An investigation of endocrine disrupting effects and toxic mechanisms modulated by benzo[a]pyrene in female scallop Chlamys farreri

Aquatic Toxicology

Volumn 144-145, Issue , 2013, Pages 162-171

  Tian, Shuangmei ^a   Pan, Luqing ^a   Sun, Xiaohua ^a  

^a Ocean University of China   (China)

Author keywords

AHR; Benzo a pyrene; Chlamys farreri; Endocrine disruption; ER; Steroidogenesis

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CYTOCHROME P450 17; CYTOCHROME P450 1A1; ESTRADIOL; ESTROGEN RECEPTOR; HYPOXIA INDUCIBLE FACTOR 1BETA; MESSENGER RNA; PROGESTERONE; TESTOSTERONE; TESTOSTERONE 17BETA DEHYDROGENASE;

BIVALVE; ENDOCRINE DISRUPTOR; IDENTIFICATION METHOD; IMMUNOASSAY; LUMINESCENCE; POLLUTION EFFECT; POLLUTION EXPOSURE; STEROID; TAXONOMY; TOXICITY;

ARTICLE; CHEMOSENSITIVITY; CHLAMYS FARRERI; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEVELOPMENTAL DISORDER; ENDOCRINE DISEASE; ENZYME REGULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; INVERTEBRATE; MARINE SPECIES; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; SEX HORMONE DETERMINATION; TESTOSTERONE SYNTHESIS; TOXICITY TESTING; TRANSCRIPTION INITIATION;

AHR; BENZO[A]PYRENE; CHLAMYS FARRERI; ENDOCRINE DISRUPTION; ER; STEROIDOGENESIS;

ANIMALS; BENZO(A)PYRENE; ENDOCRINE DISRUPTORS; FEMALE; GENE EXPRESSION REGULATION; GONADS; PECTINIDAE; STEROIDS; WATER POLLUTANTS, CHEMICAL;

EID: 84887006602     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.09.031     Document Type: Article

References (75)

1. Abdelrahim M., Ariazi E., Kim K., Khan S., Barhoumi R., Burghardt R., Liu S., Hill D., Finnell R., Wlodarczyk B., Jordan V.C., Safe S. 3-Methylcholanthrene and other aryl hydrocarbon receptor agonists directly activate estrogen receptor alpha. Cancer Res. 2006, 66:2459-2467.
2. Arcaro K.F., O'Keefe P.W., Yang Y., Clayton W., Gierthy J.F. Antiestrogenicity of environmental polycyclic aromatic hydrocarbons in human breast cancer cells. Toxicology 1999, 133:115-127.
3. Arcaro K.F., Yang Y., Gierthy J.F. Benzo[k]fluoranthene enhancement and suppression of 17beta-estradiol catabolism in MCF-7 breast cancer cells. J. Toxicol. Environ. Health Part A 1999, 58:413-426.
4. Barouki R., Morel Y. Repression of cytochrome P450 1A1 gene expression by oxidative stress: mechanisms and biological implications. Biochem. Pharmacol. 2001, 61:511-516.
5. Benedetti M., Martuccio G., Fattorini D., Canapa A., Barucca M., Nigro M., Regoli F. Oxidative and modulatory effects of trace metals on metabolism of polycyclic aromatic hydrocarbons in the Antarctic fish Trematomus bernacchiile. Aquat. Toxicol. 2007, 85:167-175.
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 1976, 72:248-254.
7. Butler R.A., Kelley M.L., Olberding K.E., Gardner G.R., Van Beneden R.J. Aryl hydrocarbon receptor (AHR)-independent effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on softshell clam (Mya arenaria) reproductive tissue. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2004, 138:375-381.
8. Cangialosi M.V., Puccia E., Mazzola A., et al. Screening of ovarian steroidogenic pathway in Ciona intestinalis and its modulation after tributyltin exposure. Toxicol. Appl Pharmacol 2010, 245(1):124-133.
9. Chen X., An H., Ao L., Sun L., Liu W., Zhou Z., Wang Y., Cao J. The combined toxicity of dibutyl phthalate and benzo(a)pyrene on the reproductive system of male Sprague Dawley rats in vivo. J. Hazard. Mater. 2011, 186:835-841.
10. Ching E.W.K., Siu W.H.L., Lam P.K.S., Xu L., Zhang Y., Richardson B., Wu R.S.S. DNA Adduct formation and DNA strand breaks in green-lipped mussels (P. viridis) exposed to benzo[a]pyrene: dose- and time-dependent relationships. Mar. Pollut. Bull. 2001, 42:603-610.
11. Chung J.-Y., Kim Y.-J., Kim J.Y., Lee S.G., Park J.-E., Kim W.R., Yoon Y.-D., Yoo K.S., Yoo Y.H., Kim J.-M. Benzo[a]pyrene reduces testosterone production in rat Leydig cells via a direct disturbance of testicular steroidogenic machinery. Environ. Health Perspect. 2011, 119:1569-1574.
12. Croll R.P., Wang C. Possible roles of sex steroids in the control of reproduction in bivalve molluscs. Aquaculture 2007, 272:76-86.
13. Daniel F.B., Haas D.L., Santi L. Quantitation of chemically induced DNA strand breaks in human cells via an alkaline unwinding assay. Anal. Biochem. 1985, 144:390-402.
14. De Lisa E., Paolucci M., Di Cosmo a. Conservative nature of oestradiol signalling pathways in the brain lobes of Octopus vulgaris involved in reproduction, learning and motor coordination. J. Neuroendocrinol. 2012, 24:275-284.
15. EPA Second EDSP List of Chemicals for Tier 1 Screening 2010, Environmental Protection Agency, United States, Available from http://www.epa.gov/endo/pubs/prioritysetting/draftlist2.html.
16. European Union Environment Study on enhancing the Endocrine Disrupter priority list with a focus on low production volume chemicals. Appendix L updated ranked priority list. 2007, Available from http://ec.europa.eu/environment/endocrine/documents/final_report_2007.pdf.
17. Fernandes D., Loi B., Porte C. Biosynthesis and metabolism of steroids in molluscs. J. Steroid Biochem. 2011, 127:189-195.
18. Fertuck K.C., Kumar S., Sikka H.C., Matthews J.B., Zacharewski T.R. Interaction of PAH-related compounds with the alpha and beta isoforms of the estrogen receptor. Toxicol. Lett. 2001, 121:167-177.
19. Fertuck K.C., Matthews J.B., Zacharewski T.R. Hydroxylated benzo[a]pyrene metabolites are responsible for in vitro estrogen receptor-mediated gene expression induced by benzo[a]pyrene, but do not elicit uterotrophic effects in vivo. Toxicol. Sci. 2001, 59(2):231-240.
20. Gagne F., Blaise C., Pellerin J., Douville E., Gauthier-Clerc S. Sex alternation in soft-shell clams (Mya arenaria) in an intertidal zone of the Saint-Lawrence River (Quebec, Canada). Comp. Biochem. Physiol. 2003, 134:189-198.
21. Gauthier-Clerc S., Pellerin J., Amiard J.C. Estradiol-17beta and testrosterone concentrations in male and female Mya arenaria (Mollusca bivalvia) during the reproductive cycle. Gen. Comp. Endocrinol. 2006, 145:133-139.
22. Gooding M.P., Wilson V.S., Folmar L.C., Marcovich D.T., LeBlanc G.A. The biocide tributyltin reduces the accumulation of testosterone as fatty acid esters in the mud snail (Ilyanassa obsoleta). Environ. Health Perspect. 2003, 111:426-430.
23. Gozgit J.M., Nestor K.M., Fasco M.J., Pentecost B.T., Arcaro K.F. Differential action of polycyclic aromatic hydrocarbons on endogenous estrogen-responsive genes and on a transfected estrogen-responsive reporter in MCF-7 cells. Toxicol. Appl. Pharmacol. 2004, 196:58-67.
24. Guo H., Bao Z., Du H., Zhang L., Wang S., Sun L., Mou X., Hu X. Identification of cytochrome P450 (CYP) genes in Zhikong scallop (Chlamys farreri). J. Ocean Univ. Chin. 2013, 12(1):97-102.
25. Hahn M.E. Aryl hydrocarbon receptors: diversity and evolution. Chem. Biol. Interact. 2002, 141:131-160.
26. Hellou J., Yeats P., Stellar S., Gagne F. Chemical contaminants and biological indicators of mussel health during gametogenesis. Environ. Toxicol. Chem. 2003, 22:2080-2087.
27. Hines G.A., Bryan P.J., Wasson K.M., McClintock J.B., Watts S.A. Sex steroid metabolism in the antarctic pteropod Clione antarctica (Mollusca: Gastropoda). Invertebr. Biol. 1996, 115:113-119.
28. Hines G.A., Watts S.A., Sower S.A., Walker C.W. Sex steroid extraction from echinoderm tissues. J. Liq. Chromatogr. 1990, 13:2489-2498.
29. Hoffmann J.L., Oris J.T. Altered gene expression: a mechanism for reproductive toxicity in zebrafish exposed to benzo[a]pyrene. Aquat. Toxicol 2006, 78:332-340.
30. Janer G., Lavado R., Thibaut R., Porte C. Effects of 17 beta-estradiol exposure in the mussel, Mytilus galloprovincialis: a possible regulating role for steroid acyltransferases. Aquat. Toxicol. 2005, 75:32-42.
31. Janer G., Porte C. Sex steroids and potential mechanisms of non-genomic endocrine disruption in invertebrates. Ecotoxicology 2007, 16:145-160.
32. Japen Chemicals Suspected of Having Endocrine Disrupting Effects in SPEED'98 1981, http://www.env.go.jp/en/chemi/ed/speed98/sp98t3.html.
33. Jing-Jing M., Lu-qing P., Jing L., Lin Z. Effects of benzo[a]pyrene on DNA damage and histological alterations in gonad of scallop Chlamys farreri. Mar. Environ. Res. 2009, 67:47-52.
34. Kajiwara M., Kuraku S., Kurokawa T., Kato K., Toda S., Hirose H., Takahashi S., Shibata Y., Iguchi T., Matsumoto T., Miyata T., Miura T., Takahashi Y. Tissue preferential expression of estrogen receptor gene in the marine snail, Thais clavigera. Gen. Comp. Endocrinol. 2006, 148:315-326.
35. Keay J., Bridgham J.T., Thornton J.W. The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology 2006, 147:3861-3869.
36. Ketata I., Guermazi F., Rebai T., et al. Variation of steroid concentrations during the reproductive cycle of the clam Ruditapes decussatus: a one year study in the gulf of Gabès area. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2007, 147(2):424-431.
37. Kummer V., Maskova J., ZRALY Z., et al. Estrogenic activity of environmental polycyclic aromatic hydrocarbons in uterus of immature Wistar rats. Toxicol. Lett. 2008, 180(3):212-221.
38. Lavado R., Janer G., Porte C. Steroid levels and steroid metabolism in the Mussel Mytilus edulis: the modulating effect of dispersed crude oil and alkylphenols. Aquat. Toxicol. 2006, 78:S65-S72.
39. Li Q., Osada M., Suzuki T., Mori K. Changes in vitellin during oogenesis and effect of estradiol-17β on vitellogenesis in the pacific oyster (Crassostrea gigas). Invertebr. Reprod. Dev. 1998, 33:87-93.
40. Liu N., Pan L., Miao J., Xu C., Zhang L. Molecular cloning and sequence analysis and the response of a aryl hydrocarbon receptor homologue gene in the clam Ruditapes philippinarum exposed to benzo(a)pyrene. Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 2010, 152:279-287.
41. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(- Delta Delta C) method. Methods 2001, 25:402-408.
42. Manoli E., Samara C. Polycyclic aromatic hydrocarbons in natural waters: sources, occurrence and analysis. TrAC, Trends Anal. Chem. 1999, 18:417-428.
43. Matsumoto T., Nakamura A.M., Mori K., Akiyama I., Hirose H., Takahashi Y. Oyster estrogen receptor: cDNA cloning and immunolocalization. Gen. Comp. Endocrinol. 2007, 151:195-201.
44. Matsumoto T., Osada M., Osawa Y., Mori K. Gonadal estrogen profile and immuno-histochemical localization of steroidogenic enzymes in the oyster and scallop during sexual maturation. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 1997, 118:811-817.
45. Monari M., Cattani O., Serrazanetti G.P., Selli A., Pagliuca G., Zironi E., Livingstone D.R. Effect of exposure to benzo[a]pyrene on SODs, CYP1A1/1A2-and CYP2E1 immunopositive proteins in the blood clam Scapharca inaequivalvis. Mar. Environ. Res. 2007, 63(3):200-218.
46. Morel Y., Barouki R. Down-regulation of cytochrome P450 1A1 gene promoter by oxidative stress. Critical contribution of nuclear factor 1. J Biol Chem. 1998, 273:26969-26976.
47. Neal M.S., Mulligan Tuttle A.M., Casper R.F., Lagunov A., Foster W.G. Aryl hydrocarbon receptor antagonists attenuate the deleterious effects of benzo[a]pyrene on isolated rat follicle development. Reprod. Biomed. Online 2010, 21(1):100-108.
48. Nebert D.W., Dalton T.P. The role of cytochrome P450 enzymes in endogenous signaling pathways and environmental carcinogenesis. Nat. Rev. Cancer 2006, 6:947-960.
49. Pan L.Q., Miao J.J., Wang J., Liu J. AHH activity, tissue dose and DNA damage in different tissues of the scallop Chlamys farreri exposed to benzo[a]pyrene. Environ. Pollut. 2008, 153:192-198.
50. Patel M., Scheffler B., Wang L., Willett K. Effects of benzo(a)pyrene exposure on killifish (Fundulus heteroclitus) aromatase activities and mRNA. Aquat. Toxicol. 2006, 77:267-278.
51. Pearce S.T., Liu H., Radhakrishnan I., Abdelrahim M., Safe S., Jordan V.C. Interaction of the aryl hydrocarbon receptor ligand 6-methyl-1,3, 8-trichlorodibenzofuran with estrogen receptor alpha. Cancer Res. 2004, 64:2889-2897.
52. Qin H., Powell-Coffman J.A. The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Dev. Biol. 2004, 270:64-75.
53. Qiu Y.W., Zhou J.L., Maskaoui K., Hong H.S., Wang Z.D. Distribution of polycyclic aromatic hydrocarbons in water and sediments from Daya Bay and their ecological hazard assessment. J. Trop. Oceanogr. 2004, 23:72-80.
54. Rocha Monteiro P.R., Reis-Henriques M., Coimbra J. Polycyclic aromatic hydrocarbons inhibit in vitro ovarian steroidogenesis in the flounder (Platichthys flesus L.). Aquat. Toxicol. (Amsterdam, Netherlands) 2000, 48:549-559.
55. Ronis M.J.J., Mason A.Z. The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: effects of tribultyl Tin. Mar. Environ. Res. 1996, 42:161-166.
56. Sadeu J.C., Foster W.G. Effect of in vitro exposure to benzo[a]pyrene, a component of cigarette smoke, on folliculogenesis, steroidogenesis and oocyte nuclear maturation. Reprod. Toxicol. (Elmsford, N.Y.) 2011, 31:402-408.
57. Safe S., Wormke M., Samudio I. Mechanisms of inhibitory aryl hydrocarbon receptor-estrogen receptor crosstalk in human breast cancer cells. J. Mammary Gland Biol. Neoplasia 2000, 5(3)):295-306.
58. Shaw J.P., Peters L.D., Chipman J.K. CYP1A- and CYP3A-immunopositive protein levels in digestive gland of the mussel Mytilus galloprovincialis from the Mediterranean Sea. Mar. Environ. Res. 2004, 58:649-653.
59. Shimada T., Hayes C.L., Yamazaki H., Amin S., Hecht S.S., Guen-gerich F.P., Sutter T.R. Activation of chemically diverse pro-carcinogens by human cytochrome P-450 1B1. Cancer Res. 1996, 56(13):2979-2984.
60. Siah a., Pellerin J., Benosman a., Gagné J.-P., Amiard J.-C. Seasonal gonad progesterone pattern in the soft-shell clam Mya arenaria. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2002, 132:499-511.
61. Spink D.C., Katz B.H., Hussain M.M., Spink B.C., Wu S.J., Liu N., Pause R., Kaminsky L.S. Induction of CYP1A1 and CYP1B1 in T-47D human breast cancer cells by benzo[a]pyrene is diminished by arsenite. Drug Metab. Dispos. 2002, 30(3):262-269.
62. Thornton J.W., Need E., Crews D. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signalling. Science 2003, 301:1714-1717.
63. Tsai K.S., Yang R.S., Liu S.H. Benzo[a]pyrene regulates osteoblast proliferation through an estrogen receptor-related cyclooxygenase-2 pathway. Chem. Res. Toxicol. 2004, 17:679-684.
64. Van Lipzig M.M.H., Vermeulen N.P.E., Gusinu R., Legler J., Frank H., Seidel A., Meerman J.H.N. Formation of estrogenic metabolites of benzo[a]pyrene and chrysene by cytochrome P450 activity and their combined and supra-maximal estrogenic activity. Environ. Toxicol. Pharmacol. 2005, 19:41-55.
65. Vondráček J., Kozubík A., Machala M. Modulation of estrogen receptor-dependent reporter construct activation and G0/G1-S-phase transition by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells. Toxicol. Sci. 2002, 70(2):193-201.
66. Wang C., Croll R.P. Effects of sex steroids on gonadal development and gender determination in the sea scallop (Placopecten magellanicus). Aquaculture 2004, 238:483-498.
67. WHO Selected Non-Heterocyclic Polycyclic Aromatic Hydrocarbons 1998, WHO, Geneva.
68. Wills E.D. Evaluation of lipid peroxidation in lipids and biological membranes. Biochemical Toxicology: A Practical Approach 1987, 127-152. IRL Press, Washington. K. Snell, B. Mullock (Eds.).
69. Xu C., Chen J.-A., Qiu Z., Zhao Q., Luo J., Yang L., Zeng H., Huang Y., Zhang L., Cao J., Shu W. Ovotoxicity and PPAR-mediated aromatase downregulation in female Sprague-Dawley rats following combined oral exposure to benzo[a]pyrene and di-(2-ethylhexyl) phthalate. Toxicol. Lett. 2010, 199:323-332.
70. Zanette J., Goldstone J.V., Bainy A.C., Stegeman J.J. Identification of CYP genes in Mytilus (mussel) and Crassostrea(oyster) species: first approach to the full complement of cytochrome P450 genes in bivalves. Mar. Environ. Res. 2010, 69:S1-S3.
71. Zanette J., Jenny M.J., Goldstone J.V., Parente T., Woodin B.R., Bainy A.C., Stegeman J.J. Identification and Expression of Multiple CYP1-like and CYP3-like Genes in the Bivalve Mollusk Mytilus edulis. Aquat. Toxicol. 2013, 128-129:101-112.
72. Zhang H., Pan L., Zhang L. Molecular cloning and characterization of estrogen receptor gene in the scallop Chlamys farreri: expression profiles in response to endocrine disrupting chemicals. Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 2012, 156:51-57.
73. Zhang Y., Song J., Yuan H., Xu Y., He Z., Duan L. Biomarker responses in the bivalve (Chlamys farreri) to exposure of the environmentally relevant concentrations of lead, mercury, copper. Environ. Toxicol. Pharmacol. 2010, 30(1):19-25.
74. Zheng R., Wang C., Zuo Z., Chen Y., Zhao Y. Combined effect of tributyltin and benzo[a] pyrene on the levels of sex hormone and vitellogenin in female Sebastiscus marmoratus. J. Environ. Sci. 2006, 18:359-363.
75. Zheng S.-J., Tian H.-J., Cao J., Gao Y.-Q. Exposure to di(n-butyl)phthalate and benzo(a)pyrene alters IL-1β secretion and subset expression of testicular macrophages, resulting in decreased testosterone production in rats. Toxicol. Appl. Pharmacol. 2010, 248:28-37.