Skip to main content

Advertisement

Log in

Superovulation does not affect the endocrine activity nor increase susceptibility to carcinogenesis of uterine and mammary glands of female offspring in mice

  • Epigenetics
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

To evaluate the dual effects of superovulation on the endocrine activity and susceptibility to carcinogenesis of uterine and mammary glands of female offspring in mice

Method

The mice were superovaluted. The relative uterine weight, ERα protein expression, and endocrine activity of female offspring (F1 generation and F2 generation) were measured. Furthermore, proliferative lesion of uterine and mammary glands of female offspring (F1 generation and F2 generation) was assessed by histopathologic examinations.

Results

There were no significant differences in relative uterine weight, ERα protein expression, incidence of proliferative lesion in mammary glands, and incidence of atypical hyperplasia, adenocarcinoma, and squamous metaplasia in uterine among the offspring (F1 generation and F2 generation) in each group. Likewise, there were no significant intergroup differences in the serum levels of sex related hormones.

Conclusions

No significant alterations were found in the endocrine activity and susceptibility to carcinogenesis of uterine and mammary glands of female offspring in mice produced by superovaluted oocytes compared with those of naturally conceived offspring.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Blyth E. Below population replacement fertility rates: Can assisted reproductive technology (ART) help reverse the trend? Asian Pacific J Reprod. 2013;2:151–8.

    Article  Google Scholar 

  2. Hart R, Norman RJ. The longer-term health outcomes for children born as a result of IVF treatment. Part II–Mental health and development outcomes. Hum Reprod Update. 2013;19:244–55.

    Article  CAS  PubMed  Google Scholar 

  3. Doyle P, Beral V, Maconochie N. Preterm delivery, low birthweight and small-for-gestational-age in live-born singleton babies resulting from in vitro fertilization. Hum Reprod. 1992;7:425–8.

    CAS  PubMed  Google Scholar 

  4. Anckaert E, Rycke MD, Smitz J. Culture of oocytes and risk of imprinting defects. Hum Reprod Update. 2013;19:52–66.

    Article  CAS  PubMed  Google Scholar 

  5. Van der Auwera I D,Hooghe T. Superovulation of female mice delays embryonic and fetal development. Hum Reprod. 2001;16:1237–43

  6. Krisher RL. The effect of oocyte quality on development. J Anim Sci. 2004;82 (E-Suppl):E14–23.

  7. Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet. 2004;13:839–49.

    Article  CAS  PubMed  Google Scholar 

  8. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T. Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells. 2006;11:353–61.

    Article  CAS  PubMed  Google Scholar 

  9. Anckaert E, Adriaenssens T, Romero S, Dremier S, Smitz J. Unaltered imprinting establishment of key imprinted genes in mouse oocytes after in vitro follicles culture under variable follicle-stimulating hormone exposure. Int J Dev Biol. 2009;53:541–8.

    Article  CAS  PubMed  Google Scholar 

  10. Denomme MM, Zhang L, Mann MR. Embryonic imprinting perturbations do not originate from superovulation-induced defects in DNA methylation acquisition. Fertil Steril. 2011;96:734–8.

    Article  CAS  PubMed  Google Scholar 

  11. Suter MA, Aaqaard K. What changes in DNA methylation take place in individuals exposed to maternal smoking in utero? Epigenomic. 2012;4:115–8.

    Article  CAS  Google Scholar 

  12. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359:61–73.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Newbold RR, Jefferson WN, Padilla-Banks E, Haseman J. Developmental exposure to diethylstilbestrol (DES) alters uterine response to estrogens in prepubescent mice: low versus high dose effects. Reprod Toxicol. 2004;18:399–406.

    Article  CAS  PubMed  Google Scholar 

  14. Kass L, Durando M, Altamirano GA, et al. Prenatal Bisphenol A exposure delays the development of the male rat mammary gland. Reprod Toxicol. 2004 (Epub ahead of print).

  15. Ho SM, Tang WY, de Frausto JB, Prins GS. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res. 2006;66:5624–32.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Herbst AL, Anderson D. Clear cell adenocarcinoma of the vagina and cervix secondary to intrauterine exposure to diethylstilbestrol. Semin Surg Oncol. 1990;6:343–6.

    Article  CAS  PubMed  Google Scholar 

  17. Swan SH. Intrauterine exposure to diethylstilbestrol: long-term effects in humans. APMIS. 2000;108:793–804.

    Article  CAS  PubMed  Google Scholar 

  18. Kawaguchi H, Umekita Y, Souda M, Gejima K, Kawashima H, et al. Effects of neonatally administered high-dose diethylstilbestrol on the induction of mammary tumors induced by 7,12-dimethylbenz [a] anthracene in female rats. Vet Pathol. 2009;46:142–50.

    Article  CAS  PubMed  Google Scholar 

  19. Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Mann MR. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum Mol Genet. 2010;19:36–51.

    Article  CAS  PubMed  Google Scholar 

  20. Balaton AJ, Ochando F, Painchaud MH. Use of microwaves of enhancing or restoring antigens before immunohistochemical staining. Ann Pathol. 1993;13:188–9.

    CAS  PubMed  Google Scholar 

  21. Guerra MT, Sanabria M, Grossman G, Petrusz P, Kempinas WG. Excess androgen during perinatal life alters steroid receptor expression, apoptosis, and cell proliferation in the uteri of the offspring. Reprod Toxicol. 2013;40:1–7.

    Article  CAS  PubMed  Google Scholar 

  22. Yoshida M, Takahashi M, Inoue K, Hayashi S, Maekawa A, et al. Delayed adverse effects of neonatal exposure to diethylstilbestrol and their dose dependency in female rats. Toxicol Pathol. 2011;39:823–34.

    Article  CAS  PubMed  Google Scholar 

  23. Taya K, Mizokawa T, Matsui T, Sasamoto S. Induction of superovulation in prepubertal female rats by anterior pituitary transplants. J Reprod Fertil. 1983;69:265–70.

    Article  CAS  PubMed  Google Scholar 

  24. Takahashi M, Inoue K, Morikawa T, Matsuo S, Hayashi S, et al. Delayed effects of neonatal exposure to 17alpha-ethynylestradiol on the estrous cycle and uterine carcinogenesis in Wistar Hannover GALAS rats. Reprod Toxicol. 2013;40:16–23.

    Article  CAS  PubMed  Google Scholar 

  25. Hamada T, Watanabe G, Kokuho T, Taya K, Sasamoto S, et al. Radioimmunoassay of inhibin in various mammals. J Endocrinol. 1989;122:697–704.

    Article  CAS  PubMed  Google Scholar 

  26. Low FM, Gluckman PD, Hanson MA. Developmental plasticity and epigenetic mechanisms underpinning metabolic and cardiovascular disease. Epigenomics. 2011;3:279–94.

    Article  CAS  PubMed  Google Scholar 

  27. Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105:17046–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. De rooij SR, Wouters H, Yonker Jf, Painyer RC, Roseboom J. Prenatal undernutrition and cognitive function in late adulthood. Proc Natl Acad Sci U S A. 2010;107:16881–6.

  29. Franks S. Animal models and the developmental origins of polycystic ovary syndrome: increasing evidence for the role of androgens in programming reproductive and metabolic dysfunction. Endocrinology. 2012;153:2536–8.

    Article  CAS  PubMed  Google Scholar 

  30. Bosquiazzo VL, Vigezzi L, Muñoz-de-Toro M, Luque EH. Preinatal exposure to diethylstilbestrol alters the functional differentiation of the adult rat uterus. J Steroid Biochem Mol Biol. 2013;138:1–9.

    Article  CAS  PubMed  Google Scholar 

  31. Carone BR, Fauquier L, Habib N, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell. 2010;143:1084–96.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308:1466–9.

    Article  CAS  PubMed  Google Scholar 

  33. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprintedloci in superovulated oocytes. Hum Reprod. 2007;22:26–35.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Mei Wang for the valuable comments on the manuscript.

Conflict of interest statement

The authors declare that there are no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jian-Min Zhang.

Additional information

Capsule

Effects of superovulation on the endocrine activity and susceptibility to carcinogenesis of offspring

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, Z., Zhang, G., Yu, J. et al. Superovulation does not affect the endocrine activity nor increase susceptibility to carcinogenesis of uterine and mammary glands of female offspring in mice. J Assist Reprod Genet 31, 1243–1249 (2014). https://doi.org/10.1007/s10815-014-0295-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10815-014-0295-z

Keywords

Navigation