Maternal exposure to dioxin disrupts gonadotropin production in fetal rats and imprints defects in sexual behavior

Journal of Pharmacology and Experimental Therapeutics

Volumn 329, Issue 3, 2009, Pages 1091-1099

  Takeda, Tomoki ^a   Matsumoto, Yuki ^a   Koga, Takayuki ^a   Mutoh, Junpei ^a   Nishimura, Yoshio ^a   Shimazoe, Takao ^a   Ishii, Yuji ^a   Ishida, Takumi ^a   Yamada, Hideyuki ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CHORIONIC GONADOTROPIN; CYTOCHROME P450 17; CYTOCHROME P450 1A1; FOLLITROPIN; GONADOTROPIN; LUTEINIZING HORMONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; FETUS; GONADOTROPIN RELEASE; IMMUNOBLOTTING; MALE; MATURATION; NONHUMAN; ORGAN WEIGHT; OVARY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPRODUCTIVE TOXICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SEXUAL BEHAVIOR; STEROIDOGENESIS; TESTIS;

ANIMALS; BODY WEIGHT; CHORIONIC GONADOTROPIN; FEMALE; FETUS; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION; GONADOTROPINS, PITUITARY; LUTEINIZING HORMONE; MALE; MATERNAL EXPOSURE; OVARY; PHOSPHOPROTEINS; PITUITARY GLAND; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROSTATE; RATS; RATS, WISTAR; SEX DIFFERENTIATION DISORDERS; SEXUAL BEHAVIOR, ANIMAL; STEROID 17-ALPHA-HYDROXYLASE; TESTIS; TETRACHLORODIBENZODIOXIN;

EID: 66749135972     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.109.151282     Document Type: Article

References (39)

1. Apostolakis EM, Garai J, Fox C, Smith CL, Watson SJ, Clark JH, and O'Malley BW (1996) Dopaminergic regulation of progesterone receptors: brain D5 dopamine receptors mediate induction of lordosis by D1-like agonists in rats. J Neurosci 16:4823-4834. (Pubitemid 26269645)
2. Arnold AP and Gorski RA (1984) Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci 7:413-442. (Pubitemid 14155304)
3. Badawi AF, Cavalieri EL, and Rogan EG (2000) Effects of chlorinated hydrocarbon on expression of cytochrome P450 1A1, 1A2 and 1B1 and 2- and 4-hydroxylation of 17ß-estradiol in female Sprague-Dawley rats. Carcinogenesis 21:1593-1599. (Pubitemid 30603982)
4. Bakker J and Baum MJ (2008) Role for estradiol in female-typical brain and behavioral sexual differentiation. Front Neuroendocrinol 29:1-16.
5. Bjerke DL, Brown TJ, MacLusky NJ, Hochberg RB, and Peterson RE (1994) Partial demasclinization and feminization of sex behavior in male rat by in utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin is not associated with alterations in estrogen receptor binding or volumes of sexually differentiated brain nuclei. Toxicol Appl Pharmacol 127:258-267. (Pubitemid 24263714)
6. Burger LL, Haisenleder DJ, Dalkin AC, and Marshall JC (2004) Regulation of gonadotropin subunit gene transcription. J Mol Endocrinol 33:559-584. (Pubitemid 40057556)
7. Carlson RL (2007) Physiology and Behavior, 9th ed., Pearson Education, Boston, MA.
8. Davies EC, Shryne JE, and Gorski RA (1995) A revised critical period for the sexual differentiation of the sexually dimorphic nucleus of preoptic area in the rat. Neuroendocrinology 62:579-585.
9. Davies W and Wilkinson LS (2006) It is not all hormones: alternative explanations for sexual differentiation of the brain. Brain Res 1126:36-45. (Pubitemid 44895536)
10. Döhler KD, Hancke JL, Srivastava SS, Hofmann C, Shryne JE, and Gorski RA (1984) Participation of estrogens in female sexual differentiation of the brain: neuroanatomocal, neuroendocrine and behavioral evidence. Prog Brain Res 61:99-117.
11. Domingo JL and Bocio A (2007) Levels of PCDD/PCDFs and PCBs in edible marine species and human intake: a literature review. Environ Int 33:397-405. (Pubitemid 46319266)
12. El-Gehani F, Tena-Sempere M, and Huhtaniemi I (2000) Evidence that pituitary adenylate cyclase-activating polypeptide is a potent regulator of fetal rat testicular steroidogenesis. Biol Reprod 63:1482-1489.
13. El-Gehani F, Tena-Sempere M, Ruskoaho H, and Huhtaniemi I (2001) Natriuretic peptides stimulate steroidogenesis in the fetal rat testis. Biol Reprod 65:595-600. (Pubitemid 32702327)
14. El-Gehani F, Zhang FP, Pakarinen P, Rannikko A, and Huhtaniemi I (1998) Gonadotropin-independent regulation of steroidogenesis in the fetal rat testis. Biol Reprod 58:116-123. (Pubitemid 28023740)
15. Faqi AS, Dalsenter PR, Merker HJ, and Chahoud I (1998) Reproductive toxicity and tissue concentrations of low doses of 2,3,7,8-tetrachlorodibenzo-p- dioxin in male offspring rats exposed throughout pregnancy and lactation. Toxicol Appl Pharmacol 150:383-392. (Pubitemid 28302523)
16. Garcia-Falgueras A, Pinos H, Collado P, Pasaro E, Fernandez R, Segovia S, and Guillamon A (2005) The expression of brain sexual dimorphism in artificial secretion of rat strains. Brain Res 1052:130-138. (Pubitemid 41116770)
17. Gray LE Jr, Kelce WR, Monosson E, Ostby JS, and Birnbaum LS (1995) Exposure to TCDD during development permanently alters reproductive function in male Long Evans rats and hamsters: reduced ejaculated and epididymal sperm numbers and sex accessory gland weights in offspring with normal androgenic status. Toxicol Appl Pharmacol 131:108-118.
18. Haavisto T, Nurmela K, Pohjanvirta R, Huuskonen H, El-Gehani F, and Paranko J (2001) Prenatal testosterone and luteinizing hormone levels in male rats exposed during pregnancy to 2,3,7,8-tetrachlorodibenzo-p-dioxin and diethylstilbestrol. Mol Cell Endocrinol 178:169-179. (Pubitemid 32515360)
19. Habert R and Picon R (1982) Control of testicular steroidogenesis in foetal rat: effect of decapitation on testosterone and plasma luteinizing hormone-like activity. Acta Endocrinol 99:466-473. (Pubitemid 12165011)
20. Hardy DF and DeBold JF (1972) Effects of coital stimulation upon behavior of the female rat. J Comp Physiol Psychol 78:400-408.
21. Ishida T, Kan-o S, Mutoh J, Takeda S, Ishii Y, Hashiguchi I, Akamine A, and Yamada H (2005) 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced change in intestinal function and pathology: evidence for the involvement of arylhydrocarbon receptor-mediated alteration of glucose transportation. Toxicol Appl Pharmacol 205:89-97. (Pubitemid 40693273)
22. Larsen JC (2006) Risk assessments of polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and dioxin-like polychlorinated biphenyls in food. Mol Nutr Food Res 50:885-896. (Pubitemid 44621794)
23. Mably TA, Moore RW, and Peterson RE (1992a) In utero and lactational exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin: 1. Effects on androgenic status. Toxicol Appl Pharmacol 114:97-107.
24. Mably TA, Moore RW, Goy RW, and Peterson RE (1992b) In utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 114:108-117.
25. MacLusky NJ and Naftolin F (1981) Sexual differentiation of the central nervous system. Science 211:1294-1302. (Pubitemid 11097283)
26. Mutoh J, Taketoh J, Okamura K, Kagawa T, Ishida T, Ishii Y, and Yamada H (2006) Fetal pituitary gonadotropin as an initial target of dioxins in its impairment of cholesterol transportation and steroidogenesis in rats. Endocrinology 147:927-936. (Pubitemid 43113011)
27. Negri-Cesi P, Colciago A, Celotti F, and Motta M (2004) Sexual differentiation of the brain: role of testosterone and its active metabolites. J Endocrinol Invest 27 (Suppl 6:120-127.
28. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, and Pfaff DW (1998) Roles of estrogen receptor-α gene expression in reproduction-related behaviors in female mice. Endocrinology 139:5070-5081. (Pubitemid 28533455)
29. Ohtake F, Baba A, Takada I, Okada M, Iwasaki K, Miki H, Takahashi S, Kouzmenko A, Nohara K, Chiba T, et al. (2007) Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446:562-566. (Pubitemid 46514731)
30. Ohtake F, Takeyama K, Matsumoto T, Kitagawa H, Yamamoto Y, Nohara K, Tohyama C, Krust A, Mimura J, Chambon P, et al. (2003) Modulation of oestrogen receptor signaling by association with the activated dioxin receptor. Nature 423:545-550. (Pubitemid 36648579)
31. Peterson RE, Theobald HM, and Kimmel GL (1993) Developmental and reproductive toxicities of dioxins and related compounds: cross-species comparisons. Crit Rev Toxicol 23:283-335. (Pubitemid 23274471)
32. Poland A and Knutson JC (1982) 2,3,7,8-Tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: examination of the mechanism of toxicity. Annu Rev Pharmacol Toxicol 22:517-554.
33. Sato T, Matsumoto T, Kawano H, Watanabe T, Uematsu Y, Sekine K, Fukuda T, Aihara K, Krust A, Yamada T, et al. (2004) Brain masculinization requires androgen receptor function. Proc Natl Acad Sci U S A 101:1673-1678. (Pubitemid 38234213)
34. Schecter A, Birnbaum L, Ryan JJ, and Constable JD (2006) Dioxins: an overview. Environ Res 101:419-428. (Pubitemid 43782675)
35. Taketoh J, Mutoh J, Takeda T, Ogishima T, Takeda S, Ishii Y, Ishida T, and Yamada H (2007) Suppression of fetal testicular cytochrome P450 17 by maternal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin: a mechanism involving an initial effect on gonadotropin synthesis in the pituitary. Life Sci 80:1259-1267. (Pubitemid 46320457)
36. Timms BG, Peterson RE, and vom Saal FS (2002) 2,3,7,8-Tetrachlorodibenzo- p-dioxin interacts with endogenous estradiol to disrupt prostate gland morphogenesis in male rat fetuses. Toxicol Sci 67:264-274.
37. Valenstein ES, Kakolewski JW, and Cox VC (1967) Sex differences in taste preference for glucose and saccharin solutions. Science 156:942-943.
38. Wilson CA and Davies DC (2007) The control of sexual differentiation of the reproductive system and brain. Reproduction 133:331-359. (Pubitemid 46359523)
39. Wilson JD, George FW, and Griffin JE (1981) The hormonal control of sexual development. Science 211:1278-1284. (Pubitemid 11097281)