Dynamic alterations of specific histone modifications during early murine development

Sarmento, Olga F.; Digilio, Laura; Wang, Yanming; Perlin, Julie R.; Herr, John C.; Allis, C. David; Coonrod, Scott A.

doi:10.1242/jcs.01328

Cited by 202 publications

(158 citation statements)

References 44 publications

(46 reference statements)

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“…Histone deacetylation accompanies oocyte maturation and inhibiting HDAC activity with TSA results in global histone hyperacetylation and chromosome segregation defects. [65][66][67][68] The responsible HDACs, however, have not been fully identified.…”

Section: Hdac2 Regulates Chromosome Segregation and Kinetochore Functmentioning

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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Section: Hdac2 Regulates Chromosome Segregation and Kinetochore Functmentioning

confidence: 99%

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

Schultz

2016

Cell Death Differ

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“…Histone modification is one such epigenetic mechanism that is critical to embryo development of several species such as mice (Corry et al 2009), cattle (Santos et al 2003, Enright et al 2005, Wee et al 2006, Maalouf et al 2008, Ross et al 2008, pig (Park et al 2009, Gao et al 2010, sheep (Hou et al 2008) and human (Zhang et al 2012). In mice, Sarmento et al (2004), describes two types of histone patterns during preimplantation development, a consistent, stable mark during development and a dynamic, reversible mark. The highly dynamic marks are often associated with critical events, such as the transition to embryonic genome activation or the first cellular differentiation from totipotent cells into the inner cell mass and trophectoderm [for review see Mason et al 2012).…”

Section: Introductionmentioning

confidence: 99%

Supplementation of fetal bovine serum alters histone modification H3R26me2 during preimplantation development of in vitro produced bovine embryos

et al. 2015

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In vitro production (IVP) of bovine embryos is not only of great economic importance to the cattle industry, but is also an important model for studying embryo development. The aim of this study was to evaluate the histone modification, H3R26me2 during pre-implantation development of IVP bovine embryos cultured with or without serum supplementation and how these in vitro treatments compared to in vivo embryos at the morula stage. After in vitro maturation and fertilization, bovine embryos were cultured with either 0 or 2.5% fetal bovine serum (FBS). Development was evaluated and embryos were collected and fixed at different stages during development (2-, 4-, 8-, 16-cell, morula and blastocyst). Fixed embryos were then used for immunofluorescence utilizing an antibody for H3R26me2. Images of stained embryos were analyzed as a percentage of total DNA. Embryos cultured with 2.5% FBS developed to blastocysts at a greater rate than 0%FBS groups (34.85±5.43% vs. 23.38±2.93%; P<0.05). Levels of H3R26me2 changed for both groups over development. In the 0%FBS group, the greatest amount of H3R26me2 staining was at the 4-cell (P<0.05), 16-cell (P<0.05) and morula (P<0.05) stages. In the 2.5%FBS group, only 4-cell stage embryos were significantly higher than all other stages (P<0.01). Morula stage in vivo embryos had similar levels as the 0%FBS group, and both were significantly higher than the 2.5%FBS group. These results suggest that the histone modification H3R26me2 is regulated during development of pre-implantation bovine embryos, and that culture conditions greatly alter this regulation.

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“…Epigenetic regulation of this process could provide an elegant mechanism for maintaining lineage identity following isolation of these progenitors from their embryonic environment during stem cell establishment. Lineagespecific differences in chromatin have been observed at the level of histone modifications (11,12). Whether these lineage-specific differences in histone marks impact transcriptional regulation and are involved in the establishment or maintenance of lineage progenitors is not known.…”

mentioning

confidence: 99%

“…Additionally, immunocytochemistry revealed lower levels of several histone modifications, including H3K27me3 and histone H3 lysine 9 acetylation (H3K9ac), in TE compared to EPI (11,12). Whether these lineage-specific differences in histone marks impact transcriptional regulation and are involved in the establishment or maintenance of lineage progenitors is not known.…”

mentioning

confidence: 99%

Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo

Rugg‐Gunn

Cox

Ralston

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

207

199

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A unique property of the mammalian embryo is that stem cells can be derived from its early tissue lineages. These lineages will give rise to the fetus as well as essential extraembryonic tissues. Understanding how chromatin regulation participates in establishment of these lineages in the embryo and their derived stem cells provides insight that will critically inform our understanding of embryogenesis and stem cell biology. Here, we compare the genomewide location of active and repressive histone modifications in embryonic stem cells, trophoblast stem cells, and extraembryonic endoderm stem cells from the mouse. Our results show that the active modification H3K4me3 has a similar role in the three stem cell types, but the repressive modification H3K27me3 varies in abundance and genomewide distribution. Thus, alternative mechanisms mediate transcriptional repression in stem cells from the embryo. In addition, using carrier chromatin immunoprecipitation we show that bivalent histone domains seen in embryonic stem cells exist in pluripotent cells of the early embryo. However, the epigenetic status of extraembryonic progenitor cells in the embryo did not entirely reflect the extraembryonic stem cell lines. These studies indicate that histone modification mechanisms may differ between early embryo lineages and emphasize the importance of examining in vivo and in vitro progenitor cells.epigenetics | methylation | embryogenesis | extraembryonic

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Dynamic alterations of specific histone modifications during early murine development

Cited by 202 publications

References 44 publications

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

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

Supplementation of fetal bovine serum alters histone modification H3R26me2 during preimplantation development of in vitro produced bovine embryos

Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo

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