A low halogenated biphenyl (PCB3) increases CYP1A1 expression and activity via the estrogen receptor beta in the porcine ovary

Journal of Physiology and Pharmacology

Volumn 59, Issue 3, 2008, Pages 577-588

  Ptak, A ^a   Ludewig, G ^b   Gregoraszczuk, Ewa Ł ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

AhR; CYP1A1; E2; ER ; ER ; PCB3; Prepubertal ovarian follicle

Indexed keywords

4 CHLOROBIPHENYL; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; POLYCHLORINATED BIPHENYL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; ESTROGEN METABOLISM; ESTROGEN RELEASE; GRANULOSA CELL; IMMUNOBLOTTING; NONHUMAN; OVARY; OVARY FOLLICLE CELL; PROTEIN EXPRESSION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SUZUKI REACTION; SWINE; SYNTHESIS; THECA CELL;

ANIMALS; BENZOFLAVONES; BIPHENYL COMPOUNDS; BLOTTING, WESTERN; COCULTURE TECHNIQUES; CYTOCHROME P-450 CYP1A1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GRANULOSA CELLS; OVARIAN FOLLICLE; OVARY; RECEPTORS, ARYL HYDROCARBON; SWINE; TAMOXIFEN; THECA CELLS;

EID: 53649086648     PISSN: 08675910     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (47)

1. Younglai EV, Foster WG, Hughes EG, Trim K, Jarrell JF. Levels of environmental contaminants in human follicular fluid, serum, and seminal plasma of couples undergoing in vitro fertilization. Arch Environ Contam Toxicol 2002; 43:121-126.
2. Kamarianos A, Karamanlis X, Goulas P, Theodosiadou E, Smokovitis A. The presence of environmental pollutants in the follicular fluid of farm animals (cattle, sheep, goats, and pigs). Reprod Toxicol 2003; 17: 185-190.
3. Hansen LG. Stepping backward to improve assessment of PCB congener toxicities. Environ Health Perspect. 1998; 106: Suppl 1, 171-189.
4. Parkinson A, Safe SH, Robertson LW, et al. Immunochemical quantitation of cytochrome P-450 isozymes and epoxide hydrolase in liver microsomes from polychlorinated or polybrominated biphenyl-treated rats. A study of structure-activity relationships. J Biol Chem 1983; 258; 5967-5976.
5. Conney AH. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G. H. A. Clowes Memorial Lecture. Cancer Res 1982; 42: 4875-4917.
6. Lee AJ, Cai MX, Thomas PE, Conney AH, Zhu BT. Characterization of the oxidative metabolites of 17beta-estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 2003; 144: 3382-3398.
7. Larsen MC, Angus WG, Brake PB, Eltom SE, Sukow KA, Jefcoate CR. Characterization of CYP1B1 and CYP1A1 expression in human mammary epithelial cells: role of the aryl hydrocarbon receptor in polycyclic aromatic hydrocarbon metabolism. Cancer Res 1998; 58: 2366-2374.
8. Hakkola J, Pasanen M, Hukkanen J et al. Expression of xenobiotic-metabolizing cytochrome P450 forms in human full-term placenta. Biochem Pharmacol 1996; 51: 403-411
9. Chakraborty C, Huet-Hudson YM, Dey SK. Catecholoestrogen synthesis and metabolism in the rabbit uterus during the periimplantation period. J Steroid Biochem 1990; 35: 39-46.
10. Leighton JK, Canning S, Guthrie HD, Hammond JM. Expression of cytochrome P450 1A1, an estrogen hydroxylase, in ovarian granulosa cells is developmentally regulated. J Steroid Biochem Mol Biol 1995; 52: 351-356.
11. Hakkola J, Pasanen M, Pelkonen O, et al. Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis 1997; 18: 391-397.
12. Bandiera S, Safe S, Okey AB. Binding of polychlorinated biphenyls classified as either phenobarbitone-, 3-methylcholanthrene- or mixed-type inducers to cytosolic Ah receptor. Chem Biol Interact 1982; 39: 259-277.
13. Whitlock JP. Induction of cytochrome P4501A1. Annu Rev Pharmacol Toxicol 1999; 39: 103-125.
14. Chaffin CL, Trewin AL, Hutz RJ. Estrous cycle-dependent changes in the expression of aromatic hydrocarbon receptor (AHR) and AHR-nuclear translocator (ARNT) mRNAs in the rat ovary and liver. Chem Biol Interact 2000; 124: 205-216.
15. Hasan A, Fischer B. Epithelial cells in the oviduct and vagina and steroid-synthesizing cells in the rabbit ovary express AhR and ARNT. Anat Embryol (Berl) 2003; 207: 9-18.
16. Khorram O, Garthwaite M, Golos T. Uterine and ovarian aryl hydrocarbon receptor (AHR) and aryl hydrocarbon receptor nuclear translocator (ARNT) mRNA expression in benign and malignant gynaecological conditions. Mol Hum Reprod 2002; 8: 75-80.
17. Robles R, Morita Y, Mann KK et al. The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology. 2000; 141: 450-453.
18. Wojtowicz A, Tomanek M, Augustowska K, Gregoraszczuk EL. Aromatic hydrocarbon receptor (AhR) in the porcine theca and granulosa cells: effect of TCDD, PCB 126 and PCB 153 on the expression of AhR. Endocr Regul 2005; 39: 109-118.
19. Kodavanti P, Tilson HA. Neurochemical effects of environmental chemicals: in vitro and in vivo correlations on second messenger pathways. Ann N Y Acad Sci 2000; 919: 97-105.
20. Raunio H, Husgafvel-Pursiainen K, Anttila S, Hietanen E, Hirvonen A, Pelkonen O. Diagnosis of polymorphisms in carcinogen-activating and inactivating enzymes and cancer susceptibility - a review. Gene 1995; 159: 113-121.
21. Nestler D, Risch M, Fischer B, Pocar P. Regulation of aryl hydrocarbon receptor activity in porcine cumulus-oocyte complexes in physiological and toxicological conditions: the role of follicular fluid. Reproduction 2007; 133: 887-897.
22. Dey A, Nebert DW. Markedly increased constitutive CYP1A1 mRNA levels in the fertilized ovum of the mouse. Biochem Biophys Res Commun 1998; 251: 657-661.
23. Pocar P, Augustin R, Fischer B. Constitutive expression of CYP1A1 in bovine cumulus oocyte-complexes in vitro: mechanisms and biological implications. Endocrinology 2004; 145: 1594-1601.
24. Myers MJ, Farrell DE, Howard KD, Kawalek JC. Identification of multiple constitutive and inducible hepatic cytochrome P450 enzymes in market weight swine. Drug Metab Dispos 2001; 29: 908-915.
25. Ptak A, Ludewig G, Kapiszewska M, et al. Induction of cytochromes P450, caspase-3 and DNA damage by PCB3 and its hydroxylated metabolites in porcine ovary. Toxicol Lett 2006; 166: 200-211.
26. Ptak A, Ludewig G, Lehmler HJ, Wojtowicz AK, Robertson LW, Gregoraszczuk E L. Comparison of the actions of 4-chlorobiphenyl and its hydroxylated metabolites on estradiol secretion by ovarian follicles in primary cells in culture. Reprod Toxicol 2005; 20: 57-64.
27. Ptak A, Ludewig G, Robertson L, Lehmler HJ, Gregoraszczuk EL. In vitro exposure of porcine prepubertal follicles to 4-chlorobiphenyl (PCB3) and its hydroxylated metabolites: effects on sex hormone levels and aromatase activity. Toxicol Lett 2006; 164: 113-122.
28. Bauer U, Amaro AR, Robertson LW. A new strategy for the synthesis of polychlorinated biphenyl metabolites. Chem Res Toxicol 1995; 8: 92-95.
29. Lehmler HJ, Robertson LW. Synthesis of hydroxylated PCB metabolites with the Suzuki-coupling. Chemosphere 2001; 45: 1119-1127.
30. Stoklosowa S, Bahr J, Gregoraszczuk E. Some morphological and functional characteristics of cells of the porcine theca interna in tissue culture. Biol Reprod 1978; 19: 712-719.
31. Stoklosowa S. Tissue culture of gonadal cells. Acta Biol Acad Sci Hung 1982; 33: 367-379.
32. Kennedy SW, Jones SP. Simultaneous measurement of cytochrome P4501A catalytic activity and total protein concentration with a fluorescence plate reader. Anal Biochem 1994; 222: 217-223.
33. Aoyama T, Korzekwa K, Nagata K, Gillette J, Gelboin HV, Gonzalez FJ. Estradiol metabolism by complementary deoxyribonucleic acid-expressed human cytochrome P450s. Endocrinology 1990; 126: 3101-3106.
34. Ball P, Knuppen R. Formation of 2- and 4-hydroxyestrogens by brain, pituitary, and liver of the human fetus. J Clin Endocrinol Metab 1978; 47: 732-737.
35. McLean MR, Bauer U, Amaro AR, Robertson LW. Identification of catechol and hydroquinone metabolites of 4-monochlorobiphenyl. Chem Res Toxicol 1996; 9: 158-164
36. Shimada T, Yamazaki H, Foroozesh M, Hopkins NE, Alworth WL, Guengerich FP. Selectivity of polycyclic inhibitors for human cytochrome P450s 1A1, 1A2, and 1B1. Chem Res Toxicol 1998; 11: 1048-56.
37. Barkhem T, Carlsson B, Nilsson Y, Enmark E, Gustafsson J, Nilsson S. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol Pharmacol 1998; 54: 105-112.
38. Ramadass P, Meerarani P, Toborek M, Robertson LW, Hennig B. Dietary flavonoids modulate PCB-induced oxidative stress, CYP1A1 induction, and AhR-DNA binding activity in vascular endothelial cells. Toxicol Sci 2003; 76: 212-9.
39. Fontaine F, Delescluse C, de Sousa G, Lesca P, Rahmani R. Cytochrome 1A1 induction by primaquine in human hepatocytes and HepG2 cells: absence of binding to the aryl hydrocarbon receptor. Biochem Pharmacol 1999; 57: 255-262.
40. Son DS, Roby KF, Rozman KK, Terranova PF. Estradiol enhances and estriol inhibits the expression of CYP1A1 induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in a mouse ovarian cancer cell line. Toxicology 2002; 176: 229-43.
41. Enmark E, Pelto-Huikko M, Grandien K, et al. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab 1997; 82: 4258-4265.
42. Couse JF, Lindzey J, Grandien K, Gustafsson JA, Korach KS. Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERalpha) and estrogen receptor-beta (ERbeta) messenger ribonucleic acid in the wild-type and ERalpha-knockout mouse. Endocrinology 1997; 138: 4613-4621.
43. Slomczynska M, Wozniak J. Differential distribution of estrogen receptor-beta and estrogen receptor-alpha in the porcine ovary. Exp Clin Endocrinol Diabetes 2001; 109: 238-244
44. Alarid ET, Bakopoulos N, Solodin N. Proteasome-madiated proteolysis if estrogen receptor: a novel component in autologous down-redulation. Mol Endocrinol 1999; 13: 1522-1534.
45. Wijayaratne AL, McDonnell DP. The human estrogen receptor- is a ubiquitinated protein whose stability is affected differentially by agonists, antagonists, and selective estrogen receptor modulators. J Biol Chem 2001; 21: 35684-35692.
46. Layton AC, Sanseverino J, Gregory BW, Easter JP, Sayler GS, Schultz TW. In vitro estrogen receptor binding of PCBs: measured activity and detection of hydroxylated metabolites in a recombinant yeast assay. Toxicol Appl Pharmacol 2002; 180: 157-163.
47. Routledge EJ, White R, Parker MG, Sumpter JP. Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ERbeta. J Biol Chem 2000; 275: 35986-35993.