Tris(1,3-dichloro-2-propyl) phosphate perturbs the expression of genes involved in immune response and lipid and steroid metabolism in chicken embryos

Toxicology and Applied Pharmacology

Volumn 275, Issue 2, 2014, Pages 104-112

  Farhat, Amani ^a,b   Buick, Julie K ^c   Williams, Andrew ^c   Yauk, Carole L ^c   O'Brien, Jason M ^c   Crump, Doug ^b   Williams, Kim L ^b   Chiu, Suzanne ^b   Kennedy, Sean W ^a,b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b ENVIRONMENT CANADA   (Canada)

^c HEALTH CANADA   (Canada)

Author keywords

Chicken; Lipid metabolism; MRNA expression microarray; Organophosphate flame retardant; Steroid metabolism; Tris(1,3 dichloro 2 propyl) phosphate

Indexed keywords

CHICKEN; LIPID METABOLISM; MRNA EXPRESSION MICROARRAY; ORGANOPHOSPHATE FLAME RETARDANT; STEROID METABOLISM; TRIS(1,3-DICHLORO-2-PROPYL) PHOSPHATE;

ANIMALS; APOLIPOPROTEINS E; BILE ACIDS AND SALTS; CHICK EMBRYO; CHOLESTEROL; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE NUCLEAR FACTOR 4; IMMUNE SYSTEM; LIPID METABOLISM; LIVER; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGANOPHOSPHORUS COMPOUNDS; PPAR ALPHA; RNA, MESSENGER; STEROIDS; THYROXINE;

EID: 84894038077     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.12.020     Document Type: Article

References (58)

1. Babich M.A. CPSC Staff Preliminary Risk Assessment of Flame Retardant (FR) Chemicals in Upholstered Furniture Foam 2006, US Consumer Product Safety Commission, 46-Bethesda, MD, 20814.
2. Bar-Shira E., Friedman A. Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick. Dev. Comp. Immunol. 2006, 30(10):930-941.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 1995, 57:289-300.
4. Carignan C., McClean M.D., Cooper E.M., Watkins D.J., Fraser A.J., Heiger-Bernays W., Stapleton H.M., Webster T.F. Predictors of tris(1,3-dichloro-2-propyl) phosphate metabolite in the urine of office workers. Environ. Int. 2013, 55:56-61.
5. Chang Q., Chen J., Beezhold K.J., Castranova V., Shi X., Chen F. JNK1 activation predicts the prognostic outcome of the human hepatocellular carcinoma. Mol. Cancer 2009, 8(64).
6. Chen D., Letcher R.J., Chu S. 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 2012, 1220:169-174.
7. Cheng J.H., She H.Y., Han Y.P., Wang J.H., Xiong S.G., Asahina K., Tsukamoto H. Wnt antagonism inhibits hepatic stellate cell activation and liver fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294(1):G39-G49.
8. Chisholm J.W., Dolphin P.J. Abnormal lipoproteins in the ANIT-treated rat: a transient and reversible animal model of intrahepatic cholestasis. J. Lipid Res. 1996, 37(5):1086-1098.
9. Crestani M., De Fabiani E., Caruso D., Mitro N., Gilardi F., Chacon A.B.V., Patelli R., Godio C., Galli G. LXR (liver X receptor) and HNF-4 (hepatocyte nuclear factor-4): key regulators in reverse cholesterol transport. Biochem. Soc. Trans. 2004, 32:92-96.
10. Crump D., Chiu S., Kennedy S.W. Effects of tris(1,3-dichloro-2-propyl) phosphate and tis(1-chloropropyl) phosphate on cytotoxicity and mRNA expression in primary cultures of avian hepatocytes and neural cells. Toxicol. Sci. 2012, 126(1):140-148.
11. Cui X., Hwang J.T., Qiu J., Blades N.J., Churchill G.A. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 2005, 6(1):59-75.
12. Diazyme Total Bile Acids Test and Clinical Diagnosis (Updated 2012. Accessed 22-11-2013). http://www.diazyme.com/websites/diazyme/images/products/pdf/TBA%20brochure%20read.pdf.
13. 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(3):281-289.
14. European Union European Union risk assessment report: tris[2-chloro-1-(chloromrthyl)ethyl] phosphate (TDCP). CAS No. 13674-87-8, EINECS No. 237-159-2 2008, European Communities, Luxembourg.
15. Farhat A., Crump D., Chiu S., Williams K.L., Letcher R.J., Gauthier L.T., Kennedy S.W. 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. 2013, 134(1):92-102.
16. Fickert P., Stoeger U., Marschall H.U., Weiglein A.H., Tsybrovskyy O., Jaeschke H., Zatloukal K., Denk H., Trauner M. A new xenobiotic-induced mouse model of sclerosing cholangitis and biliary fibrosis. Am. J. Pathol. 2007, 171(2):525-536.
17. Freudenthal R.I., Henrich R.T. Chronic toxicity and carcenogenic potential of tris-(1,3-dichloro-2-propyl) phosphate in Sprague-Dawley rat. Int. J. Toxicol. 2000, 19(2):119-125.
18. Goudriaan J.R., Dahlmans V.E.H., Teusink B., Ouwens D.M., Febbraio M., Maassen J.A., Romijn J.A., Havekes L.M., Voshol P.J. CD36 deficiency increases insulin sensitivity in muscle, but induces insulin resistance in the liver in mice. J. Lipid Res. 2003, 44(12):2270-2277.
19. Griffitts J., Tesiram Y., Reid G., Saunders D., Floyd R., Towner R. In vivo MRS assessment of altered fatty acyl unsaturation in liver tumor formation of a TGF alpha/c-myc transgenic mouse model. J. Lipid Res. 2009, 50(4):611-622.
20. Hayes J.D., Pulford D.J. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 1995, 30(6):445-600.
21. Hays T., Rusyn I., Burns A.M., Kennett M.J., Ward J.M., Gonzalez F.J., Peters J.M. Role of peroxisome proliferator-activated receptor-alpha (PPAR alpha) in bezafibrate-induced hepatocarcinogenesis and cholestasis. Carcinogenesis 2005, 26(1):219-227.
22. Heikkila M., Peltoketo H., Leppaluoto J., Ilves M., Vuolteenaho O., Vainio S. Wnt-4 deficiency alters mouse adrenal cortex function, reducing aldosterone production. Endocrinology 2002, 143(11):4358-4365.
23. Jordan B.K., Shen J.H.C., Olaso R., Ingraham H.A., Vilain E. Wnt4 overexpression disrupts normal testicular vasculature and inhibits testosterone synthesis by repressing steroidogenic factor 1/beta-catenin synergy. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(19):10866-10871.
24. Kerr M.K. Design considerations for efficient and effective microarray studies. Biometrics 2003, 59(4):822-828.
25. Kim N.D., Moon J.O., Slitt A.L., Copple B.L. Early growth response factor-1 is critical for cholestatic liver injury. Toxicol. Sci. 2006, 90(2):586-595.
26. Lee S.L., Sadovsky Y., Swirnoff A.H., Polish J.A., Goda P., Gavrilina G., Milbrandt J. Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGFI-A (Egr-1). Science 1996, 273(5279):1219-1221.
27. Leonards P., Steindal E.H., van der Veen I., Berg V., Bustnes J.O., van Leeuwen S. Screening of organophosphor flame retardants 2010. SPFO-Report 1091/2011. TA-2786/2011 2011, Klima-og Forurensnings-Direktoratet, Norway.
28. 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.
29. Luster M.I., Dean J.H., Boorman G.A., Archer D.L., Lauer L., Lawson L.D., Moore J.A., Wilson R.E. The effects of orthophenylphenol, tris(2,3-dichloropropyl) phosphate, and cyclophosphamide on the immune-system and host susceptibility of mice following sub-chronic exposure. Toxicol. Appl. Pharmacol. 1981, 58(2):252-261.
30. Lynn R.K., Wong K., Garvie-Gould C., Kennish J.M. Disposition of the flame retardant, tris(1,3-dichloro-2-propyl) phosphate, in the rat. Drug Metab. Dispos. 1981, 9(5):434-441.
31. Mahley R.W., Ji Z.S. Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E. J. Lipid Res. 1999, 40(1):1-16.
32. 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(11):1585-1591.
33. McMullen M.R., Pritchard M.T., Wang Q.F., Millward C.A., Croniger C.M., Nagy L.E. Early growth response-1 transcription factor is essential for ethanol-induced fatty liver injury in mice. Gastroenterology 2005, 128(7):2066-2076.
34. McNabb F.M. The hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction. Crit. Rev. Toxicol. 2007, 37(1-2):163-193.
35. McPherson A., Thorpe B., Blake A. Brominated Flame Retardants in Dust on Computers: The Case for Safer Chemicals and Better, Computer Design 2004.
36. Meade K.G., Higgs R., Lloyd A.T., Giles S., O'Farrelly C. Differential antimicrobial peptide gene expression patterns during early chicken embryological development. Dev. Comp. Immunol. 2009, 33(4):516-524.
37. Meeker J.D., Stapleton H.M. House dust concentrations of organophosphate flame retardants in relation to hormone levels and semen quality parameters. Environ. Health Perspect. 2010, 118(3):318-323.
38. Michalik L., Auwerx J., Berger J.P., Chatterjee V.K., Glass C.K., Gonzalez F.J., Grimaldi P.A., Kadowaki T., Lazar M.A., O'Rahilly S., Palmer C.N.A., Plutzky J., Reddy J.K., Spiegelman B.M., Staels B., Wahli W. International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacol. Rev. 2006, 58(4):726-741.
39. Modica S., Murzilli S., Moschetta A. Characterizing bile acid and lipid metabolism in the liver and gastrointestinal tract of mice. Curr. Protoc. Mouse Biol. 2011, 1:289-321.
40. Modica S., Petruzzelli M., Bellafante E., Murzilli S., Salvatore L., Celli N., Di T.G., Palasciano G., Moustafa T., Halilbasic E., Trauner M., Moschetta A. Selective activation of nuclear bile acid receptor FXR in the intestine protects mice against cholestasis. Gastroenterology 2012, 142(2):355-365.
41. Nebert D.W., Gonzalez F.J. P450 genes - structure, evolution, and regulation. Annu. Rev. Biochem. 1987, 56:945-993.
42. Nomeir A.A., Kato S., Matthews H.B. The metabolism and disposition of tris(1,3-dichloro-2-propyl) phosphate (Fyrol FR-2) in the rat. Toxicol. Appl. Pharmacol. 1981, 57(3):401-413.
43. OEHHA A chemical listed effective October 28, 2011 as known to the State of California to cause cancer tris(1,3-dichloro-propyl) phosphate (TDCPP) (Filed 28-10-2011a. Accessed 20-10-2012. CAS NO. 13674-87-8). http://oehha.ca.gov/prop65/prop65_list/102811list.html.
44. OEHHA Evidence of carcinogenicity of tris(1,3-dichloro-2-propyl) phosphate 2011, Office of Environmental Health Hazard Assessment, California Environmental Protection Agency.
45. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3(6):1101-1108.
46. Searle S.R., Speed F.M., Milliken G.A. Population marginal means in the linear-model - an alternative to least-squares means. Am. Stat. 1980, 34(4):216-221.
47. Shizuka D., Lyon B.E. Improving the reliability of molecular sexing of birds using a W-specific marker. Mol. Ecol. Resour. 2008, 8(6):1249-1253.
48. Stapleton H.M., Sharma S., Getzinger G., Ferguson P., Gabriel M., Webster T.F., Blum A. Novel and high volume use flame retardants in US couches reflective of the 2005 pentaBDE phase out. Environ. Sci. Technol. 2012, 46(24):13432-13439.
49. 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(4):943-951.
50. Ulsamer A.G., Osterberg R.E., McLaughlin J. Flame-retardant chemicals in textiles. Clin. Toxicol. 1980, 17(1):101-131.
51. van der Veen I., de Boer J. Phosphorus flame retardants: properties, production, environmental occurrence, toxicity and analysis. Chemosphere 2012, 88(10):1119-1153.
52. Wang Q., Liang K., Liu J., Yang L., Guo Y., Liu C., Zhou B. 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.
53. Wellen K.E., Hotamisligil G.S. Inflammation, stress, and diabetes. J. Clin. Investig. 2005, 115(5):1111-1119.
54. Wu H., Kerr M.K., Ciu X., Churchill G.A. MAANOVA: a softwear package for the analysis of spotted cDNA microarray experiments. The Analysis of Gene Expression Data: Methods and Software 2003, 313-431. Springer-Verlag, New York. G. Parmigiani, E.S. Garrett, R.A. Irizarry (Eds.).
55. Wu Y.L., Yang C.Y., Chung W.C., Chang K.J., Lee P.H., Tsai W.C., Kuo M.L. The roles of leukocyte cell-derived chemotaxin 2 (LECT2) in hepatocellular carcinoma invasion and metastasis. Proceedings of the American Association for Cancer Research Annual Meeting 2010, 51:821.
56. Yang Y.H., Dudoit S., Luu P., Lin D.M., Peng V., Ngai J., Speed T.P. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 2002, 30(4):e15.
57. Zhou S., Zhou Z., Yang L., Cai J. Substrates, inducers, inhibitors and structure-activity relationships of human cytochrome P450 2C9 and implications in drug development. Curr. Med. Chem. 2009, 16(27):3480-3675.
58. Zollner G., Trauner M. Molecular mechanisms of cholestasis. Wien. Med. Wochenschr. 2006, 156(13-14):380-385.