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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Morphometric, subcellular, in vitro fertilisation and embryonic developmental assessment of mouse oocytes produced by anti-inhibin serum or pregnant mare serum gonadotrophin superovulation

Liga Wuri https://orcid.org/0000-0001-8820-139X A , Cansu Agca B and Yuksel Agca A B C
+ Author Affiliations
- Author Affiliations

A Division of Animal Sciences, University of Missouri, 920 East Campus Drive, Columbia, MO 65201, USA.

B College of Veterinary Medicine, University of Missouri, 1600 East Rollins Street, Columbia, MO 65211, USA.

C Corresponding author. Email: agcay@missouri.edu

Reproduction, Fertility and Development 32(5) 474-483 https://doi.org/10.1071/RD19131
Submitted: 7 April 2019  Accepted: 1 August 2019   Published: 24 January 2020

Abstract

This study compared the morphometric, subcellular characteristics, in vitro fertilisation (IVF) and embryonic developmental potential of metaphase II (MII) mouse oocytes obtained from females superovulated with either anti-inhibin serum–human chorionic gonadotrophin (AIS-hCG) or pregnant mare serum gonadotrophin (PMSG)-hCG. The oocyte’s quantity, quality, zona pellucida (ZP) thickness, perivitelline space (PVS), diameter, microtubules, F-actin, cortical granules (CGs) and mitochondrial distribution were determined. Superovulation using AIS-hCG resulted in a higher numbers of oocyte/donor compared with PMSG-hCG (P = 0.002). There was no difference in morphologically normal and abnormal oocytes between AIS-hCG and PMSG-hCG (P = 0.425 and P = 0.194, respectively). The morphometric measurements showed no difference in oocyte diameter between AIS-hCG and PMSG-hCG (P = 0.289). However, the thickness of the ZP of oocytes from AIS-hCG females was decreased compared with PMSG-hCG (P < 0.001). The PVS of oocytes from the AIS-hCG was larger than with PMSG-hCG (P < 0.001). The microtubules of oocytes from both AIS-hCG and PMSG-hCG were normal, although there was an increased fluorescence intensity in the AIS-hCG oocytes (P < 0.001). The F-actin and CGs distribution in oocytes from both AIS-hCG and PMSG-hCG were similar (P = 0.330 and P = 0.13, respectively). Although the oocytes from PMSG-hCG females had homogenously distributed mitochondria, AIS-hCG oocytes showed more peripheral distribution with no differences in fluorescence intensity (P = 0.137). The blastocyst development rates after IVF with fresh sperm showed no difference between AIS-hCG and PMSG-hCG (P = 0.235). These data suggested that AIS-hCG superovulation produces high numbers of morphologically normal oocytes that also possess normal subcellular structures, good morphological characteristics and had high in vitro embryonic developmental potential.

Graphical Abstract Image

Additional keywords: cortical granules, F-actin, microtubules, mitochondria, zona pellucida.


References

Agca, Y. (2012). Genome resource banking of biomedically important laboratory animals. Theriogenology 78, 1653–1665.
Genome resource banking of biomedically important laboratory animals.Crossref | GoogleScholarGoogle Scholar | 22981880PubMed |

Akiyama, T., Nagata, M., and Aoki, F. (2006). Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc. Natl Acad. Sci. USA 103, 7339–7344.
Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice.Crossref | GoogleScholarGoogle Scholar | 16651529PubMed |

Azoury, J., Verlhac, M. H., and Dumont, J. (2009). Actin filaments: key players in the control of asymmetric divisions in mouse oocytes. Biol. Cell 101, 69–76.
Actin filaments: key players in the control of asymmetric divisions in mouse oocytes.Crossref | GoogleScholarGoogle Scholar |

Behringer, R., Gertsenstein, M., Nagy, K. V., and Nagy, A. (2014). ‘Manipulating the Mouse Embryo: A Laboratory Manual.’ 4th edn. (Eds M. Gertsenstein and K. V. Nagy.) (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.)

Behringer, R., Gertsenstein, M., Nagy, K. V., and Nagy, A. (2018). Administration of gonadotropins for superovulation in mice. Cold Spring Harb Protoc 2018, .
Administration of gonadotropins for superovulation in mice.Crossref | GoogleScholarGoogle Scholar | 30510124PubMed |

Bertrand, E., Van Den Bergh, M., and Englert, Y. (1995). Fertilization and early embryology: does zona pellucida thickness influence the fertilization rate? Hum. Reprod. 10, 1189–1193.
Fertilization and early embryology: does zona pellucida thickness influence the fertilization rate?Crossref | GoogleScholarGoogle Scholar | 7657763PubMed |

Bond, D. J., and Chandley, A. C. (1983). Aneuploidy. In ‘Oxford Monographs on Medical Genetics No. 11’. (Oxford University Press: Oxford.)

Ci, Q., Li, M., Zhang, Y., Ma, S., Gao, Q., and Shi, Y. (2014). Confocal microscopic analysis of the microfilament configurations from human vitrification-thawed oocytes matured in vitro. Cryo Letters 35, 544–548.
| 25583016PubMed |

Cran, D. G., and Esper, C. R. (1990). Cortical granules and the cortical reaction in mammals. J. Reprod. Fertil. Suppl. 42, 177–188.
| 2077122PubMed |

Ghetler, Y., Skutelsky, E., Ben Nun, I., Ben Dor, L., Amihai, D., and Shalgi, R. (2006). Human oocyte cryopreservation and the fate of cortical granules. Fertil. Steril. 86, 210–216.
Human oocyte cryopreservation and the fate of cortical granules.Crossref | GoogleScholarGoogle Scholar | 16756978PubMed |

Gordon, A., Aguilar, R., Garrido-Gracia, J. C., Guil-Luna, S., Sanchez Cespedes, R., Millan, Y., and Sanchez-Criado, J. E. (2010). Immunoneutralization of inhibin in cycling rats increases follicle-stimulating hormone secretion, stimulates the ovary and attenuates progesterone receptor-dependent preovulatory luteinizing hormone secretion. Neuroendocrinology 91, 291–301.
Immunoneutralization of inhibin in cycling rats increases follicle-stimulating hormone secretion, stimulates the ovary and attenuates progesterone receptor-dependent preovulatory luteinizing hormone secretion.Crossref | GoogleScholarGoogle Scholar | 20453473PubMed |

Hasegawa, A., Mochida, K., Matoba, S., Yonezawa, K., Ohta, A., Watanabe, G., Taya, K., and Ogura, A. (2012). Efficient production of offspring from Japanese wild-derived strains of mice (Mus musculus molossinus) by improved assisted reproductive technologies. Biol. Reprod. 86, 167.
Efficient production of offspring from Japanese wild-derived strains of mice (Mus musculus molossinus) by improved assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar | 22337332PubMed |

Hasegawa, A., Mochida, K., Inoue, H., Noda, Y., Endo, T., Watanabe, G., and Ogura, A. (2016). High-yield superovulation in adult mice by anti-inhibin serum treatment combined with estrous cycle synchronization. Biol. Reprod. 94, 21.
High-yield superovulation in adult mice by anti-inhibin serum treatment combined with estrous cycle synchronization.Crossref | GoogleScholarGoogle Scholar | 26632610PubMed |

Ho, Y., Wigglesworth, K., Eppig, J. J., and Schultz, R. M. (1995). Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression. Mol. Reprod. Dev. 41, 232–238.
Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression.Crossref | GoogleScholarGoogle Scholar | 7654376PubMed |

Ishigame, H., Medan, M. S., Watanabe, G., Shi, Z., Kishi, H., Arai, K. Y., and Taya, K. (2004). A new alternative method for superovulation using passive immunization against inhibin in adult rats. Biol. Reprod. 71, 236–243.
A new alternative method for superovulation using passive immunization against inhibin in adult rats.Crossref | GoogleScholarGoogle Scholar | 15031144PubMed |

Kim, N. H., Day, B. N., Lee, H. T., and Chung, K. S. (1996). Microfilament assembly and cortical granule distribution during maturation, parthenogenetic activation and fertilisation in the porcine oocyte. Zygote 4, 145–149.
Microfilament assembly and cortical granule distribution during maturation, parthenogenetic activation and fertilisation in the porcine oocyte.Crossref | GoogleScholarGoogle Scholar | 8913028PubMed |

Kishi, H., Okada, T., Otsuka, M., Watanabe, G., Taya, K., and Sasamoto, S. (1996). Induction of superovulation by immunoneutralization of endogenous inhibin through the increase in the secretion of follicle-stimulating hormone in the cyclic golden hamster. J. Endocrinol. 151, 65–75.
Induction of superovulation by immunoneutralization of endogenous inhibin through the increase in the secretion of follicle-stimulating hormone in the cyclic golden hamster.Crossref | GoogleScholarGoogle Scholar | 8943770PubMed |

Lénárt, P., Bacher, C. P., Daigle, N., Hand, A. R., Eils, R., Terasaki, M., and Ellenberg, J. (2005). A contractile nuclear actin network drives chromosome congression in oocytes. Nature 436, 812–818.
A contractile nuclear actin network drives chromosome congression in oocytes.Crossref | GoogleScholarGoogle Scholar | 16015286PubMed |

Liu, M. (2011). The biology and dynamics of mammalian cortical granules. Reprod. Biol. Endocrinol. 9, 149.
The biology and dynamics of mammalian cortical granules.Crossref | GoogleScholarGoogle Scholar | 22088197PubMed |

Liu, X., Luo, C., Deng, K., Wu, Z., Wei, Y., Jiang, J., Lu, F., and Shi, D. (2018). Cytoplasmic volume of recipient oocytes affects the nucleus reprogramming and the developmental competence of HMC buffalo (Bubalus bubalis) embryos. J. Vet. Med. Sci. 80, 1291–1300.
Cytoplasmic volume of recipient oocytes affects the nucleus reprogramming and the developmental competence of HMC buffalo (Bubalus bubalis) embryos.Crossref | GoogleScholarGoogle Scholar | 29925699PubMed |

Marco-Jiménez, F., Naturil-Alfonso, C., Jiménez-Trigos, E., Lavara, R., and Vicente, J. S. (2012). Influence of zona pellucida thickness on fertilization, embryo implantation and birth. Anim. Reprod. Sci. 132, 96–100.
Influence of zona pellucida thickness on fertilization, embryo implantation and birth.Crossref | GoogleScholarGoogle Scholar | 22607772PubMed |

Medan, M. S., Watanabe, G., Sasaki, K., Nagura, Y., Sakaime, H., Fujita, M., Sharawy, S., and Taya, K. (2003). Effects of passive immunization of goats against inhibin on follicular development, hormone profile and ovulation rate. Reproduction 125, 751–757.
Effects of passive immunization of goats against inhibin on follicular development, hormone profile and ovulation rate.Crossref | GoogleScholarGoogle Scholar | 12713438PubMed |

Medan, M. S., Arai, K. Y., Watanabe, G., and Taya, K. (2007). Inhibin: regulation of reproductive function and practical use in females. Anim. Sci. J. 78, 16–27.
Inhibin: regulation of reproductive function and practical use in females.Crossref | GoogleScholarGoogle Scholar |

Moros-Nicolás, C., Chevret, P., Izquierdo-Rico, M. J., Holt, W. V., Esteban-Díaz, D., López-Béjar, M., Martínez-Nevado, E., Nilsson, M. A., Ballesta, J., and Avilés, M. (2017). Composition of marsupial zona pellucida: a molecular and phylogenetic approach. Reprod. Fertil. Dev. 30, 721–733.
Composition of marsupial zona pellucida: a molecular and phylogenetic approach.Crossref | GoogleScholarGoogle Scholar |

Murphy, J. V., and Craig, L. (1975). Leigh’s disease: significance of the biochemical changes in brain. J. Neurol. Neurosurg. Psychiatry 38, 1100–1103.
Leigh’s disease: significance of the biochemical changes in brain.Crossref | GoogleScholarGoogle Scholar | 1206418PubMed |

Murphy, R., Turnbull, D. M., Walker, M., and Hattersley, A. T. (2008). Clinical features, diagnosis and management of maternally inherited diabetes and deafness (MIDD) associated with the 3243A>G mitochondrial point mutation. Diabet. Med. 25, 383–399.
Clinical features, diagnosis and management of maternally inherited diabetes and deafness (MIDD) associated with the 3243A>G mitochondrial point mutation.Crossref | GoogleScholarGoogle Scholar | 18294221PubMed |

Muttukrishna, S. (2004). Role of inhibin in normal and high-risk pregnancy. Semin. Reprod. Med. 22, 227–234.
Role of inhibin in normal and high-risk pregnancy.Crossref | GoogleScholarGoogle Scholar | 15319825PubMed |

Nakagata, N. (2011). Cryopreservation of mouse spermatozoa and in vitro fertilization. Methods Mol. Biol. 693, 57–73.
Cryopreservation of mouse spermatozoa and in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 21080274PubMed |

Nambo, Y., Kaneko, H., Nagata, S., Oikawa, M., Yoshihara, T., Nagamine, N., Watanabe, G., and Taya, K. (1998). Effect of passive immunization against inhibin on FSH secretion, folliculogenesis and ovulation rate during the follicular phase of the estrous cycle in mares. Theriogenology 50, 545–557.
Effect of passive immunization against inhibin on FSH secretion, folliculogenesis and ovulation rate during the follicular phase of the estrous cycle in mares.Crossref | GoogleScholarGoogle Scholar | 10732146PubMed |

Reader, K. L., Stanton, J. A., and Juengel, J. (2017). The role of oocyte organelles in determining developmental competence. Biology (Basel) 6, 35.
The role of oocyte organelles in determining developmental competence.Crossref | GoogleScholarGoogle Scholar |

Schatten, H., Sun, Q.-Y., and Prather, R. (2014). The impact of mitochondrial function/dysfunction on IVF and new treatment possibilities for infertility. Reprod. Biol. Endocrinol. 12, 111.
The impact of mitochondrial function/dysfunction on IVF and new treatment possibilities for infertility.Crossref | GoogleScholarGoogle Scholar | 25421171PubMed |

Selesniemi, K., Lee, H. J., Muhlhauser, A., and Tilly, J. L. (2011). Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc. Natl Acad. Sci. USA 108, 12319–12324.
Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies.Crossref | GoogleScholarGoogle Scholar | 21730149PubMed |

Shi, F., Mochida, K., Suzuki, O., Matsuda, J., Ogura, A., Ozawa, M., Watanabe, G., Suzuki, A., and Taya, K. (2000). Ovarian localization of immunoglobulin g and inhibin alpha subunit in guinea pigs after passive immunization against the inhibin alpha subunit. J. Reprod. Dev. 46, 293–299.
Ovarian localization of immunoglobulin g and inhibin alpha subunit in guinea pigs after passive immunization against the inhibin alpha subunit.Crossref | GoogleScholarGoogle Scholar |

Stetson, I., Aviles, M., Moros, C., Garcia-Vazquez, F. A., Gimeno, L., Torrecillas, A., Aliaga, C., Bernardo-Pisa, M. V., Ballesta, J., and Izquierdo-Rico, M. J. (2015). Four glycoproteins are expressed in the cat zona pellucida. Theriogenology 83, 1162–1173.
Four glycoproteins are expressed in the cat zona pellucida.Crossref | GoogleScholarGoogle Scholar | 25623231PubMed |

Summers, M. C. (2013). A brief history of the development of the KSOM family of media. J. Assist. Reprod. Genet. 30, 995–999.
A brief history of the development of the KSOM family of media.Crossref | GoogleScholarGoogle Scholar | 24046024PubMed |

Takedomi, T., Kaneko, H., Aoyagi, Y., Konishi, M., Kishi, H., Watanabe, G., and Taya, K. (1997). Effects of passive immunization against inhibin on ovulation rate and embryo recovery in Holstein heifers. Theriogenology 47, 1507–1518.
Effects of passive immunization against inhibin on ovulation rate and embryo recovery in Holstein heifers.Crossref | GoogleScholarGoogle Scholar | 16728094PubMed |

Takeo, T., and Nakagata, N. (2011). Re duced glutathione enhances fertility of frozen/thawed C57BL/6 mouse sperm after exposure to methyl-beta-cyclodextrin. Biol. Reprod. 85, 1066–1072.
Re duced glutathione enhances fertility of frozen/thawed C57BL/6 mouse sperm after exposure to methyl-beta-cyclodextrin.Crossref | GoogleScholarGoogle Scholar | 21778138PubMed |

Takeo, T., and Nakagata, N. (2015). Superovulation using the combined administration of inhibin antiserum and equine chorionic gonadotropin increases the number of ovulated oocytes in C57BL/6 female mice. PLoS One 10, e0128330.
Superovulation using the combined administration of inhibin antiserum and equine chorionic gonadotropin increases the number of ovulated oocytes in C57BL/6 female mice.Crossref | GoogleScholarGoogle Scholar | 26024317PubMed |

Takeo, T., and Nakagata, N. (2016). Immunotherapy using inhibin antiserum enhanced the efficacy of equine chorionic gonadotropin on superovulation in major inbred and outbred mice strains. Theriogenology 86, 1341–1346.
Immunotherapy using inhibin antiserum enhanced the efficacy of equine chorionic gonadotropin on superovulation in major inbred and outbred mice strains.Crossref | GoogleScholarGoogle Scholar | 27242176PubMed |

Takeo, T., Hoshii, T., Kondo, Y., Toyodome, H., Arima, H., Yamamura, K., and Nakagata, N. (2008). Methyl-beta-cyclodextrin improves fertilizing ability of C57BL/6 mouse sperm after freezing and thawing by facilitating cholesterol efflux from the cells. Biol. Reprod. 78, 546–551.
Methyl-beta-cyclodextrin improves fertilizing ability of C57BL/6 mouse sperm after freezing and thawing by facilitating cholesterol efflux from the cells.Crossref | GoogleScholarGoogle Scholar | 18046011PubMed |

Ten, J., Mendiola, J., Vioque, J., de Juan, J., and Bernabeu, R. (2007). Donor oocyte dysmorphisms and their influence on fertilization and embryo quality. Reprod. Biomed. Online 14, 40–48.
Donor oocyte dysmorphisms and their influence on fertilization and embryo quality.Crossref | GoogleScholarGoogle Scholar | 17207330PubMed |

Thorburn, D. R., Rahman, J., and Rahman, S. (1993). Mitochondrial DNA-associated Leigh syndrome and NARP. In ‘GeneReviews®’. (Eds M. P. Adam, H. H. Ardinger, R. A. Pagon, S. E. Wallace, L. J. H. Bean, K. Stephens, and A. Amemiya.) pp. 1–48. (University of Washington: Seattle, WA.)

Tomari, H., Honjo, K., Kunitake, K., Aramaki, N., Kuhara, S., Hidaka, N., Nishimura, K., Nagata, Y., and Horiuchi, T. (2018). Meiotic spindle size is a strong indicator of human oocyte quality. Reprod. Med. Biol. 17, 268–274.
Meiotic spindle size is a strong indicator of human oocyte quality.Crossref | GoogleScholarGoogle Scholar | 30013428PubMed |

Vogt, E., Kirsch-Volders, M., Parry, J., and Eichenlaub-Ritter, U. (2008). Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error. Mutat. Res. 651, 14–29.
Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error.Crossref | GoogleScholarGoogle Scholar | 18096427PubMed |

Wang, H., Herath, C. B., Xia, G., Watanabe, G., and Taya, K. (2001). Superovulation, fertilization and in vitro embryo development in mice after administration of an inhibin-neutralizing antiserum. Reproduction 122, 809–816.
Superovulation, fertilization and in vitro embryo development in mice after administration of an inhibin-neutralizing antiserum.Crossref | GoogleScholarGoogle Scholar | 11690542PubMed |

Wessel, G. M., Brooks, J. M., Green, E., Haley, S., Voronina, E., Wong, J., Zaydfudim, V., and Conner, S. (2001). The biology of cortical granules. Int. Rev. Cytol. 209, 117–206.
The biology of cortical granules.Crossref | GoogleScholarGoogle Scholar | 11580200PubMed |