Effects of ovarian hyperstimulation on mitochondria in oocytes and early embryos
Jing Shu A B , Li-Li Xing B C , Guo-Lian Ding C D , Xin-Mei Liu C D , Qing-Feng Yan E and He-Feng Huang C D F
+ Author Affiliations
- Author Affiliations
A Wenzhou Medical University, Wenzhou 325035, PR China.
B Department of Reproductive Endocrinology, Zhejiang Provincial People’s Hospital, No. 158, Shangtang Road, Hangzhou 310014, PR China.
C The Key Laboratory of Reproductive Genetics, Ministry of Education, Hangzhou 310058, PR China.
D International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, 910# Hengshan Road, Xuhui Area, Shanghai, PR China.
E Institute of Genetics, College of Life Science, Zhejiang University, Hangzhou 310058, PR China.
F Corresponding author. Email: huanghefg@hotmail.com
Reproduction, Fertility and Development 28(8) 1214-1222 https://doi.org/10.1071/RD14300
Submitted: 15 August 2014 Accepted: 8 December 2014 Published: 9 February 2015
Journal Compilation © CSIRO Publishing 2016 Open Access CC BY-NC-ND
Abstract
A mouse model was used to compare the number and function of mitochondria in oocytes and embryos obtained by superovulation and in a natural cycle (control group). The superovulation group had a higher number of total oocytes, MII oocytes, embryos with two pronuclei, 2-cell embryos and blastocysts than the control group (P < 0.05 for all). The superovulation group had high proportion of MII oocytes with low number of mitochondrial (mt) DNA copies. The average number of mtDNA copies, ATP level and mitochondrial membrane potential (
Ψm) in MII oocytes in the superovulation were lower than in the control group (P < 0.05 for all). However, at the blastocyst stage, mean mtDNA copies, ATP level and Ψm did not differ significantly between the two groups. These results suggest that ovarian hyperstimulation does not cause damage to the mitochondria in eggs but, rather, more eggs with poor mitochondrial quality are recruited, resulting in a decline in average mitochondrial quality.
Additional keywords: mitochondrial DNA, mitochondrial membrane potential.
References
Chao, H. T., Lee, S. Y., Lee, H. M., Liao, T. L., Wei, Y. H., and Kao, S. H. (2005). Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries. Ann. N. Y. Acad. Sci. 1042, 148–156.| Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXot1Cqsbs%3D&md5=1f05c0080bab1c1c043400b3aaa726e4CAS | 15965057PubMed |
Dumollard, R., Marangos, P., Fitzharris, G., Swann, K., Duchen, M., and Carroll, J. (2004). Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131, 3057–3067.
| Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFKlsb0%3D&md5=36d1ff554931340655c1201a3b67abb8CAS | 15163630PubMed |
Dumollard, R., Duchen, M., and Carroll, J. (2007). The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 21–49.
| The role of mitochondrial function in the oocyte and embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gltb4%3D&md5=ef902ce04a34ede18ce030f99570900eCAS | 17222699PubMed |
Edwards, L. J., Kind, K. L., Armstrong, D. T., and Thompson, J. G. (2005). Effects of recombinant human follicle-stimulating hormone on embryo development in mice. Am. J. Physiol. Endocrinol. Metab. 288, E845–E851.
| Effects of recombinant human follicle-stimulating hormone on embryo development in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlSgurY%3D&md5=92878c32520fb4ca6e078de2ee2e4858CAS | 15598671PubMed |
Fish, J., Raule, N., and Attardi, G. (2004). Discovery of a major D-loop replication origin reveals two modes of human mtDNA synthesis. Science 306, 2098–2101.
| Discovery of a major D-loop replication origin reveals two modes of human mtDNA synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOjsLrO&md5=8a565034e18b6c6ac553ba24c6f2e429CAS | 15604407PubMed |
Ge, H. S., Zhang, F., Li, X. H., Chen, H., Xi, H. T., Huang, J. Y., Zhu, C. F., and Lu, J. Q. (2013). Effects of controlled ovarian hyperstimulation on mitochondria copy number and functions in murine oocytes Zhonghua Fu Chan Ke Za Zhi 48, 858–861.
| 24444565PubMed |
Gibson, T. C., Kubisch, H. M., and Brenner, C. A. (2005). Mitochondrial DNA deletions in rhesus macaque oocytes and embryos. Mol. Hum. Reprod. 11, 785–789.
| Mitochondrial DNA deletions in rhesus macaque oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFahtrg%3D&md5=b37f72072ea1725fb56964ff9bb94a89CAS | 16373367PubMed |
Gosden, R., and Lee, B. (2010). Portrait of an oocyte: our obscure origin. J. Clin. Invest. 120, 973–983.
| Portrait of an oocyte: our obscure origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVChsrY%3D&md5=df5d04b89c5169b739dfdfe6e3419770CAS | 20364095PubMed |
Jancar, N., Virant-Klun, I., Osredkar, J., and Vrtacnik Bokal, E. (2008). Apoptosis, reactive oxygen species and follicular anti-Mullerian hormone in natural versus stimulated cycles. Reprod. Biomed. Online 16, 640–648.
| Apoptosis, reactive oxygen species and follicular anti-Mullerian hormone in natural versus stimulated cycles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntVOks7g%3D&md5=8b46e8c95152bb9df9cc9b12890eb44fCAS | 18492367PubMed |
Kankofer, M., Wawrzykowski, J., and Giergiel, M. (2013). Sex- and age-dependent activity of glutathione peroxidase in reproductive organs in pre- and post-pubertal cattle in relation to total antioxidant capacity. Aging Clin. Exp. Res. 25, 365–370.
| Sex- and age-dependent activity of glutathione peroxidase in reproductive organs in pre- and post-pubertal cattle in relation to total antioxidant capacity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sjgsVCjsA%3D%3D&md5=c793edbce60ca6bdfa6fecc5b94694f9CAS | 23740597PubMed |
Katayama, M., Zhong, Z., Lai, L., Sutovsky, P., Prather, R. S., and Schatten, H. (2006). Mitochondrial distribution and microtubule organization in fertilized and cloned porcine embryos: implications for developmental potential. Dev. Biol. 299, 206–220.
| Mitochondrial distribution and microtubule organization in fertilized and cloned porcine embryos: implications for developmental potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVygsb7K&md5=5ac42363801a53278f6c4a52c31f8732CAS | 16945363PubMed |
Lee, S. T., Kim, T. M., Cho, M. Y., Moon, S. Y., Han, J. Y., and Lim, J. M. (2005). Development of a hamster superovulation program and adverse effects of gonadotropins on microfilament formation during oocyte development. Fertil. Steril. 83, 1264–1274.
| Development of a hamster superovulation program and adverse effects of gonadotropins on microfilament formation during oocyte development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktFaru7w%3D&md5=721acb28dde8b958baeb6459d91bc5c5CAS | 15831301PubMed |
Ma, S., Kalousek, D. K., Yuen, B. H., and Moon, Y. S. (1997). Investigation of effects of pregnant mare serum gonadotropin (PMSG) on the chromosomal complement of CD-1 mouse embryos. J. Assist. Reprod. Genet. 14, 162–169.
| Investigation of effects of pregnant mare serum gonadotropin (PMSG) on the chromosomal complement of CD-1 mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3ksF2hsg%3D%3D&md5=5b5fc0760451467b26b77300e700a98cCAS | 9090560PubMed |
McKiernan, S. H., and Bavister, B. D. (1998). Gonadotrophin stimulation of donor females decreases post-implantation viability of cultured one-cell hamster embryos. Hum. Reprod. 13, 724–729.
| Gonadotrophin stimulation of donor females decreases post-implantation viability of cultured one-cell hamster embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivF2itLo%3D&md5=17efd07b5cfcfd75398100614675fe5dCAS | 9572442PubMed |
Miyamoto, K., Sato, E. F., Kasahara, E., Jikumaru, M., Hiramoto, K., Tabata, H., Katsuragi, M., Odo, S., Utsumi, K., and Inoue, M. (2010). Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria. Free Radic. Biol. Med. 49, 674–681.
| Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXoslWrsbw%3D&md5=9b24c297dade0d797b5723abe54b966fCAS | 20621580PubMed |
Parsons, T. J., Muniec, D. S., Sullivan, K., Woodyatt, N., Alliston-Greiner, R., Wilson, M. R., Berry, D. L., Holland, K. A., Weedn, V. W., Gill, P., and Holland, M. M. (1997). A high observed substitution rate in the human mitochondrial DNA control region. Nat. Genet. 15, 363–368.
| A high observed substitution rate in the human mitochondrial DNA control region.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitF2hsbY%3D&md5=ee572ef6517965e8aab4a6edf4075ef2CAS | 9090380PubMed |
Santos, T. A., El Shourbagy, S., and St John, J. C. (2006). Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 85, 584–591.
| Mitochondrial content reflects oocyte variability and fertilization outcome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVChsr0%3D&md5=44608f7ae2e3ffae80f03b8cd2a33e56CAS | 16500323PubMed |
Seyedhassani, S. M., Houshmand, M., Kalantar, S. M., Modabber, G., and Aflatoonian, A. (2010). No mitochondrial DNA deletions but more D-loop point mutations in repeated pregnancy loss. J. Assist. Reprod. Genet. 27, 641–648.
| No mitochondrial DNA deletions but more D-loop point mutations in repeated pregnancy loss.Crossref | GoogleScholarGoogle Scholar | 20499271PubMed |
Shoubridge, E. A., and Wai, T. (2007). Mitochondrial DNA and the mammalian oocyte. Curr. Top. Dev. Biol. 77, 87–111.
| Mitochondrial DNA and the mammalian oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gltbo%3D&md5=121c7deb6e125bf1e015b31d783cab46CAS | 17222701PubMed |
Shu, J., Xing, L., Ding, G., Luo, Q., Liu, X., Yan, Q., Sheng, J., and Huang, H. (2013). The effect of peritoneal fluid from patients with endometriosis on mitochondrial function and development of early mouse embryos. PLoS ONE 8, e82334.
| The effect of peritoneal fluid from patients with endometriosis on mitochondrial function and development of early mouse embryos.Crossref | GoogleScholarGoogle Scholar | 24386092PubMed |
Sondheimer, N., Glatz, C. E., Tirone, J. E., Deardorff, M. A., Krieger, A. M., and Hakonarson, H. (2011). Neutral mitochondrial heteroplasmy and the influence of aging. Hum. Mol. Genet. 20, 1653–1659.
| Neutral mitochondrial heteroplasmy and the influence of aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVKrtbc%3D&md5=4e336dab15c88229fcbf95cadce00b95CAS | 21296868PubMed |
Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., Dominko, T., Simerly, C., and Schatten, G. (1999). Ubiquitin tag for sperm mitochondria. Nature 402, 371–372.
| Ubiquitin tag for sperm mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnvVyktrs%3D&md5=388b8a034bf2dc7881b87edaea5ac773CAS | 10586873PubMed |
Thundathil, J., Filion, F., and Smith, L. C. (2005). Molecular control of mitochondrial function in preimplantation mouse embryos. Mol. Reprod. Dev. 71, 405–413.
| Molecular control of mitochondrial function in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFSltLk%3D&md5=9a7b046ebc00c7c939ee51773ec88e58CAS | 15895466PubMed |
Van Blerkom, J. (2008). Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online 16, 553–569.
| Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells.Crossref | GoogleScholarGoogle Scholar | 18413065PubMed |
Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.
| Mitochondrial function in the human oocyte and embryo and their role in developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWrsrzM&md5=d8fce630c456055ad27de96490482f43CAS | 20933103PubMed |
Van Blerkom, J., and Davis, P. (2001). Differential effects of repeated ovarian stimulation on cytoplasmic and spindle organization in metaphase II mouse oocytes matured in vivo and in vitro. Hum. Reprod. 16, 757–764.
| Differential effects of repeated ovarian stimulation on cytoplasmic and spindle organization in metaphase II mouse oocytes matured in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7ptVWlsQ%3D%3D&md5=9718c54472827e6fe81f1f53fa825ac9CAS | 11278229PubMed |
Wai, T., Ao, A., Zhang, X., Cyr, D., Dufort, D., and Shoubridge, E. A. (2010). The role of mitochondrial DNA copy number in mammalian fertility. Biol. Reprod. 83, 52–62.
| The role of mitochondrial DNA copy number in mammalian fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWqtLo%3D&md5=46ce3598089e81edd1f349205c92f95eCAS | 20130269PubMed |
Zeng, H. T., Ren, Z., Yeung, W. S., Shu, Y. M., Xu, Y. W., Zhuang, G. L., and Liang, X. Y. (2007). Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum. Reprod. 22, 1681–1686.
| Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1ejtL0%3D&md5=121d3047e27534e0e7088da721068d16CAS | 17449512PubMed |
