulation and lipid peroxidation in two reproductive stages of wild silverside (Odontesthes bonariensis). Ecotoxicol. Environ. Saf. 2014, 99:45-53.
4. Betts K.S. Exposure to TDCPP appears widespread. Environ. Health Perspect. 2013, 121:A150.
5. Blüthgen N., Zucchi S., Fent K. Effects of the UV filter benzophenone-3 (oxybenzone) at low concentrations in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 2012, 263:184-194.
6. Cao S., Zeng X., Song H., Li H., Yu Z., Sheng G., Fu J. Levels and distributions of organophosphate flame retardants and plasticizers in sediment from Taihu Lake, China. Environ. Toxicol. Chem. 2012, 31:1478-1484.
7. Chen L., Yu K., Huang C., Yu L., Zhu B., Lam P., Lam J.C., Zhou B. Prenatal transfer of polybrominated diphenyl ethers (PBDEs) results in developmental neurotoxicity in zebrafish larvae. Environ. Sci. Technol. 2012, 46:9727-9734.
8. Clelland E., Peng C. Endocrine/paracrine control of zebrafish ovarian development. Mol. Cell. Endocrinol. 2009, 312:42-52.
9. Corrales J., Thornton C., White M., Willett K.L. Multigenerational effects of benzo[a]pyrene exposure on survival and developmental deformities in zebrafish larvae. Aquat. Toxicol. 2014, 148:16-26.
10. Devlin R.H., Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 2002, 208:191-364.
11. DiMuccio T., Mukai S.T., Clelland E., Kohli G., Cuartero M., Wu T., Peng C. Cloning of a second form of activin-βA cDNA and regulation of activin-βA subunits and activin type II receptor mRNA expression by gonadotropin in the zebrafish ovary. Gen. Comp. Endocrinol. 2005, 143:287-299.
12. Dishaw L.V., Powers C.M., Ryde I.T., Roberts S.C., Seidler F.J., Slotkin T.A., Stapleton H.M. Is the PentaBDE replacement, tris(1,3-dichloro-2-propyl) phosphate (TDCPP), a developmental neurotoxicant? Studies in PC12 cells. Toxicol. Appl. Pharmacol. 2011, 256:281-289.
13. Filby A.L., Thorpe K.L., Maack G., Tyler C.R. Gene expression profiles revealing the mechanisms of anti-androgen-and estrogen-induced feminization in fish. Aquat. Toxicol. 2007, 81:219-231.
14. Folmar L.C., Denslow N.D., Rao V., Chow M., Crain D.A., Enblom J., Marcino J., Guillette L.J. Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ. Health Perspect. 1996, 104:1096-1101.
15. Fu J., Han J., Zhou B., Gong Z., Santos E.M., Huo X., Zheng W., Liu H., Yu H., Liu C. Toxicogenomic responses of zebrafish embryos/larvae to tris(1:3-dichloro-2-propyl) phosphate (TDCPP) reveal possible molecular mechanisms of developmental toxicity. Environ. Sci. Technol. 2013, 47:10574-10582.
16. Gracia T., Hilscherova K., Jones P.D., Newsted J.L., Higley E.B., Zhang X., Hecker M., Murphy M.B., Yu R.M., Lam P.K., Wu R.S., Giesy J.P. Modulation of steroidogenic gene expression and hormone production of H295R cells by pharmaceuticals and other environmentally active compounds. Toxicol. Appl. Pharmacol. 2007, 225:142-153.
17. Harries J.E., Sheahan D.A., Jobling S., Matthiessen P., Neall M., Sumpter J.P., Taylor T., Zaman N. Estrogenic activity in five United Kingdom rivers detected by measurement of vitellogenesis in caged male trout. Environ. Toxicol. Chem. 1997, 16:534-542.
18. Henry T.B., McPherson J.T., Rogers E.D., Heah T.P., Hawkins S.A., Layton A.C., Sayler G.S. Changes in the relative expression pattern of multiple vitellogenin genes in adult male and larval zebrafish exposed to exogenous estrogens. Comp. Biochem. Physiol. 2009, 154A:119-126.
19. Hu M.Y., Li J., Zhang B.B., Cui Q.L., Wei S., Yu H.X. Regional distribution of halogenated organophosphate flame retardants in seawater samples from three coastal cities in China. Mar. Pollut. Bull. 2014, 86:569-574.
20. Ji H., Li X., Wang Q., Ning Y. Differential principal component analysis of ChIP-seq. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6789-6794.
21. Kausch U., Alberti M., Haindl S., Budczies J., Hock B. Biomarkers for exposure to estrogenic compounds: gene expression analysis in zebrafish (Danio rerio). Environ. Toxicol. 2008, 23:15-24.
22. Kidd K.A., Blanchfield P.J., Mills K.H., Palace V.P., Evans R.E., Lazorchak J.M., Flick R.W. Collapse of a fish population after exposure to a synthetic estrogen. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8897-8901.
23. Kojima H., Takeuchi S., Itoh T., Iida M., Kobayashi S., Yoshida T. In vitro endocrine disruption potential of organophosphate flame retardants via human nuclear receptors. Toxicology 2013, 314:76-83.
24. Kumar R.S., Ijiri S., Trant J.M. Molecular biology of the channel catfish gonadotropin receptors: 2. Complementary DNA cloning, functional expression, and seasonal gene expression of the follicle-stimulating hormone receptor. Biol. Reprod. 2001, 65:710-717.
25. Leal M.C., Cardoso E.R., Nobrega R.H., Batlouni S.R., Bogerd J., Franca L.R., Schulz R.W. Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol. Reprod. 2009, 81:177-187.
26. Liu C.S., Yu L.Q., Deng J., Lam P.K., Wu R.S., Zhou B.S. Waterborne exposure to fluorotelomer alcohol 6:2 FTOH alters plasma sex hormone and gene transcription in the hypothalamic-pituitary-gonadal (HPG) axis of zebrafish. Aquat. Toxicol. 2009, 93:131-137.
27. Liu X., Ji K., Choi K. Endocrine disruption potentials of organophosphate flame retardants and related mechanisms in H295R and MVLN cell lines and in zebrafish. Aquat. Toxicol. 2012, 114-115:173-181.
28. Liu C.S., Wang Q.W., Liang K., Liu J.F., Zhou B.S., Zhang X.W., Liu H.L., Giesy J.P., Yu H.X. Effects of tris(1,3-dichloro-2-propyl) phosphate and triphenyl phosphate on receptor-associated mRNA expression in zebrafish embryos/larvae. Aquat. Toxicol. 2013, 128:147-157.
29. Liu X., Ji K., Jo A., Moon H.B., Choi K. 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. 2013, 134:104-111.
30. Lyche J.L., Grześ I.M., Karlsson C., Nourizadeh-Lillabadi R., Berg V., Kristoffersen A.B., Skåre J.U., Alestrøm P., Ropstad E. Parental exposure to natural mixtures of POPs reduced embryo production and altered gene transcription in zebrafish embryos. Aquat. Toxicol. 2013, 126:424-434.
31. Ma Y.B., Han J., Guo Y.Y., Lam P.K., Wu R.S., Giesy J.P., Zhang X.W., Zhou B.S. Disruption of endocrine function in in vitro H295R cell-based and in in vivo assay in zebrafish by 2,4-dichlorophenol. Aquat. Toxicol. 2012, 106:173-181.
32. Ma Y., Cui K., Zeng F., Wen J., Liu H., Zhu F., Ouyang G., Luan T., Zeng Z. Microwave-assisted extraction combined with gel permeation chromatography and silica gel cleanup followed by gas chromatography-mass spectrometry for the determination of organophosphorus flame retardants and plasticizers in biological samples. Anal. Chim. Acta 2013, 786:47-53.
33. Marklund A., Andersson B., Haglund P. Organophosphorus flame retardants and plasticizers in Swedish sewage treatment plants. Environ. Sci. Technol. 2005, 39:7423-7429.
34. Mcgee S.P., Cooper E.M., Stapleton H.M., Volz D.C. Early zebrafish embryogenesis is susceptible to developmental TDCPP exposure. Environ. Health Perspect. 2012, 120:1585-1591.
35. Nagahama Y. Endocrine regulation of gametogenesis in fish. Int. J. Dev. Biol. 1994, 38:217-229.
36. Panter G.H., Thompson R.S., Sumpter J.P. Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural oestrogens oestradiol and oestrone. Aquat. Toxicol. 1998, 42:243-253.
37. Peters R.E., Courtenay S.C., Cagampan S., Hewitt M.L., MacLatchy D.L. Effects on reproductive potential and endocrine status in the mummichog (Fundulus heteroclitus) after exposure to 17α-ethynylestradiol in a short-term reproductive bioassay. Aquat. Toxicol. 2007, 85:154-166.
38. Shang E.H., Yu R.M., Wu R.S. Hypoxia affects sex differentiation and development: leading to a male-dominated population in zebrafish (Danio rerio). Environ. Sci. Technol. 2006, 40:3118-3122.
39. Shaw S.D., Blum A., Weber R., Kannan K., Rich D., Lucas D., Koshland C.P., Dobraca D., Hanson S., Birnbaum L.S. Halogenated flame retardants: do the fire safety benefits justify the risks?. Rev. Environ. Health 2010, 25:261-305.
40. Stapleton H.M., Klosterhaus S., Eagle S., Fuh J., Meeker J.D., Blum A., Webster T.F. Detection of organophosphate flame retardants in furniture foam and U.S. house dust. Environ. Sci. Technol. 2009, 43:7490-7495.
41. Stapleton H.M., Klosterhaus S., Keller A., Ferguson P.L., van Bergen S., Cooper E., Webster T.F., Blum A. Identification of flame retardants in polyurethane foam collected from baby products. Environ. Sci. Technol. 2011, 45:5323-5331.
42. Sumpter J.P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 1995, 103:173-178.
43. Sundkvist A.M., Olofsson U., Haglund P. Organophosphorus flame retardants and plasticizers in marine and fresh water biota and in human milk. J. Environ. Monit. 2010, 12:943-951.
44. Office of Environmental Health Hazard Assessment's (OEHHA), Evidence on the Carcinogenicity of Tris(1,3-Dichloro-2-Propyl) Phosphate. Office ofEnvironmental Health Hazard Assessment's (OEHHA) http://oehha.ca.gov/prop65/hazardident/pdfzip/TDCPP070811.pdf.
45. Thompson E.D., Mayer G.D., Walsh P.J., Hogstrand C. Sexual maturation and reproductive zinc physiology in the female squirrelfish. J. Exp. Biol. 2002, 205:3367-3376.
46. Van der Veen I., de Boer J. Phosphorus flame retardants: properties, production, environmental occurrence, toxicity and analysis. Chemosphere 2012, 88:1119-1153.
47. Venier M., Dove A., Romanak K., Backus S., Hites R. Flame retardants and legacy chemicals in Great Lakes' water. Environ. Sci. Technol. 2014, 48:9563-9572.
48. Villeneuve D.L., Garcia-Reyero N., Escalon B.L., Jensen K.M., Cavallin J.E., Makynen E.A., Durhan E.J., Kahl M.D., Thomas L.M., Perkins E.J., Ankley G.T. Ecotoxicogenomics to support ecological risk assessment: a case study with bisphenol A in fish. Environ. Sci. Technol. 2012, 46:51-59.
49. Wang X., Liu J., Yin Y. Development of an ultra-high-performance liquid chromatography-tandem mass spectrometry method for high throughput determination of organophosphorus flame retardants in environmental water. J. Chromatogr. A 2011, 1218:6705-6711.
50. Wang Q.W., Liang K., Liu J.F., Yang L.H., Guo Y.Y., Liu C.S., Zhou B.S. 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. 2013, 126:207-213.
51. Wang Q.W., Lam J.C., Man Y.C., Lai N.L., Kwok K.Y., Guo Y.Y., Lam P.K., Zhou B.S. Bioconcentration metabolism and neurotoxicity of the organophorous flame retardant 1,3-dichloro 2-propyl phosphate (TDCPP) to zebrafish. Aquat. Toxicol. 2015, 158:108-115.
52. Yang F., Ding J., Huang W., Xie W., Liu W. Particle size-specific distributions and preliminary exposure assessments of organophosphate flame retardants in office air particulate matter. Environ. Sci. Technol. 2014, 48:63-70.
53. Ye T., Kang M., Huang Q., Fang C., Chen Y., Shen H., Dong S. Exposure to DEHP and MEHP from hatching to adulthood causes reproductive dysfunction and endocrine disruption in marine medaka (Oryzias melastigma). Aquat. Toxicol. 2014, 146:115-126.
54. Yu L.Q., Lam J.C.W., Guo Y.Y., Wu R.S., Lam P.K., Zhou B.S. Parental transfer of polybrominated diphenyl ethers (PBDEs) and thyroid endocrine disruption in zebrafish. Environ. Sci. Technol. 2011, 45:10652-10659.
55. Yu L.Q., Liu C.S., Chen Q., Zhou B.S. Endocrine disruption and reproduction impairment in zebrafish after long-term exposure to DE-71. Environ. Toxicol. Chem. 2014, 33:1354-1362.
56. Zeng X., He L., Cao S., Ma S., Yu Z., Gui H., Sheng G., Fu J. Occurrence and distribution of organophosphate flame retardants/plasticizers in wastewater treatment plant sludges from the Pearl River Delta, China. Environ. Toxicol. Chem. 2014, 33:1720-1725.
57. Zhang Q., Lu M., Dong X., Wang C., Zhang C., Liu W., Zhao M. Potential estrogenic effects of phosphorus-containing flame retardants. Environ. Sci. Technol. 2014, 48:6995-7001.