Size-Dependent Acquisition of Global DNA Methylation in Oocytes Is Altered by Hormonal Stimulation.

Almamun, Md; Rivera, Rocío Melissa

doi:10.1093/biolreprod/83.s1.312

Cited by 4 publications

(10 citation statements)

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“…Because superovulation serves to stimulate the growth and ovulation of follicles and oocytes, this procedure is likely to have adverse effects on physiological and epigenetic processes in the oocyte. Indeed, we have shown this to be the case in the mouse (Almamun 2011;Huffman et al 2015), where oocytes exposed to a superovulation scheme had reduced global immunoreactive 5-meC compared with oocytes developing in an unstimulated female (Almamun 2011). We also showed that the maternal pronucleus of zygotes recovered from females that had undergone a superovulation scheme had a 50% reduction in global levels of DNA methylation compared with zygotes from unstimulated females, which coincided with a 50% increase in H3K9/14 acetylation and with increased levels of gene expression of various epigenetic modifiers at the blastocyst stage (Huffman et al 2015).…”

Section: The Oocytementioning

confidence: 58%

“…ART procedures are used at times of global epigenetic reprogramming in the oocyte and embryos (Bošković et al 2012;MacDonald and Mann 2014). The mammalian oocyte acquires its epigenome during oocyte growth (Lucifero et al 2004;Almamun 2011) and ART procedures, like superovulation and IVM, have been shown to affect it. After fertilisation, the genome of the preimplantation embryo undergoes another global epigenetic restructuration, one that has been shown by a large number of investigators in several mammalian species to be labile to ART manipulations and conditions.…”

Section: Discussionmentioning

confidence: 99%

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Consequences of assisted reproductive techniques on the embryonic epigenome in cattle

Rivera¹

2020

Reprod. Fertil. Dev.

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Procedures used in assisted reproduction have been under constant scrutiny since their inception with the goal of improving the number and quality of embryos produced. However, in vitro production of embryos is not without complications because many fertilised oocytes fail to become blastocysts, and even those that do often differ in the genetic output compared with their in vivo counterparts. Thus only a portion of those transferred complete normal fetal development. An unwanted consequence of bovine assisted reproductive technology (ART) is the induction of a syndrome characterised by fetal overgrowth and placental abnormalities, namely large offspring syndrome; a condition associated with inappropriate control of the epigenome. Epigenetics is the study of chromatin and its effects on genetic output. Establishment and maintenance of epigenetic marks during gametogenesis and embryogenesis is imperative for the maintenance of cell identity and function. ARTs are implemented during times of vast epigenetic reprogramming; as a result, many studies have identified ART-induced deviations in epigenetic regulation in mammalian gametes and embryos. This review describes the various layers of epigenetic regulation and discusses findings pertaining to the effects of ART on the epigenome of bovine gametes and the preimplantation embryo.

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Section: The Oocytementioning

confidence: 58%

Section: Discussionmentioning

confidence: 99%

Consequences of assisted reproductive techniques on the embryonic epigenome in cattle

Rivera¹

2020

Reprod. Fertil. Dev.

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“…We focused our efforts on H3K9me2 as this histone post-translational modification is associated with facultative (permissive) heterochromatin (Lachner et al, 2001;Peters et al, 2001;Peters et al, 2003). During early embryogenesis, the maternal pronucleus retains H3K9 dimethylation and maternal histones possessing this mark replace protamines on the paternal genome (Arney et al, 2002;Lepikhov and Walter, 2004;Santos et al, 2005). H3K9me2 rich regions bind PCG7 (also called Stella or DPPA3) to protect DNA methylation in these regions from active demethylation by TET3 (Nakamura et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…The epigenome of the oocyte and early embryo is very dynamic. Following recruitment, growing oocytes gradually acquire DNA methylation and histone modifications until reaching the fully grown, GV oocyte stage (Monk et al, 1987;Sanford et al, 1987;Kafri et al, 1992;Lucifero et al, 2002;Lucifero et al, 2004;Hiura et al, 2006;Kageyama et al, 2007;Kota and Feil, 2010;Almamun, 2011;Hales et al, 2011;Plasschaert and Bartolomei, 2014). During progression from arrested GV stage oocyte to meiotic resumption in an MII oocyte, histones undergo global deacetylation and gene transcription ceases (Hebbes et al, 1988;Bouniol-Baly et al, 1999;Kim et al, 2003;van den Berg et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…The paternal genome decondenses and acquires maternal histones acetylated on H3K-8, -9, -14, and -18 and H4K-5, -12, and -16, and mono-methylated at H3K4, H3K9, and H3K27 to replace protamines and slowly acquires histone methylation H3K9me2. By the 4-cell stage, the pronuclei epigenomes become indistinguishable (Adenot et al, 1997;Arney et al, 2002;Lepikhov and Walter, 2004;Santos et al, 2005;Lepikhov et al, 2010;Hales et al, 2011;Beaujean, 2014).…”

Section: Introductionmentioning

confidence: 99%

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The effects of biological aging on global DNA methylation, histone modification, and epigenetic modifiers in the mouse germinal vesicle stage oocyte

Marshall¹,

Wang²,

Ji³

et al. 2018

Anim Reprod

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A cultural trend in developed countries is favoring a delay in maternal age at first childbirth. In mammals fertility and chronological age show an inverse correlation. Oocyte quality is a contributing factor to this multifactorial phenomenon that may be influenced by age-related changes in the oocyte epigenome. Based on previous reports, we hypothesized that advanced maternal age would lead to alterations in the oocyte's epigenome. We tested our hypothesis by determining protein levels of various epigenetic modifications and modifiers in fully-grown (≥70 µm), germinal vesicle (GV) stage oocytes of young (10-13 weeks) and aged (69-70 weeks) mice. Our results demonstrate a significant increase in protein amounts of the maintenance DNA methyltransferase DNMT1 (P = 0.003) and a trend toward increased global DNA methylation (P = 0.09) with advanced age. MeCP2, a methyl DNA binding domain protein, recognizes methylated DNA and induces chromatin compaction and silencing. We hypothesized that chromatin associated MeCP2 would be increased similarly to DNA methylation in oocytes of aged female mice. However, we detected a significant decrease (P = 0.0013) in protein abundance of MeCP2 between GV stage oocytes from young and aged females. Histone posttranslational modifications can also alter chromatin conformation. Di-methylation of H3K9 (H3K9me2) is associated with permissive heterochromatin while acetylation of H4K5 (H4K5ac) is associated with euchromatin. Our results indicate a trend toward decreasing H3K9me2 (P = 0.077) with advanced female age and no significant differences in levels of H4K5ac. These data demonstrate that physiologic aging affects the mouse oocyte epigenome and provide a better understanding of the mechanisms underlying the decrease in oocyte quality and reproductive potential of aged females.

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The effects of superovulation and reproductive aging on the epigenome of the oocyte and embryo

Marshall

Rivera

2018

Molecular Reproduction Devel

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A societal preference of delaying maternal age at first childbirth has increased reliance on assisted reproductive technologies/therapies (ART) to conceive a child. Oocytes that have undergone physiologic aging (≥35 years for humans) are now commonly used for ART, yet evidence is building that suboptimal reproductive environments associated with aging negatively affect oocyte competence and embryo development-although the mechanisms underlying these relationship are not yet well understood. Epigenetic programming of the oocyte occurs during its growth within a follicle, so the ovarian stimulation protocols that administer exogenous hormones, as part of the first step for all ART procedures, may prevent the gamete from establishing an appropriate epigenetic state. Therefore, understanding how oocyte. Therefore, understanding how hormone stimulation and oocyte physiologic age independently and synergistically physiologic age independently and synergistically affect the epigenetic programming of these gametes, and how this may affect their developmental competence, are crucial to improved ART outcomes. Here, we review studies that measured the developmental outcomes affected by superovulation and aging, focusing on how the epigenome (i.e., global and imprinted DNA methylation, histone modifications, and epigenetic modifiers) of gametes and embryos acquired from females undergoing physiologic aging and exogenous ovarian stimulation is affected.

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Size-Dependent Acquisition of Global DNA Methylation in Oocytes Is Altered by Hormonal Stimulation.

Cited by 4 publications

References 0 publications

Consequences of assisted reproductive techniques on the embryonic epigenome in cattle

Consequences of assisted reproductive techniques on the embryonic epigenome in cattle

The effects of biological aging on global DNA methylation, histone modification, and epigenetic modifiers in the mouse germinal vesicle stage oocyte

The effects of superovulation and reproductive aging on the epigenome of the oocyte and embryo

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