Estrogenic activity of environmental polycyclic aromatic hydrocarbons in uterus of immature Wistar rats

Toxicology Letters

Volumn 180, Issue 3, 2008, Pages 212-221

  Kummer, Vladimír ^a   Mašková, Jarmila ^a   Zralý, Zdeněk ^a   Neča, Jiří ^a   Šimečková, Pavlína ^a   Vondráček, Jan ^a,b   Machala, Miroslav ^a  

^a VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^b INSTITUTE OF BIOPHYSICS   (Czech Republic)

Author keywords

Cytochrome P450; Estradiol metabolism; Estrogen receptor; p53; Polycyclic aromatic hydrocarbons; Rat immature uterotrophic assay

Indexed keywords

BENZ[A]ANTHRACENE; BENZO[A]PYRENE; BENZO[K]FLUORANTHENE; FLUORANTHENE; FULVESTRANT; POLYCYCLIC AROMATIC HYDROCARBON; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOMETRIUM; ENZYME ACTIVITY; ESTROGEN ACTIVITY; FEMALE; GENOTOXICITY; IMMATURITY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; NONHUMAN; OXYGENATION; POLLUTANT; PRIORITY JOURNAL; RAT; UTERUS DISEASE; UTERUS HYPERTROPHY; UTERUS WEIGHT; WISTAR RAT;

ANIMALS; CYTOCHROME P-450 CYP1A1; ENDOCRINE DISRUPTORS; ENVIRONMENTAL POLLUTANTS; EPITHELIUM; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; HYDROXYLATION; IMMUNOHISTOCHEMISTRY; MICROSOMES, LIVER; ORGAN SIZE; OVARY; PHOSPHORYLATION; POLYCYCLIC HYDROCARBONS, AROMATIC; RATS; RATS, WISTAR; TUMOR SUPPRESSOR PROTEIN P53; UTERUS;

RATTUS; RATTUS NORVEGICUS;

EID: 49549091327     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2008.06.862     Document Type: Article

References (74)

1. Abdelrahim M., Ariazi E., Kim K., Khan S., Barhoumi R., Burghardt R., Liu S., Hill D., Finnell R., Wlodarczyk B., Jordan V.C., and Safe S. 3-Methylcholanthrene and other aryl hydrocarbon receptor agonists directly activate estrogen receptor alpha. Cancer Res. 66 (2006) 2459-2467
2. Andrysík Z., Machala M., Chramostová K., Hofmanová J., Kozubík A., and Vondráček J. Activation of ERK1/2 and p38 kinases by polycyclic aromatic hydrocarbons in rat liver epithelial cells is associated with induction of apoptosis. Toxicol. Appl. Pharmacol. 211 (2006) 198-208
3. Andrysík Z., Vondráček J., Machala M., Krčmář P., Švihálková-Šindlerová L., Kranz A., Weiss C., Faust D., Kozubík A., and Dietrich C. The aryl hydrocarbon receptor-dependent deregulation of cell cycle control induced by polycyclic aromatic hydrocarbons in rat liver epithelial cells. Mutat. Res. 615 (2007) 87-97
4. Arcaro K.F., O'Keefe P.W., Yang Y., Clayton W., and Gierthy J.F. Antiestrogenicity of environmental polycyclic aromatic hydrocarbons in human breast cancer cells. Toxicology 133 (1999) 115-127
5. Arcaro K.F., Yang Y., and Gierthy J.F. Benzo[k]fluoranthene enhancement and suppression of 17beta-estradiol catabolism in MCF-7 breast cancer cells. J. Toxicol. Environ. Health A 58 (1999) 413-426
6. Badawi A.F., Cavalieri E.L., and Rogan E.G. Effect of chlorinated hydrocarbons on expression of cytochrome P450 1A1 1A2 and 1B1 and 2- and 4-hydroxylation of 17beta-estradiol in female Sprague-Dawley rats. Carcinogenesis 21 (2000) 1593-1599
7. Baird W.M., Hooven L.A., and Mahadevan B. Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ. Mol. Mutagen. 45 (2005) 106-114
8. Barkhem T., Nilsson S., and Gustafsson J.A. Molecular mechanisms, physiological consequences and pharmacological implications of estrogen receptor action. Am. J. Pharmacogenomics 4 (2004) 19-28
9. Beischlag T.V., and Perdew G.H. ER alpha-AHR-ARNT protein-protein interactions mediate estradiol-dependent transrepression of dioxin-inducible gene transcription. J. Biol. Chem. 280 (2005) 21607-21611
10. Borman S.M., Christian P.J., Sipes I.G., and Hoyer P.B. Ovotoxicity in female Fischer rats and B6 mice induced by low-dose exposure to three polycyclic aromatic hydrocarbons: comparison through calculation of an ovotoxic index. Toxicol. Appl. Pharmacol. 167 (2000) 191-198
11. Boström C.E., Gerde P., Hanberg A., Jernström B., Johansson C., Kyrklund T., Rannug A., Törnqvist M., Victorin K., and Westerholm R. Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ. Health Perspect. 110 Suppl. 3 (2002) 451-488
12. Branham W.S., Fishman R., Streck R.D., Medlock K.L., De George J.J., and Sheehan D.M. ICI, 182 780 inhibits endogenous estrogen-dependent rat uterine growth and tamoxifen-induced developmental toxicity. Biol. Reprod. 54 (1996) 160-167
13. Branham W.S., Zehr D.R., and Sheehan D.M. Differential sensitivity of rat uterine growth and epithelium hypertrophy to estrogens and antiestrogens. Proc. Soc. Exp. Biol. Med. 203 (1993) 297-303
14. Carpenter D.O., Arcaro K., and Spink D.C. Understanding the human health effects of chemical mixtures. Environ. Health Perspect. 110 Suppl. 1 (2002) 25-42
15. Chaloupka K., Krishnan V., and Safe S. Polynuclear aromatic hydrocarbon carcinogens as antiestrogens in MCF-7 human breast cancer cells: role of the Ah receptor. Carcinogenesis 13 (1992) 2233-2239
16. Charles G.D., Bartels M.J., Zacharewski T.R., Gollapudi B.B., Freshour N.L., and Carney E.W. Activity of benzo[a]pyrene and its hydroxylated metabolites in an estrogen receptor-alpha reporter gene assay. Toxicol. Sci. 55 (2000) 320-326
17. Diel P., Schulz T., Smolnikar K., Strunck E., Vollmer G., and Michna H. Ability of xeno- and phytoestrogens to modulate expression of estrogen-sensitive genes in rat uterus: estrogenicity profiles and uterotropic activity. J. Steroid. Biochem. Mol. Biol. 73 (2000) 1-10
18. Durant J.L., Busby Jr. W.F., Lafleur A.L., Penman B.W., and Crespi C.L. Human cell mutagenicity of oxygenated, nitrated and unsubstituted polycyclic aromatic hydrocarbons associated with urban aerosols. Mutat. Res. 371 (1996) 123-157
19. Fertuck K.C., Kumar S., Sikka H.C., Matthews J.B., and Zacharewski T.R. Interaction of PAH-related compounds with the alpha and beta isoforms of the estrogen receptor. Toxicol. Lett. 121 (2001) 167-177
20. Fertuck K.C., Matthews J.B., and 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. 59 (2001) 231-240
21. Ford E., and Huggins C. Selective destruction in testis induced by 7,12-dimethylbenz[a]anthracene. J. Exp. Med. 118 (1963) 27-40
22. Gozgit J.M., Nestor K.M., Fasco M.J., Pentecost B.T., and 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. 196 (2004) 58-67
23. Hayes C.L., Spink D.C., Spink B.C., Cao J.Q., Walker N.J., and Sutter T.R. 17 beta-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 9776-9781
24. Jeffy B.D., Chirnomas R.B., and Romagnolo D.F. Epigenetics of breast cancer: polycyclic aromatic hydrocarbons as risk factors. Environ. Mol. Mutagen. 39 (2002) 235-244
25. Kang J.S., Lee B.J., Ahn B., Kim D.J., Nam S.Y., Yun Y.W., Nam K.T., Choi M., Kim H.S., Jang D.D., Lee Y.S., and Yang K.H. Expression of estrogen receptor alpha and beta in the uterus and vagina of immature rats treated with 17-ethinyl estradiol. J. Vet. Med. Sci. 65 (2003) 1293-1297
26. Kang K.S., Kim H.S., Ryu D.Y., Che J.H., and Lee Y.S. Immature uterotrophic assay is more sensitive than ovariectomized uterotrophic assay for the detection of estrogenicity of p-nonylphenol in Sprague-Dawley rats. Toxicol. Lett. 118 (2000) 109-115
27. Kanno J., Onyon L., Haseman J., Fenner-Crisp P., Ashby J., and Owens W. The OECD program to validate the rat uterotrophic bioassay to screen compounds for in vivo estrogenic responses: phase 1. Environ. Health Perspect. 109 (2001) 785-794
28. Kanno J., Onyon L., Peddada S., Ashby J., Jacob E., and Owens W. The OECD program to validate the rat uterotrophic bioassay. Phase 2: Dose-response studies. Environ. Health Perspect. 111 (2003) 1530-1549
29. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der Burg B., and Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139 (1998) 4252-4263
30. Kummer V., Mašková J., Zralý Z., Matiašovič J., and Faldyna M. Effect of postnatal exposure to benzo[a]pyrene on the uterus of immature rats. Exp. Toxicol. Pathol. 59 (2007) 69-76
31. Kwon Y.W., Ueda S., Ueno M., Yodoi J., and Masutani H. Mechanism of p53-dependent apoptosis induced by 3-methylcholanthrene: involvement of p53 phosphorylation and p38 MAPK. J. Biol. Chem. 277 (2002) 1837-1844
32. Lee A.J., Cai M.X., Thomas P.E., Conney A.H., and Zhu B.T. Characterization of the oxidative metabolites of 17beta-estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 144 (2003) 3382-3398
33. Liu S., Abdelrahim M., Khan S., Ariazi E., Jordan V.C., and Safe S. Aryl hydrocarbon receptor agonists directly activate estrogen receptor alpha in MCF-7 breast cancer cells. Biol. Chem. 387 (2006) 1209-1213
34. MacKenzie K.M., and Angevine D.M. Infertility in mice exposed in utero to benzo(a)pyrene. Biol. Reprod. 24 (1981) 183-191
35. Machala M., Neča J., Drábek P., Ulrich R., Šabatová V., Nezveda K., Raszyk J., and Gajdůšková V. Effects of chronic exposure to PCBs on cytochrome P450 systems and steroidogenesis in liver and testis of bulls (Bos taurus). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 120 (1998) 65-70
36. Machala M., Souček P., Neča J., Ulrich R., Lamka J., Szotáková B., and Skálová L. Inter-species comparisons of hepatic cytochrome P450 enzyme levels in male ruminants. Arch. Toxicol. 77 (2003) 555-560
37. Machala M., Vondráček J., Bláha L., Ciganek M., and Neča J. Aryl hydrocarbon receptor-mediated activity of mutagenic polycyclic aromatic hydrocarbons determined using in vitro reporter gene assay. Mutat. Res. 497 (2001) 49-62
38. Matthews J., and Gustafsson J.A. Estrogen receptor and aryl hydrocarbon receptor signaling pathways. Nucl. Recept. Signal. 4 (2006) e016
39. Medlock K.L., Branham W.S., and Sheehan D.M. Long-term effects of postnatal exposure to diethylstilbestrol on uterine estrogen receptor and growth. J. Steroid Biochem. Mol. Biol. 42 (1992) 23-28
40. Mesia-Vela S., Sanchez R.I., Li J.J., Li S.A., Conney A.H., and Kauffman F.C. Catechol estrogen formation in liver microsomes from female ACI and Sprague-Dawley rats: comparison of 2- and 4-hydroxylation revisited. Carcinogenesis 23 (2002) 1369-1372
41. Nawaz Z., Lonard D.M., Dennis A.P., Smith C.L., and O'Malley B.W. Proteasome-dependent degradation of the human estrogen receptor. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 1858-1862
42. Nebert D.W., and Dalton T.P. The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat. Rev. Cancer 6 (2006) 947-960
43. Nephew K.P., Long X., Osborne E., Burke K.A., Ahluwalia A., and Bigsby R.M. Effect of estradiol on estrogen receptor expression in rat uterine cell types. Biol. Reprod. 62 (2000) 168-177
44. Ohtake F., Baba A., Takada I., Okada M., Iwasaki K., Miki H., Takahashi S., Kouzmenko A., Nohara K., Chiba T., Fujii-Kuriyama Y., and Kato S. Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446 (2007) 562-566
45. Ohtake F., Takeyama K., Matsumoto T., Kitagawa H., Yamamoto Y., Nohara K., Tohyama C., Krust A., Mimura J., Chambon P., Yanagisawa J., Fujii-Kuriyama Y., and Kato S. Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 423 (2003) 545-550
46. Padilla-Banks E., Jefferson W.N., and Newbold R.R. The immature mouse is a suitable model for detection of estrogenicity in the uterotropic bioassay. Environ. Health Perspect. 109 (2001) 821-826
47. Pang S., Cao J.Q., Katz B.H., Hayes C.L., Sutter T.R., and Spink D.C. Inductive and inhibitory effects of non-ortho-substituted polychlorinated biphenyls on estrogen metabolism and human cytochromes P450 1A1 and 1B1. Biochem. Pharmacol. 58 (1999) 29-38
48. Pasqualini C., Sarrieau A., Dussaillant M., Corbani M., Bojda-Diolez F., Rostene W., and Kerdelhue B. Estrogen-like effects of 7, 12-dimethylbenz(a)anthracene on the female rat hypothalamo-pituitary axis. J. Steroid Biochem. 36 (1990) 485-491
49. Pearce S.T., Liu H., Radhakrishnan I., Abdelrahim M., Safe S., and Jordan V.C. Interaction of the aryl hydrocarbon receptor ligand 6-methyl-1,3,8-trichlorodibenzofuran with estrogen receptor alpha. Cancer Res. 64 (2004) 2889-2897
50. Piskorska-Pliszczynska J., Keys B., Safe S., and Newman M.S. The cytosolic receptor binding affinities and AHH induction potencies of 29 polynuclear aromatic hydrocarbons. Toxicol. Lett. 34 (1986) 67-74
51. Plíšková M., Vondráček J., Vojtěšek B., Kozubík A., and Machala M. Deregulation of cell proliferation by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells reflects both genotoxic and nongenotoxic events. Toxicol. Sci. 83 (2005) 246-256
52. Prough R.A., Burke M.D., and Mayer R.T. Direct fluorometric methods for measuring mixed function oxidase activity. Methods Enzymol. 52 (1978) 372-377
53. Rigdon R.H., and Rennels E.G. Effect of feeding benzpyrene on reproduction in the rat. Experientia 20 (1964) 224-226
54. Safe S., and Wormke M. Inhibitory aryl hydrocarbon receptor-estrogen receptor alpha cross-talk and mechanisms of action. Chem. Res. Toxicol. 16 (2003) 807-816
55. Santodonato J. Review of the estrogenic and antiestrogenic activity of polycyclic aromatic hydrocarbons: relationship to carcinogenicity. Chemosphere 34 (1997) 835-848
56. Saunders P.T., Maguire S.M., Gaughan J., and Millar M.R. Expression of oestrogen receptor beta (ER beta) in multiple rat tissues visualised by immunohistochemistry. J. Endocrinol. 154 (1997) R13-R16
57. Shimada T., Inoue K., Suzuki Y., Kawai T., Azuma E., Nakajima T., Shindo M., Kurose K., Sugie A., Yamagishi Y., Fujii-Kuriyama Y., and Hashimoto M. Arylhydrocarbon receptor-dependent induction of liver and lung cytochromes P450 1A1, 1A2, and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in genetically engineered C57BL/6J mice. Carcinogenesis 23 (2002) 1199-1207
58. Sjögren M., Ehrenberg L., and Rannug U. Relevance of different biological assays in assessing initiating and promoting properties of polycyclic aromatic hydrocarbons with respect to carcinogenic potency. Mutat. Res. 358 (1996) 97-112
59. Spink D.C., Lincoln II D.W., Dickerman H.W., and Gierthy J.F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin causes an extensive alteration of 17beta-estradiol metabolism in MCF-7 breast tumor cells. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 6917-6921
60. Spink D.C., Spink B.C., Cao J.Q., DePasquale J.A., Pentecost B.T., Fasco M.J., Li Y., and Sutter T.R. Differential expression of CYP1A1 and CYP1B1 in human breast epithelial cells and breast tumor cells. Carcinogenesis 19 (1998) 291-298
61. Ssempewba J., Carpenter D., Yilmaz B., DeCaprio A., O'Hehir D., and Arcaro K. Waste crankcase oil: an environmental contaminant with potential to modulate estrogenic responses. J. Toxicol. Environ. Health A 67 (2004) 1081-1094
62. Takemoto K., Nakajima M., Fujiki Y., Katoh M., Gonzalez F.J., and Yokoi T. Role of the aryl hydrocarbon receptor and CYP1B1 in the antiestrogenic activity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Arch. Toxicol. 78 (2004) 309-315
63. Takeyoshi M., Yamasaki K., Sawaki M., Nakai M., Noda S., and Takatsuki M. The efficacy of endocrine disruptor screening tests in detecting anti-estrogenic effects downstream of receptor-ligand interactions. Toxicol. Lett. 126 (2002) 91-98
64. Topinka J., Marvanová S., Vondráček J., Sevastyanova O., Nováková Z., Krčmář P., Pěnčíková K., and Machala M. DNA adducts formation and induction of apoptosis in rat liver epithelial 'stem-like' cells exposed to carcinogenic polycyclic aromatic hydrocarbons. Mutat. Res. 638 (2008) 122-132
65. Tsai K.S., Yang R.S., and Liu S.H. Benzo[a]pyrene regulates osteoblast proliferation through an estrogen receptor-related cyclooxygenase-2 pathway. Chem. Res. Toxicol. 17 (2004) 679-684
66. Tsuchiya Y., Nakajima M., Kyo S., Kanaya T., Inoue M., and Yokoi T. Human CYP1B1 is regulated by estradiol via estrogen receptor. Cancer Res. 64 (2004) 3119-3125
67. Tsuchiya Y., Nakajima M., and Yokoi T. Cytochrome P450-mediated metabolism of estrogens and its regulation in human. Cancer Lett. 227 (2005) 115-124
68. van Lipzig M.M.H., Vermeulen N.P.E., Gusinu R., Legler J., Frank H., Seidel A., and 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. 19 (2005) 41-55
69. Vondráček J., Kozubík A., and 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. 70 (2002) 193-201
70. Wang H., Masironi B., Eriksson H., and Sahlin L. A comparative study of estrogen receptors alpha and beta in the rat uterus. Biol. Reprod. 61 (1999) 955-964
71. WHO. Selected Non-Heterocyclic Polycyclic Aromatic Hydrocarbons (1998), WHO, Geneva
72. Xue W., and Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol. Appl. Pharmacol. 206 (2005) 73-93
73. Yamazaki H., Shaw P.M., Guengerich F.P., and Shimada T. Roles of cytochromes P450 1A2 and 3A4 in the oxidation of estradiol and estrone in human liver microsomes. Chem. Res. Toxicol. 11 (1998) 659-665
74. Yu A.M., Fukamachi K., Krausz K.W., Cheung C., and Gonzalez F.J. Potential role for human cytochrome P450 3A4 in estradiol homeostasis. Endocrinology 146 (2005) 2911-2919