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Asymmetric distribution of H3K9me3 at replicating DNA strands silences L1 retrotransposons during S phase

ABSTRACT: Asymmetric distribution of H3K9me3 at replicating DNA strands silences L1 retrotransposons during S phase

PROVIDER: PRJNA869455 | ENA |

REPOSITORIES: ENA

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			Action	DRS
	SRR21046900_1.fastq.gz	Fastqsanger.gz
	SRR21046900_2.fastq.gz	Fastqsanger.gz
	SRR21046901_1.fastq.gz	Fastqsanger.gz
	SRR21046901_2.fastq.gz	Fastqsanger.gz
	SRR21046902_1.fastq.gz	Fastqsanger.gz

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Asymmetric distribution of H3K9me3 at replicating DNA strands silences L1 retrotransposons during S phase

Project description:In higher eukaryotes, repetitive DNA sequences are transcriptionally silenced through histone H3 lysine 9 tri-methylation (H3K9me3). A loss of silencing of these elements leads to genome instability and human diseases, including cancer and aging1-3. While the role of H3K9me3 in the establishment and maintenance of heterochromatin and repression of DNA repeats has been extensively studied4-6, the pattern and mechanism underlying the partitioning of H3K9me3 at replicating DNA strands were unknown. Here, we report that H3K9me3 is preferentially transferred onto the leading strands of replication forks, which occurs predominantly at Long Interspersed Nuclear Element (LINE) retrotransposons that are theoretically transcribed at the head-on direction with replication fork movement. In contrast, all other modified forms of histones tested are distributed in a nearly symmetric manner at the leading and lagging strands. Mechanistically, the Human Silencing Hub (HUSH) complex interacts with the leading strand DNA polymerase Pol ε, and contributes to the asymmetric segregation of H3K9me3 during chromatin replication. Cells deficient for Pol ε (POLE3 and POLE4), the HUSH complex (MPP8 and TASOR), or cells expressing a MPP8 mutant defective of H3K9me3 binding, or TASOR mutants with reduced interaction with Pol ε, show compromised H3K9me3 asymmetry and increased LINE expression. These results reveal an unexpected mechanism whereby the HUSH complex functions with Pol ε to promote asymmetric H3K9me3 distribution at LINEs to suppress their expression during S phase.

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Project description:In eukaryotic cells, inheritable changes in gene expression in response to environmental and developmental stimuli is associated with changes in histone modifications and relies on the passage of these changes into daughter cells during cell division, a process that remains elusive. Here, we show that parental histone (H3-H4)2 tetramers, the primary carrier of epigenetic modifications, are assembled into nucleosomes onto both replicating leading and lagging strands, with a preference for lagging strands of DNA replication forks. This asymmetric distribution of parental (H3-H4)2 is exacerbated in cells lacking Dpb3 and Dpb4, two subunits of DNA polymerase Pol ε. Dpb3-Dpb4 binds (H3-H4)2 and participates in the transfer of parental (H3-H4)2 tetramers onto leading strands of DNA replication forks. Cells lacking Dpb3 and Dpb4 exhibits defects in epigenetic inheritance. These results reveal a previously undocumented mechanism of histone segregation and a direct role for Pol ε in this poorly understood process.

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The Mcm2-Ctf4-Pola axis facilitates parental histone transfer to lagging strands

Project description:Although essential for epigenetic inheritance, the transfer of parental histone (H3-H4)2 tetramers that contain epigenetic modifications to replicating DNA strands is poorly understood. Here, we show that the Mcm2-Ctf4-Pol axis facilitates the transfer of parental (H3-H4)2 tetramers to lagging strands of DNA replication forks. Mutating the H3-H4 binding domain of Mcm2, a subunit of the CMG (Cdc45-MCM-GINS) replicative helicase that translocates along leading strands, impairs the transfer of parental (H3-H4)2 to lagging strands. Similar effects are observed in Ctf4 and Pol-primase mutants that disrupt the connection of the CMG helicase via Ctf4-Pol to lagging strands. Our results support a model whereby parental (H3-H4)2 displaced from nucleosomes through leading-strand DNA replication are transferred to lagging strands for nucleosome assembly via the CMG-Ctf4-Pol complex.

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