Trends in Genetics
Volume 27, Issue 5, May 2011, Pages 177-185
Journal home page for Trends in Genetics

Review
Heterochromatin establishment in the context of genome-wide epigenetic reprogramming

https://doi.org/10.1016/j.tig.2011.02.002Get rights and content

Heterochromatin at pericentric satellites, characterized by a specific chromatin signature and chromocenter organization, is of paramount importance for genome function. Re-establishment of this organization after fertilization takes place in the context of genome-wide epigenetic reprogramming. We review how the asymmetry in histone variants and post-translational modifications between paternal and maternal genomes and their respective pericentric heterochromatin domains evolve during early cleavage stages in mouse. We draw a parallel between these data and the burst of pericentric satellite transcription that occurs concomitantly with the dynamic reorganization of the pericentric domains into chromocenters in two-cell stage embryos. Based on this new angle, we propose that a crucial developmental transition at the two-cell stage allows chromocenter formation by involving non-coding satellite transcripts to trigger specific chromatin changes.

Section snippets

The challenge of heterochromatin establishment

The classical definition of heterochromatin designates, as opposed to euchromatin, a chromosomal region that remains condensed through the cell cycle [1]. Within the heterochromatin transcription is generally repressed, and heterochromatinization is crucial for the transcriptional silencing of repetitive and transposable elements. In mouse the predominant heterochromatin domain discernable by cytological techniques is the pericentric heterochromatin [2]. Essentially composed of AT-rich (major)

Specific organization of pericentric domains acquired during gametogenesis

Before two specialized gametes meet at fertilization, the chromatin of oocytes and spermatids has undergone important rearrangements during gametogenesis, and these also extend to pericentric heterochromatin. During oogenesis, pericentric heterochromatin is remodeled, resulting in rings around the nucleolus in transcriptionally silent full-grown oocytes [15]. This particular organization is reiterated later in the zygote [16], and correlates with the developmental competence of the embryo,

Dynamics of histone variants and epigenetic marks during early cleavage stages

Following fertilization the oocyte completes meiosis II and extrudes one haploid genome in the form of the polar body, while the sperm genome decondenses. Two pronuclei form in the same cytoplasm, and the zygote resumes the first mitotic cell cycle. During the entire zygote stage the two parental genomes remain as separate entities characterized by distinct chromatin signatures and transcriptional competence 28, 29, 30, 31, 32. The two genomes finally align at the same metaphase plate during

Distinct chromatin signatures of the two parental pericentric domains

The pericentric domains reorganize dynamically following fertilization to form rings around the nucleolus-like bodies (Figures 2b,3a) 16, 66, similar to the organization in the oocyte nucleus. This organization is achieved in both normal and parthenogenetic embryos, and suggests a developmental stage-specific organization that is initially independent of parental origin and of epigenetic marks on the parental genomes 16, 34. Even during reprogramming of ES cell or somatic cell nuclei in eggs,

Strand-specific expression of pericentric satellites and their role in chromocenter formation and embryonic development

In recent years a role for non-coding RNA in heterochromatin establishment has emerged. In fission yeast, despite the transcription-repressed state of heterochromatin, there is clear evidence that transcription of the pericentric outer repeats and their subsequent processing plays a role in the establishment of heterochromatin 72, 73. Specifically, mutant strains in components of the RNA interference (RNAi) pathway, such as the ribonuclease Dicer, show reduced levels of the crucial

Concluding remarks and future perspectives

Important new findings have identified a crucial developmental transition during which the organization of pericentromeric repeats in chromocenters is established. The involvement of major satellite transcription and of the incorporation of specific histone variants in proper pericentric heterochromatin organization opens up new avenues for understanding the possible interdependency of these events. Future work should help to determine how these events relate to other major rearrangements,

Acknowledgments

We apologize for not having been able to acknowledge all the colleagues who contributed to this work; we thank M. Casanova, J. Clark and D. Filipescu for critical reading of the manuscript and M. Casanova for assistance with Figure 3. This work was supported by la Ligue Nationale contre le Cancer (Equipe labellisée Ligue 2010), PIC Programs, the European Commission Network of Excellence Epigenome (LSHG-CT-2004-503433), the European Commission ITN FP7-PEOPLE-2007 “Image DDR” and FP7-PEOPLE-2008

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