Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

In utero exposure to the oestrogen mimic diethylstilbestrol disrupts gonadal development in a viviparous reptile

Laura M. Parsley A , Erik Wapstra A B and Susan M. Jones A
+ Author Affiliations
- Author Affiliations

A School of Zoology, University of Tasmania, Private Bag 5, Hobart, Tas. 7001, Australia.

B Corresponding author. Email: erik.wapstra@utas.edu.au

Reproduction, Fertility and Development 27(7) 1106-1114 https://doi.org/10.1071/RD13411
Submitted: 2 December 2013  Accepted: 19 March 2014   Published: 10 April 2014

Abstract

The ubiquitous presence of endocrine-disrupting chemicals (EDCs) in the environment is of major concern. Studies on oviparous reptiles have significantly advanced knowledge in this field; however, 30% of reptilian species are viviparous (live-bearing), a parity mode in which both yolk and a placenta support embryonic development, thus exposure to EDCs may occur via multiple routes. In this first study of endocrine disruption in a viviparous lizard (Niveoscincus metallicus), we aimed to identify effects of the oestrogen mimic diethylstilbestrol (DES) on gonadal development. At the initiation of sexual differentiation, pregnant N. metallicus were treated with a single dose of DES at 100 or 10 µg kg­–1, a vehicle solvent or received no treatment. There was no dose-response effect, but the testes of male neonates born to DES-exposed mothers showed reduced organisation of seminiferous tubules and a lack of germ cells compared with those from control groups. The ovaries of female neonates born to DES-exposed mothers exhibited phenotypic abnormalities of ovarian structure, oocytes and follicles compared with controls. The results indicate that, in viviparous lizards, maternal exposure to oestrogenic EDCs during gestation may have profound consequences for offspring reproductive fitness.

Additional keywords: endocrine disruption, oestrogenic, ovary, placenta, testis, viviparity.


References

Atkins, N., Swain, R., and Jones, S. M. (2006). Does date of birth or a capacity for facultative placentotrophy influence offspring quality in a viviparous skink, Niveoscincus microlepidotus? Aust. J. Zool. 54, 369–374.
Does date of birth or a capacity for facultative placentotrophy influence offspring quality in a viviparous skink, Niveoscincus microlepidotus?CrossRef |

Bergeron, J. M., Crews, D., and McLachlan, J. A. (1994). PCBs as environmental oestrogens: turtle sex determination as a biomarker of environmental contamination. Environ. Health Perspect. 102, 780–781.
PCBs as environmental oestrogens: turtle sex determination as a biomarker of environmental contamination.CrossRef | 1:CAS:528:DyaK2MXhtlyqsbo%3D&md5=dad7b079038c7770f48f03829d05f593CAS | 9657710PubMed |

Blackburn, D. G. (1993). Chorioallantoic placentation in squamate reptiles: structure, function, development and evolution. J. Exp. Zool. 266, 414–430.
Chorioallantoic placentation in squamate reptiles: structure, function, development and evolution.CrossRef |

Brown, I. A., and Austin, D. W. (2012). Maternal transfer of mercury to the developing embryo/fetus: is there a safe level? Toxicol. Environ. Chem. 94, 1610–1627.
Maternal transfer of mercury to the developing embryo/fetus: is there a safe level?CrossRef | 1:CAS:528:DC%2BC38Xht1OlsrzJ&md5=6415fd47ba12256987e1c2e09f10bddbCAS |

Conley, A. J., Elf, P., Corbin, C. J., Dubowsky, S., Fivizzani, A., and Lang, J. W. (1997). Yolk steroids decline during sexual differentiation in the alligator. Gen. Comp. Endocrinol. 107, 191–200.
Yolk steroids decline during sexual differentiation in the alligator.CrossRef | 1:CAS:528:DyaK2sXkvFOlsb0%3D&md5=d4f1824f924325c38a776b1c3aab1eb6CAS | 9245527PubMed |

Crain, D. A., and Guillette, L. J. J. (1998). Reptiles as models of contaminant-induced endocrine disruption. Anim. Reprod. Sci. 53, 77–86.
Reptiles as models of contaminant-induced endocrine disruption.CrossRef | 1:CAS:528:DyaK1cXns1yksLk%3D&md5=3278feeb464e43cf0331f37a0654a0c5CAS | 9835368PubMed |

Crews, D., Putz, O., Thomas, P., Hayes, T., and Howdeshell, K. (2003). Wildlife as models for the study of how mixtures, low doses and the embryonic environment modulate the action of endocrine-disrupting chemicals. Pure Appl. Chem. 75, 2305–2320.
Wildlife as models for the study of how mixtures, low doses and the embryonic environment modulate the action of endocrine-disrupting chemicals.CrossRef | 1:CAS:528:DC%2BD2cXnslOhtQ%3D%3D&md5=67bde93bf88847ca995951f784c82e65CAS |

Dufaure, J. P., and Hubert, J. (1961). Table de developpement du lezard vivipare Lacerta (Zootaca) vivipara Jacquin. Arch. Anat. Micros. Exp. 50, 309–328.

Edlow, A. G., Chen, M., Smith, N. A., Lu, C., and McElrath, T. F. (2012). Fetal bisphenol A exposure: concentration of conjugated and unconjugated bisphenol A in amniotic fluid in the second and third trimesters. Reprod. Toxicol. 34, 1–7.
Fetal bisphenol A exposure: concentration of conjugated and unconjugated bisphenol A in amniotic fluid in the second and third trimesters.CrossRef | 1:CAS:528:DC%2BC38XmtlWisrs%3D&md5=1eaec6564ddbe6f4c05556c4750d82f3CAS | 22516041PubMed |

Findholt, S. L. (1984). Organochlorine residues, eggshell thickness and reproductive success of snowy egrets nesting in Idaho. Condor 86, 163–169.
Organochlorine residues, eggshell thickness and reproductive success of snowy egrets nesting in Idaho.CrossRef |

Foster, W. G., Hughes, C. L., Chan, S., and Platt, L. (2002). Human developmental exposure to endocrine active compounds. Environ. Toxicol. Pharmacol. 12, 75–81.
Human developmental exposure to endocrine active compounds.CrossRef | 1:CAS:528:DC%2BD38XltFWhsbg%3D&md5=95e15addb8adc2bd5d1a6e378da08b0aCAS | 21782626PubMed |

Fry, D. M., and Toone, K. (1981). DDT-induced feminisation of gull embryos. Science 213, 922–924.
DDT-induced feminisation of gull embryos.CrossRef | 1:CAS:528:DyaL3MXlt1Ojs7w%3D&md5=361c6567bc374cfca019419a59d81aabCAS | 7256288PubMed |

Girling, J. E., Jones, S. M., and Swain, R. (2002). Induction of parturition in snow skinks: can low temperatures inhibit the actions of AVT? J. Exp. Zool. 293, 525–531.
Induction of parturition in snow skinks: can low temperatures inhibit the actions of AVT?CrossRef | 12486812PubMed |

Guarino, F. M., Paulesu, L., Cardone, A., Bellini, L., Ghiara, G., and Angelini, F. (1998). Endocrine activity of the corpus luteum and placenta during pregnancy in Chalcides chalcides (Reptilia, Squamata). Gen. Comp. Endocrinol. 111, 261–270.
Endocrine activity of the corpus luteum and placenta during pregnancy in Chalcides chalcides (Reptilia, Squamata).CrossRef | 1:CAS:528:DyaK1cXls1alu7c%3D&md5=d7be478d7ea6395bbc2ea5094350e828CAS | 9707472PubMed |

Guillette, L. J. J., and Edwards, T. M. (2008). Environmental influences on fertility: can we learn lessons from studies of wildlife? Fertil. Steril. 89, e21–e24.
Environmental influences on fertility: can we learn lessons from studies of wildlife?CrossRef |

Guillette, L. J. J., and Gunderson, M. P. (2001). Alterations in development of reproductive and endocrine systems of wildlife populations exposed to endocrine-disrupting contaminants. Reproduction 122, 857–864.
Alterations in development of reproductive and endocrine systems of wildlife populations exposed to endocrine-disrupting contaminants.CrossRef | 1:CAS:528:DC%2BD38XhvVWjtg%3D%3D&md5=3e0678ce1455effa62bf39df0b77305fCAS |

Guillette, L. J. J., 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.
Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida.CrossRef | 1:CAS:528:DyaK2MXhsl2qsr8%3D&md5=df8dcc256361faaf1aba6cfa5abe1747CAS |

Guillette, L. J., Crain, D. A., Rooney, A. A., and Pickford, D. B. (1995). Organization versus activation: The role of endocrine-disrupting contaminants (EDCs) during embryonic development in wildlife. Environ. Health Perspect. 103, 157–164.
| 1:CAS:528:DyaK28XlvFehsQ%3D%3D&md5=b05110d14a880d4aa56de050593563a6CAS | 8593864PubMed |

Guillette, L. J. J., Brock, J. W., Rooney, A. A., and Woodward, A. R. (1999). Serum concentrations of various environmental contaminants and their relationship to sex-steroid concentrations and phallus size in juvenile American alligators. Arch. Environ. Contam. Toxicol. 36, 447–455.
Serum concentrations of various environmental contaminants and their relationship to sex-steroid concentrations and phallus size in juvenile American alligators.CrossRef | 1:CAS:528:DyaK1MXivFSmu7Y%3D&md5=0d9934cb35ab6fcccbe476977f9783dcCAS |

Guillette, L. J., Crain, D. A., and Gunderson, M. P. (2000). Alligators and endocrine-disrupting contaminants: a current perspective. Am. Zool. 40, 438–452.
Alligators and endocrine-disrupting contaminants: a current perspective.CrossRef | 1:CAS:528:DC%2BD3cXnvVOisr0%3D&md5=6442c021a5606cadc61109d74ede68ddCAS |

Hamlin, H. J., Lowers, R. H., Albergotti, L. C., McCoy, M. W., Mutz, J., and Guillette, L. J. (2010). Environmental influence on yolk steroids in American alligators (Alligator mississippiensis). Biol. Reprod. 83, 736–741.
Environmental influence on yolk steroids in American alligators (Alligator mississippiensis).CrossRef | 1:CAS:528:DC%2BC3cXhtlGls77O&md5=bc0caec03ade28e087a609245bcef801CAS | 20650885PubMed |

Hayes, T. B., Collins, A., Lee, M., Mendoza, M., Noriega, N., Stuart, A. A., and Vonk, A. (2002). Hermaphroditic, demasculinised frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc. Natl. Acad. Sci. USA 99, 5476–5480.
Hermaphroditic, demasculinised frogs after exposure to the herbicide atrazine at low ecologically relevant doses.CrossRef | 1:CAS:528:DC%2BD38XjtFKlsbc%3D&md5=d66ab40dac007b06bf2d52bc3e0d6984CAS | 11960004PubMed |

Hayes, T. B., Khoury, V., Narayan, A., Nazir, M., Parka, A., Brown, T., Adame, L., Chan, E., Buchholz, D., Stueve, T., and Gallipeau, S. (2010). Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proc. Natl. Acad. Sci. USA 107, 4612–4617.
Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis).CrossRef | 1:CAS:528:DC%2BC3cXjs1emurk%3D&md5=765583351d34804cf3ec76566456ec47CAS | 20194757PubMed |

Hayes, T. B., Anderson, L. L., Beasley, V. R., De Solla, S. R., Iguchi, T., Ingraham, H., Kestemont, P., Kniewald, J., Kniewald, Z., Langlois, V. S., Luque, E. H., McCoy, K. A., Muñoz-De-Toro, M., Oka, T., Oliveira, C. A., Orton, F., Ruby, S., Suzawa, M., Tavera-Mendoza, L. E., Trudeau, V. L., Victor-Costa, A. B., and Willingham, E. (2011). Demasculinisation and feminisation of male gonads by atrazine: consistent effects across vertebrate classes. J. Steroid Biochem. Mol. Biol. 127, 64–73.
Demasculinisation and feminisation of male gonads by atrazine: consistent effects across vertebrate classes.CrossRef | 1:CAS:528:DC%2BC3MXht12ru7jJ&md5=d2082264211cfc49c41b757af76f551eCAS | 21419222PubMed |

Hernández-Franyutti, A., Uribe Aranzábal, M. C., and Guillette Jr, L. J. (2005). Oogenesis in the viviparous matrotrophic lizard Mabuya brachypoda. J. Morphol. 265, 152–164.
Oogenesis in the viviparous matrotrophic lizard Mabuya brachypoda.CrossRef | 15959907PubMed |

Holmes, M. M., and Wade, J. (2005). Sexual differentiation of the copulatory neuromuscular system in green anoles (Anolis carolinensis): normal ontogeny and manipulation of steroid hormones. J. Comp. Neurol. 489, 480–490.
Sexual differentiation of the copulatory neuromuscular system in green anoles (Anolis carolinensis): normal ontogeny and manipulation of steroid hormones.CrossRef | 1:CAS:528:DC%2BD2MXpsVWltLk%3D&md5=9cc0d024d7223126fd8c669d84712dbfCAS | 16025462PubMed |

Iguchi, T., and Takasugi, N. (1986). Polyovular follicles in the ovary of immature mice exposed prenatally to diethylstilbestrol. Anat. Embryol. (Berl.) 175, 53–55.
Polyovular follicles in the ovary of immature mice exposed prenatally to diethylstilbestrol.CrossRef | 1:STN:280:DyaL2s%2Fpsl2ltA%3D%3D&md5=02597866ead8cd65dd5f8510c4c50391CAS | 3799991PubMed |

Iguchi, T., Takasugi, N., Bern, H. A., and Mills, K. T. (1986). Frequent occurrence of polyovular follicles in ovaries of mice exposed neonatally to diethylstilbestrol. Teratology 34, 29–35.
Frequent occurrence of polyovular follicles in ovaries of mice exposed neonatally to diethylstilbestrol.CrossRef | 1:CAS:528:DyaL28Xls1Ggsbo%3D&md5=bf964e5ee23f5972f1cd57781ad95b6bCAS | 3764775PubMed |

Inamdar, L. S., Vani, V. V., and Rao, G. M. A. (2012). Dimorphic hemipenis correlates the pathways of gonadal sex differentiation in the lizard, Calotes versicolor (Daud.). J Adv Zool. 33, 31–37.

Itonaga, K., Wapstra, E., and Jones, S. M. (2011). Evidence for placental transfer of maternal corticosterone in a viviparous lizard. Comp. Physiol. A. Mol. Integr. Physiol. 160, 184–189.
Evidence for placental transfer of maternal corticosterone in a viviparous lizard.CrossRef | 1:CAS:528:DC%2BC3MXpsFaku7g%3D&md5=1aab2e04fcf009b61fc99695096c2a3aCAS |

Jespersen, Ã., Rasmussen, T. H., Hirche, M., Sørensen, K. J. K., and Korsgaard, B. (2010). Effects of exposure to the xenoestrogen octylphenol and subsequent transfer to clean water on liver and gonad ultrastructure during early development of Zoarces viviparus embryos. J. Exp. Zool. A. Ecol. Genet. Physiol. 313A, 399–409.
Effects of exposure to the xenoestrogen octylphenol and subsequent transfer to clean water on liver and gonad ultrastructure during early development of Zoarces viviparus embryos.CrossRef | 1:CAS:528:DC%2BC3cXhtVyjurjO&md5=d792c6f35ddd6a8a608eec870a2bd236CAS |

Jones, S. M. (2011). Hormonal regulation of ovarian function in reptiles. In ‘Hormones and Reproduction of Vertebrates’. (Eds D. O. Norris and K. H. Lopez.) pp. 89–115. (Academic Press: Burlington.)

Jones, S. M., and Swain, R. (1996). Annual reproductive cycle and annual cycles of reproductive hormones in plasma of female Niveoscincus metallicus (Scincidae) from Tasmania. J. Herpetol. 30, 140–146.
Annual reproductive cycle and annual cycles of reproductive hormones in plasma of female Niveoscincus metallicus (Scincidae) from Tasmania.CrossRef |

Jones, S. M., Bennett, E. J., and Swadling, K. M. (1998). Lipids in yolks and neonates of the viviparous lizard Niveoscincus metallicus. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 121, 465–470.
Lipids in yolks and neonates of the viviparous lizard Niveoscincus metallicus.CrossRef |

Kim, H., Nakajima, T., Hayashi, S., Chambon, P., Watanabe, H., Iguchi, T., and Sato, T. (2009). Effects of diethylstilbestrol on programmed oocyte death and induction of polyovular follicles in neonatal mouse ovaries. Biol. Reprod. 81, 1002–1009.
Effects of diethylstilbestrol on programmed oocyte death and induction of polyovular follicles in neonatal mouse ovaries.CrossRef | 19553606PubMed |

Kuiper, G. G. J. M., Carlsson, B., Grandien, K., Enmark, E., Häggblad, J., Nilsson, S., and Gustafsson, J. Å. (1997). Comparison of the ligand-binding specificity and transcript tissue distribution of oestrogen receptors α and β. Endocrinology 138, 863–870.
| 1:CAS:528:DyaK2sXht1OksrY%3D&md5=601621d52ffe2deb72b42b36d7e34f3aCAS |

LaRocca, J., Boyajian, A., Brown, C., Smith, S. D., and Hixon, M. (2011). Effects of in utero exposure to bisphenol A or diethylstilbestrol on the adult male reproductive system. Birth Defects Res. B Dev. Reprod. Toxicol. 92, 526–533.
Effects of in utero exposure to bisphenol A or diethylstilbestrol on the adult male reproductive system.CrossRef | 1:CAS:528:DC%2BC3MXhs1Sgu73M&md5=bc2f004933759d9b6f543e948927b6eaCAS | 21922642PubMed |

Le Galliard, J. F., Clobert, J., and Ferrière, R. (2004). Physical performance and Darwinian fitness in lizards. Nature 432, 502–505.
Physical performance and Darwinian fitness in lizards.CrossRef | 1:CAS:528:DC%2BD2cXhtVWitbvI&md5=6b354b6c38a28f07880e440911df2167CAS | 15565154PubMed |

Melville, J., and Swain, R. (2003). Evolutionary correlations between escape behaviour and performance ability in eight species of snow skinks (Niveoscincus: Lygosominae) from Tasmania. J. Zool. (Lond.) 261, 79–89.
Evolutionary correlations between escape behaviour and performance ability in eight species of snow skinks (Niveoscincus: Lygosominae) from Tasmania.CrossRef |

Miller, R. K., Heckmann, M. E., and McKenzie, R. C. (1982). Diethylstilbestrol: placental transfer, metabolism, covalent binding and fetal distribution in the Wistar rat. J. Pharmacol. Exp. Ther. 220, 358–365.
| 1:CAS:528:DyaL38XhsFGrsrY%3D&md5=5e294ac245c378e83c018d34ac45e25fCAS | 7057397PubMed |

Moodley, G. K., and Van Wyk, J. H. (2007). Folliculogenesis and ovarian histology of the oviparous gecko, Hemidactylus mabouia (Sauria: Gekkonidae). Afr. J. Herpetol. 56, 115–135.
Folliculogenesis and ovarian histology of the oviparous gecko, Hemidactylus mabouia (Sauria: Gekkonidae).CrossRef |

Moore, B. C., Hamlin, H. J., Botteri, N. L., Lawler, A. N., Mathavan, K. K., and Guillette, L. J. (2010). Post-hatching development of Alligator mississippiensis ovary and testis. J. Morphol. 271, 580–595.
| 20013789PubMed |

Neaves, L., Wapstra, E., Birch, D., Girling, J. E., and Joss, J. M. P. (2006). Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus. J. Exp. Zool. A Comp. Exp. Biol. 305A, 74–82.
Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus.CrossRef |

Newbold, R. (1995). Cellular and molecular effects of developmental exposure to diethylstilbestrol: implications for other environmental oestrogens. Environ. Health Perspect. 103, 83–87.
| 1:CAS:528:DyaK28XlvFeisA%3D%3D&md5=e43d83834ebdecc2d3a418b4027781e8CAS | 8593881PubMed |

Newbold, R. R. (2004). Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol. Appl. Pharmacol. 199, 142–150.
Lessons learned from perinatal exposure to diethylstilbestrol.CrossRef | 1:CAS:528:DC%2BD2cXmslaltr8%3D&md5=97c8b91ff28d6d01685e79a5a2064850CAS | 15313586PubMed |

Newbold, R. R. (2012). Prenatal exposure to diethylstilbestrol and long-term impact on the breast and reproductive tract in humans and mice. J. Dev. Orig. Heal. Dis. 3, 73–82.
Prenatal exposure to diethylstilbestrol and long-term impact on the breast and reproductive tract in humans and mice.CrossRef | 1:CAS:528:DC%2BC38Xjt1WhsbY%3D&md5=533459552693d7756ba1d98863af3635CAS |

Nonclercq, D., Reverse, D., Toubeau, G., Beckers, J. F., Sulon, J., Laurent, G., Zanen, J., and Heuson-Stiennon, J. A. (1996). In situ demonstration of germinal-cell apoptosis during diethylstilbestrol-induced testis regression in adult male Syrian hamsters. Biol. Reprod. 55, 1368–1376.
In situ demonstration of germinal-cell apoptosis during diethylstilbestrol-induced testis regression in adult male Syrian hamsters.CrossRef | 1:CAS:528:DyaK2sXkvFWitA%3D%3D&md5=43ccb6defc1dc722c1c11fe1af38ae1dCAS | 8949895PubMed |

Painter, D. L., and Moore, M. C. (2005). Steroid hormone metabolism by the chorioallantoic placenta of the mountain spiny lizard Sceloporus jarrovi as a possible mechanism for buffering maternal–fetal hormone exchange. Physiol. Biochem. Zool. 78, 364–372.
Steroid hormone metabolism by the chorioallantoic placenta of the mountain spiny lizard Sceloporus jarrovi as a possible mechanism for buffering maternal–fetal hormone exchange.CrossRef | 1:CAS:528:DC%2BD2MXlvVGgsbg%3D&md5=2f9754ea156867d04951c69c8e926d2bCAS | 15887083PubMed |

Pasqualini, J. R. (2005). Enzymes involved in the formation and transformation of steroid hormones in the fetal and placental compartments. J. Steroid Biochem. Mol. Biol. 97, 401–415.
Enzymes involved in the formation and transformation of steroid hormones in the fetal and placental compartments.CrossRef | 1:CAS:528:DC%2BD2MXht1OntL3K&md5=6a11a07edb83263d00706cd5ec64405fCAS | 16202579PubMed |

Pérez-Martínez, C., Ferreras-Estrada, M. C., García-Iglesias, M. J., Bravo-Moral, A. M., Espinosa-Alvarez, J., and Escudero-Diez, A. (1997). Effects of in utero exposure to nonsteroidal oestrogens on mouse testis. Can. J. Vet. Res. 61, 94–98.
| 9114959PubMed |

Pieau, C., Dorizzi, M., and Richard-Mercier, N. (1999). Temperature-dependent sex determination and gonadal differentiation in reptiles. Cell. Mol. Life Sci. 55, 887–900.
Temperature-dependent sex determination and gonadal differentiation in reptiles.CrossRef | 1:CAS:528:DyaK1MXkt1altbw%3D&md5=85115f281c8a663731b2812014beb4edCAS | 10412370PubMed |

Ramaswami, L. S., and Jacob, D. (1965). Effect of testosterone propionate on the urogenital organs of immature crocodile Crocodylus palustris lesson. Experientia 21, 206–207.
Effect of testosterone propionate on the urogenital organs of immature crocodile Crocodylus palustris lesson.CrossRef | 1:CAS:528:DyaF2MXktVClu7g%3D&md5=b392cce06496fd6b4d160c52769cdcc6CAS | 5845262PubMed |

Simon, L., Avery, L., Braden, T. D., Williams, C. S., Okumu, L. A., Williams, J. W., and Goyal, H. O. (2012). Exposure of neonatal rats to anti-androgens induces penile mal-developments and infertility comparable to those induced by oestrogens. Int. J. Androl. 35, 364–376.
Exposure of neonatal rats to anti-androgens induces penile mal-developments and infertility comparable to those induced by oestrogens.CrossRef | 1:CAS:528:DC%2BC38XhtFCisrfP&md5=70b9ceb8964832abb6b36dcf71ca8fe9CAS | 22150386PubMed |

Slikker, W. Slikker, W. (1982). Comparison of the transplacental pharmacokinetics of 17β-oestradiol and diethylstilbestrol in the subhuman primate. J. Pharmacol. Exp. Ther. 221, 173–182.
| 1:CAS:528:DyaL38XitFWhtr4%3D&md5=df2ac1bbc3c4a1b8ededd5ea01bef02dCAS | 7062281PubMed |

Stewart, J. R. (2013). Fetal nutrition in lecithotrophic squamate reptiles: toward a comprehensive model for evolution of viviparity and placentation. J. Morphol. 274, 824–843.
Fetal nutrition in lecithotrophic squamate reptiles: toward a comprehensive model for evolution of viviparity and placentation.CrossRef | 23520054PubMed |

Strauss, J. F., Martinez, F., and Kiriakidou, M. (1996). Placental steroid hormone synthesis: unique features and unanswered questions. Biol. Reprod. 54, 303–311.
Placental steroid hormone synthesis: unique features and unanswered questions.CrossRef | 1:CAS:528:DyaK28XltF2qtw%3D%3D&md5=75eaebfa8a06a2eee9e344b4b099c163CAS | 8788180PubMed |

Susiarjo, M., Sasson, I., Mesaros, C., and Bartolomei, M. S. (2013). Bisphenol A exposure disrupts genomic imprinting in the mouse. PLoS Genet. 9, e1003401.
Bisphenol A exposure disrupts genomic imprinting in the mouse.CrossRef | 1:CAS:528:DC%2BC3sXnt1aqsLo%3D&md5=a83f9a380ea76d75e102daa0c41d035cCAS | 23593014PubMed |

Vandenberg, L. N., Colborn, T., Hayes, T. B., Heindel, J. J., Jacobs, D. R., Lee, D. H., Shioda, T., Soto, A. M., vom Saal, F. S., Welshons, W. V., Zoeller, R. T., and Myers, J. P. (2012). Hormones and endocrine-disrupting chemicals: low-dose effects and non-monotonic dose responses. Endocr. Rev. 33, 378–455.
Hormones and endocrine-disrupting chemicals: low-dose effects and non-monotonic dose responses.CrossRef | 1:CAS:528:DC%2BC38XhtFSrtr7L&md5=deab2425c3239cecc0089bc19b6be058CAS | 22419778PubMed |

Wapstra, E., and O’Reilly, J. M. (2001). Potential ‘costs of reproduction’ in a skink: inter- and intrapopulational variation. Austral Ecol. 26, 179–186.
Potential ‘costs of reproduction’ in a skink: inter- and intrapopulational variation.CrossRef |

Yamaguchi, M., Mitsumori, F., Watanabe, H., Takaya, N., and Minami, M. (2009). Visualisation of seminiferous tubules in rat testes in normal and diseased conditions by high-resolution MRI. Magn. Reson. Med. 62, 637–644.
Visualisation of seminiferous tubules in rat testes in normal and diseased conditions by high-resolution MRI.CrossRef | 19526509PubMed |

Yoshimura, Y., and Fujita, M. (2005). Endocrine disruption in avian reproduction: the histological analysis. Avian Poult. Biol. Rev. 16, 29–40.
Endocrine disruption in avian reproduction: the histological analysis.CrossRef |



Rent Article (via Deepdyve) Export Citation Cited By (2)