Insufficient histone-3 lysine-9 deacetylation in human oocytes matured in vitro is associated with aberrant meiosis

Jia, Hongyu; Li, Tao; Ding, Chenhui; Brosens, Jan J.; Zhou, Canquan; Xu, Yanwen

doi:10.1016/j.fertnstert.2011.10.023

Cited by 26 publications

(12 citation statements)

References 28 publications

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“…Similar profiles for HDAC1 and HAT1 mRNAs have been previously observed in bovine oocytes (McGraw et al 2003). On the other hand, two studies described a decrease in HDAC1 mRNA during IVM in human oocytes Huang et al 2012). To the best of our knowledge, in these studies a mix of oligo-dT and random primers was used for reverse transcription, possibly introducing a bias for polyadenylated mRNA species rather than detecting a difference in the total mRNA abundance.…”

Section: Discussionsupporting

confidence: 70%

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

Franciosi

Goudet

Tessaro

et al. 2017

Reprod. Fertil. Dev.

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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.

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Section: Discussionsupporting

confidence: 70%

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

Franciosi

Goudet

Tessaro

et al. 2017

Reprod. Fertil. Dev.

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“…For instance, histone H3K9 deacetylation is followed by its trimethylation during oocyte maturation ( Peters et al , 2001 ; Grewal and Jia, 2007 ; Russo et al , 2013 ). Insufficient H3K9 deacetylation in in vitro -matured human oocytes was associated with aberrant meiosis ( Huang et al , 2012 ). Loss of H3K9 methylation was reported in chronologically aged and in vitro aged mouse oocytes ( Yu et al , 2007 ; Manosalva and González, 2010 ).…”

Section: Discussionmentioning

confidence: 99%

Postovulatory aging affects dynamics of mRNA, expression and localization of maternal effect proteins, spindle integrity and pericentromeric proteins in mouse oocytes

et al. 2015

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STUDY QUESTIONIs the postovulatory aging-dependent differential decrease of mRNAs and polyadenylation of mRNAs coded by maternal effect genes associated with altered abundance and distribution of maternal effect and RNA-binding proteins (MSY2)?SUMMARY ANSWERPostovulatory aging results in differential reduction in abundance of maternal effect proteins, loss of RNA-binding proteins from specific cytoplasmic domains and critical alterations of pericentromeric proteins without globally affecting protein abundance.WHAT IS KNOWN ALREADYOocyte postovulatory aging is associated with differential alteration in polyadenylation and reduction in abundance of mRNAs coded by selected maternal effect genes. RNA-binding and -processing proteins are involved in storage, polyadenylation and degradation of mRNAs thus regulating stage-specific recruitment of maternal mRNAs, while chromosomal proteins that are stage-specifically expressed at pericentromeres, contribute to control of chromosome segregation and regulation of gene expression in the zygote.STUDY DESIGN, SIZE, DURATIONGerminal vesicle (GV) and metaphase II (MII) oocytes from sexually mature C57B1/6J female mice were investigated. Denuded in vivo or in vitro matured MII oocytes were postovulatory aged and analyzed by semiquantitative confocal microscopy for abundance and localization of polyadenylated RNAs, proteins of maternal effect genes (transcription activator BRG1 also known as ATP-dependent helicase SWI/SNF related, matrix associated, actin dependent regulator of chromatin, subfamily a, member 4 (SMARCA4) and NOD-like receptor family pyrin domain containing 5 (NLRP5) also known as MATER), RNA-binding proteins (MSY2 also known as germ cell-specific Y-box-binding protein, YBX2), and post-transcriptionally modified histones (trimethylated histone H3K9 and acetylated histone H4K12), as well as pericentromeric ATRX (alpha thalassemia/mental retardation syndrome X-linked, also termed ATP-dependent helicase ATRX or X-linked nuclear protein (XNP)). For proteome analysis five replicates of 30 mouse oocytes were analyzed by selected reaction monitoring (SRM).MATERIAL AND METHODSGV and MII oocytes were obtained from large antral follicles or ampullae of sexually mature mice, respectively. Denuded MII oocytes were aged for 24 h post ovulation. For analysis of distribution and abundance of polyadenylated RNAs fixed oocytes were in situ hybridized to Cy5 labeled oligo(dT)20 nucleotides. Absolute quantification of protein concentration per oocyte of selected proteins was done by SRM proteome analysis. Relative abundance of ATRX was assessed by confocal laser scanning microscopy (CLSM) of whole mount formaldehyde fixed oocytes or after removal of zona and spreading. MSY2 protein distribution and abundance was studied in MII oocytes prior to, during and after exposure to nocodazole, or after aging for 2 h in presence of H2O2 or for 24 h in presence of a glutathione donor, glutathione ethylester (GEE).MAIN RESULTS AND ROLE OF CHANCEThe significant reduction in abundance of pr...

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“…This task is classified as one of the early actions of maternal effects and is essential for normal meiosis and quality of the oocyte and prevent of aneuploidy in the embryo (Figure 1). Recent studies revealed epigenetic changes in the genome that enable meiosis (Huang et al, 2012; Ma & Schultz, 2013). These changes also control gene expression, at least during initial stages of embryogenesis.…”

Section: Oocyte Histones and Histone Modifiersmentioning

confidence: 99%

“…Histone deacetylation also contributes to transcriptional silencing and formation of the surrounded nucleolus nuclear state in oocytes (De La Fuente, Viveiros, Burns, et al, 2004; De La Fuente, Viveiros, Wiggleworth, & Eppig, 2004; Lee, Wildt, & Comizzoli, 2015). Inadequate histone deacetylation is associated with increased aneuploidy, aberrant oocyte meiosis (Huang et al, 2012; Ma & Schultz, 2013, 2016), and with reduced oocyte quality accompanying aging (van den Berg et al, 2011). Histone deacetylases also regulate the activities of other proteins, and inhibition of this process can also disrupt spindle formation in mitotic and meiotic cells (Chuang, Pan, Hawke, Lin, & Yu‐Lee, 2013; Gabrielli & Brown, 2012; X. Li et al, 2017; Shin et al, 2003).…”

Section: Oocyte Histones and Histone Modifiersmentioning

confidence: 99%

Listening to mother: Long‐term maternal effects in mammalian development

Ruebel

Latham

2020

Molecular Reproduction Devel

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The oocyte is a complex cell that executes many crucial and unique functions at the start of each life. These functions are fulfilled by a unique collection of macromolecules and other factors, all of which collectively support meiosis, oocyte activation, and embryo development. This review focuses on the effects of oocyte components on developmental processes that occur after the initial stages of embryogenesis. These include long-term effects on genome function, metabolism, lineage allocation, postnatal progeny health, and even subsequent generations.Factors that regulate chromatin structure, genome programming, and mitochondrial function are elements that contribute to these oocyte functions. K E Y W O R D S chromatin, embryo gene regulation, maternal effect, oocyte 400 |

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Insufficient histone-3 lysine-9 deacetylation in human oocytes matured in vitro is associated with aberrant meiosis

Cited by 26 publications

References 28 publications

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

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

Postovulatory aging affects dynamics of mRNA, expression and localization of maternal effect proteins, spindle integrity and pericentromeric proteins in mouse oocytes

Listening to mother: Long‐term maternal effects in mammalian development

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