DNA methylation establishment during oocyte growth: mechanisms and significance

Tomizawa, Shin-ichi; Nowacka‐Woszuk, Joanna; Kelsey, Gavin

doi:10.1387/ijdb.120152gk

Cited by 86 publications

(66 citation statements)

References 53 publications

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“…To circumvent these issues, we developed two methods of oocyte isolation using FACS, which allow us to process many mice in parallel in a relatively short time. We concentrated on two time points in oogenesis: The first, E18.5, represents the "ground state" of the oocyte epigenome, as oocytes contain very little DNA methylation (Smallwood et al 2011;Shirane et al 2013); at the second, P10, de novo DNA methylation commences (Tomizawa et al 2012).…”

Section: Resultsmentioning

confidence: 99%

Dynamic changes in histone modifications precede de novo DNA methylation in oocytes

et al. 2015

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Erasure and subsequent reinstatement of DNA methylation in the germline, especially at imprinted CpG islands (CGIs), is crucial to embryogenesis in mammals. The mechanisms underlying DNA methylation establishment remain poorly understood, but a number of post-translational modifications of histones are implicated in antagonizing or recruiting the de novo DNA methylation complex. In mouse oogenesis, DNA methylation establishment occurs on a largely unmethylated genome and in nondividing cells, making it a highly informative model for examining how histone modifications can shape the DNA methylome. Using a chromatin immunoprecipitation (ChIP) and genome-wide sequencing (ChIP-seq) protocol optimized for low cell numbers and novel techniques for isolating primary and growing oocytes, profiles were generated for histone modifications implicated in promoting or inhibiting DNA methylation. CGIs destined for DNA methylation show reduced protective H3K4 dimethylation (H3K4me2) and trimethylation (H3K4me3) in both primary and growing oocytes, while permissive H3K36me3 increases specifically at these CGIs in growing oocytes. Methylome profiling of oocytes deficient in H3K4 demethylase KDM1A or KDM1B indicated that removal of H3K4 methylation is necessary for proper methylation establishment at CGIs. This work represents the first systematic study performing ChIP-seq in oocytes and shows that histone remodeling in the mammalian oocyte helps direct de novo DNA methylation events.

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Section: Resultsmentioning

confidence: 99%

Dynamic changes in histone modifications precede de novo DNA methylation in oocytes

et al. 2015

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“…These processes are best understood in the mouse (Cedar and Bergman 2009;Tomizawa et al 2012), with only limited data available in ruminants (Thurston et al 2008). The dynamics of imprint establishment during gametogenesis and early embryogenesis (coincident with procedures used in ART) are such that, depending on the precise timing and nature of the procedural insult, it is highly probable that different combinations of imprinted genes may be affected to a greater or lesser extent.…”

Section: Epigenetic Programming Of Long-term Developmentmentioning

confidence: 99%

Epigenetics and developmental programming of welfare and production traits in farm animals

Sinclair

Rutherford

Wallace

et al. 2016

Reprod. Fertil. Dev.

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Abstract. The concept that postnatal health and development can be influenced by events that occur in utero originated from epidemiological studies in humans supported by numerous mechanistic (including epigenetic) studies in a variety of model species. Referred to as the 'developmental origins of health and disease' or 'DOHaD' hypothesis, the primary focus of large-animal studies until quite recently had been biomedical. Attention has since turned towards traits of commercial importance in farm animals. Herein we review the evidence that prenatal risk factors, including suboptimal parental nutrition, gestational stress, exposure to environmental chemicals and advanced breeding technologies, can determine traits such as postnatal growth, feed efficiency, milk yield, carcass composition, animal welfare and reproductive potential. We consider the role of epigenetic and cytoplasmic mechanisms of inheritance, and discuss implications for livestock production and future research endeavours. We conclude that although the concept is proven for several traits, issues relating to effect size, and hence commercial importance, remain. Studies have also invariably been conducted under controlled experimental conditions, frequently assessing single risk factors, thereby limiting their translational value for livestock production. We propose concerted international research efforts that consider multiple, concurrent stressors to better represent effects of contemporary animal production systems.

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“…59 Maternalspecific de novo DNA methylation likely contributes to gene regulation in the oocyte and marks specific genes for activity in the embryo, as in the case of imprinted genes. 60 Indeed, Hdac1/2 mutant oocytes fail to establish normal imprinting DNA methylation marks. 45 Surprisingly, a significant decrease of nuclear-associated DNMT3A2, the predominant isoform of DNMT3A in oocytes, is observed in Hdac1:2 −/− oocytes, and could in principle be responsible for the decreased global DNA methylation and failure to establish DNA methylation of imprinted genes.…”

Section: Hdac2 Regulates Global Dna Methylation and Genomic Imprintinmentioning

confidence: 99%

HDAC1 and HDAC2 in mouse oocytes and preimplantation embryos: Specificity versus compensation

Schultz

2016

Cell Death Differ

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Oocyte and preimplantation embryo development entail dynamic changes in chromatin structure and gene expression, which are regulated by a number of maternal and zygotic epigenetic factors. Histone deacetylases (HDACs), which tighten chromatin structure, repress transcription and gene expression by removing acetyl groups from histone or non-histone proteins. HDAC1 and HDAC2 are two highly homologous Class I HDACs and display compensatory or specific roles in different cell types or in response to different stimuli and signaling pathways. We summarize here the current knowledge about the functions of HDAC1 and HDAC2 in regulating histone modifications, transcription, DNA methylation, chromosome segregation, and cell cycle during oocyte and preimplantation embryo development. What emerges from these studies is that although HDAC1 and HDAC2 are highly homologous, HDAC2 is more critical than HDAC1 for oocyte development and reciprocally, HDAC1 is more critical than HDAC2 for preimplantation development. In eukaryotes, DNA is organized into a highly ordered nucleoprotein assembly called chromatin, whose fundamental unit is the nucleosome. The nucleosome consists of 146 bp of DNA wrapped around a histone core comprised of two molecules each of histones H2A, H2B, H3 and H4. Histone H1 is bound to linker DNA between nucleosomes. 1,2 Histones are subject to multiple post-translational modifications (PTMs), including acetylation, methylation, ubiquitylation, phosphorylation, and sumoylation. These PTMs determine open and closed chromatin conformations, which, in turn, regulate the differential access and recruitment of transcription factors and other regulatory chromatin-binding proteins to DNA. 3-5 Among these histone modifications, histone acetylation is the most well-studied modification, which occurs at the ε-amino groups of evolutionarily conserved lysine residues located at the N termini. Although all core histones are acetylated in vivo, modifications of histones H3 and H4 are more extensively characterized than those of H2A and H2B. Abbreviations: HDAC, histone deacetylase; HAT, histone acetyl transferase; PTM, post-translational modification; KDAC, lysine deacetylase; TSA, trichostatin A; NAD + , nicotinamide adenine dinucleotide; HAD, HDAC association domain ; GVBD, germinal vesicle breakdown; ChIP-seq, chromatin immunoprecipitation sequencing; TFIID, transcription factor II D; YY1, yin yang 1; Pol II CTD S2, serine 2 within the RNApolymerase II C-terminal domain; H3K4, lysine 4 of histone 3; H3K9, lysine 9 of histone 3; H4K16, lysine 16 of histone 4; SIRT, NAD-dependent deacetylase sirtuin; TBP2, TATA-binding protein 2; DNMT, DNA methyltransferases; RBAP46, retinoblastoma binding protein P46; RNAi, RNA interference; aa, amino acidic; BrUTP, 5-Bromouridine 5′-triphosphate; qRT-PCR, quantitative reverse transcription polymerase chain reaction;

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DNA methylation establishment during oocyte growth: mechanisms and significance

Cited by 86 publications

References 53 publications

Dynamic changes in histone modifications precede de novo DNA methylation in oocytes

Dynamic changes in histone modifications precede de novo DNA methylation in oocytes

Epigenetics and developmental programming of welfare and production traits in farm animals

HDAC1 and HDAC2 in mouse oocytes and preimplantation embryos: Specificity versus compensation

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