Linker histone H1 and H3K56 acetylation are antagonistic regulators of nucleosome dynamics

Bernier, Morgan; Luo, Yi; Nwokelo, Kingsley C.; Goodwin, Michelle F.; Dreher, Sarah J.; Zhang, Pei; Parthun, Mark R.; Fondufe‐Mittendorf, Yvonne; Ottesen, Jennifer J.; Poirier, Michael G.

doi:10.1038/ncomms10152

Cited by 46 publications

(70 citation statements)

References 71 publications

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“…40 PIFE (and also FRET) has also been used to investigate interactions of histone H1 with transcriptional activator Gal4. 65 Here the observation of +14 PIFE in the 2 °C CC corroborates information from footprinting 14 and FRET that this CC is advanced, with the downstream duplex bent into the active site cleft as proposed previously. 1,12 These +14 PIFE effects in CC may reflect interactions with DME of RNAP, which include the lineage-specific insert β i4 (also called Sequence Insertion 1 or SI1), the β ′ clamp, and the β ′ jaw (see Figure 6A,B).…”

Section: Discussionsupporting

confidence: 88%

Fluorescence Resonance Energy Transfer Characterization of DNA Wrapping in Closed and Open Escherichia coli RNA Polymerase−λP_R Promoter Complexes

et al. 2016

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Initial recognition of promoter DNA by RNA polymerase (RNAP) is proposed to trigger a series of conformational changes beginning with bending and wrapping of the 40–50 bp of DNA immediately upstream of the −35 region. Kinetic studies demonstrated that the presence of upstream DNA facilitates bending and entry of the downstream duplex (to +20) into the active site cleft to form an advanced closed complex (CC), prior to melting of ~13 bp (−11 to +2), including the transcription start site (+1). Atomic force microscopy and footprinting revealed that the stable open complex (OC) is also highly wrapped (−60 to +20). To test the proposed bent-wrapped model of duplex DNA in an advanced RNAP–λPR CC and compare wrapping in the CC and OC, we use fluorescence resonance energy transfer (FRET) between cyanine dyes at far-upstream (−100) and downstream (+14) positions of promoter DNA. Similarly large intrinsic FRET efficiencies are observed for the CC (0.30 ± 0.07) and the OC (0.32 ± 0.11) for both probe orientations. Fluorescence enhancements at +14 are observed in the single-dye-labeled CC and OC. These results demonstrate that upstream DNA is extensively wrapped and the start site region is bent into the cleft in the advanced CC, reducing the distance between positions −100 and +14 on promoter DNA from >300 to <100 Å. The proximity of upstream DNA to the downstream cleft in the advanced CC is consistent with the proposed mechanism for facilitation of OC formation by upstream DNA.

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Section: Discussionsupporting

confidence: 88%

Fluorescence Resonance Energy Transfer Characterization of DNA Wrapping in Closed and Open Escherichia coli RNA Polymerase−λP_R Promoter Complexes

et al. 2016

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“…Consistent with the ability of H1 to organize linker DNA into a stem-like structure (Fig. 4), H1 has been proposed to repress transcription by limiting nucleosome unwrapping as opposed to physically blocking transcription factor binding (76). This is consistent with genome-wide analyses that point to extensive H1 displacement in transcriptionally active genes (68,77).…”

Section: Figsupporting

confidence: 82%

Yeast HMO1: Linker Histone Reinvented

Panday

Grove

2017

Microbiol Mol Biol Rev

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SUMMARY Eukaryotic genomes are packaged in chromatin. The higher-order organization of nucleosome core particles is controlled by the association of the intervening linker DNA with either the linker histone H1 or high mobility group box (HMGB) proteins. While H1 is thought to stabilize the nucleosome by preventing DNA unwrapping, the DNA bending imposed by HMGB may propagate to the nucleosome to destabilize chromatin. For metazoan H1, chromatin compaction requires its lysine-rich C-terminal domain, a domain that is buried between globular domains in the previously characterized yeast Saccharomyces cerevisiae linker histone Hho1p. Here, we discuss the functions of S. cerevisiae HMO1, an HMGB family protein unique in containing a terminal lysine-rich domain and in stabilizing genomic DNA. On ribosomal DNA (rDNA) and genes encoding ribosomal proteins, HMO1 appears to exert its role primarily by stabilizing nucleosome-free regions or “fragile” nucleosomes. During replication, HMO1 likewise appears to ensure low nucleosome density at DNA junctions associated with the DNA damage response or the need for topoisomerases to resolve catenanes. Notably, HMO1 shares with the mammalian linker histone H1 the ability to stabilize chromatin, as evidenced by the absence of HMO1 creating a more dynamic chromatin environment that is more sensitive to nuclease digestion and in which chromatin-remodeling events associated with DNA double-strand break repair occur faster; such chromatin stabilization requires the lysine-rich extension of HMO1. Thus, HMO1 appears to have evolved a unique linker histone-like function involving the ability to stabilize both conventional nucleosome arrays as well as DNA regions characterized by low nucleosome density or the presence of noncanonical nucleosomes.

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“…The H3K56ac mark, in turn, facilitates Rme1 recruitment, and activation of IRT1 Moretto et al 20 transcription. Our results are consistent with a model describing that H3K56ac increases nucleosome unwrapping facilitating transcription factor (TF) binding and transcription activation (Bernier et al, 2015;Neumann et al, 2009;Williams et al, 2008). At IRT2, partial unwinding of H3K56ac nucleosomes may provide access for Rme1 binding and thus subsequent IRT1 activation.…”

Section: Mechanism Of Irt2 Mediated Activation Of Transcriptionsupporting

confidence: 91%

Transcription levels of a long noncoding RNA orchestrate opposing regulatory and cell fate outcomes in yeast

Moretto

Wood

Chia

et al. 2019

Preprint

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Many long noncoding RNAs (lncRNAs) act in cis through transcription-coupled chromatin alterations that drive changes in local gene expression. How some cisacting lncRNAs promote and others repress gene expression remains poorly understood. Here we report that in S. cerevisiae transcription levels of the lncRNA IRT2, located upstream in the promoter of the inducer of meiosis gene, regulate opposing chromatin and transcription states. Low IRT2 transcription displays enhancer RNA-like features. At these levels, IRT2 promotes histone exchange delivering acetylated histone H3 lysine 56 to chromatin thereby facilitating recruitment of a transcription factor and consequently activating transcription.Conversely, increasing IRT2 transcription enhances chromatin assembly and transcriptional repression. The opposing functions of IRT2 direct a regulatory circuit, which ensures that cells expressing opposite, but not one of either, mating-type loci enter meiosis. Our data demonstrate that the transcription levels of an lncRNA are key to controlling gene expression and cell fate outcomes. Moretto et al.3

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Linker histone H1 and H3K56 acetylation are antagonistic regulators of nucleosome dynamics

Cited by 46 publications

References 71 publications

Fluorescence Resonance Energy Transfer Characterization of DNA Wrapping in Closed and Open Escherichia coli RNA Polymerase−λP_R Promoter Complexes

Fluorescence Resonance Energy Transfer Characterization of DNA Wrapping in Closed and Open Escherichia coli RNA Polymerase−λP_R Promoter Complexes

Yeast HMO1: Linker Histone Reinvented

Transcription levels of a long noncoding RNA orchestrate opposing regulatory and cell fate outcomes in yeast

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Linker histone H1 and H3K56 acetylation are antagonistic regulators of nucleosome dynamics

Cited by 46 publications

References 71 publications

Fluorescence Resonance Energy Transfer Characterization of DNA Wrapping in Closed and Open Escherichia coli RNA Polymerase−λPR Promoter Complexes

Fluorescence Resonance Energy Transfer Characterization of DNA Wrapping in Closed and Open Escherichia coli RNA Polymerase−λPR Promoter Complexes

Yeast HMO1: Linker Histone Reinvented

Transcription levels of a long noncoding RNA orchestrate opposing regulatory and cell fate outcomes in yeast

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Product

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Fluorescence Resonance Energy Transfer Characterization of DNA Wrapping in Closed and Open Escherichia coli RNA Polymerase−λP_R Promoter Complexes

Fluorescence Resonance Energy Transfer Characterization of DNA Wrapping in Closed and Open Escherichia coli RNA Polymerase−λP_R Promoter Complexes