Effects of maternal exposure to di-isononylphthalate (DINP) and 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene (p,p′-DDE) on steroidogenesis in the fetal rat testis and adrenal gland

Reproductive Toxicology

Volumn 28, Issue 1, 2009, Pages 66-74

  Adamsson, A ^a   Salonen, V ^a   Paranko, J ^a   Toppari, J ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

1,1 Dichloro 2,2 bis(p chlorophenyl)ethylene; Adrenal; Di isononylphthalate; Environmental antiandrogen; Fetus; Rat; Steroidogenesis; Testis

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ANDROGEN RECEPTOR; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); DI ISONONYLPHTHALATE; PHTHALIC ACID; STEROIDOGENIC ACUTE REGULATORY PROTEIN; UNCLASSIFIED DRUG;

ADRENAL CELL; ADRENAL GLAND; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; FEMALE; FETUS; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRENATAL EXPOSURE; PROTEIN EXPRESSION; RAT; SEX DIFFERENTIATION; STEROIDOGENESIS; STRUCTURE ANALYSIS; TESTIS; TESTIS CELL;

3-HYDROXYSTEROID DEHYDROGENASES; ADRENAL CORTEX HORMONES; ADRENAL GLANDS; ANDROGEN ANTAGONISTS; ANIMALS; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; DICHLORODIPHENYL DICHLOROETHYLENE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GESTATIONAL AGE; GONADAL STEROID HORMONES; MALE; MATERNAL EXPOSURE; PHOSPHOPROTEINS; PHTHALIC ACIDS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ANDROGEN; RNA, MESSENGER; TESTIS;

RATTUS;

EID: 67349201658     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2009.03.002     Document Type: Article

References (49)

1. Bay K., Asklund C., Skakkebaek N.E., and Andersson A.M. Testicular dysgenesis syndrome: possible role of endocrine disrupters. Best Pract Res Clin Endocrinol Metab 20 (2006) 77-90
2. Hotchkiss A.K., Rider C.V., Blystone C.R., Wilson V.S., Hartig P.C., Ankley G.T., et al. Fifteen years after "Wingspread"-environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol Sci 105 (2008) 235-259
3. Skakkebaek N.E., Jorgensen N., Main K.M., Rajpert-De Meyts E., Leffers H., Andersson A.M., et al. Is human fecundity declining?. Int J Androl 29 (2006) 2-11
4. Gray Jr. L.E., Wilson V.S., Stoker T., Lambright C., Furr J., Noriega N., et al. Adverse effects of environmental antiandrogens and androgens on reproductive development in mammals. Int J Androl 29 (2006) 96-104 discussion 105-8
5. Wilson V.S., Blystone C.R., Hotchkiss A.K., Rider C.V., and Gray Jr. L.E. Diverse mechanisms of anti-androgen action: impact on male rat reproductive tract development. Int J Androl 31 (2008) 178-187
6. Wilson J.D. Sexual differentiation. Annu Rev Physiol 40 (1978) 279-306
7. Kelce W.R., Stone C.R., Laws S.C., Gray L.E., Kemppainen J.A., and Wilson E.M. Persistent DDT metabolite p,p′-DDE is a potent androgen receptor antagonist. Nature 375 (1995) 581-585
8. Gray Jr. L.E., Ostby J.S., and Kelce W.R. Developmental effects of an environmental antiandrogen: the fungicide vinclozolin alters sex differentiation of the male rat. Toxicol Appl Pharmacol 129 (1994) 46-52
9. Welsh M., Saunders P.T., Fisken M., Scott H.M., Hutchison G.R., Smith L.B., et al. Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. J Clin Invest 118 (2008) 1479-1490
10. El-Gehani F., Zhang F.P., Pakarinen P., Rannikko A., and Huhtaniemi I. Gonadotropin-independent regulation of steroidogenesis in the fetal rat testis. Biol Reprod 58 (1998) 116-123
11. Tapanainen J., Kuopio T., Pelliniemi L.J., and Huhtaniemi I. Rat testicular endogenous steroids and number of Leydig cells between the fetal period and sexual maturity. Biol Reprod 31 (1984) 1027-1035
12. Dupouy J.P., Coffigny H., and Magre S. Maternal and foetal corticosterone levels during late pregnancy in rats. J Endocrinol 65 (1975) 347-352
13. Kalavsky S.M. Fetal rat adrenal steroidogenesis. Biol Neonate 17 (1971) 427-435
14. Liggins G.C. The role of cortisol in preparing the fetus for birth. Reprod Fertil Dev 6 (1994) 141-150
15. Gotoh H., Kusakabe M., Shiroishi T., and Moriwaki K. Survival of steroid 21-hydroxylase-deficient mice without endogenous corticosteroids after neonatal treatment and genetic rescue by transgenesis as a model system for treatment of congenital adrenal hyperplasia in humans. Endocrinology 135 (1994) 1470-1476
16. Kavlock R., Boekelheide K., Chapin R., Cunningham M., Faustman E., Foster P., et al. NTP Center for the Evaluation of Risks to Human Reproduction: phthalates expert panel report on the reproductive and developmental toxicity of di-isononyl phthalate. Reprod Toxicol 16 (2002) 679-708
17. Babich M.A., Chen S.B., Greene M.A., Kiss C.T., Porter W.K., Smith T.P., et al. Risk assessment of oral exposure to diisononyl phthalate from children's products. Regul Toxicol Pharmacol 40 (2004) 151-167
18. Gray Jr. L.E., Ostby J., Furr J., Price M., Veeramachaneni D.N., and Parks L. Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci 58 (2000) 350-365
19. Barlow N.J., Phillips S.L., Wallace D.G., Sar M., Gaido K.W., and Foster P.M. Quantitative changes in gene expression in fetal rat testes following exposure to di(n-butyl) phthalate. Toxicol Sci 73 (2003) 431-441
20. Borch J., Ladefoged O., Hass U., and Vinggaard A.M. Steroidogenesis in fetal male rats is reduced by DEHP and DINP, but endocrine effects of DEHP are not modulated by DEHA in fetal, prepubertal and adult male rats. Reprod Toxicol 18 (2004) 53-61
21. Parks L.G., Ostby J.S., Lambright C.R., Abbott B.D., Klinefelter G.R., Barlow N.J., et al. The plasticizer diethylhexyl phthalate induces malformations by decreasing fetal testosterone synthesis during sexual differentiation in the male rat. Toxicol Sci 58 (2000) 339-349
22. Lehmann K.P., Phillips S., Sar M., Foster P.M., and Gaido K.W. Dose-dependent alterations in gene expression and testosterone synthesis in the fetal testes of male rats exposed to di (n-butyl) phthalate. Toxicol Sci 81 (2004) 60-68
23. Thompson C.J., Ross S.M., Hensley J., Liu K., Heinze S.C., Young S.S., et al. Differential steroidogenic gene expression in the fetal adrenal gland versus the testis and rapid and dynamic response of the fetal testis to di(n-butyl) phthalate. Biol Reprod 73 (2005) 908-917
24. Dustman E.H., and Stickel L.F. The occurrence and significance of pesticide residues in wild animals. Ann NY Acad Sci 160 (1969) 162-172
25. Morgan D.P., and Roan C.C. Absorption, storage, and metabolic conversion of ingested DDT and DDT metabolites in man. Arch Environ Health 22 (1971) 301-308
26. You L., Casanova M., Archibeque-Engle S., Sar M., Fan L.Q., and Heck H.A. Impaired male sexual development in perinatal Sprague-Dawley and Long-Evans hooded rats exposed in utero and lactationally to p,p′-DDE. Toxicol Sci 45 (1998) 162-173
27. Gonzalez R.J., Tamm E.P., Ng C., Phan A.T., Vassilopoulou-Sellin R., Perrier N.D., et al. Response to mitotane predicts outcome in patients with recurrent adrenal cortical carcinoma. Surgery 142 (2007) 867-875 discussion 867-75
28. Schteingart D.E., Motazedi A., Noonan R.A., and Thompson N.W. Treatment of adrenal carcinomas. Arch Surg 117 (1982) 1142-1146
29. Orth D.N. Cushing's syndrome. N Engl J Med 332 (1995) 791-803
30. Haavisto T., Nurmela K., Pohjanvirta R., Huuskonen H., El-Gehani F., and Paranko J. 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 (2001) 169-179
31. Haavisto A.M., Pettersson K., Bergendahl M., Perheentupa A., Roser J.F., and Huhtaniemi I. A supersensitive immunofluorometric assay for rat luteinizing hormone. Endocrinology 132 (1993) 1687-1691
32. Rozen S., and Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132 (2000) 365-386
33. Wilson V.S., Lambright C., Furr J., Ostby J., Wood C., Held G., et al. Phthalate ester-induced gubernacular lesions are associated with reduced insl3 gene expression in the fetal rat testis. Toxicol Lett 146 (2004) 207-215
34. Barlow N.J., McIntyre B.S., and Foster P.M. Male reproductive tract lesions at 6, 12 and 18 months of age following in utero exposure to di(n-butyl) phthalate. Toxicol Pathol 32 (2004) 79-90
35. Supornsilchai V., Soder O., and Svechnikov K. Stimulation of the pituitary-adrenal axis and of adrenocortical steroidogenesis ex vivo by administration of di-2-ethylhexyl phthalate to prepubertal male rats. J Endocrinol 192 (2007) 33-39
36. Nef S., and Parada L.F. Cryptorchidism in mice mutant for Insl3. Nat Genet 22 (1999) 295-299
37. Zimmermann S., Steding G., Emmen J.M., Brinkmann A.O., Nayernia K., Holstein A.F., et al. Targeted disruption of the Insl3 gene causes bilateral cryptorchidism. Mol Endocrinol 13 (1999) 681-691
38. Mylchreest E., Sar M., Cattley R.C., and Foster P.M. Disruption of androgen-regulated male reproductive development by di(n-butyl) phthalate during late gestation in rats is different from flutamide. Toxicol Appl Pharmacol 156 (1999) 81-95
39. Thompson C.J., Ross S.M., and Gaido K.W. Di(n-butyl) phthalate impairs cholesterol transport and steroidogenesis in the fetal rat testis through a rapid and reversible mechanism. Endocrinology 145 (2004) 1227-1237
40. Mu X., Liu K., Kleymenova E., Sar M., Young S.S., and Gaido K.W. Gene expression profiling of androgen receptor antagonists in the rat fetal testis reveals few common gene targets. J Biochem Mol Toxicol 20 (2006) 7-17
41. O'Shaughnessy P.J., Johnston H., Willerton L., and Baker P.J. Failure of normal adult Leydig cell development in androgen-receptor-deficient mice. J Cell Sci 115 (2002) 3491-3496
42. Freyberger A., Ellinger-Ziegelbauer H., and Krotlinger F. Evaluation of the rodent Hershberger bioassay: testing of coded chemicals and supplementary molecular-biological and biochemical investigations. Toxicology 239 (2007) 77-88
43. Jonsson J., Rodriguez-Martinez H., and Brandt I. Transplacental toxicity of 3-methylsulphonyl-DDE in the developing adrenal cortex in mice. Reprod Toxicol 9 (1995) 257-264
44. Lindstrom V., Brandt I., and Lindhe O. Species differences in 3-methylsulphonyl-DDE bioactivation by adrenocortical tissue. Arch Toxicol 82 (2008) 159-163
45. Lund B.O., and Lund J. Novel involvement of a mitochondrial steroid hydroxylase (P450c11) in xenobiotic metabolism. J Biol Chem 270 (1995) 20895-20897
46. Jonsson C.J., Rodriguez-Martinez H., Lund B.O., Bergman A., and Brandt I. Adrenocortical toxicity of 3-methylsulfonyl-DDE in mice. II. Mitochondrial changes following ecologically relevant doses. Fundam Appl Toxicol 16 (1991) 365-374
47. Lindhe O., Lund B.O., Bergman A., and Brandt I. Irreversible binding and adrenocorticolytic activity of the DDT metabolite 3-methylsulfonyl-DDE examined in tissue-slice culture. Environ Health Perspect 109 (2001) 105-110
48. Ferreira F.M., Madeira V.M., and Moreno A.J. Interactions of 2,2-bis(p-chlorophenyl)-1, 1-dichloroethylene with mitochondrial oxidative phosphorylation. Biochem Pharmacol 53 (1997) 299-308
49. Hatano O., Takakusu A., Nomura M., and Morohashi K. Identical origin of adrenal cortex and gonad revealed by expression profiles of Ad4BP/SF-1. Genes Cells 1 (1996) 663-671