Formation of estrogenic metabolites of benzo[a]pyrene and chrysene by cytochrome P450 activity and their combined and supra-maximal estrogenic activity

Environmental Toxicology and Pharmacology

Volumn 19, Issue 1, 2005, Pages 41-55

  Van Lipzig, Marola M H ^a   Vermeulen, Nico P E ^a   Gusinu, Renato ^a   Legler, Juliette ^b   Frank, Heinz ^c   Seidel, Albrecht ^c   Meerman, John H N ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b INSTITUTE FOR ENVIRONMENTAL STUDIES   (Netherlands)

^c Prof Dr Gernot Grimmer Foundation   (Germany)

Author keywords

Aryl hydrocarbon receptor; Benzo a pyrene; Chrysene; Cytochrome P450; Estrogen receptor; Mixture effects

Indexed keywords

3',4' DIMETHOXYFLAVONE; AROMATIC HYDROCARBON; BENZO[A]PYRENE; CHRYSENE; CYTOCHROME P450; HORMONE ANTAGONIST; UNCLASSIFIED DRUG;

ARTICLE; BINDING ASSAY; CONCENTRATION (PARAMETERS); ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HORMONE ACTION; HORMONE BLOOD LEVEL; HUMAN; HUMAN CELL; HYDROXYLATION; LIVER MICROSOME; MAMMAL; PRIORITY JOURNAL; RECEPTOR AFFINITY; RECEPTOR BLOCKING; REPORTER GENE; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

MAMMALIA;

EID: 10044239183     PISSN: 13826689     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.etap.2004.03.010     Document Type: Article

References (66)

1. J.B. Adams, N.S. Phillips, and C.E. Young Formation of glucuronides of estradiol-17 beta by human mammary cancer cells J. Steroid Biochem. 33 5 1989 1023 1025
2. E.T. Alarid, N. Bakopoulos, and N. Solodin Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation Mol. Endocrinol. 13 9 1999 1522 1534
3. R. Altenburger, W. Bodeker, M. Faust, and L.H. Grimme Evaluation of the isobologram method for the assessment of mixtures of chemicals. Combination effect studies with pesticides in algal biotests Ecotoxicol. Environ. Saf. 20 1 1990 98 114
4. W.G. Angus, M.C. Larsen, and C.R. Jefcoate Expression of CYP1A1 and CYP1B1 depends on cell-specific factors in human breast cancer cell lines: role of estrogen receptor status Carcinogenesis 20 6 1999 947 955
5. G.M. Anstead, K.E. Carlson, and J.A. Katzenellenbogen The estradiol pharmacophore: ligand structure-estrogen receptor binding affinity relationships and a model for the receptor binding site Steroids 62 3 1997 268 303
6. K.F. Arcaro, P.W. O'Keefe, Y. Yang, W. Clayton, and J.F. Gierthy Antiestrogenicity of environmental polycyclic aromatic hydrocarbons in human breast cancer cells Toxicology 133 2-3 1999 115 127
7. F. Ariese, W.H.O. Ernst, and D.T.H.M. Sijm Natural and synthetic organic compounds in the environment - a symposium report Environ. Toxicol. Phar. 10 3 2001 65 80
8. K.E. Aspry, and L.F. Bjeldanes Effects of dietary broccoli and butylated hydroxyanisole on liver-mediated metabolism of benzo[a]pyrene Food Chem. Toxicol. 21 2 1983 133 142
9. T. Backhaus, M. Scholze, and L.H. Grimme The single substance and mixture toxicity of quinolones to the bioluminescent bacterium Vibrio fischeri Aquat. Toxicol. 49 1/2 2000 49 61
10. E. Bauer, Z. Guo, Y.F. Ueng, L.C. Bell, D. Zeldin, and F.P. Guengerich Oxidation of benzo[a]pyrene by recombinant human cytochrome P450 enzymes Chem. Res. Toxicol. 8 1 1995 136 142
11. J.G. Bessems, J.M. Te Koppele, P.A. Van Dijk, L.L. Van Stee, J.N. Commandeur, and N.P. Vermeulen Rat liver microsomal cytochrome P450-dependent oxidation of 3,5-disubstituted analogues of paracetamol Xenobiotica 26 6 1996 647 666
12. H.K. Bhat, J.V. Vadgama, and T. Loya Critical role of oxidative stress in estrogen-induced carcinogenesis Proceedings of the AACR 93rd Annual Meeting San Francisco 2002
13. A.M. Brzozowski, A.C. Pike, Z. Dauter, R.E. Hubbard, T. Bonn, O. Engstrom, L. Ohman, G.L. Greene, J.A. Gustafsson, and M. Carlquist Molecular basis of agonism and antagonism in the oestrogen receptor Nature 389 6652 1997 753 758
14. E.L. Cavalieri, S. Higginbotham, N.V. RamaKrishna, P.D. Devanesan, R. Todorovic, E.G. Rogan, and S. Salmasi Comparative dose-response tumorigenicity studies of dibenzo[alpha,l]pyrene versus 7,12-dimethylbenz[alpha]anthracene, benzo[alpha]pyrene and two dibenzo[alpha,l]pyrene dihydrodiols in mouse skin and rat mammary gland Carcinogenesis 12 10 1991 1939 1944
15. C.Y. Chang, and A. Puga Constitutive activation of the aromatic hydrocarbon receptor Mol. Cell. Biol. 18 1 1998 525 535
16. G.D. Charles, M.J. Bartels, T.R. Zacharewski, B.B. Gollapudi, N.L. Freshour, and E.W. Carney Activity of benzo[a]pyrene and its hydroxylated metabolites in an estrogen receptor-alpha reporter gene assay Toxicol. Sci. 55 2 2000 320 326
17. A.O. Cheek, P.M. Vonier, E. Oberdorster, B.C. Burow, and J.A. McLachlan Environmental signaling: a biological context for endocrine disruption Environ. Health Perspect. 106 Suppl. 1 1998 5 10
18. J.W. Cook, E.C. Dodds, C.L. Hewett, and C.W. Lawson The oestrogenic activity of some condensed-ring compounds in relation to their other biological activities Proc. R. Soc. B 114 1934 272 286
19. J.W. Cook, E.C. Dodds, and C.L. Hewett A synthetic oestrus-exciting compound Nature 14 1933
20. B.J. Danzo Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins Environ. Health Perspect. 105 3 1997 294 301
21. M. Denison, A. Pandini, S. Nagy, E. Baldwin, and L. Bonati Ligand binding and activation of the Ah receptor Chem. Biol. Interact. 141 1-2 2002 3
22. R.M. Evans The steroid and thyroid hormone receptor superfamily Science 240 4854 1988 889 895
23. K.C. Fertuck, S. Kumar, H.C. Sikka, J.B. Matthews, and T.R. Zacharewski Interaction of PAH-related compounds with the alpha and beta isoforms of the estrogen receptor Toxicol. Lett. 121 3 2001 167 177
24. K.C. Fertuck, J.B. Matthews, and T.R. Zacharewski 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 2 2001 231 240
25. B.D. Gehm, J.M. McAndrews, P.Y. Chien, and J.L. Jameson Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor Proc. Natl. Acad. Sci. U.S.A. 94 25 1997 14138 14143
26. D.J. Gmur, and U. Varanasi Characterization of benzo[a]pyrene metabolites isolated from muscle, liver, and bile of a juvenile flatfish Carcinogenesis 3 12 1982 1397 1403
27. F.J. Gonzalez, C.L. Crespi, and H.V. Gelboin DNA-expressed human cytochrome P450s: a new age of molecular toxicology and human risk assessment Mutat. Res. 247 1 1991 113 127
28. G. Grimmer Analysis of automobile exhaust condensates IARC Sci. Publ. 16 1977 29 39
29. S.S. Hecht, K. el-Bayoumy, A. Rivenson, and S. Amin Potent mammary carcinogenicity in female CD rats of a fjord region diol-epoxide of benzo[c]phenanthrene compared to a bay region diol-epoxide of benzo[a]pyrene Cancer Res. 54 1 1994 21 24
30. T. Hirose, K. Morito, R. Kizu, A. Toriba, K. Hayakawa, S. Ogawa, S. Inoue, M. Muramatsu, and Y. Masamune Estrogenic/antiestrogenic activities of benzo[a]pyrene monohydroxy derivatives J. Health Sci. 47 6 2001 552 558
31. IARC Benzo[a]pyrene. IARC Monograms on the Evaluation of the carcinogenic Risk of Chemicals to Man 1973 International Agency for Research on Cancer Lyon, France pp. 91-136
32. J. Jacob, G. Grimmer, G. Raab, M. Emura, M. Riebe, and U. Mohr Comparison of chrysene metabolism in epithelial human bronchial and Syrian hamster lung cells Cancer Lett. 38 1/2 1987 171 180
33. I. Kharat, and F. Saatcioglu Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin are mediated by direct transcriptional interference with the liganded estrogen receptor. Cross-talk between aryl hydrocarbon- and estrogen-mediated signaling J. Biol. Chem. 271 18 1996 10533 10537
34. J.H. Kim, K.H. Stansbury, N.J. Walker, M.A. Trush, P.T. Strickland, and T.R. Sutter Metabolism of benzo[a]pyrene and benzo[a]pyrene-7,8-diol by human cytochrome P450 1B1 Carcinogenesis 19 10 1998 1847 1853
35. A. Kortenkamp, and R. Altenburger Approaches to assessing combination effects of oestrogenic environmental pollutants Sci. Total Environ. 233 1-3 1999 131 140
36. G.G. Kuiper, B. Carlsson, K. Grandien, E. Enmark, J. Haggblad, S. Nilsson, and J.A. Gustafsson Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta Endocrinology 138 3 1997 863 870
37. J.E. Lee, and S. Safe 3′,4′-Dimethoxyflavone as an aryl hydrocarbon receptor antagonist in human breast cancer cells Toxicol. Sci. 58 2 2000 235 242
38. J. Legler, C.E. van den Brink, A. Brouwer, A.J. Murk, P.T. van der Saag, A.D. Vethaak, and B. van der Burg Development of a stably transfected estrogen receptor-mediated luciferase reporter gene assay in the human T47D breast cancer cell line Toxicol. Sci. 48 1 1999 55 66
39. W. Levin, A.W. Wood, R.L. Chang, H. Yagi, H.D. Mah, D.M. Jerina, and A.H. Conney Evidence for bay region activation of chrysene 1,2-dihydrodiol to an ultimate carcinogen Cancer Res. 38 6 1978 1831 1834
40. J.J. Li, X. Hou, J. Bentel, E.M. Yazlovitskaya, and S.A. Li Prevention of estrogen carcinogenesis in the hamster kidney by ethinylestradiol: some unique properties of a synthetic estrogen Carcinogenesis 19 3 1998 471 477
41. T. Madigou, C. Tiffoche, G. Lazennec, J. Pelletier, and M.L. Thieulant The sheep estrogen receptor: cloning and regulation of expression in the hypothalamo-pituitary axis Mol. Cell. Endocrinol. 121 2 1996 153 163
42. J.A. McLachlan, K.S. Korach, R.R. Newbold, and G.H. Degen Diethylstilbestrol and other estrogens in the environment Fundam. Appl. Toxicol. 4 5 1984 686 691
43. C.E. Morreal, S.L. Schneider, D.K. Sinha, and R.E. Bronstein Estrogenic properties of 3,9-dihydroxy-7,12-dimethylbenz[a]anthracene in rats J. Natl. Cancer Inst. 62 6 1979 1585 1588
44. A.J. Murk, J. Legler, M.M.H. van Lipzig, J.H. Meerman, A.C. Belfroid, A. Spenkelink, B. van der Burg, G.B. Rijs, and D. Vethaak Detection of estrogenic potency in wastewater and surface water with three in vitro bioassays Environ. Toxicol. Chem. 21 1 2002 16 23
45. F. Ohtake, K. Takeyama, T. Matsumoto, H. Kitagawa, Y. Yamamoto, K. Nohara, C. Tohyama, A. Krust, J. Mimura, P. Chambon, J. Yanagisawa, Y. Fujii-Kuriyama, and S. Kato Modulation of oestrogen receptor signalling by association with the activated dioxin receptor Nature 423 6939 2003 545 550
46. R.v.d. Oost, J. Beyer, and N.P.E. Vermeulen Fish biomarkers and environmental risk assessment: a review Environ. Toxicol. Appl. Pharmacol. 13 2003 57 149
47. O. Pelkonen, and D.W. Nebert Metabolism of polycyclic aromatic hydrocarbons: etiologic role in carcinogenesis Pharmacol. Rev. 34 2 1982 189 222
48. J.J. Pink, and V.C. Jordan Models of estrogen receptor regulation by estrogens and antiestrogens in breast cancer cell lines Cancer Res. 56 10 1996 2321 2330
49. P.J. Ruddock, D.J. Bird, and D.V. McCalley Bile metabolites of polycyclic aromatic hydrocarbons in three species of fish from the Severn Estuary Ecotoxicol. Environ. Saf. 51 2 2002 97 105
50. S. Safe, and V. Krishnan Chlorinated hydrocarbons: estrogens and antiestrogens Toxicol. Lett. 82/83 1995 731 736
51. J. Santodonato Review of the estrogenic and antiestrogenic activity of polycyclic aromatic hydrocarbons: relationship to carcinogenicity Chemosphere 34 4 1997 835 848
52. T. Shimada, C.L. Hayes, H. Yamazaki, S. Amin, S.S. Hecht, F.P. Guengerich, and T.R. Sutter Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1 Cancer Res. 56 13 1996 2979 2984
53. P. Skehan, R. Storeng, D. Scudiero, A. Monks, J. McMahon, D. Vistica, J.T. Warren, H. Bokesch, S. Kenney, and M.R. Boyd New colorimetric cytotoxicity assay for anticancer-drug screening J. Natl. Cancer Inst. 82 13 1990 1107 1112
54. A.M. Soto, C. Sonnenschein, K.L. Chung, M.F. Fernandez, N. Olea, and F.O. Serrano The E-screen assay as a tool to identify estrogens: an update on estrogenic environmental pollutants Environ. Health Perspect. 103 Suppl. 7 1995 113 122
55. B.C. Spink, B.H. Katz, M.M. Hussain, S. Pang, S.P. Connor, K.M. Aldous, J.F. Gierthy, and D.C. Spink SULT1A1 catalyzes 2-methoxyestradiol sulfonation in MCF-7 breast cancer cells Carcinogenesis 21 11 2000 1947 1957
56. D.C. Spink, B.H. Katz, M.M. Hussain, B.C. Spink, S.J. Wu, N. Liu, R. Pause, and L.S. Kaminsky Induction of CYP1A1 and CYP1B1 in T-47D human breast cancer cells by benzo[a]pyrene is diminished by arsenite Drug Metab. Dispos. 30 3 2002 262 269
57. P.W. Sylvester, C.F. Aylsworth, D.A. Van Vugt, and J. Meites Effects of alterations in early hormonal environment on development and hormone dependency of carcinogen-induced mammary tumors in rats Cancer Res. 43 11 1983 5342 5346
58. M.J. Thirman, J.H. Albrecht, M.A. Krueger, R.R. Erickson, D.L. Cherwitz, S.S. Park, H.V. Gelboin, and J.L. Holtzman Induction of cytochrome CYPIA1 and formation of toxic metabolites of benzo[a]pyrene by rat aorta: a possible role in atherogenesis Proc. Natl. Acad. Sci. U.S.A. 91 12 1994 5397 5401
59. Y. Tian, S. Ke, T. Thomas, R.J. Meeker, and M.A. Gallo Transcriptional suppression of estrogen receptor gene expression by 2,3,7,8-tetrachlorodibenzo- p-dioxin (TCDD) J. Steroid Biochem. Mol. Biol. 67 1 1998 17 24
60. D.Q. Tran, C.F. Ide, J.A. McLachlan, and S.F. Arnold The anti-estrogenic activity of selected polynuclear aromatic hydrocarbons in yeast expressing human estrogen receptor Biochem. Biophys. Res. Commun. 229 1 1996 101 108
61. T. Tsutsui, and J.C. Barrett Neoplastic transformation of cultured mammalian cells by estrogens and estrogenlike chemicals Environ. Health Perspect. 105 Suppl. 3 1997 619 624
62. van Lipzig, M.M.H., Laak, A.M.t., Jongejan, A., Vermeulen, N.P.E., Wamelink, M., Geerke, D., Meerman, J.H.N., 2004. Prediction of ligand binding affinity and orientation of (Xeno)estrogens to the estrogen receptor by molecular dynamics simulations and the linear interaction energy method. J. Med. Chem. 47 (4), 1018-1030.
63. E.A. Vladusic, A.E. Hornby, F.K. Guerra-Vladusic, J. Lakins, and R. Lupu Expression and regulation of estrogen receptor beta in human breast tumors and cell lines Oncol. Rep. 7 1 2000 157 167
64. C.L. Waller, T.I. Oprea, K. Chae, H.K. Park, K.S. Korach, S.C. Laws, T.E. Wiese, W.R. Kelce, and L.E. Gray Jr. Ligand-based identification of environmental estrogens Chem. Res. Toxicol. 9 8 1996 1240 1248
65. M. Wormke, M. Stoner, B. Saville, and S. Safe Crosstalk between estrogen receptor alpha and the aryl hydrocarbon receptor in breast cancer cells involves unidirectional activation of proteasomes FEBS Lett. 478 1/2 2000 109 112
66. N.C. Yang, A.J. Castro, M. Lewis, and T.W. Wong Polynuclear aromatic hydrocarbons, steroids and carcinogenesis Science 134 1961 386 387