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TFIIIC binding to Alu elements controls gene expression via chromatin looping and histone acetylation

ABSTRACT: How repetitive elements, epigenetic modifications and architectural proteins interact ensuring proper genome expression remains poorly understood. Here we report regulatory mechanisms unveiling a central role of Alu elements (AEs) and RNA polymerase III transcription factor C (TFIIIC) in structurally and functionally modulating the genome via chromatin looping and histone acetylation. Upon serum deprivation, a subset of AEs pre-marked by the Activity-Dependent Neuroprotector Homeobox protein (ADNP) and located near cell cycle genes recruits TFIIIC, which alters their chromatin accessibility by direct acetylation of histone H3 lysine-18 (H3K18). This facilitates the contacts of AEs with distant CTCF sites near promoter of other cell cycle genes, which also become hyperacetylated at H3K18. These changes ensure basal transcription of cell cycle genes and are critical for their re-activation upon serum re-exposure. Our study reveals how direct manipulation of the epigenetic state of AEs by a general transcription factor regulates 3D genome folding and expression.

ORGANISM(S): Homo sapiens

PROVIDER: GSE120162 | GEO | 2019/11/21

REPOSITORIES: GEO

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TFIIIC dinamically binds Alu elements to control gene expression through chromatin looping

Project description:Folding of the mammalian genome is governed by architectural proteins, such asCTCF. TFIIIC, a RNA polymerase III transcription factor, has been identified as aninsulator but its role in genome topology is totally unknown. Here, we show that TFIIICestablishes long-range genomic interactions that affect gene expression. Upon serumstarvation (SS), TFIIIC occupancy increases at Alu elements (AEs) near promoters ofcell cycle-related genes. Bound AEs become H3K18 hyper-acetylated and fold tocontact distal pre-loaded CTCF sites near other cell cycle genes. The promoters ofthese genes also become hyper-acetylated ensuring their basal transcription during SSand their increased expression during serum re-exposure. Ablation of TFIIIC ordeletion of the TFIIIC-bound AE that loops to the G2/M cycling F (CCNF) locus affectsits expression and nuclear positioning. These results illustrate a novel function ofhuman TFIIIC in changing 3D genome topology through the epigenetic state of AEs.

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Genome-wide nucleosome, TFIIIC and TFIIIB occupancies in Saccharomyces cerevisiae

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Genome-wide binding of condensin II and TFIIIC upon respective knockdown of a TFIIIC and condensin II subunit

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A role for TFIIIC transcription factor complex in genome organization

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Genome-wide binding of condensin II and TFIIIC in human HEK293 cells

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ZSCAN5B and its primate-specific paralogs bind RNA polymerase III genes and extra-TFIIIC (ETC) sites to modulate mitotic progression [SiRNA RNA-Seq data set]

Project description:Particularly in the context of differentiation and development, the importance of three-dimensional chromatin architecture to gene regulatory mechanisms is becoming increasingly clear. The most ancient known mechanism of chromatin organization involves TFIIIC, a transcription factor (TF) that recruits RNA polymerase III (Pol III) for transcription of tRNA and other types of non-coding RNA genes. From yeast to mammals, TFIIIC binds to tRNA genes (tDNAs) and scattered “extra-TFIIIC” (ETC) loci and serves to tether these loci together as anchors of chromatin loops. TFIIIC activities are modulated by MAF, MYC, and other TF proteins that are still unidentified. Here we identify the ZSCAN5 TF family - including mammalian ZSCAN5B and its primate-specific paralogs - as proteins that occupy mammalian Pol III promoters and ETC sites. We show that ZSCAN5B binds with high specificity to a conserved subset of tDNA loci and other Pol III genes in human and mouse and that primate-specific ZSCAN5A and ZSCAN5D also bind Pol III genes, although ZSCAN5D preferentially localizes to MIR SINE- and LINE2-associated ETC sites. ZSCAN5 genes are expressed in proliferating cell populations and are cell-cycle regulated, and gene expression data suggested that they might cooperate to regulate basic cellular functions including mitotic progression. Consistent with this predicted role, ZSCAN5A knockdown led to increasing numbers of cells in mitotic cells and aneuploidy in cultured cells. Together these data implicate ZSCAN5 genes in regulation of Pol III gene transcription and nearby Pol II genes, ultimately influencing cell cycle progression and differentiation in a variety of tissues.

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ZSCAN5B and its primate-specific paralogs bind RNA polymerase III genes and extra-TFIIIC (ETC) sites to modulate mitotic progression [Mouse Placenta ChIP-Seq data set]

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