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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Increased frequency of chromosome congression defects and aneuploidy in mouse oocytes cultured at lower temperature

Jitka Danadova A , Natalie Matijescukova A , Anna Mac Gillavry Danylevska A and Martin Anger A B
+ Author Affiliations
- Author Affiliations

A Central European Institute of Technology, Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic.

B Corresponding author. Email: anger@vri.cz

Reproduction, Fertility and Development 29(5) 968-974 https://doi.org/10.1071/RD15306
Submitted: 29 July 2015  Accepted: 19 January 2016   Published: 9 March 2016

Abstract

Optimal culture conditions are essential for successful IVM of mammalian oocytes and for their further development into an embryo. In the present study we used live cell imaging microscopy to assess the effects of suboptimal culture temperature on various aspects of IVM, including duration of meiosis I, dynamics of polar body extrusion, chromosome congression, anaphase-promoting complex/cyclosome (APC/C) activation and aneuploidy. The data showed that even a small deviation from the optimal incubation temperature causes marked changes in the duration and synchronicity of meiosis, APC/C activity and the frequency of chromosome congression and segregation errors. In vitro manipulation and maturation of germ cells is widely used in both human and animal artificial reproduction techniques. Mammalian oocytes are naturally prone to chromosomal segregation errors, which are responsible for severe mental and developmental disorders. The data presented herein demonstrate that exposure of mouse oocytes to suboptimal temperature during manipulation and maturation could further increase the frequency of chromosome segregation defects in these cells.

Additional keywords: anaphase-promoting complex/cyclosome, chromosome misalignment, culture temperature, IVM.


References

Abeydeera, L. R., Wang, W. H., Prather, R. S., and Day, B. N. (2001). Effect of incubation temperature on in vitro maturation of porcine oocytes: nuclear maturation, fertilisation and developmental competence. Zygote 9, 331–337.
Effect of incubation temperature on in vitro maturation of porcine oocytes: nuclear maturation, fertilisation and developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2FktlGksw%3D%3D&md5=7c743165aea2e8aa9cf0a36671e7234aCAS | 11771900PubMed |

Barati, F., Agung, B., Wongsrikeao, P., Taniguchi, M., Nagai, T., and Otoi, T. (2008). Meiotic competence and DNA damage of porcine oocytes exposed to an elevated temperature. Theriogenology 69, 767–772.
Meiotic competence and DNA damage of porcine oocytes exposed to an elevated temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVWhsLg%3D&md5=9c80f7d9bc24d7f3c76a8d9476d8d08aCAS | 18242671PubMed |

Brinster, R. L. (1969). In vitro cultivation of mammalian ova. Adv. Biosci. 4, 199–233.
| 1:CAS:528:DyaE38Xotlyruw%3D%3D&md5=e67a2c5d49e979d3b0c001ad66c54a20CAS |

Danylevska, A., Kovacovicova, K., Awadova, T., and Anger, M. (2014). The frequency of precocious segregation of sister chromatids in mouse female meiosis I is affected by genetic background. Chromosome Res. 22, 365–373.
The frequency of precocious segregation of sister chromatids in mouse female meiosis I is affected by genetic background.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvVeht7o%3D&md5=280ddc99f9cbaff35d7d10f71906825eCAS | 24935618PubMed |

Duncan, F. E., Chiang, T., Schultz, R. M., and Lampson, M. A. (2009). Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol. Reprod. 81, 768–776.
Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFyhsLnE&md5=26aac7d4f718b1436ac77fe430f55a8dCAS | 19553597PubMed |

Edwards, R. G. (1965). Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208, 349–351.
Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF287lsVagsg%3D%3D&md5=fe7219ddd2cffc714612a5b90c64f533CAS | 4957259PubMed |

Eng, L. A., Kornegay, E. T., Huntington, J., and Wellman, T. (1986). Effects of incubation temperature and bicarbonate on maturation of pig oocytes in vitro. J. Reprod. Fertil. 76, 657–662.
Effects of incubation temperature and bicarbonate on maturation of pig oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL287pvFyrug%3D%3D&md5=a6f648748da255b5595859351788f704CAS | 3701704PubMed |

Foley, E. A., and Kapoor, T. M. (2013). Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol. 14, 25–37.
Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKgurjP&md5=45034d2cc8dd7157d47689f3028653b8CAS | 23258294PubMed |

Hong, K. H., Lee, H., Forman, E. J., Upham, K. M., and Scott, R. T. J. (2014). Examining the temperature of embryo culture in in vitro fertilization: a randomized controlled trial comparing traditional core temperature (37 degrees C) to a more physiologic, cooler temperature (36 degrees C). Fertil. Steril. 102, 767–773.
Examining the temperature of embryo culture in in vitro fertilization: a randomized controlled trial comparing traditional core temperature (37 degrees C) to a more physiologic, cooler temperature (36 degrees C).Crossref | GoogleScholarGoogle Scholar | 25044079PubMed |

McGuinness, B. E., Anger, M., Kouznetsova, A., Gil-Bernabe, A. M., Helmhart, W., Kudo, N. R., Wuensche, A., Taylor, S., Hoog, C., Novak, B., and Nasmyth, K. (2009). Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr. Biol. 19, 369–380.
Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVKit7o%3D&md5=8c93cec283d8441360296f076e7fe455CAS | 19249208PubMed |

Nagaoka, S. I., Hodges, C. A., Albertini, D. F., and Hunt, P. A. (2011). Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr. Biol. 21, 651–657.
Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFyjurs%3D&md5=929c91ea590a9bf14c992265d6cd3556CAS | 21497085PubMed |

Pesin, J. A., and Orr-Weaver, T. L. (2008). Regulation of APC/C activators in mitosis and meiosis. Annu. Rev. Cell Dev. Biol. 24, 475–499.
Regulation of APC/C activators in mitosis and meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlOgtbfO&md5=ca29d9ed699d3980a5b5b05f7ce7b561CAS | 18598214PubMed |

Pickering, S. J., and Johnson, M. H. (1987). The influence of cooling on the organization of the meiotic spindle of the mouse oocyte. Hum. Reprod. 2, 207–216.
| 1:STN:280:DyaL2s3ltFartg%3D%3D&md5=780eb8f1400e16e134f8d8e3eaf96c87CAS | 3597741PubMed |

Pincus, G., and Enzmann, E. V. (1935). The comparative behavior of mammalian eggs in vivo and in vitro: I. the activation of ovarian eggs. J. Exp. Med. 62, 665–675.
The comparative behavior of mammalian eggs in vivo and in vitro: I. the activation of ovarian eggs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3crjs1agtA%3D%3D&md5=32054261a149d243f8112768a2cd519fCAS | 19870440PubMed |

Sanchez-Alavez, M., Alboni, S., and Conti, B. (2011). Sex- and age-specific differences in core body temperature of C57Bl/6 mice. Age (Dordr.) 33, 89–99.
Sex- and age-specific differences in core body temperature of C57Bl/6 mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitlKltrY%3D&md5=8f4420e79cbf8a916a9ed41aca263a59CAS | 20635153PubMed |

Sebestova, J., Danylevska, A., Novakova, L., Kubelka, M., and Anger, M. (2012). Lack of response to unaligned chromosomes in mammalian female gametes. Cell Cycle 11, 3011–3018.
Lack of response to unaligned chromosomes in mammalian female gametes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWlt7nN&md5=e6ec64b2275aeab5fdf809a32a0a538fCAS | 22871737PubMed |

Tong, G. Q., Heng, B. C., Chen, N. Q., Yip, W. Y., and Ng, S. C. (2004). Effects of elevated temperature in vivo on the maturational and developmental competence of porcine germinal vesicle stage oocytes. J. Anim. Sci. 82, 3175–3180.
| 1:CAS:528:DC%2BD2cXovVyjtr0%3D&md5=5960686d1a61ca1c3d4776e2964bc156CAS | 15542463PubMed |

Wang, W. H., Meng, L., Hackett, R. J., Odenbourg, R., and Keefe, D. L. (2001). Limited recovery of meiotic spindles in living human oocytes after cooling–rewarming observed using polarized light microscopy. Hum. Reprod. 16, 2374–2378.
| 1:STN:280:DC%2BD3MnmvFeqsw%3D%3D&md5=2e97053fdd778f0a37dcb1e98e4ddff9CAS | 11679523PubMed |

Ye, J., Coleman, J., Hunter, M. G., Craigon, J., Campbell, K. H., and Luck, M. R. (2007). Physiological temperature variants and culture media modify meiotic progression and developmental potential of pig oocytes in vitro. Reproduction 133, 877–886.
Physiological temperature variants and culture media modify meiotic progression and developmental potential of pig oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlGnurc%3D&md5=2e5f4c04c143ee845fc6a6271c18f18fCAS | 17616718PubMed |