Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-21T01:42:21.720Z Has data issue: false hasContentIssue false
  • English
  • Français

Overweight negatively affects outcome of superovulation treatment in female mice

Published online by Cambridge University Press:  27 November 2017

Dušan Fabian ,
Janka Babeľová ,
Štefan Čikoš  and
Zuzana Šefčíková
Dušan Fabian*
Affiliation:
Institute of Animal Physiology, Slovak Academy of Sciences, Šoltésovej 4/6, 04001 Košice, Slovakia.
Janka Babeľová
Affiliation:
Institute of Animal Physiology, Slovak Academy of Sciences, 04001 Košice, Slovakia.
Štefan Čikoš
Affiliation:
Institute of Animal Physiology, Slovak Academy of Sciences, 04001 Košice, Slovakia.
Zuzana Šefčíková
Affiliation:
Institute of Animal Physiology, Slovak Academy of Sciences, 04001 Košice, Slovakia.
*
All correspondence to: Dušan Fabian. Institute of Animal Physiology, Slovak Academy of Sciences, Šoltésovej 4/6, 04001 Košice, Slovakia. Tel: +421 55 727 6274. E-mail: fabian@saske.sk
Get access Rights & Permissions [Opens in a new window]

Summary

Superovulatory response is characterized by a high degree of variability and unpredictability. The aim of the present experimental study was to examine whether the amount of maternal body fat can influence the efficiency of ovarian stimulation with gonadotropins. Female mice of two body condition types, normal and obese, produced in a standardized two-generation model, were subjected to ovarian stimulation using eCG and hCG followed by natural mating. Produced ova and embryos were recovered on day 1 and day 4 of pregnancy respectively, and several quantitative, qualitative and developmental parameters were evaluated in them. The overall response of mouse females with normal and elevated amounts of body fat to superovulation was similar: They produced almost the same numbers of ova and embryos on average. Conversely, a higher number of immature oocytes, non-fertilized mature oocytes and lower-stage zygotes were collected from fat females. In both groups, the majority of fertilized oocytes was able to cleave and reach the higher stages of development. However, in the group of fat mice, a lower number of blastocysts was collected, and these blastocysts showed increased incidence of apoptotic cell death. In conclusion, although the response of normal and fat mice to superovulatory treatment was similar, the quality and developmental capacities of produced ova were lower in the group of fat donors.

Keywords

ApoptosisMouse modelOvarian stimulationOverweightPreimplantation development
Type
Research Article
Information
Zygote , Volume 25 , Issue 6 , December 2017 , pp. 751 - 759
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adenot, P.G., Mercier, Y., Renard, J.P. & Thompson, E.M. (1997). Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124, 4615–25.CrossRefGoogle ScholarPubMed
Bakhtari, A., Rahmani, H.R., Bonakdar, E., Jafarpour, F., Asgari, V., Hosseini, S.M., Hajian, M., Edriss, M.A. & Nasr-Esfahani, M.H. (2014). The interfering effects of superovulation and vitrification upon some important epigenetic biomarkers in mouse blastocyst. Cryobiology 69, 419–27.CrossRefGoogle ScholarPubMed
Blondin, P., Coenen, K., Guilbault, L.A. & Sirard, M.A. (1996). Superovulation can reduce the developmental competence of bovine embryos. Theriogenology 46, 1191–203.CrossRefGoogle ScholarPubMed
Bonakdar, E., Edriss, M.A., Bakhtari, A., Jafarpour, F., Asgari, V., Hosseini, S.M., Sadeghi Boroujeni, N., Hajian, M., Rahmani, H.R. & Nasr-Esfahani, M.H. (2015). A physiological, rather than a superovulated, post-implantation environment can attenuate the compromising effect of assisted reproductive techniques on gene expression in developing mice embryos. Mol. Reprod. Dev. 82, 191–206.CrossRefGoogle ScholarPubMed
Brannian, J.D., Furman, G.M. & Diggins, M. (2005). Declining fertility in the lethal yellow mouse is related to progressive hyperleptinemia and leptin resistance. Reprod. Nutr. Dev. 45, 143–50.CrossRefGoogle ScholarPubMed
Brewer, C.J. & Balen, A.H. (2010). The adverse effects of obesity on conception and implantation. Reproduction 140, 347–64.CrossRefGoogle ScholarPubMed
Brinton, L.A., Moghissi, K.S., Scoccia, B., Westhoff, C.L. & Lamb, E.J. (2005). Ovulation induction and cancer risk. Fertil. Steril. 83, 261–74.CrossRefGoogle ScholarPubMed
Chrenek, P., Makarevich, A., Vasícek, D., Laurincík, J., Bulla, J., Gajarská, T. & Rafay, J. (1998). Effects of superovulation, culture and microinjection on development of rabbit embryos in vitro . Theriogenology 50, 659–66.CrossRefGoogle ScholarPubMed
Chu, T., Dufort, I. & Sirard, M.A. (2012). Effect of ovarian stimulation on oocyte gene expression in cattle. Theriogenology 77, 1928–38.CrossRefGoogle ScholarPubMed
Dechaud, H., Anahory, T., Reyftmann, L., Loup, V., Hamamah, S. & Hedon, B. (2006). Obesity does not adversely affect results in patients who are undergoing in vitro fertilization and embryo transfer. Eur. J. Obstet. Gynecol. Reprod. Biol. 127, 88–93.CrossRefGoogle Scholar
Elbling, L. & Colot, M. (1985). Abnormal development and transport and increased sister-chromatid exchange in preimplantation embryos following superovulation in mice. Mutat. Res. 147, 189–95.CrossRefGoogle ScholarPubMed
Ertzeid, G. & Storeng, R. (2001). The effect of ovarian stimulation on implantation and fetal development in mice. Hum. Reprod. 16, 221–5.CrossRefGoogle ScholarPubMed
Fabian, D., Makarevich, A. V, Chrenek, P., Bukovská, A. & Koppel, J. (2007). Chronological appearance of spontaneous and induced apoptosis during preimplantation development of rabbit and mouse embryos. Theriogenology 68, 1271–81.CrossRefGoogle ScholarPubMed
Fabian, D., Bystriansky, J., Makarevich, A. V., Chrenek, P. & Koppel, J. (2009). Variability in apoptosis incidence in mouse blastocysts in relation to their age and the type of their derivation. Slovak J. Anim. Sci. 4, 155–8.Google Scholar
Fabian, D., Kubandová, J., Čikoš, Š., Burkuš, J., Fabianová, K., Račeková, E. & Czikková, S., Koppel, J. (2015). The effect of maternal body condition on in vivo production of zygotes and behavior of delivered offspring in mice. Theriogenology 83, 577–89.CrossRefGoogle ScholarPubMed
Fedorcsák, P., Dale, P.O., Storeng, R., Tanbo, T. & Abyholm, T. (2001). The effect of obesity and insulin resistance on the outcome of IVF or ICSI in women with polycystic ovarian syndrome. Hum. Reprod. 16, 1086–91.CrossRefGoogle ScholarPubMed
Freret, S., Grimard, B., Ponter, A.A., Joly, C., Ponsart, C. & Humblot, P. (2006). Reduction of body-weight gain enhances in vitro embryo production in overfed superovulated dairy heifers. Reproduction 131, 783–94.CrossRefGoogle ScholarPubMed
Greve, T., Callesen, H., Hyttel, P., Høier, R. & Assey, R. (1995). The effects of exogenous gonadotropins on oocyte and embryo quality in cattle. Theriogenology 43, 41–50.CrossRefGoogle Scholar
Hasler, J.F., McCauley, A.D., Lathrop, W.F. & Foote, R.H. (1987). Effect of donor-embryo-recipient interactions on pregnancy rate in a large-scale bovine embryo transfer program. Theriogenology 27, 139–68.CrossRefGoogle Scholar
Huffman, S.R., Pak, Y. & Rivera, R.M. (2015). Superovulation induces alterations in the epigenome of zygotes, and results in differences in gene expression at the blastocyst stage in mice. Mol. Reprod. Dev. 82, 207–17.CrossRefGoogle ScholarPubMed
Hunter, R.H. (1968). Effect of progesterone on fertilization in the golden hamster. J. Reprod. Fertil. 16, 499–502.CrossRefGoogle ScholarPubMed
Hyttel, P., Callesen, H., & Greve, T. (1986). Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J. Reprod. Fertil. 76, 645–56.CrossRefGoogle ScholarPubMed
Igosheva, N., Abramov, A.Y., Poston, L., Eckert, J.J., Fleming, T.P., Duchen, M.R. & McConnell, J. (2010). Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 5, e10074.CrossRefGoogle ScholarPubMed
Janštová, Ž., Burkuš, J., Kubandová, J., Fabian, D., Koppel, J. & Čikoš, Š., 2017. The effect of maternal stress on blastocyst quality depends on maternal physiological status. Gen. Physiol. Biophys. 36, 53–63.CrossRefGoogle ScholarPubMed
Jungheim, E.S., Schoeller, E.L., Marquard, K.L., Louden, E.D., Schaffer, J.E. & Moley, K.H. (2010). Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 151, 4039–46.CrossRefGoogle ScholarPubMed
Kubandová, J., Čikoš, S., Burkuš, J., Czikková, S., Koppel, J. & Fabian, D. (2014). Amount of maternal body fat significantly affected the quality of isolated mouse preimplantation embryos and slowed down their development. Theriogenology 81, 187–95.CrossRefGoogle ScholarPubMed
Lashen, H., Ledger, W., Bernal, A.L. & Barlow, D. (1999). Extremes of body mass do not adversely affect the outcome of superovulation and in-vitro fertilization. Hum. Reprod. 14, 712–5.CrossRefGoogle Scholar
Lopes da Costa, L., Silva, J.C. & Silva, J.R. (2001). Treatment with different gonadotrophins in native cattle. Theriogenology 56, 65–77.CrossRefGoogle ScholarPubMed
Martinuzzi, K., Ryan, S., Luna, M. & Copperman, A.B. (2008). Elevated body mass index (BMI) does not adversely affect in vitro fertilization outcome in young women. J. Assist. Reprod. Genet. 25, 169–75.CrossRefGoogle Scholar
Merton, J.S., de Roos, A.P.W., Mullaart, E., de Ruigh, L., Kaal, L., Vos, P.L.A.M. & Dieleman, S.J. (2003). Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry. Theriogenology 59, 651–74.CrossRefGoogle ScholarPubMed
Minge, C.E., Bennett, B.D., Norman, R.J. & Robker, R.L. (2008). Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality. Endocrinology 149, 2646–56.CrossRefGoogle ScholarPubMed
Purcell, S.H. & Moley, K.H. (2011). The effect of obesity on egg quality. J. Assist. Reprod. Genet. 28, 517–24.CrossRefGoogle ScholarPubMed
Sirotkin, A.V., Fabian, D., Babeľová-Kubandová, J., Vlčková, R., Alwasel, S. & Abdel, H.H. (2017). Body fat affects mouse reproduction, ovarian hormone release, and response to FSH. Reproductive Biology. In press, available online December 2017.Google Scholar
Tamer Erel, C. & Senturk, L.M. (2009). The effect of body mass index on assisted reproduction. Curr. Opin. Obstet. Gynecol. 21, 228–35.CrossRefGoogle ScholarPubMed
Tortoriello, D. V, McMinn, J. & Chua, S.C. (2004). Dietary-induced obesity and hypothalamic infertility in female DBA/2J mice. Endocrinology 145, 1238–47.CrossRefGoogle ScholarPubMed
Van der Auwera, I. & D'Hooghe, T. (2001). Superovulation of female mice delays embryonic and fetal development. Hum. Reprod. 16, 1237–43.CrossRefGoogle ScholarPubMed
Velazquez, M.A. (2011). The role of nutritional supplementation on the outcome of superovulation in cattle. Anim. Reprod. Sci. 126, 1–10.CrossRefGoogle ScholarPubMed
Velazquez, M.A., Zaraza, J., Oropeza, A., Webb, R. & Niemann, H. (2009). The role of IGF1 in the in vivo production of bovine embryos from superovulated donors. Reproduction 137, 161–80.CrossRefGoogle ScholarPubMed
Velazquez, M.A., Hadeler, K.-G., Herrmann, D., Kues, W.A., Ulbrich, S., Meyer, H.H.D., Remy, B., Beckers, J.-F., Sauerwein, H., Niemann, H. & Niemann, H. (2011). In vivo oocyte developmental competence is reduced in lean but not in obese superovulated dairy cows after intraovarian administration of IGF1. Reproduction 142, 41–52.CrossRefGoogle Scholar
Wakefield, S.L., Lane, M., Schulz, S.J., Hebart, M.L., Thompson, J.G. & Mitchell, M. (2008). Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am. J. Physiol. Endocrinol. Metab. 294, E425–34.CrossRefGoogle ScholarPubMed
Wang, Y., Ock, S.-A. & Chian, R.-C. (2006). Effect of gonadotrophin stimulation on mouse oocyte quality and subsequent embryonic development in vitro . Reprod. Biomed. Online 12, 304–14.CrossRefGoogle ScholarPubMed
Wang, L.Y., Wang, N., Le, F., Li, L., Lou, H.Y., Liu, X.Z., Zheng, Y.M., Qian, Y.Q., Chen, Y.L., Jiang, X.H., Huang, H.F. & Jin, F. (2015). Superovulation induced changes of lipid metabolism in ovaries and embryos and its probable mechanism. PLoS One 10, 1–14.Google ScholarPubMed
Wu, B.J., Xue, H.Y., Chen, L.P., Dai, Y. feng, Guo, J.T. & Li, X.H. (2013). Effect of PMSG/hCG superovulation on mouse embryonic development. J. Integr. Agric. 12, 1066–72.CrossRefGoogle Scholar