Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

In vitro maturation affects chromosome segregation, spindle morphology and acetylation of lysine 16 on histone H4 in horse oocytes

Federica Franciosi A I , Ghylene Goudet B C D E , Irene Tessaro A , Pascal Papillier B C D E , Rozenn Dalbies-Tran B C D E , Fabrice Reigner F , Stefan Deleuze G , Cecile Douet B C D E , Ileana Miclea H , Valentina Lodde A and Alberto M. Luciano A
+ Author Affiliations
- Author Affiliations

A Reproductive and Developmental Biology Laboratory, Department of Health, Animal Science and Food Safety, University of Milan, via Celoria, 10, Milan, 20133, Italy.

B INRA, UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, F-37380, France.

C CNRS, UMR7247, Nouzilly, F-37380, France.

D Université François Rabelais, 60 Rue du Plat d’Étain, Tours, F-37000, France.

E IFCE, Nouzilly, F-37380, France.

F INRA, UEPAO, Nouzilly, F-37380, France.

G Université de Liège, Clinique des Animaux de Compagnie et des Équidés, Place du 20 Août 7, Liège, 4000, Belgium.

H University of Agricultural Sciences and Veterinary Medicine, Calea Mănătur 3-5, Cluj-Napoca 400372, Romania.

I Corresponding author. Email: federica.franciosi1@unimi.it

Reproduction, Fertility and Development 29(4) 721-730 https://doi.org/10.1071/RD15350
Submitted: 28 August 2015  Accepted: 12 November 2015   Published: 14 December 2015

Abstract

Implantation failure and genetic developmental disabilities in mammals are caused by errors in chromosome segregation originating mainly in the oocyte during meiosis I. Some conditions, like maternal ageing or in vitro maturation (IVM), increase the incidence of oocyte aneuploidy. Here oocytes from adult mares were used to investigate oocyte maturation in a monovulatory species. Experiments were conducted to compare: (1) the incidence of aneuploidy, (2) the morphology of the spindle, (3) the acetylation of lysine 16 on histone H4 (H4K16) and (4) the relative amount of histone acetyltransferase 1 (HAT1), K(lysine) acetyltransferase 8 (KAT8, also known as MYST1), histone deacetylase 1 (HDAC1) and NAD-dependent protein deacetylase sirtuin 1 (SIRT1) mRNA in metaphase II stage oocytes that were in vitro matured or collected from peri-ovulatory follicles. The frequency of aneuploidy and anomalies in spindle morphology was increased following IVM, along with a decrease in H4K16 acetylation that was in agreement with our previous observations. However, differences in the amount of the transcripts investigated were not detected. These results suggest that the degradation of transcripts encoding for histone deacetylases and acetyltransferases is not involved in the changes of H4K16 acetylation observed following IVM, while translational or post-translational mechanisms might have a role. Our study also suggests that epigenetic instabilities introduced by IVM may affect the oocyte and embryo genetic stability.

Additional keywords: aneuploidy, histone acetyl-transferases, histone deacetylases, meiosis.


References

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 | 1:CAS:528:DC%2BD28XkslOrs70%3D&md5=b77dfbf9abcd923fb4f5b9d0a8ae6b82CAS | 16651529PubMed |

Bartmann, A. K., Romao, G. S., Ramos Eda, S., and Ferriani, R. A. (2004). Why do older women have poor implantation rates? A possible role of the mitochondria. J. Assist. Reprod. Genet. 21, 79–83.
Why do older women have poor implantation rates? A possible role of the mitochondria.Crossref | GoogleScholarGoogle Scholar | 15202735PubMed |

Campos-Chillon, F., Farmerie, T. A., Bouma, G. J., Clay, C. M., and Carnevale, E. M. (2015). Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells. Reprod. Fertil. Dev. , .
Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells.Crossref | GoogleScholarGoogle Scholar | 25786490PubMed |

Carnevale, E. M. (2008). The mare model for follicular maturation and reproductive ageing in the woman. Theriogenology 69, 23–30.
The mare model for follicular maturation and reproductive ageing in the woman.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmu7nN&md5=b1d730b243c0636c9f9498a2aecbc1f0CAS | 17976712PubMed |

Chen, J., Melton, C., Suh, N., Oh, J. S., Horner, K., Xie, F., Sette, C., Blelloch, R., and Conti, M. (2011). Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev. 25, 755–766.
Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvFCrtbk%3D&md5=f93fe3bcaec1e3de3ec934bd2bfb2e0aCAS | 21460039PubMed |

Cheng, E. Y., Hunt, P. A., Naluai-Cecchini, T. A., Fligner, C. L., Fujimoto, V. Y., Pasternack, T. L., Schwartz, J. M., Steinauer, J. E., Woodruff, T. J., Cherry, S. M., Hansen, T. A., Vallente, R. U., Broman, K. W., and Hassold, T. J. (2009). Meiotic recombination in human oocytes. PLoS Genet. 5, e1000661.
Meiotic recombination in human oocytes.Crossref | GoogleScholarGoogle Scholar | 19763179PubMed |

Chiang, T., Duncan, F. E., Schindler, K., Schultz, R. M., and Lampson, M. A. (2010). Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr. Biol. 20, 1522–1528.
Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFGgsL7O&md5=1dae052aacd019cba2493b0628e16814CAS | 20817534PubMed |

Choi, Y. H., Hochi, S., Braun, J., Sato, K., and Oguri, N. (1993). In vitro maturation of equine oocytes collected by follicle aspiration and by the slicing of ovaries. Theriogenology 40, 959–966.
In vitro maturation of equine oocytes collected by follicle aspiration and by the slicing of ovaries.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVWgug%3D%3D&md5=a2ec492ce1f7a429bf23e70ec493fc75CAS | 16727378PubMed |

Clayton, A. L., Hazzalin, C. A., and Mahadevan, L. C. (2006). Enhanced histone acetylation and transcription: a dynamic perspective. Mol. Cell 23, 289–296.
Enhanced histone acetylation and transcription: a dynamic perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVWlurw%3D&md5=5e921c72b08dded04d7d9f61a96bc2bdCAS | 16885019PubMed |

Cox, L., Vanderwall, D. K., Parkinson, K. C., Sweat, A., and Isom, S. C. (2015). Expression profiles of select genes in cumulus–oocyte complexes from young and aged mares. Reprod. Fertil. Dev. , .
Expression profiles of select genes in cumulus–oocyte complexes from young and aged mares.Crossref | GoogleScholarGoogle Scholar | 25976356PubMed |

Donadeu, F. X., and Pedersen, H. G. (2008). Follicle development in mares. Reprod. Domest. Anim. 43, 224–231.
Follicle development in mares.Crossref | GoogleScholarGoogle Scholar | 18638128PubMed |

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=7de5f3bcadcf7c30c83d7a450f3584c8CAS | 19553597PubMed |

Eichenlaub-Ritter, U. (2012). Oocyte ageing and its cellular basis. Int. J. Dev. Biol. 56, 841–852.
Oocyte ageing and its cellular basis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvVyqsLs%3D&md5=950703bbfc5109771a2f0adc7c59c5f6CAS | 23417406PubMed |

Eichenlaub-Ritter, U., Vogt, E., Yin, H., and Gosden, R. (2004). Spindles, mitochondria and redox potential in ageing oocytes. Reprod. Biomed. Online 8, 45–58.
Spindles, mitochondria and redox potential in ageing oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1Ojsb0%3D&md5=f9462779f0def4474ea137805b1c04cdCAS | 14759287PubMed |

Emery, B. R., Wilcox, A. L., Aoki, V. W., Peterson, C. M., and Carrell, D. T. (2005). In vitro oocyte maturation and subsequent delayed fertilisation is associated with increased embryo aneuploidy. Fertil. Steril. 84, 1027–1029.
In vitro oocyte maturation and subsequent delayed fertilisation is associated with increased embryo aneuploidy.Crossref | GoogleScholarGoogle Scholar | 16213866PubMed |

Franciosi, F., Lodde, V., Goudet, G., Duchamp, G., Deleuze, S., Douet, C., Tessaro, I., and Luciano, A. M. (2012). Changes in histone H4 acetylation during in vivo versus in vitro maturation of equine oocytes. Mol. Hum. Reprod. 18, 243–252.
Changes in histone H4 acetylation during in vivo versus in vitro maturation of equine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xms1ynsrc%3D&md5=340df51d5b076b752bca97cf6ed8f2a2CAS | 22155671PubMed |

Ginther, O. J. (2012). The mare: a 1000-pound guinea pig for study of the ovulatory follicular wave in women. Theriogenology 77, 818–828.
The mare: a 1000-pound guinea pig for study of the ovulatory follicular wave in women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFOmtr0%3D&md5=70b0fd61b4e52fe96ad3b2cd47244b16CAS | 22115815PubMed |

Ginther, O. J., Gastal, E. L., Gastal, M. O., Bergfelt, D. R., Baerwald, A. R., and Pierson, R. A. (2004). Comparative study of the dynamics of follicular waves in mares and women. Biol. Reprod. 71, 1195–1201.
Comparative study of the dynamics of follicular waves in mares and women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqtLo%3D&md5=1cea972231e85796c187aa4e767ad3a9CAS | 15189824PubMed |

Goudet, G., Bezard, J., Duchamp, G., Gerard, N., and Palmer, E. (1997). Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment. Biol. Reprod. 57, 232–245.
Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslWit7o%3D&md5=4c998c9687bdcab6c44f6f8b07f56b1bCAS | 9241036PubMed |

Hassold, T., and Hunt, P. (2001). To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280–291.
To err (meiotically) is human: the genesis of human aneuploidy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisVCqurY%3D&md5=4cf61a1fb0dd5369fde81e47e793636bCAS | 11283700PubMed |

Hendriks, W. K., Colleoni, S., Galli, C., Paris, D. B., Colenbrander, B., Roelen, B. A., and Stout, T. A. (2015). Maternal age and in vitro culture affect mitochondrial number and function in equine oocytes and embryos. Reprod. Fertil. Dev. , .
Maternal age and in vitro culture affect mitochondrial number and function in equine oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 25881326PubMed |

Hinrichs, K., Schmidt, A. L., Friedman, P. P., Selgrath, J. P., and Martin, M. G. (1993). In vitro maturation of horse oocytes: characterisation of chromatin configuration using fluorescence microscopy. Biol. Reprod. 48, 363–370.
In vitro maturation of horse oocytes: characterisation of chromatin configuration using fluorescence microscopy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s7ns12jtw%3D%3D&md5=54c4401fb1ebec69d06446de4e8f091dCAS | 8439626PubMed |

Homer, H. A., McDougall, A., Levasseur, M., Yallop, K., Murdoch, A. P., and Herbert, M. (2005). Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev. 19, 202–207.
Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXotlSltg%3D%3D&md5=14e903db75e06bf70d8a7245f4a3249fCAS | 15655110PubMed |

Huang, J., Li, T., Ding, C. H., Brosens, J., Zhou, C. Q., Wang, H. H., and Xu, Y. W. (2012). Insufficient histone-3 lysine-9 deacetylation in human oocytes matured in vitro is associated with aberrant meiosis. Fertil. Steril. 97, 178–184e3.
Insufficient histone-3 lysine-9 deacetylation in human oocytes matured in vitro is associated with aberrant meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht12qsw%3D%3D&md5=c0641954b2a535f1cf3bd3004c6f9eedCAS | 22100169PubMed |

Jones, K. T., and Lane, S. I. (2013). Molecular causes of aneuploidy in mammalian eggs. Development 140, 3719–3730.
Molecular causes of aneuploidy in mammalian eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1CktL7K&md5=45a269b027800d700f39dffb679a338eCAS | 23981655PubMed |

Klinker, H., Mueller-Planitz, F., Yang, R., Forne, I., Liu, C. F., Nordenskiold, L., and Becker, P. B. (2014). ISWI remodelling of physiological chromatin fibres acetylated at lysine 16 of histone H4. PLoS One 9, e88411.
ISWI remodelling of physiological chromatin fibres acetylated at lysine 16 of histone H4.Crossref | GoogleScholarGoogle Scholar | 24516652PubMed |

Li, X. C., Bolcun-Filas, E., and Schimenti, J. C. (2011). Genetic evidence that synaptonemal complex axial elements govern recombination pathway choice in mice. Genetics 189, 71–82.
Genetic evidence that synaptonemal complex axial elements govern recombination pathway choice in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlelsb%2FE&md5=4f78b794a747ff6ad775dc2fe685b4e0CAS | 21750255PubMed |

Lombardi, P. M., Cole, K. E., Dowling, D. P., and Christianson, D. W. (2011). Structure, mechanism and inhibition of histone deacetylases and related metalloenzymes. Curr. Opin. Struct. Biol. 21, 735–743.
Structure, mechanism and inhibition of histone deacetylases and related metalloenzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOhurrJ&md5=a04e8a86f3e61915453af0d19c2212d3CAS | 21872466PubMed |

Luciano, A. M., Goudet, G., Perazzoli, F., Lahuec, C., and Gerard, N. (2006). Glutathione content and glutathione peroxidase expression in in vivo- and in vitro-matured equine oocytes. Mol. Reprod. Dev. 73, 658–666.
Glutathione content and glutathione peroxidase expression in in vivo- and in vitro-matured equine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1Kitb4%3D&md5=1b55fb205b82b911bf19dd12626f381aCAS | 16493673PubMed |

Luo, Y. B., Ma, J. Y., Zhang, Q. H., Lin, F., Wang, Z. W., Huang, L., Schatten, H., and Sun, Q. Y. (2013). MBTD1 is associated with Pr-Set7 to stabilise H4K20me1 in mouse oocyte meiotic maturation. Cell Cycle 12, 1142–1150.
MBTD1 is associated with Pr-Set7 to stabilise H4K20me1 in mouse oocyte meiotic maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsV2msrg%3D&md5=45e3a4f22951c4fb01955011b629af66CAS | 23475131PubMed |

Luzzo, K. M., Wang, Q., Purcell, S. H., Chi, M., Jimenez, P. T., Grindler, N., Schedl, T., and Moley, K. H. (2012). High-fat diet-induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS One 7, e49217.
High-fat diet-induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKjtrvN&md5=9bc77d7bb0f30a2e41cdb8f2da55d9a2CAS | 23152876PubMed |

Ma, P., and Schultz, R. M. (2008). Histone deacetylase 1 (HDAC1) regulates histone acetylation, development and gene expression in preimplantation mouse embryos. Dev. Biol. 319, 110–120.
Histone deacetylase 1 (HDAC1) regulates histone acetylation, development and gene expression in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1yjtrs%3D&md5=06dd589b247ecdcc9ec1e5e3b70f3befCAS | 18501342PubMed |

Ma, P., and Schultz, R. M. (2013). Histone deacetylase 2 (HDAC2) regulates chromosome segregation and kinetochore function via H4K16 deacetylation during oocyte maturation in mouse. PLoS Genet. 9, e1003377.
Histone deacetylase 2 (HDAC2) regulates chromosome segregation and kinetochore function via H4K16 deacetylation during oocyte maturation in mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvValtLw%3D&md5=27905fffb8c00ecc058cb454c592513aCAS | 23516383PubMed |

Ma, J., Flemr, M., Strnad, H., Svoboda, P., and Schultz, R. M. (2013). Maternally recruited DCP1A and DCP2 contribute to messenger RNA degradation during oocyte maturation and genome activation in mouse. Biol. Reprod. 88, 11.
Maternally recruited DCP1A and DCP2 contribute to messenger RNA degradation during oocyte maturation and genome activation in mouse.Crossref | GoogleScholarGoogle Scholar | 23136299PubMed |

Marmorstein, R., and Zhou, M. M. (2014). Writers and readers of histone acetylation: structure, mechanism and inhibition. Cold Spring Harb. Perspect. Biol. 6, a018762.
Writers and readers of histone acetylation: structure, mechanism and inhibition.Crossref | GoogleScholarGoogle Scholar | 24984779PubMed |

McGraw, S., Robert, C., Massicotte, L., and Sirard, M. A. (2003). Quantification of histone acetyltransferase and histone deacetylase transcripts during early bovine embryo development. Biol. Reprod. 68, 383–389.
Quantification of histone acetyltransferase and histone deacetylase transcripts during early bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVCjsg%3D%3D&md5=327e1f3f7113d046719fcebb363ac77fCAS | 12533400PubMed |

Nabti, I., Marangos, P., Bormann, J., Kudo, N. R., and Carroll, J. (2014). Dual-mode regulation of the APC/C by CDK1 and MAPK controls meiosis I progression and fidelity. J. Cell Biol. 204, 891–900.
Dual-mode regulation of the APC/C by CDK1 and MAPK controls meiosis I progression and fidelity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlt1emtrc%3D&md5=ed44883cc2c7ff2fa9d0de021db38c51CAS | 24637322PubMed |

Nichols, S. M., Gierbolini, L., Gonzalez-Martinez, J. A., and Bavister, B. D. (2010). Effects of in vitro maturation and age on oocyte quality in the rhesus macaque Macaca mulatta. Fertil. Steril. 93, 1591–1600.
Effects of in vitro maturation and age on oocyte quality in the rhesus macaque Macaca mulatta.Crossref | GoogleScholarGoogle Scholar | 19249021PubMed |

Nogueira, D., Staessen, C., Van de Velde, H., and Van Steirteghem, A. (2000). Nuclear status and cytogenetics of embryos derived from in vitro-matured oocytes. Fertil. Steril. 74, 295–298.
Nuclear status and cytogenetics of embryos derived from in vitro-matured oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvht1WjsQ%3D%3D&md5=d6abc1ffa6049186829e5638e735d98fCAS | 10927047PubMed |

Parthun, M. R. (2007). Hat1: the emerging cellular roles of a type B histone acetyltransferase. Oncogene 26, 5319–5328.
Hat1: the emerging cellular roles of a type B histone acetyltransferase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFeku74%3D&md5=cb0aad0a4cbfeb19be931cdc871bed17CAS | 17694075PubMed |

Peng, L., Ling, H., Yuan, Z., Fang, B., Bloom, G., Fukasawa, K., Koomen, J., Chen, J., Lane, W. S., and Seto, E. (2012). SIRT1 negatively regulates the activities, functions and protein levels of hMOF and TIP60. Mol. Cell. Biol. 32, 2823–2836.
SIRT1 negatively regulates the activities, functions and protein levels of hMOF and TIP60.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVeqsb3K&md5=6e95c7caabcccbc6cbdaaadab4499286CAS | 22586264PubMed |

Rambags, B. P., Krijtenburg, P. J., Drie, H. F., Lazzari, G., Galli, C., Pearson, P. L., Colenbrander, B., and Stout, T. A. (2005). Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro. Mol. Reprod. Dev. 72, 77–87.
Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntlClsL4%3D&md5=1bef0fdd69e6a6a4d68533a79897d616CAS | 15948165PubMed |

Rambags, B. P., van Boxtel, D. C., Tharasanit, T., Lenstra, J. A., Colenbrander, B., and Stout, T. A. (2014). Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro. Theriogenology 81, 959–965.
Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsF2gurc%3D&md5=ad6e368a68b30907f0750967a230eb4dCAS | 24576711PubMed |

Requena, A., Bronet, F., Guillen, A., Agudo, D., Bou, C., and Garcia-Velasco, J. A. (2009). The impact of in vitro maturation of oocytes on aneuploidy rate. Reprod. Biomed. Online 18, 777–783.
The impact of in vitro maturation of oocytes on aneuploidy rate.Crossref | GoogleScholarGoogle Scholar | 19490781PubMed |

Roberts, R., Iatropoulou, A., Ciantar, D., Stark, J., Becker, D. L., Franks, S., and Hardy, K. (2005). Follicle-stimulating hormone affects metaphase I chromosome alignment and increases aneuploidy in mouse oocytes matured in vitro. Biol. Reprod. 72, 107–118.
Follicle-stimulating hormone affects metaphase I chromosome alignment and increases aneuploidy in mouse oocytes matured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtlOj&md5=0a9771deb55bf32bd6ceca3bae872cd3CAS | 15371272PubMed |

Robin, P., Fritsch, L., Philipot, O., Svinarchuk, F., and Ait-Si-Ali, S. (2007). Post-translational modifications of histones H3 and H4 associated with the histone methyltransferases Suv39h1 and G9a. Genome Biol. 8, R270.
Post-translational modifications of histones H3 and H4 associated with the histone methyltransferases Suv39h1 and G9a.Crossref | GoogleScholarGoogle Scholar | 18096052PubMed |

Ruggeri, E., DeLuca, K. F., Galli, C., Lazzari, G., DeLuca, J. G., and Carnevale, E. M. (2015). Cytoskeletal alterations associated with donor age and culture interval for equine oocytes and potential zygotes that failed to cleave after intracytoplasmic sperm injection. Reprod. Fertil. Dev. , .
Cytoskeletal alterations associated with donor age and culture interval for equine oocytes and potential zygotes that failed to cleave after intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 25798646PubMed |

Sanfins, A., Lee, G. Y., Plancha, C. E., Overstrom, E. W., and Albertini, D. F. (2003). Distinctions in meiotic spindle structure and assembly during in vitro and in vivo maturation of mouse oocytes. Biol. Reprod. 69, 2059–2067.
Distinctions in meiotic spindle structure and assembly during in vitro and in vivo maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCnsbY%3D&md5=2976474c9697e6afb806c15ba4d42b24CAS | 12930715PubMed |

Shin, Y. H., Choi, Y., Erdin, S. U., Yatsenko, S. A., Kloc, M., Yang, F., Wang, P. J., Meistrich, M. L., and Rajkovic, A. (2010). Hormad1 mutation disrupts synaptonemal complex formation, recombination and chromosome segregation in mammalian meiosis. PLoS Genet. 6, e1001190.
Hormad1 mutation disrupts synaptonemal complex formation, recombination and chromosome segregation in mammalian meiosis.Crossref | GoogleScholarGoogle Scholar | 21079677PubMed |

Shogren-Knaak, M., Ishii, H., Sun, J. M., Pazin, M. J., Davie, J. R., and Peterson, C. L. (2006). Histone H4–K16 acetylation controls chromatin structure and protein interactions. Science 311, 844–847.
Histone H4–K16 acetylation controls chromatin structure and protein interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFylsLY%3D&md5=33b197522c631075471ea127b99fef69CAS | 16469925PubMed |

Shomper, M., Lappa, C., and FitzHarris, G. (2014). Kinetochore microtubule establishment is defective in oocytes from aged mice. Cell Cycle 13, 1171–1179.
Kinetochore microtubule establishment is defective in oocytes from aged mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFWgs7nF&md5=adf770823c0faa6837b57a87fe649420CAS | 24553117PubMed |

te Velde, E. R., and Pearson, P. L. (2002). The variability of female reproductive ageing. Hum. Reprod. Update 8, 141–154.
The variability of female reproductive ageing.Crossref | GoogleScholarGoogle Scholar | 12099629PubMed |

Tsutsumi, M., Fujiwara, R., Nishizawa, H., Ito, M., Kogo, H., Inagaki, H., Ohye, T., Kato, T., Fujii, T., and Kurahashi, H. (2014). Age-related decrease of meiotic cohesins in human oocytes. PLoS One 9, e96710.
Age-related decrease of meiotic cohesins in human oocytes.Crossref | GoogleScholarGoogle Scholar | 24806359PubMed |

Turner, B. M. (2014). Nucleosome signalling: an evolving concept. Biochim. Biophys. Acta 1839, 623–626.
Nucleosome signalling: an evolving concept.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsV2hsr8%3D&md5=80384ff6c00aff95462360bc6fbb8617CAS | 24412235PubMed |

Wang, N., Le, F., Zhan, Q. T., Li, L., Dong, M. Y., Ding, G. L., Xu, C. M., Jiang, S. W., Huang, H. F., and Jin, F. (2010). Effects of in vitro maturation on histone acetylation in metaphase II oocytes and early cleavage embryos. Obstet. Gynecol. Int. 2010, 989278.
Effects of in vitro maturation on histone acetylation in metaphase II oocytes and early cleavage embryos.Crossref | GoogleScholarGoogle Scholar | 20613962PubMed |

Yang, F., Baumann, C., Viveiros, M. M., and De La Fuente, R. (2012). Histone hyperacetylation during meiosis interferes with large-scale chromatin remodelling, axial chromatid condensation and sister chromatid separation in the mammalian oocyte. Int. J. Dev. Biol. 56, 889–899.
Histone hyperacetylation during meiosis interferes with large-scale chromatin remodelling, axial chromatid condensation and sister chromatid separation in the mammalian oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvVyqsb4%3D&md5=6ed237360596cff974d1f5f909d15d04CAS | 23417411PubMed |

Yun, Y., Holt, J. E., Lane, S. I., McLaughlin, E. A., Merriman, J. A., and Jones, K. T. (2014). Reduced ability to recover from spindle disruption and loss of kinetochore spindle assembly checkpoint proteins in oocytes from aged mice. Cell Cycle 13, 1938–1947.
Reduced ability to recover from spindle disruption and loss of kinetochore spindle assembly checkpoint proteins in oocytes from aged mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFantbnE&md5=c4c9a4a77904498bddb87094dc71e4a4CAS | 24758999PubMed |

Zentner, G. E., and Henikoff, S. (2014). Regulation of nucleosome dynamics by histone modifications. Nat. Struct. Mol. Biol. 20, 259–266.
Regulation of nucleosome dynamics by histone modifications.Crossref | GoogleScholarGoogle Scholar |