Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis

Burton, Adam; Torres-Padilla, Maria-Elena

doi:10.1038/nrm3885

Cited by 220 publications

(178 citation statements)

References 135 publications

Supporting

Mentioning

160

Contrasting

Order By: Relevance

“…The maternal cytoplasm thus has the remarkable ability to reset the chromatin state of a terminally differentiated nucleus. An analogous process occurs after fertilization: The transition from specialized and transcriptionally silent gametes into a totipotent and transcriptionally active embryo requires comprehensive reorganization of zygotic chromatin (Biechele et al, 2015; Bultman et al, 2006; Burton and Torres-Padilla, 2014). …”

Section: Two Broad Categories Of Pre-gastrulation Vertebrate Embryo Dmentioning

confidence: 99%

Zygotic Genome Activation in Vertebrates

2017

View full text Add to dashboard Cite

The first major developmental transition in vertebrate embryos is the maternal-to-zygotic transition (MZT) when maternal mRNAs are degraded and zygotic transcription begins. During the MZT, the embryo takes charge of gene expression to control cell differentiation and further development. This spectacular organismal transition requires nuclear reprogramming and the initiation of RNAPII at thousands of promoters. Zygotic genome activation (ZGA) is mechanistically coordinated with other embryonic events including changes in the cell cycle, chromatin state, and nuclear-to-cytoplasmic component ratios. Here, we review progress in understanding vertebrate ZGA dynamics in frogs, fish, mice, and humans to explore differences and emphasize common features.

show abstract

Section: Two Broad Categories Of Pre-gastrulation Vertebrate Embryo Dmentioning

confidence: 99%

Zygotic Genome Activation in Vertebrates

2017

View full text Add to dashboard Cite

show abstract

“…Firstly, PRC1.6 is the only PRC1 complex that, in addition to catalytic activity toward H2AK119, possesses histone deacetylation activity 13 and, therefore, could also contribute to the rapid changes in histone acetylation that characterize pre-implantation development. 1,2,4 Secondly, PRC1.6 contains a recognition module, through L3MBTL2, for H4K20me1, which is essential for pre-implantation development, as deletion of PR-Set7 results in lethality by the 8-cell stage, in a manner dependent of its methyltransferase activity. 13,21 Since L3MBTL2 is a defining, unique feature of PRC1.6, we therefore assessed its localization through preimplantation development.…”

Section: L3mbtl2 a Specific Subunit Of Non-canonical Prc16 Complex mentioning

confidence: 99%

“…35 The molecular mechanisms behind epigenetic reprogramming include histone variant exchange, changes in nuclear organization and DNA methylation, the activation of a large fraction of transposable elements, but also rapid and drastic changes in histone modifications. 4,14 Among them, H3K27me3, catalyzed by the Polycomb Repressive Complex 2 (PRC2) and, in general, Polycomb group (PcG) proteins have been shown to play important roles from the earliest stages of development. 8,25,27 At large, PcG repression is achieved through 2 major types of complexes that mediate various biochemical functions including histone modifying activities, recognition of covalent modifications, and physical compaction of chromatin.…”

Section: Introductionmentioning

confidence: 99%

Characterization of non-canonical Polycomb Repressive Complex 1 subunits during early mouse embryogenesis

Eid

Torres-Padilla

2016

Epigenetics

Self Cite

View full text Add to dashboard Cite

An intense period of chromatin remodeling takes place after fertilization in mammals, which is thought necessary for epigenetic reprogramming to start a new developmental program. While much attention has been given to the role of Polycomb Repressive Complex 2 (PRC2) and to canonical PRC1 complexes during this process, little is known as to whether there is any contribution of non-canonical PRC1 in shaping the chromatin landscape after fertilization. Here, we first describe in detail the temporal dynamics and abundance of H2A ubiquitylation (H2AK119ub), a histone modification catalyzed by PRC1, during preimplantation mouse development. In addition, we have analyzed the presence of the 2 characteristic subunits of non-canonical PRC1 complexes, RYBP and its homolog YAF-2. Our results indicate that H2AK119ub is inherited from the sperm, rapidly removed from the paternal chromatin after fertilization, but detected again prior to the first mitosis, suggesting that PRC1 activity occurs as early as the zygotic stage. RYBP and YAF-2, together with the non-canonical subunit L3MBTL2, are all present during preimplantation development but show different temporal dynamics. While RYBP is absent in the zygote, it is strongly induced from the 4-cell stage onwards. YAF-2 is inherited maternally and localizes to the pericentromeric regions in the zygote, is strongly induced between the 2-and 4-cell stages but then remains weak to undetectable subsequently. All together, our data suggest that non-canonical PRC1 is active during pre-implantation development and should be regarded as an additional component during epigenetic reprogramming and in the establishment of cellular plasticity of the early embryo.

show abstract

“…In addition, the paternal and maternal chromatin remain physically segregated in two separate pronuclei that maintain distinctive chromatin marks, with the maternal chromatin containing most constitutive heterochromatin PTMs, while the paternal chromatin is enriched with PTMs of facultative heterochromatin, thought to substitute for the absence of constitutive heterochromatin therein (for review, see Burton and Torres-Padilla 2014). The histone H4 Lys20 dimethylation and trimethylation (H4K20me2/3) are hallmarks of constitutive heterochromatin in somatic cells.…”

mentioning

confidence: 99%

SUV4-20 activity in the preimplantation mouse embryo controls timely replication

et al. 2016

Self Cite

View full text Add to dashboard Cite

Extensive chromatin remodeling after fertilization is thought to take place to allow a new developmental program to start. This includes dynamic changes in histone methylation and, in particular, the remodeling of constitutive heterochromatic marks such as histone H4 Lys20 trimethylation (H4K20me3). While the essential function of H4K20me1 in preimplantation mouse embryos is well established, the role of the additional H4K20 methylation states through the action of the SUV4-20 methyltransferases has not been addressed. Here we show that Suv4-20h1/h2 are mostly absent in mouse embryos before implantation, underscoring a rapid decrease of H4K20me3 from the two-cell stage onward. We addressed the functional significance of this remodeling by introducing Suv4-20h1 and Suv4-20h2 in early embryos. Ectopic expression of Suv4-20h2 leads to sustained levels of H4K20me3, developmental arrest, and defects in S-phase progression. The developmental phenotype can be partially overcome through inhibition of the ATR pathway, suggesting that the main function for the remodeling of H4K20me3 after fertilization is to allow the timely and coordinated progression of replication. This is in contrast to the replication program in somatic cells, where H4K20me3 has been shown to promote replication origin licensing, and anticipates a different regulation of replication during this early developmental time window.

show abstract

Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis

Cited by 220 publications

References 135 publications

Zygotic Genome Activation in Vertebrates

Zygotic Genome Activation in Vertebrates

Characterization of non-canonical Polycomb Repressive Complex 1 subunits during early mouse embryogenesis

SUV4-20 activity in the preimplantation mouse embryo controls timely replication

Contact Info

Product

Resources

About