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

Oocyte IVM or vitrification significantly impairs DNA methylation patterns in blastocysts as analysed by single-cell whole-genome methylation sequencing

Ya-Han Zhao A * , Jing-Jing Wang A * , Pei-Pei Zhang A * , Hai-Sheng Hao A , Yun-Wei Pang A , Hao-Yu Wang A , Wei-Hua Du A , Shan-Jiang Zhao A , Wei-Min Ruan B , Hui-Ying Zou A , Tong Hao A , Hua-Bin Zhu A and Xue-Ming Zhao https://orcid.org/0000-0001-6110-2690 A C
+ Author Affiliations
- Author Affiliations

A Embryo Biotechnology and Reproduction Laboratory and the Centre of Domestic Animal Reproduction and Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, No. 2 Yuanmingyuan Western Road, Haidian District, Beijing 100193, PR China.

B International Joint Center for Biomedical Innovation, School of Life Sciences, Henan University, Ming Lun Street, Kaifeng, Henan, 475004, PR China.

C Corresponding author. Email: zhaoxueming@caas.cn

Reproduction, Fertility and Development 32(7) 676-689 https://doi.org/10.1071/RD19234
Submitted: 26 June 2019  Accepted: 14 November 2019   Published: 11 March 2020

Abstract

To explore the mechanisms leading to the poor quality of IVF blastocysts, the single-cell whole-genome methylation sequencing technique was used in this study to analyse the methylation patterns of bovine blastocysts derived from in vivo, fresh (IVF) or vitrified (V_IVF) oocytes. Genome methylation levels of blastocysts in the IVF and V_IVF groups were significantly lower than those of the in vivo group (P < 0.05). In all, 1149 differentially methylated regions (DMRs) were identified between the IVF and in vivo groups, 1578 DMRs were identified between the V_IVF and in vivo groups and 151 DMRs were identified between the V_IVF and IVF groups. For imprinted genes, methylation levels of insulin-like growth factor 2 receptor (IGF2R) and protein phosphatase 1 regulatory subunit 9A (PPP1R9A) were lower in the IVF and V_IVF groups than in the in vivo group, and the methylation level of paternally expressed 3 (PEG3) was lower in the V_IVF group than in the IVF and in vivo groups. Genes with DMRs between the IVF and in vivo and the V_IVF and IVF groups were primarily enriched in oocyte maturation pathways, whereas DMRs between the V_IVF and in vivo groups were enriched in fertilisation and vitrification-vulnerable pathways. The results of this study indicate that differences in the methylation of critical DMRs may contribute to the differences in quality between in vitro- and in vivo-derived embryos.

Graphical Abstract Image

Additional keywords: bovine, development, embryo, mechanism.


References

Akizawa, H., Nagatomo, H., Odagiri, H., Kohri, N., Yamauchi, N., Yanagawa, Y., Nagano, M., Takahashi, M., and Kawahara, M. (2016). Conserved roles of fibroblast growth factor receptor 2 signaling in the regulation of inner cell mass development in bovine blastocysts. Mol. Reprod. Dev. 83, 516–525.
Conserved roles of fibroblast growth factor receptor 2 signaling in the regulation of inner cell mass development in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 27060901PubMed |

Anchordoquy, J. M., Anchordoquy, J. P., Testa, J. A., Sirini, M. A., and Furnus, C. C. (2015). Influence of vascular endothelial growth factor and cysteamine on in vitro bovine oocyte maturation and subsequent embryo development. Cell Biol. Int. 39, 1090–1098.
Influence of vascular endothelial growth factor and cysteamine on in vitro bovine oocyte maturation and subsequent embryo development.Crossref | GoogleScholarGoogle Scholar | 25879691PubMed |

Andrade, G. M., da Silveira, J. C., Perrini, C., Del Collado, M., Gebremedhn, S., Tesfaye, D., Meirelles, F. V., and Perecin, F. (2017). The role of the PI3K–Akt signaling pathway in the developmental competence of bovine oocytes. PLoS One 12, e0185045.
The role of the PI3K–Akt signaling pathway in the developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 28922408PubMed |

Barrera, A. D., Garcia, E. V., Hamdi, M., Sanchez-Calabuig, M. J., Lopez-Cardona, A. P., Balvis, N. F., Rizos, D., and Gutierrez-Adan, A. (2017). Embryo culture in presence of oviductal fluid induces DNA methylation changes in bovine blastocysts. Reproduction 154, 1–12.
Embryo culture in presence of oviductal fluid induces DNA methylation changes in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 28408706PubMed |

Biswas, D., and Hyun, S. H. (2011). Supplementation with vascular endothelial growth factor during in vitro maturation of porcine cumulus oocyte complexes and subsequent developmental competence after in vitro fertilization. Theriogenology 76, 153–160.
Supplementation with vascular endothelial growth factor during in vitro maturation of porcine cumulus oocyte complexes and subsequent developmental competence after in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 21640250PubMed |

Bolger, A. M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.
Trimmomatic: a flexible trimmer for Illumina sequence data.Crossref | GoogleScholarGoogle Scholar | 24695404PubMed |

Brackett, B. G., and Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–274.
Capacitation of rabbit spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1122333PubMed |

Canovas, S., Ivanova, E., Romar, R., Garcia-Martinez, S., Soriano-Ubeda, C., Garcia-Vazquez, F. A., Saadeh, H., Andrews, S., and Kelsey, G. (2017). DNA methylation and gene expression changes derived from assisted reproductive technologies can be decreased by reproductive fluids. eLife 6, e23670.
DNA methylation and gene expression changes derived from assisted reproductive technologies can be decreased by reproductive fluids.Crossref | GoogleScholarGoogle Scholar | 28134613PubMed |

Cao, Z., Zhang, M., Xu, T., Chen, Z., Tong, X., Zhang, D., Wang, Y., Zhang, L., Gao, D., Luo, L., Khan, I. M., and Zhang, Y. (2019). Vitrification of murine mature metaphase II oocytes perturbs DNA methylation reprogramming during preimplantation embryo development. Cryobiology 87, 91–98.
Vitrification of murine mature metaphase II oocytes perturbs DNA methylation reprogramming during preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar | 30707961PubMed |

Castilho, A. C., Nogueira, M. F., Fontes, P. K., Machado, M. F., Satrapa, R. A., Razza, E. M., and Barros, C. M. (2014). Ovarian superstimulation using FSH combined with equine chorionic gonadotropin (eCG) upregulates mRNA-encoding proteins involved with LH receptor intracellular signaling in granulosa cells from Nelore cows. Theriogenology 82, 1199–1205.
Ovarian superstimulation using FSH combined with equine chorionic gonadotropin (eCG) upregulates mRNA-encoding proteins involved with LH receptor intracellular signaling in granulosa cells from Nelore cows.Crossref | GoogleScholarGoogle Scholar | 25219847PubMed |

Cheeseman, L. P., Boulanger, J., Bond, L. M., and Schuh, M. (2016). Two pathways regulate cortical granule translocation to prevent polyspermy in mouse oocytes. Nat. Commun. 7, 13726.
Two pathways regulate cortical granule translocation to prevent polyspermy in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 27991490PubMed |

Chen, Z., Hagen, D. E., Elsik, C. G., Ji, T., Morris, C. J., Moon, L. E., and Rivera, R. M. (2015). Characterization of global loss of imprinting in fetal overgrowth syndrome induced by assisted reproduction. Proc. Natl Acad. Sci. USA 112, 4618–4623.
Characterization of global loss of imprinting in fetal overgrowth syndrome induced by assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 25825726PubMed |

Chen, X., Huang, Y., Huang, H., Guan, Y., Li, M., Jiang, X., Yu, M., and Yang, X. (2018). Effects of superovulation, in vitro fertilization, and oocyte in vitro maturation on imprinted gene Grb10 in mouse blastocysts. Arch. Gynecol. Obstet. 298, 1219–1227.
Effects of superovulation, in vitro fertilization, and oocyte in vitro maturation on imprinted gene Grb10 in mouse blastocysts.Crossref | GoogleScholarGoogle Scholar | 30251157PubMed |

Cheng, K. R., Fu, X. W., Zhang, R. N., Jia, G. X., Hou, Y. P., and Zhu, S. E. (2014). Effect of oocyte vitrification on deoxyribonucleic acid methylation of H19, Peg3, and Snrpn differentially methylated regions in mouse blastocysts. Fertil. Steril. 102, 1183–1190.e3.
Effect of oocyte vitrification on deoxyribonucleic acid methylation of H19, Peg3, and Snrpn differentially methylated regions in mouse blastocysts.Crossref | GoogleScholarGoogle Scholar | 25064401PubMed |

DeBaun, M. R., Niemitz, E. L., and Feinberg, A. P. (2003). Association of in vitro fertilization with Beckwith–Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am. J. Hum. Genet. 72, 156–160.
Association of in vitro fertilization with Beckwith–Wiedemann syndrome and epigenetic alterations of LIT1 and H19.Crossref | GoogleScholarGoogle Scholar | 12439823PubMed |

Deshmukh, R. S., Ostrup, O., Ostrup, E., Vejlsted, M., Niemann, H., Lucas-Hahn, A., Petersen, B., Li, J., Callesen, H., and Hyttel, P. (2011). DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer. Epigenetics 6, 177–187.
DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 20935454PubMed |

Doherty, A. S., Mann, M. R., Tremblay, K. D., Bartolomei, M. S., and Schultz, R. M. (2000). Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62, 1526–1535.
Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 10819752PubMed |

Driver, A. M., Penagaricano, F., Huang, W., Ahmad, K. R., Hackbart, K. S., Wiltbank, M. C., and Khatib, H. (2012). RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo- and in vitro-derived bovine blastocysts. BMC Genomics 13, 118.
RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo- and in vitro-derived bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 22452724PubMed |

Ealy, A. D., Wooldridge, L. K., and McCoski, S. R. (2019). Post-transfer consequences of in vitro-produced embryos in cattle. J. Anim. Sci. 97, 2555–2568.
Post-transfer consequences of in vitro-produced embryos in cattle.Crossref | GoogleScholarGoogle Scholar | 30968113PubMed |

Fan, H. Y., and Sun, Q. Y. (2004). Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol. Reprod. 70, 535–547.
Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals.Crossref | GoogleScholarGoogle Scholar | 14613897PubMed |

Fang, Z., and Luna, E. J. (2013). Supervillin-mediated suppression of p53 protein enhances cell survival. J. Biol. Chem. 288, 7918–7929.
Supervillin-mediated suppression of p53 protein enhances cell survival.Crossref | GoogleScholarGoogle Scholar | 23382381PubMed |

Fong, K. W., Au, F. K. C., Jia, Y., Yang, S., Zhou, L., and Qi, R. Z. (2017). Microtubule plus-end tracking of end-binding protein 1 (EB1) is regulated by CDK5 regulatory subunit-associated protein 2. J. Biol. Chem. 292, 7675–7687.
Microtubule plus-end tracking of end-binding protein 1 (EB1) is regulated by CDK5 regulatory subunit-associated protein 2.Crossref | GoogleScholarGoogle Scholar | 28320860PubMed |

Frey, W. D., Sharma, K., Cain, T. L., Nishimori, K., Teruyama, R., and Kim, J. (2018). Oxytocin receptor is regulated by Peg3. PLoS One 13, e0202476.
Oxytocin receptor is regulated by Peg3.Crossref | GoogleScholarGoogle Scholar | 30106994PubMed |

Goto, S., Naito, K., Ohashi, S., Sugiura, K., Naruoka, H., Iwamori, N., and Tojo, H. (2002). Effects of spindle removal on MPF and MAP kinase activities in porcine matured oocytes. Mol. Reprod. Dev. 63, 388–393.
Effects of spindle removal on MPF and MAP kinase activities in porcine matured oocytes.Crossref | GoogleScholarGoogle Scholar | 12237955PubMed |

Gravina, S., Dong, X., Yu, B., and Vijg, J. (2016). Single-cell genome-wide bisulfite sequencing uncovers extensive heterogeneity in the mouse liver methylome. Genome Biol. 17, 150.
Single-cell genome-wide bisulfite sequencing uncovers extensive heterogeneity in the mouse liver methylome.Crossref | GoogleScholarGoogle Scholar | 27380908PubMed |

Hannan, N. J., Paiva, P., Meehan, K. L., Rombauts, L. J., Gardner, D. K., and Salamonsen, L. A. (2011). Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology 152, 4948–4956.
Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation.Crossref | GoogleScholarGoogle Scholar | 22028446PubMed |

Hao, Y., Zhang, Z., Han, D., Cao, Y., Zhou, P., Wei, Z., Lv, M., and Chen, D. (2017). Gene expression profiling of human blastocysts from in vivo and ‘rescue IVM’ with or without melatonin treatment. Mol. Med. Rep. 16, 1278–1288.
Gene expression profiling of human blastocysts from in vivo and ‘rescue IVM’ with or without melatonin treatment.Crossref | GoogleScholarGoogle Scholar | 28627630PubMed |

Harwood, B. N., Cross, S. K., Radford, E. E., Haac, B. E., and De Vries, W. N. (2008). Members of the WNT signaling pathways are widely expressed in mouse ovaries, oocytes, and cleavage stage embryos. Dev. Dyn. 237, 1099–1111.
Members of the WNT signaling pathways are widely expressed in mouse ovaries, oocytes, and cleavage stage embryos.Crossref | GoogleScholarGoogle Scholar | 18351675PubMed |

Hayakawa, H., Hirai, T., Takimoto, A., Ideta, A., and Aoyagi, Y. (2009). Superovulation and embryo transfer in Holstein cattle using sexed sperm. Theriogenology 71, 68–73.
Superovulation and embryo transfer in Holstein cattle using sexed sperm.Crossref | GoogleScholarGoogle Scholar | 18951623PubMed |

Heinzmann, J., Hansmann, T., Herrmann, D., Wrenzycki, C., Zechner, U., Haaf, T., and Niemann, H. (2011). Epigenetic profile of developmentally important genes in bovine oocytes. Mol. Reprod. Dev. 78, 188–201.
Epigenetic profile of developmentally important genes in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 21290475PubMed |

Hou, Y. P., Dai, Y. P., Zhu, S. E., Zhu, H. B., Wu, T. Y., Gong, G. C., Wang, H. P., Wang, L. L., Liu, Y., Li, R., Wan, R., and Li, N. (2005). Bovine oocytes vitrified by the open pulled straw method and used for somatic cell cloning supported development to term. Theriogenology 64, 1381–1391.
Bovine oocytes vitrified by the open pulled straw method and used for somatic cell cloning supported development to term.Crossref | GoogleScholarGoogle Scholar | 16139614PubMed |

Hsieh, M., Lee, D., Panigone, S., Horner, K., Chen, R., Theologis, A., Lee, D. C., Threadgill, D. W., and Conti, M. (2007). Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol. Cell. Biol. 27, 1914–1924.
Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation.Crossref | GoogleScholarGoogle Scholar | 17194751PubMed |

Iijima, K., Jiang, J. Y., Shimizu, T., Sasada, H., and Sato, E. (2005). Acceleration of follicular development by administration of vascular endothelial growth factor in cycling female rats. J. Reprod. Dev. 51, 161–168.
Acceleration of follicular development by administration of vascular endothelial growth factor in cycling female rats.Crossref | GoogleScholarGoogle Scholar | 15750308PubMed |

Iwasaki, S., Yoshiba, N., Ushijima, H., Watanabe, S., and Nakahara, T. (1990). Morphology and proportion of inner cell mass of bovine blastocysts fertilized in vitro and in vivo. J. Reprod. Fertil. 90, 279–284.
Morphology and proportion of inner cell mass of bovine blastocysts fertilized in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar | 2231548PubMed |

Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S., Tokimatsu, T., and Yamanishi, Y. (2007). KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36, D480–D484.
KEGG for linking genomes to life and the environment.Crossref | GoogleScholarGoogle Scholar | 18077471PubMed |

Karami, K., Zerehdaran, S., Javadmanesh, A., Shariati, M. M., and Fallahi, H. (2019). Characterization of bovine (Bos taurus) imprinted genes from genomic to amino acid attributes by data mining approaches. PLoS. One 14, .
Characterization of bovine (Bos taurus) imprinted genes from genomic to amino acid attributes by data mining approaches.Crossref | GoogleScholarGoogle Scholar | 31170205PubMed |

Kerjean, A., Couvert, P., Heams, T., Chalas, C., Poirier, K., Chelly, J., Jouannet, P., Paldi, A., and Poirot, C. (2003). In vitro follicular growth affects oocyte imprinting establishment in mice. Eur. J. Hum. Genet. 11, 493–496.
In vitro follicular growth affects oocyte imprinting establishment in mice.Crossref | GoogleScholarGoogle Scholar | 12825069PubMed |

Khosla, S., Dean, W., Reik, W., and Feil, R. (2001). Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Hum. Reprod. Update 7, 419–427.
Culture of preimplantation embryos and its long-term effects on gene expression and phenotype.Crossref | GoogleScholarGoogle Scholar | 11476355PubMed |

Kisielnicka, E., Minasaki, R., and Eckmann, C. R. (2018). MAPK signaling couples SCF-mediated degradation of translational regulators to oocyte meiotic progression. Proc. Natl Acad. Sci. USA 115, E2772–E2781.
MAPK signaling couples SCF-mediated degradation of translational regulators to oocyte meiotic progression.Crossref | GoogleScholarGoogle Scholar | 29496961PubMed |

Krueger, F., and Andrews, S. R. (2011). Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571–1572.
Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications.Crossref | GoogleScholarGoogle Scholar | 21493656PubMed |

Krüssel, J. S., Bielfeld, P., Polan, M. L., and Simon, C. (2003). Regulation of embryonic implantation. Eur. J. Obstet. Gynecol. Reprod. Biol. 110, S2–S9.
Regulation of embryonic implantation.Crossref | GoogleScholarGoogle Scholar | 12965085PubMed |

Kumar, M., Camlin, N. J., Holt, J. E., Teixeira, J. M., McLaughlin, E. A., and Tanwar, P. S. (2016). Germ cell specific overactivation of WNT/betacatenin signalling has no effect on folliculogenesis but causes fertility defects due to abnormal foetal development. Sci. Rep. 6, 27273.
Germ cell specific overactivation of WNT/betacatenin signalling has no effect on folliculogenesis but causes fertility defects due to abnormal foetal development.Crossref | GoogleScholarGoogle Scholar | 27265527PubMed |

Kyriakis, J. M., and Avruch, J. (2001). Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81, 807–869.
Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation.Crossref | GoogleScholarGoogle Scholar | 11274345PubMed |

Lee, H. S., Kim, K. H., Kim, E. Y., Lee, S. Y., Ko, J. J., and Lee, K. A. (2016). Obox4-silencing-activated STAT3 and MPF/MAPK signaling accelerate nuclear membrane breakdown in mouse oocytes. Reproduction 151, 369–378.
Obox4-silencing-activated STAT3 and MPF/MAPK signaling accelerate nuclear membrane breakdown in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 26762402PubMed |

Liang, C. G., Su, Y. Q., Fan, H. Y., Schatten, H., and Sun, Q. Y. (2007). Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol. Endocrinol. 21, 2037–2055.
Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 17536005PubMed |

Liang, Y., Fu, X. W., Li, J. J., Yuan, D. S., and Zhu, S. E. (2014). DNA methylation pattern in mouse oocytes and their in vitro fertilized early embryos: effect of oocyte vitrification. Zygote 22, 138–145.
DNA methylation pattern in mouse oocytes and their in vitro fertilized early embryos: effect of oocyte vitrification.Crossref | GoogleScholarGoogle Scholar | 23174120PubMed |

Lin, T., Lee, J. E., Kang, J. W., Shin, H. Y., Lee, J. B., and Jin, D. I. (2019). Endoplasmic reticulum (ER) stress and unfolded protein response (UPR) in mammalian oocyte maturation and preimplantation embryo development. Int. J. Mol. Sci. 20, 409.
Endoplasmic reticulum (ER) stress and unfolded protein response (UPR) in mammalian oocyte maturation and preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar |

Liu, W., Xin, Q., Wang, X., Wang, S., Wang, H., Zhang, W., Yang, Y., Zhang, Y., Zhang, Z., Wang, C., Xu, Y., Duan, E., and Xia, G. (2017). Estrogen receptors in granulosa cells govern meiotic resumption of pre-ovulatory oocytes in mammals. Cell Death Dis. 8, e2662.
Estrogen receptors in granulosa cells govern meiotic resumption of pre-ovulatory oocytes in mammals.Crossref | GoogleScholarGoogle Scholar | 29072682PubMed |

Liu, X. M., Yan, M. Q., Ji, S. Y., Sha, Q. Q., Huang, T., Zhao, H., Liu, H. B., Fan, H. Y., and Chen, Z. J. (2018). Loss of oocyte Rps26 in mice arrests oocyte growth and causes premature ovarian failure. Cell Death Dis. 9, 1144.
Loss of oocyte Rps26 in mice arrests oocyte growth and causes premature ovarian failure.Crossref | GoogleScholarGoogle Scholar | 30451825PubMed |

Liu, L., Yin, T. L., Chen, Y., Li, Y., Yin, L., Ding, J., Yang, J., and Feng, H. L. (2019). Follicular dynamics of glycerophospholipid and sphingolipid metabolisms in polycystic ovary syndrome patients. J. Steroid Biochem. Mol. Biol. 185, 142–149.
Follicular dynamics of glycerophospholipid and sphingolipid metabolisms in polycystic ovary syndrome patients.Crossref | GoogleScholarGoogle Scholar | 30121347PubMed |

Lowther, K. M., Weitzman, V. N., Maier, D., and Mehlmann, L. M. (2009). Maturation, fertilization, and the structure and function of the endoplasmic reticulum in cryopreserved mouse oocytes. Biol. Reprod. 81, 147–154.
Maturation, fertilization, and the structure and function of the endoplasmic reticulum in cryopreserved mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 19299317PubMed |

Lu, C., Zhang, Y., Zheng, X., Song, X., Yang, R., Yan, J., Feng, H., and Qiao, J. (2018). Current perspectives on in vitro maturation and its effects on oocyte genetic and epigenetic profiles. Sci. China Life Sci. 61, 633–643.
Current perspectives on in vitro maturation and its effects on oocyte genetic and epigenetic profiles.Crossref | GoogleScholarGoogle Scholar | 29569023PubMed |

Luo, H., Kimura, K., Aoki, M., and Hirako, M. (2002). Effect of vascular endothelial growth factor on maturation, fertilization and developmental competence of bovine oocytes. J. Vet. Med. Sci. 64, 803–806.
Effect of vascular endothelial growth factor on maturation, fertilization and developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 12399605PubMed |

Madan, P., Calder, M. D., and Watson, A. J. (2005). Mitogen-activated protein kinase (MAPK) blockade of bovine preimplantation embryogenesis requires inhibition of both p38 and extracellular signal-regulated kinase (ERK) pathways. Reproduction 130, 41–51.
Mitogen-activated protein kinase (MAPK) blockade of bovine preimplantation embryogenesis requires inhibition of both p38 and extracellular signal-regulated kinase (ERK) pathways.Crossref | GoogleScholarGoogle Scholar | 15985630PubMed |

Makker, A., Goel, M. M., and Mahdi, A. A. (2014). PI3K/PTEN/Akt and TSC/mTOR signaling pathways, ovarian dysfunction, and infertility: an update. J. Mol. Endocrinol. 53, R103–R118.
PI3K/PTEN/Akt and TSC/mTOR signaling pathways, ovarian dysfunction, and infertility: an update.Crossref | GoogleScholarGoogle Scholar | 25312969PubMed |

Mann, M. R., Chung, Y. G., Nolen, L. D., Verona, R. I., Latham, K. E., and Bartolomei, M. S. (2003). Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos. Biol. Reprod. 69, 902–914.
Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos.Crossref | GoogleScholarGoogle Scholar | 12748125PubMed |

Miao, Y. L., and Williams, C. J. (2012). Calcium signaling in mammalian egg activation and embryo development: the influence of subcellular localization. Mol. Reprod. Dev. 79, 742–756.
Calcium signaling in mammalian egg activation and embryo development: the influence of subcellular localization.Crossref | GoogleScholarGoogle Scholar | 22888043PubMed |

Miao, Y. L., Stein, P., Jefferson, W. N., Padilla-Banks, E., and Williams, C. J. (2012). Calcium influx-mediated signaling is required for complete mouse egg activation. Proc. Natl Acad. Sci. USA 109, 4169–4174.
Calcium influx-mediated signaling is required for complete mouse egg activation.Crossref | GoogleScholarGoogle Scholar | 22371584PubMed |

Movahed, E., Soleimani, M., Hosseini, S., Akbari Sene, A., and Salehi, M. (2019). Aberrant expression of miR-29a/29b and methylation level of mouse embryos after in vitro fertilization and vitrification at two-cell stage. J. Cell. Physiol. , .
Aberrant expression of miR-29a/29b and methylation level of mouse embryos after in vitro fertilization and vitrification at two-cell stage.Crossref | GoogleScholarGoogle Scholar | 30916357PubMed |

Nandi, S., Raghu, H., Ravindranatha, B., and Chauhan, M. (2002). Production of buffalo (Bubalus bubalis) embryos in vitro: premises and promises. Reprod. Domest. Anim. 37, 65–74.
Production of buffalo (Bubalus bubalis) embryos in vitro: premises and promises.Crossref | GoogleScholarGoogle Scholar | 11975742PubMed |

Natale, D. R., Paliga, A. J., Beier, F., D’Souza, S. J. A., and Watson, A. J. (2004). p38 MAPK signaling during murine preimplantation development. Dev Biol. 268, 76–88.
p38 MAPK signaling during murine preimplantation development.Crossref | GoogleScholarGoogle Scholar | 15031106PubMed |

Nichols, J., Silva, J., Roode, M., and Smith, A. (2009). Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 136, 3215–3222.
Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo.Crossref | GoogleScholarGoogle Scholar | 19710168PubMed |

Ortiz-Escribano, N., Szymanska, K. J., Bol, M., Vandenberghe, L., Decrock, E., Van Poucke, M., Peelman, L., Van den Abbeel, E., Van Soom, A., and Leybaert, L. (2017). Blocking connexin channels improves embryo development of vitrified bovine blastocysts. Biol. Reprod. 96, 288–301.
Blocking connexin channels improves embryo development of vitrified bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 28203704PubMed |

Paliga, A. J. M., Natale, D. R., and Watson, A. J. (2005). p38 mitogen-activated protein kinase (MAPK) first regulates filamentous actin at the 8–16-cell stage during preimplantation development. Biol. Cell 97, 629–640.
p38 mitogen-activated protein kinase (MAPK) first regulates filamentous actin at the 8–16-cell stage during preimplantation development.Crossref | GoogleScholarGoogle Scholar |

Perry, P. (2015). Statistics of embryo collection and transfer in domestic farm animals. Embryo Technol. Newsl. 35, 8–23.

Pikiou, O., Vasilaki, A., Leondaritis, G., Vamvakopoulos, N., and Messinis, I. E. (2015). Effects of metformin on fertilisation of bovine oocytes and early embryo development: possible involvement of AMPK3-mediated TSC2 activation. Zygote 23, 58–67.
Effects of metformin on fertilisation of bovine oocytes and early embryo development: possible involvement of AMPK3-mediated TSC2 activation.Crossref | GoogleScholarGoogle Scholar | 23870192PubMed |

Poole, D. H., Ocon-Grove, O. M., and Johnson, A. L. (2016). Anti-Mullerian hormone (AMH) receptor type II expression and AMH activity in bovine granulosa cells. Theriogenology 86, 1353–1360.
Anti-Mullerian hormone (AMH) receptor type II expression and AMH activity in bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 27268296PubMed |

Rancourt, R. C., Harris, H. R., and Michels, K. B. (2012). Methylation levels at imprinting control regions are not altered with ovulation induction or in vitro fertilization in a birth cohort. Hum. Reprod. 27, 2208–2216.
Methylation levels at imprinting control regions are not altered with ovulation induction or in vitro fertilization in a birth cohort.Crossref | GoogleScholarGoogle Scholar | 22587996PubMed |

Reik, W., Constancia, M., Fowden, A., Anderson, N., Dean, W., Ferguson-Smith, A., Tycko, B., and Sibley, C. (2003). Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J. Physiol. 547, 35–44.
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes.Crossref | GoogleScholarGoogle Scholar | 12562908PubMed |

Richani, D., and Gilchrist, R. B. (2018). The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum. Reprod. Update 24, 1–14.
The epidermal growth factor network: role in oocyte growth, maturation and developmental competence.Crossref | GoogleScholarGoogle Scholar | 29029246PubMed |

Rosenkrans, C. F., and First, N. L. (1994). Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro. J. Anim. Sci. 72, 434–437.
Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro.Crossref | GoogleScholarGoogle Scholar | 8157527PubMed |

Salilew-Wondim, D., Saeed-Zidane, M., Hoelker, M., Gebremedhn, S., Poirier, M., Pandey, H. O., Tholen, E., Neuhoff, C., Held, E., and Besenfelder, U. (2018). Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation. BMC Genomics 19, 424.
Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation.Crossref | GoogleScholarGoogle Scholar | 29859035PubMed |

Shi, M., Cheng, J., He, Y., Jiang, Z., Bodinga, B. M., Liu, B., Chen, H., and Li, Q. (2018). Effect of FH535 on in vitro maturation of porcine oocytes by inhibiting WNT signaling pathway. Anim. Sci. J. 89, 631–639.
Effect of FH535 on in vitro maturation of porcine oocytes by inhibiting WNT signaling pathway.Crossref | GoogleScholarGoogle Scholar | 29284185PubMed |

Sirard, M. A. (2017). The influence of in vitro fertilization and embryo culture on the embryo epigenetic constituents and the possible consequences in the bovine model. J. Dev. Orig. Health Dis. 8, 411–417.
The influence of in vitro fertilization and embryo culture on the embryo epigenetic constituents and the possible consequences in the bovine model.Crossref | GoogleScholarGoogle Scholar | 28260557PubMed |

Smallwood, S. A., Lee, H. J., Angermueller, C., Krueger, F., Saadeh, H., Peat, J., Andrews, S. R., Stegle, O., Reik, W., and Kelsey, G. (2014). Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat. Methods 11, 817–820.
Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity.Crossref | GoogleScholarGoogle Scholar | 25042786PubMed |

Snoeck, F., Szymanska, K. J., Sarrazin, S., Ortiz-Escribano, N., Leybaert, L., and Van Soom, A. (2018). Blocking connexin channels during vitrification of immature cat oocytes improves maturation capacity after warming. Theriogenology 122, 144–149.
Blocking connexin channels during vitrification of immature cat oocytes improves maturation capacity after warming.Crossref | GoogleScholarGoogle Scholar | 30268031PubMed |

Song, Z., Min, L., Pan, Q., Shi, Q., and Shen, W. (2009). Maternal imprinting during mouse oocyte growth in vivo and in vitro. Biochem. Biophys. Res. Commun. 387, 800–805.
Maternal imprinting during mouse oocyte growth in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 19646963PubMed |

Spate, L. D., Brown, A. N., Redel, B. K., Whitworth, K. M., Murphy, C. N., and Prather, R. S. (2014). Dickkopf-related protein 1 inhibits the WNT signaling pathway and improves pig oocyte maturation. PLoS One 9, e95114.
Dickkopf-related protein 1 inhibits the WNT signaling pathway and improves pig oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 24739947PubMed |

Spinaci, M., Vallorani, C., Bucci, D., Tamanini, C., Porcu, E., and Galeati, G. (2012). Vitrification of pig oocytes induces changes in histone H4 acetylation and histone H3 lysine 9 methylation (H3K9). Vet. Res. Commun. 36, 165–171.
Vitrification of pig oocytes induces changes in histone H4 acetylation and histone H3 lysine 9 methylation (H3K9).Crossref | GoogleScholarGoogle Scholar | 22706936PubMed |

Sugimoto, A., Miyazaki, A., Kawarabayashi, K., Shono, M., Akazawa, Y., Hasegawa, T., Ueda-Yamaguchi, K., Kitamura, T., Yoshizaki, K., Fukumoto, S., and Iwamoto, T. (2017). Piezo type mechanosensitive ion channel component 1 functions as a regulator of the cell fate determination of mesenchymal stem cells. Sci. Rep. 7, 17696.
Piezo type mechanosensitive ion channel component 1 functions as a regulator of the cell fate determination of mesenchymal stem cells.Crossref | GoogleScholarGoogle Scholar | 29255201PubMed |

Tachibana, M., Sugimoto, K., Nozaki, M., Ueda, J., Ohta, T., Ohki, M., Fukuda, M., Takeda, N., Niida, H., Kato, H., and Shinkai, Y. (2002). G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16, 1779–1791.
G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 12130538PubMed |

Tachibana, M., Ueda, J., Fukuda, M., Takeda, N., Ohta, T., Iwanari, H., Sakihama, T., Kodama, T., Hamakubo, T., and Shinkai, Y. (2005). Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3–K9. Genes Dev. 19, 815–826.
Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3–K9.Crossref | GoogleScholarGoogle Scholar | 15774718PubMed |

Tan, K., An, L., Miao, K., Ren, L., Hou, Z., Tao, L., Zhang, Z., Wang, X., Xia, W., Liu, J., Wang, Z., Xi, G., Gao, S., Sui, L., Zhu, D. S., Wang, S., Wu, Z., Bach, I., Chen, D. B., and Tian, J. (2016). Impaired imprinted X chromosome inactivation is responsible for the skewed sex ratio following in vitro fertilization. Proc. Natl. Acad. Sci. USA 113, 3197–3202.
Impaired imprinted X chromosome inactivation is responsible for the skewed sex ratio following in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 26951653PubMed |

Tian, X. C. (2014). Genomic imprinting in farm animals. Annu. Rev. Anim. Biosci. 2, 23.
Genomic imprinting in farm animals.Crossref | GoogleScholarGoogle Scholar | 25384133PubMed |

Tunster, S. J., Boque-Sastre, R., McNamara, G. I., Hunter, S. M., Creeth, H. D. J., and John, R. M. (2018). Peg3 deficiency results in sexually dimorphic losses and gains in the normal repertoire of placental hormones. Front. Cell. Dev.Biol. 6, 123.
Peg3 deficiency results in sexually dimorphic losses and gains in the normal repertoire of placental hormones.Crossref | GoogleScholarGoogle Scholar | 30320110PubMed |

Urrego, R., Bernal-Ulloa, S. M., Chavarria, N. A., Herrera-Puerta, E., Lucas-Hahn, A., Herrmann, D., Winkler, S., Pache, D., Niemann, H., and Rodriguez-Osorio, N. (2017). Satellite DNA methylation status and expression of selected genes in Bos indicus blastocysts produced in vivo and in vitro. Zygote 25, 131–140.
Satellite DNA methylation status and expression of selected genes in Bos indicus blastocysts produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 28137339PubMed |

van den Hurk, R., and Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–1751.
Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 15763114PubMed |

Vermeiden, J. P., and Bernardus, R. E. (2013). Are imprinting disorders more prevalent after human in vitro fertilization or intracytoplasmic sperm injection? Fertil. Steril. 99, 642–651.
Are imprinting disorders more prevalent after human in vitro fertilization or intracytoplasmic sperm injection?Crossref | GoogleScholarGoogle Scholar | 23714438PubMed |

Wang, Y., Wang, F., Sun, T., Trostinskaia, A., Wygle, D., Puscheck, E., and Rappolee, D. A. (2004). Entire mitogen activated protein kinase (MAPK) pathway is present in preimplantation mouse embryos. Dev. Dyn. 231, 72–87.
Entire mitogen activated protein kinase (MAPK) pathway is present in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 15305288PubMed |

Wang, H. H., Zhang, Y., Tang, F., Pan, M. H., Wan, X., Li, X. H., and Sun, S. C. (2019). Rab23/Kif17 regulate meiotic progression in oocytes by modulating tubulin acetylation and actin dynamics. Development 146, dev171280.
Rab23/Kif17 regulate meiotic progression in oocytes by modulating tubulin acetylation and actin dynamics.Crossref | GoogleScholarGoogle Scholar | 30696709PubMed |

Wright, K., Brown, L., Brown, G., Casson, P., and Brown, S. (2011). Microarray assessment of methylation in individual mouse blastocyst stage embryos shows that in vitro culture may have widespread genomic effects. Hum. Reprod. 26, 2576–2585.
Microarray assessment of methylation in individual mouse blastocyst stage embryos shows that in vitro culture may have widespread genomic effects.Crossref | GoogleScholarGoogle Scholar | 21685140PubMed |

Wu, H. M., Wang, H. S., Huang, H. Y., Soong, Y. K., MacCalman, C. D., and Leung, P. C. (2009). GnRH signaling in intrauterine tissues. Reproduction 137, 769–777.
GnRH signaling in intrauterine tissues.Crossref | GoogleScholarGoogle Scholar | 19208750PubMed |

Wu, X., Zhang, Y., Xu, S., Chang, Y., Ye, Y., Guo, A., Kang, Y., Guo, H., Xu, H., Chen, L., Zhao, X., and Guan, G. (2019). Loss of Gsdf leads to a dysregulation of Igf2bp3-mediated oocyte development in medaka. Gen. Comp. Endocrinol. , .
Loss of Gsdf leads to a dysregulation of Igf2bp3-mediated oocyte development in medaka.Crossref | GoogleScholarGoogle Scholar | 31536721PubMed |

Yan, L. Y., Yan, J., Qiao, J., Zhao, P. L., and Liu, P. (2010). Effects of oocyte vitrification on histone modifications. Reprod. Fertil. Dev. 22, 920–925.
Effects of oocyte vitrification on histone modifications.Crossref | GoogleScholarGoogle Scholar | 20591326PubMed |

Yan, L., Luo, H., Gao, X., Liu, K., and Zhang, Y. (2012). Vascular endothelial growth factor-induced expression of its receptors and activation of the MAPK signaling pathway during ovine oocyte maturation in vitro. Theriogenology 78, 1350–1360.
Vascular endothelial growth factor-induced expression of its receptors and activation of the MAPK signaling pathway during ovine oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 22898011PubMed |

Ying, X., Liu, Y., Guo, Q., Qu, F., Guo, W., Zhu, Y., and Ding, Z. (2010). Endoplasmic reticulum protein 29 (ERp29), a protein related to sperm maturation is involved in sperm–oocyte fusion in mouse. Reprod. Biol. Endocrinol. 8, 10.
Endoplasmic reticulum protein 29 (ERp29), a protein related to sperm maturation is involved in sperm–oocyte fusion in mouse.Crossref | GoogleScholarGoogle Scholar | 20132541PubMed |

Young, L. E., Sinclair, K. D., and Wilmut, I. (1998). Large offspring syndrome in cattle and sheep. Rev. Reprod. 3, 155–163.
Large offspring syndrome in cattle and sheep.Crossref | GoogleScholarGoogle Scholar | 9829550PubMed |

Young, L. E., Fernandes, K., McEvoy, T. G., Butterwith, S. C., Gutierrez, C. G., Carolan, C., Broadbent, P. J., Robinson, J. J., Wilmut, I., and Sinclair, K. D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–154.
Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture.Crossref | GoogleScholarGoogle Scholar | 11175780PubMed |

Zhao, X., Hao, H., Du, W., and Zhu, H. (2015). Effect of vitrification on the microRNA transcriptome in mouse blastocysts. PLoS One 10, e0123451.
Effect of vitrification on the microRNA transcriptome in mouse blastocysts.Crossref | GoogleScholarGoogle Scholar | 26713754PubMed |

Zullo, G., De Canditiis, C., Pero, M. E., Albero, G., Salzano, A., Neglia, G., Campanile, G., and Gasparrini, B. (2016). Crocetin improves the quality of in vitro-produced bovine embryos: implications for blastocyst development, cryotolerance, and apoptosis. Theriogenology 86, 1879–1885.
Crocetin improves the quality of in vitro-produced bovine embryos: implications for blastocyst development, cryotolerance, and apoptosis.Crossref | GoogleScholarGoogle Scholar | 27393222PubMed |