235
Views
1
CrossRef citations to date
0
Altmetric
Original Articles

Differential expression of hepatic genes with embryonic exposure to an environmentally relevant PCB mixture in Japanese quail (Coturnix japonica)

ORCID Icon, , & ORCID Icon
Pages 691-704 | Received 21 Feb 2018, Accepted 31 May 2018, Published online: 22 Jun 2018

References

  • Barhoumi, B., C. Clerandeau, P.-Y. Gourves, K. Le Menach, Y. El Megdiche, L. Peluhet, H. Budzinski, M. Baudrimont, M. Driss, and J. Cachot. 1994. Pollution biomonitoring in the Bizerte lagoon (Tunisia), using combined chemical and biomarker analyses in grass goby, Zosterisessor ophiocephalus (Teleostei, Gobiidae). Marine Environmental Research 101:184–95. doi:10.1016/j.marenvres.2014.07.002.
  • Brazma, A., P. Hingamp, J. Quackenbush, G. Sherlock, P. Spellman, C. Stoeckert, J. Aach, W. Ansorge, C. A. Ball, H. C. Causton, T. Gaasterland, P. Glenisson, F. C. P. Holstege, I. F. Kim, V. Markowitz, U. Sarkans, S. Schulze-Kremer, J. Stewart, R. Taylor, J. Vilo, and M. Vingron. 2001. Minimum information about a microarray experiment (MIAME) – Toward standards for microarray data. Nature Genetics 29:365–71. doi:10.1038/ng1201-365.
  • Brown, J., D. Bedard, M. Brennan, J. Carnahan, H. Feng, and R. Wagner. 1987. Polychlorinated biphenyls dechlorination in aquatic sediments. Science 236:709–12. doi:10.1126/science.236.4802.709.
  • Brunström, B., and K. Halldin. 1998. EROD induction by environmental contaminants in avian embryo livers. Comparative Biochemistry and Physiology. C: Comparative Pharmacology 121:213–19. doi:10.1016/S0742-8413(98)10042-7.
  • Cesh, L., K. Elliott, S. Quade, M. McKinney, F. Maisoneuve, D. Garcelon, C. Sandau, R. Letcher, T. Williams, and J. Elliott. 2010. Polyhalogenated aromatic hydrocarbons and metabolites: Relation to circulating thyroid hormone and retinol in nestling bald eagles (Haliaeetus leucocephalus). Environmental Toxicology and Chemistry / SETAC 29:1301–10. doi:10.1002/etc.165.
  • Cogburn, L., X. Wang, W. Carre, L. Rejto, S. Aggrey, M. Duclos, J. Simon, and T. Porter. 2004. Functional genomics in chickens: Development of integrated-systems microarrays for transcriptional profiling and discovery of regulatory pathways. Comparative Function Genome 5:253–61. doi:10.1002/cfg.402.
  • Custer, T., C. Custer, and B. Gray. 2010. Polychlorinated biphenyls, dioxins, furans, and organochlorine pesticides in spotted sandpiper eggs from the upper Hudson River basin, New York. Ecotoxicology 19:391–404. doi:10.1007/s10646-009-0425-z.
  • Dalton, T., A. Puga, and H. Shertzer. 2002. Induction of cellular oxidative stress by aryl hydrocarbon receptor activation. Chemico-Biological Interactions 141:77–95. doi:10.1016/S0009-2797(02)00067-4.
  • Di Giulio, R. T., and B. W. Clark. 2015. The Elizabeth River story: A case study in evolutionary toxicology. Journal Toxicogical Environment Health B 18:259–98. doi:10.1080/15320383.2015.1074841.
  • Droppelmann, C., D. Saez, J. Asenjo, A. Yanez, M. Garcia-Rocha, I. Concha, M. Grez, J. Guinovart, and J. Slebe. 2015. A new level of regulation in gluconeogenesis: Metabolic state modulates the intracellular localization of aldolase B and its interaction with liver fructose-1,6-biphosphatase. The Biochemical Journal 472:225–37. doi:10.1042/BJ20150269.
  • Elliott, J., S. Kennedy, D. Peakall, and H. Won. 1990. Polychlorinated biphenyl (PCB) effects on hepatic mixed function oxidases and porphyria in birds. I. Japanese quail. Comparative Biochemistry and Physiology. C: Comparative Pharmacology 96:205–10. doi:10.1016/0742-8413(90)90069-L.
  • El-Shahawi, M., A. Hamza, A. Bashammakh, and W. Al-Saggaf. 2010. An overview on the accumulation, distribution, transformations, toxicity, and analytical methods for the monitoring of persistent organic pollutants. Talanta 80:1587–97. doi:10.1016/j.talanta.2009.09.055.
  • Faust, D., J. Vondracek, P. Krcmar, L. Smerdova, J. Prochazkova, E. Hruba, P. Hulinkova, B. Kaina, C. Dietrich, and M. Machala. 2013. AhR-mediated changes in global gene expression in rat liver progenitor cells. Archives of Toxicology 87:681–98. doi:10.1007/s00204-012-0979-z.
  • Fernie, K., and G. Bortolotti. 2003. Reproductive abnormalities, teratogenicity, and developmental problems in American kestrels (Falco sparverius) exposed to polychlorinated biphenyls. Journal of Toxicology and Environmental Health. Part A 66:2089–103. doi:10.1080/15287390390211270.
  • Fernie, K., J. Smits, and G. Bortolotti. 2003. Developmental toxicity of in ovo exposure to polychlorinated biphenyls: I. Immediate and subsequent effects on first-generation nestling American kestrels (Falco sparverius). Environmental Toxicology and Chemistry / SETAC 22:554–60. doi:10.1897/1551-5028(2003)022<0554:DTOIOE>2.0.CO;2.
  • Frame, G., J. Cochran, and S. Bowad. 1996a. Complete PCB congener distributions for 17 Aroclor mixtures determined by 3 HRGC systems optimized for comprehensive, quantitative, congener-specific analysis. Journal High Researcher Chromatographic 19:657–68. WOS: A11996WC95300001. doi:10.1002/jhrc.1240191202.
  • Frame, G., R. Wagner, J. Carnahan, J. Brown, Jr, R. May, L. Smullen, and D. Bedard. 1996b. Comprehensive, quantitative, congener-specific analyses of eight Aroclors and complete PCB congener assignments on DB-1 capillary GC columns. Chemosphere 33:603–23. doi:10.1016/0045-6535(96)00214-7.
  • Gao, L., E. Mutlu, L. B. Collins, N. J. Walker, H. J. Hartwell, J. R. Olson, W. Sun, A. Gold, L. M. Ball, and J. A. Swenberg. 2017. DNA product formation in female Sprague-Dawley rats following polyhalogenated aromatic hydrocarbon (PHAH) exposure. Chemical Research in Toxicology 30:794–803. doi:10.1021/acs.chemrestox.6b00368.
  • Giesy, J., J. Ludwig, and D. Tillitt. 1994. Deformities in birds of the Great Lakes region: Assigning causality. Environmental Science & Technology 28:A128–A135. doi:10.1021/es00052a002.
  • Gilbertson, M., T. Kubiak, J. Ludwig, and G. Fox. 1991. Great Lakes embryo mortality, edema, and deformities syndrome (GLEMEDS) in colonial fish-eating birds: Similarity to chick-edema disease. Journal of Toxicology and Environmental Health 33:455–520. WOS: A19911GD12600005. doi:10.1080/15287399109531538.
  • Grasman, K., G. Fox, P. Scanlon, and J. Ludwig. 1994. Organochlorine-associated immunosuppression in prefledgling Caspian terns and herring gulls from the Great Lakes: An ecoepidemiological study. Environment Health Perspectives 104(Supplement 4):829–42. doi:10.2307/3432714.
  • Grasman, K., P. Scanlon, and G. Fox. 1998. Reproductive and physiological effects of environmental contaminants in fish-eating birds of the Great Lakes: A review of historical trends. Environmental Monitoring and Assessment 53:117–45. doi:10.1023/A:1005915514437.
  • Head, J., and S. Kennedy. 2007. Same-sample analysis of ethoxyresorufin-O-deethylase activity and cytochrome P450 1A mRNA abundance in chicken embryo hepatocytes. Analytical Biochemistry 360:294–302. doi:10.1016/j.ab.2006.10.033.
  • Head, J., and S. Kennedy. 2010. Correlation between an in vitro and an in vivo measure of dioxin sensitivity in birds. Ecotoxicology 19:377–82. doi:10.1007/s10646-009-0421-3.
  • Helgason, L., A. Arukwe, G. Gabrielsen, M. Harju, M. Hegseth, E. Heimstad, E. Jorgensen, A. Mortensen, and J. Wolkers. 2010. Biotransformation of PCBs in arctic seabirds: Characterization of phase I and II pathways at transcriptional, translational, and activity levels. Comparative Biochemistry and Physiology. C: Comparative Pharmacology 152:34–41. doi:10.1016/j.cbpc.2010.02.009.
  • Hervé, J., D. Crump, S. Jones, L. Mundy, J. Giesy, M. Zwiernik, S. Bursian, P. Jones, S. Wiseman, Y. Wan, and S. Kennedy. 2010. Cytochrome P4501A induction 2,3,7,8-tetrachlorodibenzo-p-dioxin and two chlorinated dibenzofurans in primary hepatocyte cultures of three avian species. Toxicological Sciences : an Official Journal of the Society of Toxicology 113:380–91. doi:10.1093/toxsci/kfp270.
  • Hestermann, E., J. Stegeman, and M. Hahn. 2000. Relative contributions of affinity and intrinsic efficacy to aryl hydrocarbon receptor ligand potency. Toxicology and Applied Pharmacology 168:160–72. doi:10.1006/taap.2000.9026.
  • Hoffman, D., M. Melancon, P. Klein, J. Eisemann, and J. Spann. 1998. Comparative developmental toxicity of planar polychlorinated biphenyl congeners in chickens, American kestrels, and common terns. Environmental Toxicology and Chemistry / SETAC 17:747–57. doi:10.1897/1551-5028(1998)017<0747:CDTOPP>2.3.CO;2.
  • Hudson River Natural Resources Trustees (HRNRT). 2013. PCB Contamination of the Hudson River Ecosystem: Compilation of contamination data through 2008. January, 2013. U.S. Department of Commerce, Silver Spring, MD.
  • Johnson, B., H. Hicks, W. Cibulas, O. Faroon, A. Ashizawa, C. DeRosa, J. Cogliano, and M. Clark. 2000. Public health implications of exposure to polychlorinated biphenyls (PCBs). Atlanta, GA: Agency for Toxic Substances and Disease Registry, Division of Toxicology. https://www.epa.gov/sites/production/files/2015-01/documents/pcb99.pdf.
  • Knerr, S., and D. Schrenk. 2006. Carcinogenicity of “non-dioxinlike” polychlorinated biphenyls. Critical Reviews in Toxicology 36:663–94. doi:10.1080/10408440600845304.
  • Kubota, A., H. Iwata, H. Goldstone, E.-Y. Kim, J. Stegeman, and S. Tanabe. 2006. Cytochrome P450 1A4 and 1A5 in common cormorant (Phalacrocorax carbo): Evolutionary relationships and functional implications associated with dioxin and related compounds. Toxicological Sciences : an Official Journal of the Society of Toxicology 92:394–408. doi:10.1093/toxsci/kfl001.
  • Lavoie, E., and K. Grasman. 2007. Effects of in ovo exposure to PCBs 126 and 77 on mortality, deformities, and post-hatch immune function in chickens. Journal of Toxicology and Environmental Health. Part A 70:547–58. doi:10.1080/15287390600882226.
  • Mandal, P. K. 2005. Dioxin: A review of its environmental effects and its aryl hydrocarbon receptor biology. Journal Comparative Physical B 175:221–30. doi:10.1007/s00360-005-0483-3.
  • Manning, G., L. Mundy, D. Crump, S. Jones, S. Chiu, J. Klein, A. Konstantinov, D. Potter, and S. Kennedy. 2013. Cytochrome P4501A induction in avian hepatocyte cultures exposed to polychlorinated biphenyls: Comparisons with AHR1-mediated reporter gene activity and in ovo toxicity. Toxicology and Applied Pharmacology 266:38–47. doi:10.1016/j.taap.2012.10.030.
  • Mates, J. M., J. A. Segura, F. J. Alonso, and J. Marquez. 2010. Roles of dioxins and heavy metals in cancer and neurological diseases using ROS-mediated mechanisms. Free Radical Biology & Medicine 49:1328–41. doi:10.1016/j.freeradbiomed.2010.07.028.
  • McKernan, M., B. Rattner, J. Hatfield, R. Hale, and M. Ottinger. 2010. Absorption and biotransformation of polybrominated diphenyl ethers DE-71 and DE-79 in chicken (Gallus gallus), mallard (Anas platyrhynchos), American kestrel (Falco sparverius), and black-crowned night heron (Nycticorax nycticorax) eggs. Chemosphere 79:100–09. doi:10.1016/j.chemosphere.2009.12.023.
  • Melancon, M., A. Kutay, B. Woodin, and J. Stegeman. 2006. Evaluating cytochrome P450 in lesser scaup (Aythya affinis) and tree swallow (Tachycineta bicolor) by monooxygenase activity and immunohistochemistry: Possible nonlethal assessment by skin immunohistochemistry. Environmental Toxicology and Chemistry / SETAC 25:2613–17. doi:10.1897/2605021.1.
  • Morozov, A., G. Chiuko, and E. Brodskii. 2012. Functional state of the liver antioxidant system of the bream Abaramis brama (L.) from Rybinsk reservoir regions with different anthropogenic loads. Inland Water Biologic 5:147–52. doi:10.1134/S1995082911040134.
  • Morozov, A., and V. Yurichenko. 2016. Responses of hepatic biochemical markers in bream Abramis brama L. to dietary administered polychlorinated biphenyls. Contemporary Problems Ecology 9:78–85. doi:10.1134/S1995425516010108.
  • Ohtake, F., A. Baba, I. Takada, M. Okada, K. Iwasaki, H. Miki, S. Takahashi, A. Kouzmenko, K. Nohara, and T. Chiba. 2006. Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446:562–66. doi:10.1038/nature05683.
  • Ottinger, M., T. Carro, M. Bohannon, L. Baltos, A. Marcell, M. McKernan, K. Dean, E. Lavoie, and M. Abdelnabi. 2013. Assessing effects of environmental chemicals on neuroendocrine systems: Potential mechanisms and functional outcomes. General and Comparative Endocrinology 190:194–202. doi:10.1016/j.ygcen.2013.06.004.
  • Ottinger, M., E. Lavoie, M. Abdelnabi, M. Quinn, Jr, A. Marcell, and K. Dean. 2009. An overview of dioxin-like compounds, PCB, and pesticide exposures associated with sexual differentiation of neuroendocrine systems, fluctuating asymmetry, and behavioral effects in birds. Journal of Environmental Science and Health. Part C: Environmental Health Sciences 27:286–300. doi:10.1080/10590500903310229.
  • Palkova, L., J. Vondracek, L. Trilecova, M. Ciganek, K. Pencikova, J. Neca, A. Milcova, J. Topinka, and M. Machala. 2015. The aryl hydrocarbon receptor-mediated and genotoxic effects of fractionated extract of standard reference diesel exhaust particle material in pulmonary, liver and prostate cells. Toxicology in Vitro : an International Journal Published in Association with BIBRA 29:438–48. doi:10.1016/j.tiv.2014.12.002.
  • Porter, T., and L. Ellestad. 2005. Gene expression profiling in the developing neuroendocrine system of the chick. In Functional avian endocrinology, A. Dawson and P. Sharp. ed., 45–56. New Delhi, India: Narosa.
  • Rattner, B., J. Hatfield, M. Melancon, T. Custer, and D. Tillitt. 1994. Relation among cytochrome-P450, AH active PCB congeners and dioxin equivalents in pipping black-crowned night-heron embryos. Environmental Toxicology and Chemistry / SETAC 13:1805–12. doi:10.1897/1552-8618(1994)13[1805:RACPAP]2.0.CO;2.
  • Rattner, B., M. Melancon, T. Custer, and R. Hothem. 1996. Cytochrome P450 and contaminant concentrations in nestling black-crowned night-herons and their interrelation with sibling embryos. Environmental Toxicology and Chemistry / SETAC 15:715–21. doi:10.1897/1551-5028(1996)015<0715:CPACCI>2.3.CO;2.
  • Rattner, B., M. Melancon, C. Rice, W. Riley, Jr, J. Eisemann, and R. Hines. 1997. Cytochrome P450 and organochlorine contaminants in black-crowned night herons from the Chesapeake Bay region, USA. Environmental Toxicology and Chemistry / SETAC 16:2315–22. doi:10.1897/1551-5028(1997)016<2315:CPAOCI>2.3.CO;2.
  • Reich, M., K. Ohm, M. Angelo, P. Tamayo, and J. Mesirov. 2004. GeneCluster 2.0: An advanced toolset for bioarray analysis. Bioinformatics 20:1797–98. doi:10.1093/bioinformatics/bth138.
  • Rice, C., P. O’Keefe, and T. Kubiak. 2003. Sources, pathways, and effects of PCBs, dioxins, and dibenzofurans. In Handbook of toxicology, ed. D. Hoffman, B. Rattner, G. Burton Jr, and J. Cairs Jr, 501–73. 2nd ed., Boca Raton, FL: Lewis Publishers.
  • Rousseau, M., K. Sant, L. Borden, D. Franks, M. Hahn, and A. Timme-Laragy. 2015. Regulation of AhR signaling by Nrf2 during development: Effects of Nrf2 deficiency on PCB126 embryotoxicity in zebrafish (Danio rerio). Aquatic Toxicology (Amsterdam, Netherlands) 167:157–71. doi:10.1016/j.aquatox.2015.08.002.
  • Rousselet, E., M. Levin, E. Gebhard, B. M. Higgings, S. DeGuise, and C. A. J. Godard-Codding. 2017. Polychlorinated biphenyls (PCBs) modulate both phagocytosis and NK cell activity in vitro in juvenile loggerhead sea turtles (Caretta caretta). Journal of Toxicology and Environmental Health. Part A 80:556–61. doi:10.1080/15287394.2017.1363102.
  • Saeed, A., V. Sharov, J. White, J. Li, W. Liang, N. Bhagabati, J. Braisted, M. Klapa, T. Currier, and M. Thiagarajan. 2003. TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34:374–78. WOS: 000180892500018.
  • Schlezinger, J., W. Struntz, J. Goldstone, and J. Stegeman. 2006. Uncoupling of cytochrome P450 1A and stimulation of reactive oxygen species production by co-planar polychlorinated biphenyl congeners. Aquatic Toxicology (Amsterdam, Netherlands) 77:422–32. doi:10.1016/j.aquatox.2006.01.012.
  • Sheehan, D., G. Meade, V. Foley, and C. Dowd. 2001. Structure, function, and evolution of glutathione transferases: Implications for classification of non-mammalian members of an ancient enzyme superfamily. The Biochemical Journal 360:1–16. doi:10.1042/0264-6021:3600001.
  • Swedenborg, E., J. Rüegg, S. Mäkelä, and I. Pongratz. 2009. Endocrine disruptive chemicals: Mechanisms of action and involvement in metabolic disorders. Journal of Molecular Endocrinology 43:1–10. doi:10.1677/JME-08-0132.
  • Tairova, Z., J. Strand, R. Bossi, M. M. Larsen, L. Forlin, A. Bignert, J. Hedman, J. Gercken, T. Lang, N. F. Fricke, G. Asmund, M. Long, and E. C. Bonefeld-Jorgensen. 2017. Persistent organic pollutants and related biological responses measured in coastal fish using chemical and biological screening methods. Journal of Toxicology and Environmental Health. Part A 80:862–80. doi:10.1080/15287394.2017.1372870.
  • Tharappel, J., E. Lee, L. Robertson, B. Spear, and H. Glauert. 2002. Regulation of cell proliferation, apoptosis, and transcription factor activities during the promotion of liver carcinogensis by polychlorinated biphenyls. Toxicology and Applied Pharmacology 179:172–84. doi:10.1006/taap.2001.9360.
  • Tian, X., E. Song, R. Pi, X. Zhu, L. Liu, X. Ma, H. Dong, J. Liu, and Y. Song. 2012. Polychlorinated biphenyls and their different level metabolites as inhibitors of glutathione S-transferase isozymes. Chemico-Biological Interactions 198:1–8. doi:10.1016/j.cbi.2012.04.002.
  • Tomza-Marciniak, A., A. Marciniak, B. Pilarczyk, R. Drozd, M. Ligocki, and A. Prokulewicz. 2014. Wild boar (Sus scrofa) as a bioindicator of organochlorine compound contamination in terrestrial ecosystems of West Pomeranian Province, NW Poland. Environmental Monitoring and Assessment 186:229–38. doi:10.1007/s10661-013-3368-z.
  • USEPA. Summary of TSCA | Laws and Regulations | US EPA. Accessed October 21, 2010. http://www.epa.gov/lawsregs/laws/tsca.html
  • Van den Berg, M., L. Birnbaum, A. Bosveld, B. Brunström, P. Cook, M. Feeley, J. Giesy, A. Hanberg, R. Hasegawa, and S. Kennedy. 1998. Toxic equivalency factors (TEQs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environment Health Perspectives 106:775–92. doi:10.1289/ehp.98106775.
  • Van den Berg, M., L. Birnbaum, M. Denison, M. De Vito, W. Farland, M. Feeley, H. Fiedler, H. Hakansson, A. Hanberg, and L. Haws. 2005. The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicological Sciences : an Official Journal of the Society of Toxicology 93:223–41. doi:10.1016/j.toxlet.2006.06.116.
  • Wirgin, I., N. Roy, M. Loftus, R. Chambers, D. Franks, and M. Hahn. 2011. Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River. Science 331:1322–25. doi:10.1126/science.1197296.
  • Wright, D., and P. Welbourn. 2002. Cambridge environmental chemistry series, volume 11: Environmental toxicology. Cambridge, UK: Cambridge University Press.
  • Yoon, B. I., Y. Hirabayashi, T. Kaneko, Y. Kodama, J. Kanno, J. Yodoi, D. Y. Kim, and T. Inoue. 2001. Transgene expression of thioredoxin (TRX/ADF) protects against 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced hematotoxicity. Archives of Environmental Contamination and Toxicology 41:232–36. doi:10.1007/s002440010242.
  • You, L. 2004. Steroid hormone biotransformation and xenobiotic induction of hepatic steroid metabolizing enzymes. Chemico-Biological Interactions 147:233–46. doi:10.1016/j.cbi.2004.01.006.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.