Key Points
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The chromatin landscape is a key aspect of epigenetic regulation in eukaryotes.
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Old histones are recycled during DNA replication, therefore providing a blueprint for the duplication of their modifications following DNA replication.
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Positive-feedback loops and cooperativity among chromatin-modifying complexes are crucial for the propagation of histone marks.
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The nuclear architecture and long-range interactions are likely to contribute to inheritance of epigenetic information.
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The concerted action of trans-acting factors and the chromatin landscape dictate the inheritance of epigenetic information.
Abstract
Although it is widely accepted that the regulation of the chromatin landscape is pivotal to conveying the epigenetic program, it is still unclear how a defined chromatin domain is reproduced following DNA replication and transmitted from one cell generation to the next. Here, we review the multiple mechanisms that potentially affect the inheritance of epigenetic information in somatic cells. We consider models of how histones might be recycled following replication, and discuss the importance of positive-feedback loops, long-range gene interactions and the complex network of trans-acting factors in the transmission of chromatin states.
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Acknowledgements
We thank D. Beck, R. Bonasio and E. Campos for their critical reading of the manuscript. We are grateful to L. Vales and J. Hurwitz for critical reading of this manuscript and active discussions. We apologize to authors whose studies could not be cited due to space limitations. Work in the laboratory of D.R. is funded by the US National Institutes of Health (grants RO1GM064844 and 4R37GM037120) and the Howard Hughes Medical Institute.
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Glossary
- Histone variants
-
Structurally distinct, non-typical versions of histone proteins. They are encoded by independent genes and are often subject to regulation that is distinct from that of the canonical histones.
- Heterochromatin
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The portion of the genome that stays highly condensed throughout the cell cycle. It contains lot of repetitive sequences, is gene-poor overall and is enriched for histone marks, such as histone 3 lysine 9 trimethylation (H3K9me3) and H4K20me3.
- Euchromatin
-
In contrast to heterochromatin, euchromatin is decondensed and is enriched in active genes and histone marks, such as histone 3 lysine 4 trimethylation or histone 3 acetylation, that are associated with active transcription.
- Regulon
-
A group of transcriptional units or operons that are coordinately controlled by a regulator.
- Chromatin remodelling
-
An ATP-dependent enzymatic process that alters histone–DNA interactions or regulates the position of nucleosomes. Chromatin remodelling can also be ATP-independent in the case of the facilitates chromatin transcription (FACT) complex.
- Nuclear periphery
-
The area at the edge of the nucleus. It is normally associated with gene silencing.
- Heterokaryon
-
A cell with two nuclei that share the same cytoplasm.
- RNA interference
-
A cellular mechanism involved in gene silencing and 'protection' from retroviral and transposable element invasion. It is regulated by proteins such as Dicer and Argonaute, which are responsible for the production of small interfering RNAs that target mRNAs for cleavage and that localize silencing factors to heterochromatic regions.
- Mini-chromosome maintenance complex
-
An oligomeric complex that is suggested to be the helicase involved in replication.
- Histone chaperone
-
A protein that binds and escorts histones. Chaperones contribute to histone deposition into chromatin in an ATP-independent manner.
- Chromosome conformation capture
-
A technique used to study the long-distance interactions between genomic regions. These interactions can be used to study the three-dimensional architecture of chromosomes in a cell nucleus.
- Small nuclear RNAs
-
RNAs that are involved in precursor mRNA processing.
- Dicer
-
Dicer proteins are a highly conserved family of RNase III enzymes that mediate dsRNA cleavage. This produces the small RNAs that direct targeted silencing in RNA interference pathways.
- Chromatin readers
-
Protein domains that show high binding affinity for histone post-translational modifications and function in downstream effects.
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Margueron, R., Reinberg, D. Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11, 285–296 (2010). https://doi.org/10.1038/nrg2752
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DOI: https://doi.org/10.1038/nrg2752
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