New Insights into the Regulation of Heterochromatin - PubMed
Review
New Insights into the Regulation of Heterochromatin
Jiyong Wang et al. Trends Genet. 2016 May.
Abstract
All living organisms are constantly exposed to stresses from internal biological processes and surrounding environments, which induce many adaptive changes in cellular physiology and gene expression programs. Unexpectedly, constitutive heterochromatin, which is generally associated with the stable maintenance of gene silencing, is also dynamically regulated in response to stimuli. In this review we discuss the mechanism of constitutive heterochromatin assembly, its dynamic nature, and its responses to environmental changes.
Keywords: constitutive heterochromatin; dynamics; epigenetic adaptation; stress.
Copyright © 2016 Elsevier Ltd. All rights reserved.
Figures

A step-wise model of heterochromatin assembly. Histone H3K9 methyltransferases (HMTs) are first recruited to heterochromatin nucleation centers, leading to H3K9 methylation (red dots associated with the chromosome), which is subsequently recognized and bound by heterochromatin protein 1 (HP1). Additional HMTases are recruited either directly through recognizing H3K9me or association with HP1, leading to the methylation of adjacent nucleosomes. The repetition of such binding-methylation cycles results in heterochromatin spreading in a sequence-independent manner.

Dynamics of HP1 proteins. Contrary to the general conception that HP1 is a static component of heterochromatin, it dynamically exchanges between the heterochromatin-bound and free forms, which gives other factors access to the underlying DNA, such as RNA Pol II shown here. HP1 also exchanges rapidly between heterochromatin domains, such as centromeres and telomeres, to buffer changes in heterochromatin stability.

Transcription-dependent heterochromatin assembly at repetitive DNA elements in fission yeast. During S phase of the cell cycle, DNA repeats are transcribed by RNA polymerase II (Pol II). These transcripts are converted into double-stranded RNAs by the RNA-dependent RNA polymerase complex (RDRC) and then processed into small interfering RNAs (siRNAs) by the RNAi machinery. The siRNAs guide the RNA-induced transcriptional silencing (RITS) complex back to nascent transcripts. RITS associates with Clr4 methyltransferase complex (CLRC), which initiates H3K9 methylation and heterochromatin assembly.

Pericentric heterochromatin disassembly in response to stresses in Drosophila. Under normal conditions, the transcription factor dATF-2 is in a hypophosphorylated form, which recruits HP1 to establish constitutive heterochromatin at pericentric regions. In response to stress, the MAPK pathway phosphorylates dATF-2, thus reducing its binding to pericentric heterochromatin and releasing HP1.

Heterochromatin-mediated epigenetic adaptation in fission yeast. The negative regulators of heterochromatin, Mst2 and Epe1, prevent promiscuous heterochromatin spreading in wild type cells. However, in mst2Δ epe1Δ cells, uncontrolled heterochromatin spreading inactivates essential genes, resulting in severe growth defects during early stage of development. Gradually, cells form heterochromatin at the clr4+ locus to reduce Clr4 expression levels, resulting in a new equilibrium that maintains heterochromatin at critical locations but minimizes heterochromatin spreading, leading to the normal growth during late stages of development.
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