Dynamics of genomic 5‐hydroxymethylcytosine during mouse oocyte growth

Sakashita, Akihiko; Kobayashi, Hisato; Wakai, Toshifumi; Sotomaru, Yusuke; Hata, Kenichiro; Kono, Toru

doi:10.1111/gtc.12164

Cited by 16 publications

(14 citation statements)

References 33 publications

(71 reference statements)

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“…Analysis of gene expression during oocyte maturation showed no variation in mRNA abundance between GV and MII stages in oocytes derived from adult donors, in accordance with observations during meiotic progression of fully grown oocytes in mouse and pig (Lee et al 2014, Sakashita et al 2014. However, analysis of the transcripts in a model of differential developmental competence revealed an association between TET enzyme expression and oocyte quality.…”

Section: Discussionsupporting

confidence: 83%

“…Interestingly, the signal is not uniformly distributed throughout the chromatin, but seems to cluster in restricted areas (dot-like; Fig. 5) as described in growing oocytes in mouse (Yamaguchi et al 2013, Sakashita et al 2014.…”

Section: Discussionmentioning

confidence: 64%

“…Studies in mouse, bovine, rabbit and pig reported different and sometimes contradictory patterns of TET1, TET2 and TET3 expressions during oogenesis and early development. A consensus regards Tet3 very high expression in the oocyte and zygote in all species (Iqbal et al 2011, Wossidlo et al 2011, Lee et al 2014, Page-Lariviere & Sirard 2014, Sakashita et al 2014, Salvaing et al 2016, while data on Tet1 and Tet2 are inconsistent. Sakashita and coworkers (Sakashita et al 2014) reported a significant increase in Tet3 expression during mouse oocyte growth, but failed to report the expression of Tet1 or Tet2 in growing or GV oocytes.…”

Section: Discussionmentioning

confidence: 99%

“…A consensus regards Tet3 very high expression in the oocyte and zygote in all species (Iqbal et al 2011, Wossidlo et al 2011, Lee et al 2014, Page-Lariviere & Sirard 2014, Sakashita et al 2014, Salvaing et al 2016, while data on Tet1 and Tet2 are inconsistent. Sakashita and coworkers (Sakashita et al 2014) reported a significant increase in Tet3 expression during mouse oocyte growth, but failed to report the expression of Tet1 or Tet2 in growing or GV oocytes. Similarly, Iqbal and coworkers (Iqbal et al 2011) observed Tet3, but not Tet1 or Tet2, high expression in mouse oocytes and zygotes that was drastically down regulated at the two-cell stage; however, they detected Tet1 at low levels in the two-and four-cell stage embryo.…”

Section: Discussionmentioning

confidence: 99%

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Methylation dynamics during folliculogenesis and early embryo development in sheep

Masala¹,

Burrai²,

Bellu³

et al. 2017

Reproduction

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Genome-wide DNA methylation reprogramming occurs during mammalian gametogenesis and early embryogenesis. Post-fertilization demethylation of paternal and maternal genomes is considered to occur by an active and passive mechanism respectively, in most mammals but sheep; in this species no loss of methylation was observed in either pronucleus. Post-fertilization reprogramming relies on methylating and demethylating enzymes and co-factors that are stored during oocyte growth, concurrently with the re-methylation of the oocyte itself. The crucial remodelling of the oocyte epigenetic baggage often overlaps with potential interfering events such as exposure to assisted reproduction technologies or environmental changes. Here, we report a temporal analysis of methylation dynamics during folliculogenesis and early embryo development in sheep. We characterized global DNA methylation and hydroxymethylation by immunofluorescence and relatively quantified the expression of the enzymes and co-factors mainly responsible for their remodelling (DNA methyltransferases (DNMTs), ten-eleven translocation (TET) proteins and methyl-CpG-binding domain (MBD) proteins). Our results illustrate for the first time the patterns of hydroxymethylation during oocyte growth. We observed different patterns of methylation and hydroxymethylation between the two parental pronuclei, suggesting that male pronucleus undergoes active demethylation also in sheep. Finally, we describe gene-specific accumulation dynamics for methylating and demethylating enzymes during oocyte growth and observe patterns of expression associated with developmental competence in a differential model of oocyte potential. Our work contributes to the understanding of the methylation dynamics during folliculogenesis and early embryo development and improves the overall picture of early rearrangements that will originate the embryo epigenome.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 64%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Methylation dynamics during folliculogenesis and early embryo development in sheep

Masala¹,

Burrai²,

Bellu³

et al. 2017

Reproduction

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“…This expression profile may suggest that during maturation, a DNA demethylation process starts up in the oocyte genome. Sakashita et al () reported the presence of 5hmC in the oocyte genome during maturation. Taken together, these results suggest that TET enzymatic activity (from at least one of the isoforms) exists in oocytes.…”

Section: Discussionmentioning

confidence: 99%

The dynamics of gene expression, lipid composition and DNA methylation reprogramming are different during in vitro maturation of pig oocytes obtained from prepubertal gilts and cycling sows

Braga

Silva

Marques

et al. 2019

Reprod Domestic Animals

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This study aimed to characterize the gene expression, lipid composition and DNA methylation reprogramming during in vitro maturation (IVM) of pig oocytes with different developmental competencies. We used prepubertal gilts and cycling sows as a model to obtain oocytes with different levels of competency. We found that genes involved in lipid metabolism, SLC27A4, CPT2 and PLIN2, and DNA methylation, DNMT3A, TET1 and TET3, possessed altered transcript expression levels during IVM. Specifically, SLC27A4 mRNA (p = 0.05) increased in oocytes from cycling females, whereas CPT2 (p = 0.05), PLIN2 (p = 0.02) and DNMT3A (p = 0.02) increased in oocytes from prepubertal females during IVM. Additionally, TET3 mRNA increased during IVM in oocytes from prepubertal (p = 0.0005) and cycling females (p = 0.02).The TET1 transcript decreased (p = 0.05) during IVM in oocytes from cycling sows.Regarding lipid composition, mass spectrometry revealed a cluster of ions, with molecular masses higher than m/z 700, which comprises a group of complex phospholipids, was identified in all groups of oocytes, except in those from prepubertal gilts.With respect to DNA methylation reprogramming, it was noted that the less competent oocytes were not able to reprogramme the XIST gene during IVM. We conclude that the maternal mRNA store, lipid composition and epigenetic reprogramming are still being established during maturation and are related to oocyte competence. In addition, we propose that the methylation pattern of the XIST may be used as molecular marker for oocyte competence in pigs. K E Y W O R D S Epigenetics, gene expression, molecular markers, oocyte competence, pig How to cite this article: Braga TF, Silva TCF, Marques MG, et al. The dynamics of gene expression, lipid composition and DNA methylation reprogramming are different during in vitro maturation of pig oocytes obtained from prepubertal gilts and cycling sows.

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Similar kinetics for 5‐methylcytosine and 5‐hydroxymethylcytosine during human preimplantation development in vitro

Petrussa

Rycke

2016

Molecular Reproduction Devel

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After fertilization, the mammalian embryo undergoes epigenetic reprogramming with genome-wide DNA demethylation and subsequent remethylation. Oxidation of 5-methylcytosine (5mC) into 5-hydroxymethylcytosine (5hmC) was suggested to be an intermediate step in the DNA demethylation pathway. Other evidence, such as the stability of 5hmC in specific tissues, suggests that 5hmC constitutes a new epigenetic modification with its own biological function. Since few studies have been conducted on human material compared to animal models and species-specific epigenetic differences have been reported, we studied global DNA methylation and hydroxymethylation patterns in human in vitro preimplantation embryos using immunocytochemistry, comparing these patterns in good-quality and abnormally developing embryos. Our data showed that DNA methylation and hydroxymethylation modifications co-exist. 5mC and 5hmC signals were found in oocytes and in paternal and maternal pronuclei of zygotes, present in non-reciprocal patterns-which contrasts published data for the mouse. These two epigenetic modifications are present between Days 1 and 7 of in vitro development, with 5mC levels declining over cell divisions without noticeable remethylation during this period. A main decline in 5mC and 5hmC occurred as the embryo progressed from compaction to the blastocyst stage. No difference in (hydroxy)methylation was found between the inner cell mass and trophectoderm. When comparing normally and abnormally developing embryos, DNA (hydroxy)methylation reprogramming was abnormal in poor-quality embryos, especially during the first cleavages. Mol. Reprod. Dev. 83: 594-605, 2016 © 2016 Wiley Periodicals, Inc.

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Dynamics of genomic 5‐hydroxymethylcytosine during mouse oocyte growth

Cited by 16 publications

References 33 publications

Methylation dynamics during folliculogenesis and early embryo development in sheep

Methylation dynamics during folliculogenesis and early embryo development in sheep

The dynamics of gene expression, lipid composition and DNA methylation reprogramming are different during in vitro maturation of pig oocytes obtained from prepubertal gilts and cycling sows

Similar kinetics for 5‐methylcytosine and 5‐hydroxymethylcytosine during human preimplantation development in vitro

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