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Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p,p'-DDE, and ketoconazole) and toxic substances (dibutyl- and diethylhexyl phthalate, PCB 169, and ethane dimethane sulphonate) during sexual differentiation produces diverse profiles of reproductive malformations in the male rat
Cynthia Wolf
Endocrinology Branch, Reproductive Toxicology Division, National Health and Environmental Effects Research Laboratory, United States Environmental Protection Agency, Research Triangle Park, North Carolina
Christy Lambright
Endocrinology Branch, Reproductive Toxicology Division, National Health and Environmental Effects Research Laboratory, United States Environmental Protection Agency, Research Triangle Park, North Carolina
Peter Mann
Experimental Pathology Labs, Inc., Research Triangle Park, North Carolina
Matthew Price
Endocrinology Branch, Reproductive Toxicology Division, National Health and Environmental Effects Research Laboratory, United States Environmental Protection Agency, Research Triangle Park, North Carolina
Ralph L. Cooper
Endocrinology Branch, Reproductive Toxicology Division, National Health and Environmental Effects Research Laboratory, United States Environmental Protection Agency, Research Triangle Park, North Carolina
Joseph Ostby
Endocrinology Branch, Reproductive Toxicology Division, National Health and Environmental Effects Research Laboratory, United States Environmental Protection Agency, Research Triangle Park, North Carolina
L. Earl Gray, Jr.
Endocrinology Branch, Reproductive Toxicology Division, National Health and Environmental Effects Research Laboratory, United States Environmental Protection Agency, Research Triangle Park, North Carolina, gray.earl{at}epamail.epa.gov
Antiandrogenic chemicals alter sexual differentiation by a variety of mechanisms, and as a consequence, they induce different profiles of effects. For example, in utero treatment with the androgen receptor (AR) antagonist, flutamide, produces ventral prostate agenesis and testicular nondescent, while in contrast, finasteride, an inhibitor of 5 -dihydrotestosterone (DHT) synthesis, rarely, if ever, induces such malformations. In this regard, it was recently proposed that dibutyl phthalate (DBP) alters reproductive development by a different mechanism of action than flutamide or vinclozolin (V), which are AR antagonists, because the male offsprings display an unusually high incidence of testicular and epididymal alterations—effects rarely seen after in utero flutamide or V treatment. In this study, we present original data describing the reproductive effects of 10 known or suspected anti-androgens, including a Leydig cell toxicant ethane dimethane sulphonate (EDS, 50 mg kg–1 day–1), linuron (L, 100 mg kg–1 day–1), p,p'-DDE (100 mg kg–1 day–1), ketoconazole (12-50 mg kg–1 day–1), procymidone (P, 100 mg kg–1 day–1), chlozolinate (100 mg kg–1 day–1), iprodione (100 mg kg–1 day–1), DBP (500 mg kg–1 day–1), diethylhexyl phthalate (DEHP, 750 mg kg–1 day–1), and polychlorinated biphenyl (PCB) congener no. 169 (single dose of 1.8 mg kg–1). Our analysis indicates that the chemicals discussed here can be clustered into three or four separate groups, based on the resulting profiles of reproductive effects. Vinclozolin, P, and DDE, known AR ligands, produce similar profiles of toxicity. However, p,p'-DDE is less potent in this regard. DBP and DEHP produce a profile distinct from the above AR ligands. Male offsprings display a higher incidence of epididymal and testicular lesions than generally seen with flutamide, P, or V even at high dosage levels. Linuron treatment induced a level of external effects consistent with its low affinity for AR [reduced anogenital distance (AGD), retained nipples, and a low incidence of hypospadias]. However, L treatment also induced an unanticipated degree of malformed epididymides and testis atrophy. In fact, the profile of effects induced by L was similar to that seen with DBP. These results suggest that L may display several mechanisms of endocrine toxicity, one of which involves AR binding. Chlozolinate and iprodione did not produce any signs of maternal or fetal endocrine toxicity at 100 mg kg–1 day–1. EDS produced severe maternal toxicity and a 45% reduction in size at birth, which resulted in the death of all neonates by 5 days of age. However, EDS only reduced AGD in male pups by 15%. Ketoconazole did not demasculinize or feminize males but rather displayed anti-hormonal activities, apparently by inhibiting ovarian hormone synthesis, which resulted in delayed delivery and whole litter loss. In summary, the above in vivo data suggest that the chemicals we studied alter male sexual differentiation via different mechanisms. The anti-androgens V, P, and p,p'-DDE produce flutamide-like profiles that are distinct from those seen with DBP, DEHP, and L. The effects of PCB 169 bear little resemblance to those of any known anti-androgen. Only in depth in vitro studies will reveal the degree to which one can rely upon in vivo studies, like those presented here, to predict the cellular and molecular mechanisms of developmental toxicity.
Key Words: anti-androgen • developmental reproductive toxicology • endocrine disruptor • inhibition of steroid synthesis • pesticides • phthalate • sex reversal • steroid receptors
Toxicology and Industrial Health, Vol. 15, No. 1-2,
94-118 (1999)
DOI: 10.1177/074823379901500109
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V. S. Wilson, C. Lambright, J. Ostby, and L. E. Gray Jr.
In Vitro and in Vivo Effects of 17{beta}-Trenbolone: A Feedlot Effluent Contaminant
Toxicol. Sci.,
December 1, 2002;
70(2):
202 - 211.
[Abstract]
[Full Text]
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A. M. Vinggaard, C. Nellemann, M. Dalgaard, E. B. Jorgensen, and H. R. Andersen
Antiandrogenic Effects in Vitro and in Vivo of the Fungicide Prochloraz
Toxicol. Sci.,
October 1, 2002;
69(2):
344 - 353.
[Abstract]
[Full Text]
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K. J. Turner, N. J. Barlow, M. F. Struve, D. G. Wallace, K. W. Gaido, D. C. Dorman, and P. M. D. Foster
Effects of in Utero Exposure to the Organophosphate Insecticide Fenitrothion on Androgen-Dependent Reproductive Development in the Crl:CD(SD)BR Rat
Toxicol. Sci.,
July 1, 2002;
68(1):
174 - 183.
[Abstract]
[Full Text]
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H. S. Kim, J.-H. Shin, H. J. Moon, T. S. Kim, I. H. Kang, J.-H. Seok, I. Y. Kim, K. L. Park, and S. Y. Han
Evaluation of the 20-Day Pubertal Female Assay in Sprague-Dawley Rats Treated with DES, Tamoxifen, Testosterone, and Flutamide
Toxicol. Sci.,
May 1, 2002;
67(1):
52 - 62.
[Abstract]
[Full Text]
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V. S. Wilson, K. Bobseine, C. R. Lambright, and L. E. Gray Jr.
A Novel Cell Line, MDA-kb2, That Stably Expresses an Androgen- and Glucocorticoid-Responsive Reporter for the Detection of Hormone Receptor Agonists and Antagonists
Toxicol. Sci.,
March 1, 2002;
66(1):
69 - 81.
[Abstract]
[Full Text]
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P. M.D. Foster and B. S. Mcintyre
Endocrine Active Agents: Implications of Adverse and Non-Adverse Changes
Toxicol Pathol,
January 1, 2002;
30(1):
59 - 65.
[Abstract]
[PDF]
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B. S. McIntyre, N. J. Barlow, and P. M. D. Foster
Male Rats Exposed to Linuron in Utero Exhibit Permanent Changes in Anogenital Distance, Nipple Retention, and Epididymal Malformations That Result in Subsequent Testicular Atrophy
Toxicol. Sci.,
January 1, 2002;
65(1):
62 - 70.
[Abstract]
[Full Text]
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B. T. Akingbemi, R. T. Youker, C. M. Sottas, R. Ge, E. Katz, G. R. Klinefelter, B. R. Zirkin, and M. P. Hardy
Modulation of Rat Leydig Cell Steroidogenic Function by Di(2-Ethylhexyl)Phthalate
Biol Reprod,
October 1, 2001;
65(4):
1252 - 1259.
[Abstract]
[Full Text]
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B. S. McIntyre, N. J. Barlow, and P. M. D. Foster
Androgen-Mediated Development in Male Rat Offspring Exposed to Flutamide in Utero: Permanence and Correlation of Early Postnatal Changes in Anogenital Distance and Nipple Retention with Malformations in Androgen-Dependent Tissues
Toxicol. Sci.,
August 1, 2001;
62(2):
236 - 249.
[Abstract]
[Full Text]
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L. G. Parks, C. S. Lambright, E. F. Orlando, L. J. Guillette Jr., G. T. Ankley, and L. E. Gray Jr.
Masculinization of Female Mosquitofish in Kraft Mill Effluent-Contaminated Fenholloway River Water Is Associated with Androgen Receptor Agonist Activity
Toxicol. Sci.,
August 1, 2001;
62(2):
257 - 267.
[Abstract]
[Full Text]
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D.N.R. Veeramachaneni, J.S. Palmer, and R.P. Amann
Long-term effects on male reproduction of early exposure to common chemical contaminants in drinking water
Hum. Reprod.,
May 1, 2001;
16(5):
979 - 987.
[Abstract]
[Full Text]
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H. Leffers, M. Nasby, B. Vendelbo, N. E. Skakkebak, and M. Jorgensen
Oestrogenic potencies of Zeranol, oestradiol, diethylstilboestrol, Bisphenol-A and genistein: implications for exposure assessment of potential endocrine disrupters
Hum. Reprod.,
May 1, 2001;
16(5):
1037 - 1045.
[Abstract]
[Full Text]
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H. Tamura, S. C. Maness, K. Reischmann, D. C. Dorman, L. E. Gray, and K. W. Gaido
Androgen Receptor Antagonism by the Organophosphate Insecticide Fenitrothion
Toxicol. Sci.,
March 1, 2001;
60(1):
56 - 62.
[Abstract]
[Full Text]
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T. J. Murray, P. A. Fowler, D. R. Abramovich, N. Haites, and R. G. Lea
Human Fetal Testis: Second Trimester Proliferative and Steroidogenic Capacities
J. Clin. Endocrinol. Metab.,
December 1, 2000;
85(12):
4812 - 4817.
[Abstract]
[Full Text]
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L. G. Parks, J. S. Ostby, C. R. Lambright, B. D. Abbott, G. R. Klinefelter, N. J. Barlow, and L. E. Gray Jr.
The Plasticizer Diethylhexyl Phthalate Induces Malformations by Decreasing Fetal Testosterone Synthesis during Sexual Differentiation in the Male Rat
Toxicol. Sci.,
December 1, 2000;
58(2):
339 - 349.
[Abstract]
[Full Text]
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L. E. Gray Jr., J. Ostby, J. Furr, M. Price, D. N. R. Veeramachaneni, and L. Parks
Perinatal Exposure to the Phthalates DEHP, BBP, and DINP, but Not DEP, DMP, or DOTP, Alters Sexual Differentiation of the Male Rat
Toxicol. Sci.,
December 1, 2000;
58(2):
350 - 365.
[Abstract]
[Full Text]
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E. Mylchreest, D. G. Wallace, R. C. Cattley, and P. M. D. Foster
Dose-Dependent Alterations in Androgen-Regulated Male Reproductive Development in Rats Exposed to Di(n-butyl) Phthalate during Late Gestation
Toxicol. Sci.,
May 1, 2000;
55(1):
143 - 151.
[Abstract]
[Full Text]
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C. J. Wolf, G. A. LeBlanc, J. S. Ostby, and L. E. Gray Jr.
Characterization of the Period of Sensitivity of Fetal Male Sexual Development to Vinclozolin
Toxicol. Sci.,
May 1, 2000;
55(1):
152 - 161.
[Abstract]
[Full Text]
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D. A. Keire, P. Anton, K. F. Faull, E. Ruth, J. H. Walsh, P. Chew, D. Quisimoro, M. Territo, and J. R. Reeve Jr.
Diethyl Phthalate, a Chemotactic Factor Secreted by Helicobacter pylori
J. Biol. Chem.,
December 21, 2001;
276(52):
48847 - 48853.
[Abstract]
[Full Text]
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