2,3,7,8-Tetrachlorodibenzo-p-dioxin activates the aryl hydrocarbon receptor and alters sex steroid hormone secretion without affecting growth of mouse antral follicles in vitro

Toxicology and Applied Pharmacology

Volumn 261, Issue 1, 2012, Pages 88-96

  Karman, Bethany N ^a   Basavarajappa, Mallikarjuna S ^a   Craig, Zelieann R ^a   Flaws, Jodi A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Antral follicle; Aryl hydrocarbon receptor; Ovary; Proliferation; Steroidogenesis; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ANDROSTENEDIONE; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1B1; ESTRADIOL; PROGESTERONE; SEX HORMONE; TESTOSTERONE;

ANDROSTENEDIONE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ESTRADIOL BLOOD LEVEL; FEMALE; HORMONE RELEASE; IN VITRO STUDY; MOUSE; NONHUMAN; OVARY FOLLICLE; PROGESTERONE BLOOD LEVEL; STEROIDOGENESIS; TESTOSTERONE BLOOD LEVEL;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; DIOXINS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GONADAL STEROID HORMONES; MICE; OVARIAN FOLLICLE; PREGNENOLONE; RECEPTORS, ARYL HYDROCARBON; TIME FACTORS;

EID: 84860515849     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.03.015     Document Type: Article

References (67)

1. Baba T., Mimura J., Nakamura N., Harada N., Yamamoto M., Morohashi K., Fujii-Kuriyama Y. Intrinsic function of the aryl hydrocarbon (dioxin) receptor as a key factor in female reproduction. Mol. Cell. Biol. 2005, 25:10040-10051.
2. Badawi A.F., Cavalieri E.L., Rogan E.G. Role of human cytochrome P450 1A1, 1A2, 1B1, and 3A4 in the 2-, 4-, and 16[alpha]-hydroxylation of 17[beta]-estradiol. Metabolism 2001, 50:1001-1003.
3. Baldridge M.G., Hutz R.J. Autoradiographic localization of aromatic hydrocarbon receptor (AHR) in rhesus monkey ovary. Am. J. Primatol. 2007, 69:681-691.
4. Bengtsson M., Rydstrom J. Regulation of carcinogenic metabolism in the rat ovary by the estrous cycle and gonadotropin. Science 1983, 219:1437-1438.
5. Bhattacharyya K.K., Brake P.B., Eltom S.E., Otto S.A., Jefcoate C.R. Identification of a rat adrenal cytochrome P450 active in polycyclic hydrocarbon metabolism as rat CYP1B1. Demonstration of a unique tissue-specific pattern of hormonal and aryl hydrocarbon receptor-linked regulation. J. Biol. Chem. 1995, 270:11595-11602.
6. Birnbaum L.S., DeVito M.J. Use of toxic equivalency factors for risk assessment for dioxins and related compounds. Toxicology 1995, 105:391-401.
7. Brake P.B., Jefcoate C.R. Regulation of cytochrome P4501B1 in cultured rat adrenocortical cells by cyclic adenosine 3',5'-monophosphate and 2,3,7,8-tetrachlorodibenzo-p-dioxin. Endocrinology 1995, 136:5034-5041.
8. Cao J., Patisaul H.B., Petersen S.L. Aryl hydrocarbon receptor activation in lactotropes and gonadotropes interferes with estradiol-dependent and -independent preprolactin, glycoprotein alpha and luteinizing hormone beta gene expression. Mol. Cell. Endocrinol. 2011, 333:151-159.
9. Chaffin C.L., Peterson R.E., Hutz R.J. In utero and lactational exposure of female Holtzman rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin: modulation of the estrogen signal. Biol. Reprod. 1996, 55:62-67.
10. Cortvrindt R.G., Smitz J.E. Follicle culture in reproductive toxicology: a tool for in-vitro testing of ovarian function?. Hum. Reprod. Update 2002, 8:243-254.
11. Cortvrindt R., Smitz J., Van Steirteghem A.C. Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Hum. Reprod. 1997, 12:759-768.
12. Dasmahapatra A.K., Wimpee B.A., Trewin A.L., Wimpee C.F., Ghorai J.K., Hutz R.J. Demonstration of 2,3,7,8-tetrachlorodibenzo-p-dioxin attenuation of P450 steroidogenic enzyme mRNAs in rat granulosa cell in vitro by competitive reverse transcriptase-polymerase chain reaction assay. Mol. Cell. Endocrinol. 2000, 164:5-18.
13. Dasmahapatra A.K., Wimpee B.A., Trewin A.L., Hutz R.J. 2,3,7,8-Tetrachlorodibenzo-p-dioxin increases steady-state estrogen receptor-beta mRNA levels after CYP1A1 and CYP1B1 induction in rat granulosa cells in vitro. Mol. Cell. Endocrinol. 2001, 182:39-48.
14. Dasmahapatra A.K., Trewin A.L., Hutz R.J. Estrous cycle-regulated expression of CYP1B1 mRNA in the rat ovary. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2002, 133:127-134.
15. DeVito M.J., Thomas T., Martin E., Umbreit T.H., Gallo Antiestrogenic action of 2,3,7,8-tetrachlorodibenzo-p-dioxin: tissue specific regulation of estrogen receptor in CD1 mice. Toxicol. Appl. Pharmacol. 1992, 113:284-292.
16. DiBartolomeis M.J., Moore R.W., Peterson R.E., Christian B.J., Jefcoate C.R. Altered regulation of adrenal steroidogenesis in 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated rats. Biochem. Pharmacol. 1987, 36:59-67.
17. Edson M.A., Nagaraja A.K., Matzuk M.M. The mammalian ovary from genesis to revelation. Endocr. Rev. 2009, 30:624-712.
18. Eskenazi B., Warner M., Marks A.R., Samuels S., Gerthoux P.M., Vercellini P., Olive D.L., Needham L., Patterson D. Serum dioxin concentrations and age at menopause. Environ. Health Perspect. 2005, 113:858-862.
19. Frakes R.A., Zeeman C.Q., Mower B. Bioaccumulation of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) by fish downstream of pulp and paper mills in Maine. Ecotoxicol. Environ. Saf. 1993, 25:244-252.
20. Franczak A., Nynca A., Valdez K.E., Mizinga K.M., Petroff B.K. Effects of acute and chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin on the transition to reproductive senescence in female Sprague-Dawley rats. Biol. Reprod. 2006, 74:125-130.
21. Gao X., Mizuyachi K., Terranova P.F., Rozman K.K. 2,3,7,8-Tetrachlorodibenzo-p-dioxin decreases responsiveness of the hypothalamus to estradiol as a feedback inducer of preovulatory gonadotropin secretion in the immature gonadotropin-primed rat. Toxicol. Appl. Pharmacol. 2001, 170:181-190.
22. Gierthy J.F. Testing for endocrine disruption: how much is enough?. Toxicol. Sci. 2002, 68:1-3.
23. Gore A.C., Heindel J.J., Zoeller R.T. Endocrine disruption for endocrinologists (and others). Endocrinology 2006, 147:S1-S3.
24. Gray L.E., Ostby J.S. In utero 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters reproductive morphology and function in female rat offspring. Toxicol. Appl. Pharmacol. 1995, 133:285-294.
25. Gregoraszczuk E.L. Dioxin exposure and porcine reproductive hormonal activity. Cad. Saude Publica 2002, 18:453-462.
26. Gregoraszczuk E.L., Wójtowicz A.K., Zabielny E., Grochowalski A. Dose-and-time dependent effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on progesterone secretion by porcine luteal cells cultured in vitro. J. Physiol. Pharmacol. 2000, 51:127-135.
27. Gregoraszczuk E.L., Zabielny E., Ochwat D. Aryl hydrocarbon receptor (AhR)-linked inhibition of luteal cell progesterone secretion in 2,3,7,8-tetrachlorodibenzo-p-dioxin treated cells. J. Physiol. Pharmacol. 2001, 52:303-311.
28. Grochowalski A., Pieklo R., Gasinska A., Chrzaszcz R., Gregoraszczuk E.L. Accumulation of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in porcine preovulatory follicles after in vitro exposure to TCDD: effects on steroid secretion and cell proliferation. Cytobios 2000, 102:21-31.
29. Grochowalski A., Chrzaszcz R., Pieklo R., Gregoraszczuk E.L. Estrogenic and antiestrogenic effect of in vitro treatment of follicular cells with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Chemosphere 2001, 43:823-827.
30. Gupta R.K., Miller K.P., Babus J.K., Flaws J.A. Methoxychlor inhibits growth and induces atresia of antral follicles through an oxidative stress pathway. Toxicol. Sci. 2006, 93:382-389.
31. Hayes C.L., Spink D.C., Spink B.C., Cao J.Q., Walker N.J., Sutter T.R. 17 beta-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9776-9781.
32. Heimler I., Rawlins R.G., Owen H., Hutz R.J. Dioxin perturbs, in a dose- and time-dependent fashion, steroid secretion, and induces apoptosis of human luteinized granulosa cells. Endocrinology 1998, 139:4373-4379.
33. Heimler I., Trewin A.L., Chaffin C.L., Rawlins R.G., Hutz R.J. Modulation of ovarian follicle maturation and effects on apoptotic cell death in holtzman rats exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in utero and lactationally. Reprod. Toxicol. 1998, 12:69-73.
34. Hernández-Ochoa I., Karman B.N., Flaws J.A. The role of the aryl hydrocarbon receptor in the female reproductive system. Biochem. Pharmacol. 2009, 77:547-559.
35. Hirshfield A.N. Development of follicles in the mammalian ovary. Int. Rev. Cytol. 1991, 43-101.
36. Hites R.A. Dioxins: an overview and history. Environ. Sci. Technol. 2011, 45:16-20.
37. Humblet O., Williams P.L., Korrick S.A., Sergeyev O., Emond C., Birnbaum L.S., Burns J.S., Altshul L., Patterson D.G., Turner W.E., Lee M.M., Revich B., Hauser R. Dioxin and polychlorinated biphenyl concentrations in mother's serum and the timing of pubertal onset in sons. Epidemiology 2011, 22:827-835.
38. Jablonska O., Shi Z., Valdez K.E., Ting A.Y., Petroff B.K. Temporal and anatomical sensitivities to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin leading to premature acyclicity with age in rats. Int. J. Androl. 2010, 33:405-412.
39. Kleeman J.M., Moore R.W., Peterson R.E. Inhibition of testicular steroidogenesis in 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated rats: evidence that the key lesion occurs prior to or during pregnenolone formation. Toxicol. Appl. Pharmacol. 1990, 106:112-125.
40. Li X.L., Johnson D.C., Rozman K.K. Reproductive effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in female rats: ovulation, hormonal regulation, and possible mechanism(s). Toxicol. Appl. Pharmacol. 1995, 133:321-327.
41. Mizuyachi K., Son D.S., Rozman K.K., Terranova P.F. Alteration in ovarian gene expression in response to 2,3,7,8-tetrachlorodibenzo-p-dioxin: reduction of cyclooxygenase-2 in the blockage of ovulation. Reprod. Toxicol. 2002, 16:299-307.
42. Moore R.W., Jefcoate C.R., Peterson R.E. 2,3,7,8-Tetrachlorodibenzo-p-dioxin inhibits steroidogenesis in the rat testis by inhibiting the mobilization of cholesterol to cytochrome P450scc. Toxicol. Appl. Pharmacol. 1991, 109:85-97.
43. Morán F.M., Conley A.J., Corbin C.J., Enan E., VandeVoort C., Overstreet J.W., Lasley B.L. 2,3,7,8-Tetrachlorodibenzo-p-dioxin decreases estradiol production without altering the enzyme activity of cytochrome P450 aromatase of human luteinized granulosa cells in vitro. Biol. Reprod. 2000, 62:1102-1108.
44. Morán F.M., Vandevoort C.A., Overstreet J.W., Lasley B.L., Conley A.J. Molecular target of endocrine disruption in human luteinizing granulosa cells by 2,3,7,8-tetrachlorodibenzo-p-dioxin: inhibition of estradiol secretion due to decreased 17 alpha-hydroxylase/17,20-lyase cytochrome P450 expression. Endocrinology 2003, 144:467-473.
45. Morán F.M., Lohstroh P., Vandevoort C.A., Chen J., Overstreet J.W., Conley A.J., Lasley B.L. Exogenous steroid substrate modifies the effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on estradiol production of human luteinized granulosa cells in vitro. Biol. Reprod. 2003, 68:244-251.
46. Myllymäki S.A., Haavisto T.E., Brokken L.J., Viluksela M., Toppari J., Paranko J. In utero and lactational exposure to TCDD; steroidogenic outcomes differ in male and female rat pups. Toxicol. Sci. 2005, 88:534-544.
47. Otto S., Bhattacharyya K.K., Jefcoate C.R. Polycyclic aromatic hydrocarbon metabolism in rat adrenal, ovary, and testis microsomes is catalyzed by the same novel cytochrome P450 (P450RAP). Endocrinology 1992, 131:3067-3076.
48. Pesonen S.A., Haavisto T.E., Viluksela M., Toppari J., Paranko J. Effects of in utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on rat follicular steroidogenesis. Reprod. Toxicol. 2006, 22:521-528.
49. Petroff B.K., Mizinga K.M. Pharmacokinetics of ovarian steroids in Sprague-Dawley rats after acute exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Reprod. Biol. 2003, 3:131-141.
50. Petroff B.K., Roby K.F., Gao X., Son D.S., Williamsn S., Johnson D., Rozman K.K., Terranova P.F. A review of mechanisms controlling ovulation with implications for the anovulatory effects of polychlorinated dibenzo-p-dioxins in rodents. Toxicology 2001, 158:91-107.
51. Petroff B.K., Croutch C.R., Hunter D.M., Wierman M.E., Gao X. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) stimulates gonadotropin secretion in the immature female Sprague-Dawley rat through a pentobarbital- and estradiol-sensitive mechanism but does not alter gonadotropin-releasing hormone (GnRH) secretion by immortalized GnRH neurons in vitro. Biol. Reprod. 2003, 68:2100-2106.
52. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
53. Rowlands J.C., Gustafsson J.A. Aryl hydrocarbon receptor-mediated signal transduction. Crit. Rev. Toxicol. 1997, 27:109-134.
54. Savas U., Bhattacharyya K.K., Christou M., Alexander D.L., Jefcoate C.R. Mouse cytochrome P-450EF, representative of a new 1B subfamily of cytochrome P-450s. Cloning, sequence determination, and tissue expression. J. Biol. Chem. 1994, 269:14905-14911.
55. Schecter A., Birnbaum L., Ryan J.J., Constable J.D. Dioxins: an overview. Environ. Res. 2006, 101:419-428.
56. Shen Z., Wells R.L., Liu J., Elkind M.M. Identification of a cytochrome P450 gene by reverse transcription-PCR using degenerate primers containing inosine. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11483-11487.
57. Shen Z., Liu J., Wells R.L., Elkind M.M. cDNA cloning, sequence analysis, and induction by aryl hydrocarbons of a murine cytochrome P450 gene, Cyp1b1. DNA Cell Biol. 1994, 13:763-769.
58. Shi Z., Valdez K.E., Ting A.Y., Franczak A., Gum S.L., Petroff B.K. Ovarian endocrine disruption underlies premature reproductive senescence following environmentally relevant chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biol. Reprod. 2007, 76:198-202.
59. Smitz J.E., Cortvrindt R.G. The earliest stages of folliculogenesis in vitro. Reproduction 2002, 123:185-202.
60. Son D.S., Ushinohama K., Gao X., Taylor C.C., Roby K.F., Rozman K.K., Terranova P.F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) blocks ovulation by a direct effect on the ovary without alteration of ovarian steroidogenesis: lack of a direct effect on ovarian granulosa and thecal-interstitial cell steroidogenesis in vitro. Reprod. Toxicol. 1999, 13:521-530.
61. Spink D.C., Katz B.H., Hussain M.M., Pentecost B.T., Cao Z., Spink B.C. Estrogen regulates Ah responsiveness in MCF-7 breast cancer cells. Carcinogenesis 2003, 24:1941-1950.
62. Sutter T.R., Tang Y.M., Hayes C.L., Wo Y.Y., Jabs E.W., Li X., Yin H., Cody C.W., Greenlee W.F. Complete cDNA sequence of a human dioxin-inducible mRNA identifies a new gene subfamily of cytochrome P450 that maps to chromosome 2. J. Biol. Chem. 1994, 269:13092-13099.
63. Tsutsumi O., Uechi H., Sone H., Yonemoto J., Takai Y., Momoeda M., Tohyama C., Hashimoto S., Morita M., Taketani Y. Presence of dioxins in human follicular fluid: their possible stage-specific action on the development of preimplantation mouse embryos. Biochem. Biophys. Res. Commun. 2011, 250:498-501.
64. Tuppurainen K., Asikainen A., Ruokojärvi P., Ruuskanen J. Perspectives on the formation of polychlorinated dibenzo-p-dioxins and dibenzofurans during municipal solid waste (MSW) incineration and other combustion processes. Acc. Chem. Res. 2003, 36:652-658.
65. Ulaszewska M.M., Zuccato E., Davoli E. PCDD/Fs and dioxin-like PCBs in human milk and estimation of infants' daily intake: a review. Chemosphere 2011, 83:774-782.
66. Warner M., Eskenazi B., Olive D.L., Samuels S., Quick-Miles S., Vercellini P., Mocarelli P. Serum dioxin concentrations and quality of ovarian function in women of Seveso. Environ. Health Perspect. 2007, 115:336-340.
67. Wojtowicz A., Tomanek M., Augustowska K., Gregoraszczuk E.L. 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.