Neonatal diethylstilbestrol exposure disrupts female reproductive tract structure/function via both direct and indirect mechanisms in the hamster

Reproductive Toxicology

Volumn 32, Issue 4, 2011, Pages 472-483

  Alwis, Imala D ^a   Maroni, Dulce M ^a   Hendry, Isabel R ^a   Roy, Shyamal K ^b,c   May, Jeffrey V ^a   Leavitt, Wendell W ^a   Hendry, William J ^a  

^a WICHITA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Diethylstilbestrol; Endocrine disruption; Female reproductive tract; Hamster; Ovary

Indexed keywords

DIETHYLSTILBESTROL; ESTRADIOL; FOLLITROPIN; LUTEINIZING HORMONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS LUTEUM; CYSTIC OVARIAN FOLLICLE; ENDOMETRIUM DYSPLASIA; ENDOMETRIUM HYPERPLASIA; ESTRUS CYCLE; FEMALE; FEMALE GENITAL TRACT MALFORMATION; HAMSTER; HYPOPHYSIS; HYPOTHALAMUS; NEWBORN; NONHUMAN; OVARIAN POLYOVULAR FOLLICLE; OVARIAN SALPINGITIS; PERINATAL DRUG EXPOSURE; REPRODUCTIVE TOXICITY; VAGINAL HYPOSPADIA;

ANIMALS; ANIMALS, NEWBORN; CERVIX UTERI; CRICETINAE; DIETHYLSTILBESTROL; ESTROGENS, NON-STEROIDAL; ESTROUS CYCLE; FALLOPIAN TUBES; FEMALE; GENITALIA, FEMALE; HORMONES; HYPOTHALAMUS; MESOCRICETUS; OVARIECTOMY; OVARY; PITUITARY GLAND; PREGNANCY; SEXUAL MATURATION; UTERUS; VAGINA;

CRICETINAE;

EID: 82155195869     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2011.09.006     Document Type: Article

References (67)

1. Dodds E.C., Goldberg L., Lawson W., Robinson R. Estrogenic activity of certain synthetic compounds. Nature 1938, 141:247-248.
2. Swan S.H. Intrauterine exposure to diethylstilbestrol: long-term effects in humans. Apmis 2000, 108:793-804.
3. Herbst A.L., Ulfelder H., Poskanzer D.C. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 1971, 284:878-881.
4. Blunt E. Diethylstilbestrol exposure: it's still an issue. Holist Nurs Pract 2004, 18:187-191.
5. Kaufman R.H., Adam E. Findings in female offspring of women exposed in utero to diethylstilbestrol. Obstet Gynecol 2002, 99:197-200.
6. Kruse K., Lauver D., Hanson K. Clinical implications of DES. Nurse Pract 2003, 28. pp. 26-32,35, table of contents; quiz 35-27.
7. Lauver D., Nelles K.K., Hanson K. The health effects of diethylstilbestrol revisited. J Obstet Gynecol Neonatal Nurs 2005, 34:494-499.
8. Newbold R.R. Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol Appl Pharmacol 2004, 199:142-150.
9. Rubin M.M. Antenatal exposure to DES: lessons learned ... future concerns. Obstet Gynecol Surv 2007, 62:548-555.
10. Schrager S., Potter B.E. Diethylstilbestrol exposure. Am Fam Physician 2004, 69:2395-2400.
11. Veurink M., Koster M., Berg L.T. The history of DES, lessons to be learned. Pharm World Sci 2005, 27:139-143.
12. Anderson L.M. Predictive values of traditional animal bioassay studies for human perinatal carcinogenesis risk determination. Toxicol Appl Pharmacol 2004, 199:162-174.
13. Bern H.A. Diethylstilbestrol (DES) syndrome: present status of animal and human studies. Hormonal carcinogenesis 1991, 1-8. Springer-Verlag, New York. J.J. Li, S. Nandi (Eds.).
14. Greco T.L., Duello T.M., Gorski J. Estrogen receptors, estradiol, and diethylstilbestrol in early development: the mouse as a model for the study of estrogen receptors and estrogen sensitivity in embryonic development of male and female reproductive tracts. Endocr Rev 1993, 14:59-71.
15. Hendry W.J., Sheehan D.M., Khan S.A., May J.V. Developing a laboratory animal model for perinatal endocrine disruption: the hamster chronicles. Exp Biol Med 2002, 227:709-723.
16. Leavitt W.W., Evans R.W., Hendry W.J. Etiology of DES-induced uterine tumors in the Syrian hamster. Adv Exp Med Biol 1982, 138:63-86.
17. Newbold R. Cellular and molecular effects of developmental exposure to diethylstilbestrol: implications for other environmental estrogens. Environ Health Perspect 1995, 103(Suppl. 7):83-87.
18. Rustia M., Shubik P. Transplacental effects of diethylstilbestrol on the genital tract of hamster offspring. Cancer Lett 1976, 1:139-146.
19. Rustia M., Shubik P. Effects of transplacental exposure to diethylstilbestrol on carcinogenic susceptibility during postnatal life in hamster progeny. Cancer Res 1979, 39:4636-4644.
20. Halling A., Forsberg J.G. Ovarian reproductive function after exposure to diethylstilbestrol in neonatal life. Biol Reprod 1990, 43:472-477.
21. Haney A.F., Newbold R.R., McLachlan J.A. Prenatal diethylstilbestrol exposure in the mouse: effects on ovarian histology and steroidogenesis in vitro. Biol Reprod 1984, 30:471-478.
22. Iguchi T., Fukazawa Y., Uesugi Y., Takasugi N. Polyovular follicles in mouse ovaries exposed neonatally to diethylstilbestrol in vivo and in vitro. Biol Reprod 1990, 43:478-484.
23. Iguchi T., Takasugi N. Polyovular follicles in the ovary of immature mice exposed prenatally to diethylstilbestrol. Anat Embryol (Berl) 1986, 175:53-55.
24. Iguchi T., Takasugi N., Bern H.A., Mills K.T. Frequent occurrence of polyovular follicles in ovaries of mice exposed neonatally to diethylstilbestrol. Teratology 1986, 34:29-35.
25. McLachlan J.A., Newbold R.R., Bullock B.C. Long-term effects on the female mouse genital tract associated with prenatal exposure to diethylstilbestrol. Cancer Res 1980, 40:3988-3999.
26. Newbold R.R., Bullock B.C., Mc Lachlan J.A. Exposure to diethylstilbestrol during pregnancy permanently alters the ovary and oviduct. Biol Reprod 1983, 28:735-744.
27. Tenenbaum A., Forsberg J.G. Structural and functional changes in ovaries from adult mice treated with diethylstilboestrol in the neonatal period. J Reprod Fertil 1985, 73:465-477.
28. Wordinger R.J., Highman B. Histology and ultrastructure of the adult mouse ovary following a single prenatal exposure to diethylstilbestrol. Virchows Arch B Cell Pathol Incl Mol Pathol 1984, 45:241-253.
29. Caldwell B.V., Pawling R.S., Wright P.A. Reestablishment of ovarian periodicity after transplantation to the Syrian hamster cheek pouch. Proc Soc Exp Biol Med 1966, 123:551-553.
30. Hendry W.J., Branham W.S., Sheehan D.M. The hamster cheek pouch as a convenient ectopic site for studies of uterine morphogenesis and endocrine responsiveness. Differentiation 1992, 51:49-54.
31. Hendry W.J., Zheng X., Leavitt W.W., Branham W.S., Sheehan D.M. Endometrial hyperplasia and apoptosis following neonatal diethylstilbestrol exposure and subsequent estrogen stimulation in both host and transplanted hamster uteri. Cancer Res 1997, 57:1903-1908.
32. Hendry W.J., DeBrot B.L., Zheng X., Branham W.S., Sheehan D.M. Differential activity of diethylstilbestrol versus estradiol as neonatal endocrine disruptors in the female hamster (Mesocricetus auratus) reproductive tract. Biol Reprod 1999, 61:91-100.
33. Herbst A.L., Scully R.E., Robboy S.J. Prenatal diethylstilbestrol exposure and human genital tract abnormalities. Natl Cancer Inst Monogr 1979, 25-35.
34. Hendry W.J., Branham W.S., Sheehan D.M. Diethylstilbestrol versus estradiol as neonatal disruptors of the hamster (Mesocricetus auratus) cervix. Biol Reprod 2004, 70:1306-1316.
35. Hendry W.J., Leavitt W.W. Binding and retention of estrogen in the uterus of hamsters treated neonatally with diethylstilbestrol. J Steroid Biochem 1982, 17:479-487.
36. Hendry W.J., Leavitt W.W. Altered morphogenesis of the immature hamster uterus following neonatal exposure to diethylstilbestrol. Differentiation 1993, 52:221-227.
37. Zheng X., Hendry W.J. Neonatal diethylstilbestrol treatment alters the estrogen-regulated expression of both cell proliferation and apoptosis-related protooncogenes (c-jun, c-fos, c-myc, bax, bcl-2 and bcl-x) in the hamster uterus. Cell Growth Differ 1997, 8:425-434.
38. Hendry W.J., Weaver B.P., Naccarato T.R., Khan S.A. Differential progression of neonatal diethylstilbestrol-induced disruption of the hamster testis and seminal vesicle. Reprod Toxicol 2006, 21:225-240.
39. Karri S., Johnson H., Hendry W.J., Williams S.C., Khan S.A. Neonatal exposure to diethylstilbestrol leads to impaired action of androgens in adult male hamsters. Reprod Toxicol 2004, 19:53-63.
40. Khan S.A., Ball R.B., Hendry W.J. Effects of neonatal administration of diethylstilbestrol in male hamsters: disruption of reproductive function in adults after apparently normal pubertal development. Biol Reprod 1998, 58:137-142.
41. Siegal H.I. Appendix-characteristics of Mesocricetus auratus. The hamster: reproduction and behavior 1985, 435-436. Plenum Press, New York. H.I. Siegel (Ed.).
42. Terranova P.F., Greenwald G.S. Steroid and gonadotropin levels during the luteal-follicular shift of the cyclic hamster. Biol Reprod 1978, 18:170-175.
43. Miller K.P., Borgeest C., Greenfeld C., Tomic D., Flaws J.A. In utero effects of chemicals on reproductive tissues in females. Toxicol Appl Pharmacol 2004, 198:111-131.
44. Kirigaya A., Kim H., Hayashi S., Chambon P., Watanabe H., Lguchi T., et al. Involvement of estrogen receptor beta in the induction of polyovular follicles in mouse ovaries exposed neonatally to diethylstilbestrol. Zool Sci 2009, 26:704-712.
45. Kim H., Nakajima T., Hayashi S., Chambon P., Watanabe H., Iguchi T., et al. Effects of diethylstilbestrol on programmed oocyte death and induction of polyovular follicles in neonatal mouse ovaries. Biol Reprod 2009, 81:1002-1009.
46. Jefferson W., Newbold R., Padilla-Banks E., Pepling M. Neonatal genistein treatment alters ovarian differentiation in the mouse: inhibition of oocyte nest breakdown and increased oocyte survival. Biol Reprod 2006, 74:161-168.
47. Pepling M.E., Spradling A.C. Female mouse germ cells form synchronously dividing cysts. Development 1998, 125:3323-3328.
48. Pepling M.E., Spradling A.C. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 2001, 234:339-351.
49. Guillette L.J., Moore B.C. Environmental contaminants, fertility, and multioocytic follicles: a lesson from wildlife?. Semin Reprod Med 2006, 24:134-141.
50. Schmidt G., Fowler W.C. Gynecologic operative experience in women exposed to DES in utero. South Med J 1982, 75:260-263.
51. Sinkevicius K.W., Burdette J.E., Woloszyn K., Hewitt S.C., Hamilton K., Sugg S.L., et al. An estrogen receptor-alpha knock-in mutation provides evidence of ligand-independent signaling and allows modulation of ligand-induced pathways in vivo. Endocrinology 2008, 149:2970-2979.
52. Monniaux D., Clemente N., Touze J.L., Belville C., Rico C., Bontoux M., et al. Intrafollicular steroids and anti-mullerian hormone during normal and cystic ovarian follicular development in the cow. Biol Reprod 2008, 79:387-396.
53. Hendry W.J., Zheng X., Leavitt W.W., Branham W.S., Sheehan D.M. Synthetic estrogen mediated alterations in uterine cell fate. Serono international symposium on cell death in reproductive physiology 1997, 272-291. Springer-Verlag, Inc., New York. J.L. Tilly, J.F. Strauss, M. Tenniswood (Eds.).
54. Newbold R.R., Bullock B.C., McLachlan J.A. Diverticulosis and salpingitis isthmica nodosa (SIN) of the fallopian tube. Estrogen-induced diverticulosis and SIN of the mouse oviduct. Am J Pathol 1984, 117:333-335.
55. Rothschild T.C., Calhoon R.E., Boylan E.S. Genital tract abnormalities in female rats exposed to diethylstilbestrol in utero. Reprod Toxicol 1987, 1:193-202.
56. Balasch J., Coll O., Jove I., Moreno V., Mulet J., Vanrell J.A. Diethylstilbestrol-induced mullerian abnormalities, septate uterus, genital tuberculosis and twin pregnancy with term delivery after in-vitro fertilization. Hum Reprod 1991, 6:690-693.
57. Caldwell B.V., Mazer R.S., Wright P.A. Luteolysis as affected by uterine transplantation in the Syrian hamster. Endocrinology 1967, 80:477-482.
58. Duby R.T., McDaniel J.W., Black D.L. Homo-transplantation of the hamster uterus. Nature 1965, 205:720.
59. Evans R.W., Chen T.J., Hendry W.J., Leavitt W.W. Progesterone regulation of estrogen receptor in the hamster uterus during the estrous cycle. Endocrinology 1980, 107:383-390.
60. Ying S.Y. Inhibins and activins: chemical properties and biological activity. Proc Soc Exp Biol Med 1987, 186:253-264.
61. Miyagawa S., Buchanan D.L., Sato T., Ohta Y., Nishina Y., Iguchi T. Characterization of diethylstilbestrol-induced hypospadias in female mice. Anat Rec 2002, 266:43-50.
62. Dunn T.B. Cancer and other lesions in mice receiving estrogens. Recent Results Cancer Res 1979, 66:175-192.
63. Iguchi T., Takasugi N. Occurrence of permanent changes in vaginal and uterine epithelia in mice treated neonatally with progestin, estrogen and aromatizable or non-aromatizable androgens. Endocrinol Jpn 1976, 23:327-332.
64. Warner M.R., Warner R.L., Clinton C.W. Reproductive tract calculi, their induction, age incidence, composition and biological effects in Balb/c Crgl mice injected as newborns with estradiol-17 beta. Biol Reprod 1979, 20:310-322.
65. Bast J.D., Greenwald G.S. Serum profiles of follicle-stimulating hormone, luteinizing hormone and prolactin during the estrous cycle of the hamster. Endocrinology 1974, 94:1295-1299.
66. Ridley K., Greenwald G.S. Progesterone levels measured every two hours in the cyclic hamster. Proc Soc Exp Biol Med 1975, 149:10-12.
67. Saidapur S.K., Greenwald G.S. Peripheral blood and ovarian levels of sex steroids in the cyclic hamster. Biol Reprod 1978, 18:401-408.