Characterization of the period of sensitivity of fetal male sexual development to vinclozolin

Toxicological Sciences

Volumn 55, Issue 1, 2000, Pages 152-161

  Wolf, Cynthia J ^a,b   LeBlanc, Gerald A ^b   Ostby, Joseph S ^a   Gray Jr , L Earl ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Androgen receptor; Anogenital distance; Antiandrogen; Critical period; Hypospadias; Levator ani; Male reproductive development; Vinclozolin

Indexed keywords

FUNGICIDE; VINCLOZOLIN;

ANIMAL MODEL; ARTICLE; DOSE RESPONSE; FETUS; FETUS DEVELOPMENT; FETUS MALFORMATION; HYPOSPADIAS; MALE; NONHUMAN; PREGNANCY; REPRODUCTIVE TOXICITY; SEXUAL DEVELOPMENT;

EID: 0034068757     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/55.1.152     Document Type: Article

References (59)

1. Bentvelsen, F., Brinkman, A., van der Schoot, P., van der Linden, J., van der Kwast, T., Boersma, W., Schroder, F., and Nijman, J. (1995). Developmental pattern and regulation by androgens of androgen receptor expression in the urogenital tract of the rat. Mol. Cell. Endocrinol. 113, 245-253.
2. Breedlove, S., and Arnold, A. (1983). Sex differences in the pattern of steroid accumulation by motoneurons of the rat lumbar spinal cord. J. Comp. Neurol. 215, 211-216.
3. Butler, H., and Juurlink, B. H. J. (1987). An Atlas for Staging Mammalian and Chick Embryos, pp. 193-194. CRC Press, Boca Raton, FL.
4. Cain, M., Kramer, S., Tindall, D., and Husmann, D. (1995). Flutamide-induced cryptorchidism in the rat is associated with altered gubemacular morphology. Urology 46, 553-558.
5. Carlsen, E., Giwercman, A., Keiding, N., and Skakkebaek, N. (1992). Evidence for decreasing quality of semen during past 50 years. Br. Med. J. 305, 609-613.
6. Chambers, E. L., and Malone, P. S. (1999). The incidence of hypospadias in two English cities: A case-control comparison of possible causal factors. BJU Int. 84, 95-98.
7. Clark, R., Anderson, C., Prahalada, S., Robertson, R., Lochry, E., Leonard, Y., Stevens, J., and Hoberman, A. (1993). Critical developmental periods for effects on male rat genitalia induced by finasteride, a 5α-reductase inhibitor. Toxicol. Appl. Pharmacol. 119, 34-40.
8. Cooke, P., Young, P., and Cunha, G. (1991). Androgen receptor expression in developing male reproductive organs. Endocrinology 128, 2867-2873.
9. Cunha, G., Alarid, E., Turner, T., Donjacour, A., Boutin, E., and Foster, B. (1992). Normal and abnormal development of the male urogenital tract. Role of androgens, mesenchymal-epithelial interactions, and growth factors. J. Androl. 13, 465-475.
10. Dolk, H. (1998). Rise in prevalence of hypospadias. Lancet. 351, 770.
11. Ema, M., Miyawaki, E., and Kawashima, K. (1998). Further evaluation of developmental toxicity of di-n-butyl phthalate following administration during late pregnancy in rats. Toxicol. Lett. 98, 87-93.
12. Facemire, C. F., Gross, T. S., and Guillette, L. J., Jr. (1995). Reproductive impairment in the Florida panther: Nature or nurture? Environ. Health Perspect. 103(Suppl. 4), 79-86.
13. Feyk, L. A., and Giesy, J. P. (1998). Xenobiotic modulation of endocrine function in birds. In: Principles and Processes for Evaluating Endocrine Disruption in Wildlife (R. Kendall, R. Dickerson, J. Giesy, and W. Suk, Eds.), pp. 121-140. Setac Press, Pensacola, FL.
14. Fleming, L. E., Bean, J. A., Rudolph, M., and Hamilton, K. (1999). Cancer incidence in a cohort of licensed pesticide applicators in Florida. J Occup. Environ. Med. 41, 279-288.
15. Gallo, M. A., and Doull, J. (1993). History and scope of toxicology. In Casarett and Doull's Toxicology (M. O. Amdur, J, D. Doull, and C. D. Klaasen, Eds.), pp. 3-11. McGraw-Hill, New York.
16. Gibbs, P. E., Pascoe, P. L., and Bryan, G. W. (1991). Tributyltin-induced imposex in stenoglossan gastropods: Pathological effects on the female reproductive system. Comp. Biochem. Physiol. 100, 231-236.
17. Gray, L. E., Jr., Ostby, J., and Kelce, W. (1994). Developmental effects of an environmental antiandrogen: The fungicide vinclozolin alters sex differentiation of the male rat. Toxicol. Appl. Pharmacol. 129, 46-52.
18. Gray, L. E., Jr., Ostby, J., Monosson, E., and Kelce, W. (1999a). Environmental antiandrogens: Low doses of the fungicide vinclozolin alter sexual differentation of the male rat. Toxicol. Ind. Health 15, 48-64.
19. Gray, L. E., Jr., Wolf, C., Lambright, C., Mann, P., Price, M., Cooper, R. L., and Ostby, J. (1999b) Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p,p′-DDE, and ketaconazole) 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. Toxicol. Ind. Health 15, 94-118.
20. Grier, J. W. (1982). Ban of DDT and subsequent recovery of reproduction in bald eagles. Science 218, 1232-1235.
21. Guillette, L. J., Jr., Gross, T. S., Masson, G. R., Matter, J. M., Percival, H. F., and Woodward, A. R. (1994). Developmental Abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 102, 680-688.
22. Hayward, S. W., Baskin, L. S., Haughney, P. C., Foster B. A., Cunha, A. R., Dahiya, R., Prins, G. S., and Cunha, G. R. (1996). Stromal development in the ventral prostate, anterior prostate, and seminal vesicle of the rat. Acta Anat. (Basel) 155, 94-103.
23. Hunt, G. L., and Hunt, M. W. (1973). Clutch size, hatching success, and eggshell thinning in Western gulls. Condor 75, 483-486.
24. Hunt, G. L., and Hunt, M. W. (1977). Female-female pairing in Western gulls (Laris Occidentalis) in southern California. Science 196, 1466-1467.
25. Husmann, D., and McPhaul, M. (1991a). Time-specific androgen blockade with flutamide inhibits testicular descent in the rat. Endocrinology 129, 1409-1416.
26. Husmann, D. A., and McPhaul, M. J. (1991b). Localization of the androgen receptor in the developing rat gubernaculum. Endocrinology 128, 383-387.
27. Imagawa, W., Yang, J., Guzman, R., and Nandi, S. (1994). Control of mammary gland development. In: The Physiology of Reproduction, 2nd ed. (E. Knobill and J. D. Kneil, Eds.), pp. 1033-1063. Raven Press, Ltd., New York.
28. Imperato-McGinley, J., Sanchez, R. S., Spencer, J. R., Yee, B., and Vaughan, E. D. (1992). Comparison of the effects of the 5α-reductase inhibitor finasteride and the antiandrogen flutamide on prostate and genital differentiation: Dose-response studies. Endocrinology 131, 1149-1156.
29. Jordan, C., Padgett, B., Hershey, J., Prins, G., and Arnold, A. (1997). Ontogeny of androgen receptor immunoreactivity in lumbar motoneurons and in the sexually dimorphic lavator ani muscle of male rats. J. Comp. Neurol. 379, 88-98.
30. Kelce, W. R., Zirkin, B. R., and Ewing, L. L. (1991). Immature rat Leydig cells are intrinsically less sensitive than adult Leydig cells to ethanedimethane-sulfonate. Toxicol. Appl. Pharmacol. 111, 189-200.
31. Kelce, W., Monosson, E., Gamcsik, M., Laws, S., and Gray, L. E., Jr. (1994). Environmental hormone disruptors: Evidence that vinclozolin developmental toxicity is mediated by antiandrogenic metabolites. Toxicol. Appl. Pharmacol. 126, 276-285.
32. Kelce, W., Lambright, C., Gray, L. E., Jr., and Roberts, K. (1997). Vinclozolin and p,p′-DDE alter androgen-dependent gene expression: In vivo confirmation of an androgen receptor-mediated mechanism. Toxicol. Appl. Pharmacol. 142, 192-200.
33. Levy, J., and Husmann, D. (1995). The hormonal control of testicular descent. J. Androl. 16, 459-463.
34. Lucas, J. C., Renfree, M. B., Shaw, G., and Butler, C. M. (1997). The influence of the anti-androgen flutamide on early sexual differentiation of the marsupial male. J Reprod. Fertil. 109, 205-212.
35. Lundholm, C. E. (1984). Comparison of the effect of DDE on the Ca metabolism of the eggshell gland and its subcellular fractions of the duck and the domestic fowl. Acta Pharmacol. Toxicol. (Copenh.) 54, 400-407.
36. Monosson, E., Kelce, W., Lambright, C., Ostby, J., and Gray, L. E., Jr. (1999). Peripubertal exposure to the antiandrogenic fungicide, vinclozolin, delays puberty, inhibits the development of androgen-dependent tissues, and alters androgen receptor function in the male rat. Toxicol. Ind. Health 15, 65-79.
37. Moore, C. G., and Stevenson, J. M. (1991). The occurrence of intersexuality in harpacticoid copepods and its relationship with pollution. Mar. Pollut. Bull. 22, 72-74.
38. Mylchreest, E., Cattley, R., and Foster, P. (1998). Male reproductive tract malformations in rats following gestational and lactational exposure to di-n-butyl) phthalate: An antiandrogenic mechanism? Toxicol. Sci. 43, 47-60.
39. Neumann, F., Von Berswordt-Wallrabe, R. vo., Elger, W., Steinbeck, H., Hahn, J., and Kramer, M. (1970). Aspects of androgen-dependent events as studied by antiandrogens. Recent Prog. Horm. Res. 26, 337-410.
40. Ostby, J., Kelce, W., Lambright, C., Wolf, C., Mann, P., and Gray, L. E. Jr. (1999). The fungicide procymidone alters sexual differentiation in the male rat by acting as an androgen-receptor antagonist in vivo and in vitro. Toxicol. Ind. Health 15, 80-93.
41. Picon, R. (1976) Testosterone secretion by fetal rat testes in vitro. J. Endocrinol. 71, 231-238.
42. Prahalada, S., Tarantal, A., Harris, G., Ellsworth, K., Clarke, A., Skiles, G., MacKenzie, K., Kruk, L., Ablin, D., Cukierski, M., Peter, C., van Zwieten, M., and Hendrickx, A. (1997). Effects of finasteride, a type 2 5-alpha reductase inhibitor, on fetal development in the rhesus monkey (Macaca mulatta). Teratology 55, 119-131.
43. Prins, G., and Birch, L. (1995). The developmental pattern of androgen receptor expression in rat prostate lobes is altered after neonatal exposure to estrogen. Endocrinology 136, 1303-1314.
44. Quigley, C. A., De Bellis, A., Marschke, K. B., el Awady, M. K., Wilson, E. M., and French, F. S. (1995). Androgen receptor defects: Historical, clinical, and molecular perspectives. Endocr. Rev. 16, 271-321.
45. Rajfer, J., Namkung, P. C., and Petra, P. H. (1980). Identification, partial characterization, and age-related changes of a cytoplasmic androgen receptor in the rat penis. J. Steroid Biochem. 13, 1489-1492.
46. Silversides, D., Price, C., and Cooke, G. (1995). Effects of short-term esposure to hydroxyflutamide in utero on the development of the reproductive tract in male mice. Can. J. Physiol. Pharmacol. 73, 1582-1588.
47. Skakkebaek, N. E., Rajpert-De Meyts, E., Jorgensen, N., Carlsen, E., Petersen, P. M., Giwercman, A., Andersen, A. G., Jensen, T. K., Andersson, A. M., and Muller, J. (1998). Germ cell cancer and disorders of spermatogenesis: An environmental connection? APMIS 106, 3-11.
48. Spencer, J., Torrado, T., Sanchez, R., Vaughan, E. D. Jr., and Imperato-McGinley, J. (1991). Effects of flutamide and finasteride on rat testicular descent. Endocrinology 129, 741-748.
49. Tobin, C., and Joubert, Y. (1991). Testosterone-induced development of the rat levator ani muscle. Dev. Biol. 146, 131-138.
50. Topper, Y. J., and Freeman, C. S. (1980). Multiple hormone interactions in the developmental biology of the mammary gland. Physiol. Rev. 60, 1049-1106
51. USEPA, (1993). Developmental and Reproductive Peer Review of Vinclozolin. Draft Report, Office of Prevention, Pesticides and Toxic Substances.
52. USEPA (1998). Federal Register 63, 59557-59558.
53. van der Schoot, P. (1992). Disturbed testicular descent in the rat after prenatal exposure to the antiandrogen flutamide. J. Reprod. Fertil. 96, 483-496.
54. Wasner, G., Hennermann, I., and Kratochwil, K. (1983). Ontogeny of mesenchymal androgen receptors in the embryonic mouse mammary gland. Endocrinology 113, 1771-1780.
55. Weir H. K., Marrett, L. D., and Moravan, V. (1999). Trends in the incidence of testicular germ cell cancer in Ontario by histologic subgroup. 1964-1996. Can. Med. A. J. 160, 201-205.
56. Wilson, J. D., George, F. W., and Renfree, M. B. (1995). The endocrine role in mammalian sexual differentiation. Recent Prog. Horm. Res. 50, 349-364.
57. Wong, C., Kelce, W., Sar, M., and Wilson, E. (1995). Androgen receptor antagonist versus agonist activities of the fungicide vinclozolin relative to hydroxyflutamide. J. Biol. Chem. 270, 19998-20003.
58. You, L., and Sar, M. (1998). Androgen receptor expression in the testes and epididymides of prenatal and postnatal Sprague-Dawley rats. Endocrine 9, 253-261.
59. You, L., Casanova, M., Archibeque-Engle, S., Sar, M., Fan, L., and Heck, H. (1998) 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, 162-173.