Histone fold modifications control nucleosome unwrapping and disassembly

Simon, Marek; North, Justin A.; Shimko, John C.; Forties, Robert A.; Ferdinand, Michelle B.; Manohar, Mridula; Zhang, Meng; Fishel, Richard; Ottesen, Jennifer J.; Poirier, Michael G.

doi:10.1073/pnas.1106264108

Cited by 173 publications

(209 citation statements)

References 53 publications

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“…1F). Thus, acetylation of H3K56 not only decreases nucleosome stability (29), increases unwrapping of nucleosomal DNA ends, and may affect histonehistone interactions (27,30), but H3K56ac may also free H3K56 sufficiently from local nucleosomal constraints to enable H3K56ac recognition by Oct4. Taken together, our data indicate that H3K56ac interacts with Oct4 in vivo in mouse ESCs and directly in vitro.…”

Section: H3k56ac Presence Is Correlated With That Of Key Transcriptionalmentioning

confidence: 99%

Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency

Tan

Xue

Song

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The presence of acetylated histone H3K56 (H3K56ac) in human ES cells (ESCs) correlates positively with the binding of Nanog, Sox2, and Oct4 (NSO) transcription factors at their target gene promoters. However, the function of H3K56ac there has been unclear. We now report that Oct4 interacts with H3K56ac in mouse ESC nuclear extracts and that perturbing H3K56 acetylation decreases Oct4-H3 binding. This interaction is likely to be direct because it can be recapitulated in vitro in an H3K56ac-dependent manner and is functionally important because H3K56ac combines with NSO factors in chromatin immunoprecipitation sequencing to mark the regions associated with pluripotency better than NSO alone. Moreover, reducing H3K56ac by short hairpin Asf1a decreases expression of pluripotency-related markers and increases expression of differentiation-related ones. Therefore, our data suggest that H3K56ac plays a central role in binding to Oct4 to promote the pluripotency of ESCs.

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Section: H3k56ac Presence Is Correlated With That Of Key Transcriptionalmentioning

confidence: 99%

Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency

Tan

Xue

Song

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Biophysical studies with H3K115ac and H3K122ac nucleosomes showed that these modifications reduce the affinity of the histone octamer for DNA and mildly increase thermal repositioning of nucleosomes (16). When combined with mechanical unwrapping of DNA, these modifications facilitate release of histone octamer from DNA (17), and these modifications also enhance nucleosome disassembly rates by a DNA repair factor (21). In vivo, these PTMs are implicated in altering gene silencing at ribosomal DNA loci and telomeres (22), DNA repair (22,23), and transcription activation (19,23).…”

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confidence: 99%

“…Some of these nucleosome core PTMs are located in the histone-DNA interface (15,16). Several of them colocalize with known SIN mutations (15) and reduce DNA binding affinity (15)(16)(17) or interfere with DNA wrapping about the lateral surface of the nucleosome (17, 18).Acetylation of histone H3 lysines 115 (H3K115ac) and 122 (H3K122ac) were first identified to occur individually and in combination (H3K115acK122ac) based on mass spectrometric analysis of bovine histones (12). Recently, H3K122ac was shown to be catalyzed by the histone acetyl transferases p300/CBP in response to estrogen receptor signaling (19).…”

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confidence: 99%

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Histone Acetylation near the Nucleosome Dyad Axis Enhances Nucleosome Disassembly by RSC and SWI/SNF

Chatterjee

North

Dechassa

et al. 2015

Molecular and Cellular Biology

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e Signaling associated with transcription activation occurs through posttranslational modification of histones and is best exemplified by lysine acetylation. Lysines are acetylated in histone tails and the core domain/lateral surface of histone octamers. While acetylated lysines in histone tails are frequently recognized by other factors referred to as "readers," which promote transcription, the mechanistic role of the modifications in the lateral surface of the histone octamer remains unclear. By using X-ray crystallography, we found that acetylated lysines 115 and 122 in histone H3 are solvent accessible, but in biochemical assays they appear not to interact with the bromodomains of SWI/SNF and RSC to enhance recruitment or nucleosome mobilization, as previously shown for acetylated lysines in H3 histone tails. Instead, we found that acetylation of lysines 115 and 122 increases the predisposition of nucleosomes for disassembly by SWI/SNF and RSC up to 7-fold, independent of bromodomains, and only in conjunction with contiguous nucleosomes. Thus, in combination with SWI/SNF and RSC, acetylation of lateral surface lysines in the histone octamer serves as a crucial regulator of nucleosomal dynamics distinct from the histone code readers and writers. N ucleosomes, the basic building blocks of eukaryotic chromatin, impose a physical barrier to regulatory proteins and repress various DNA-mediated transactions (1). Despite spontaneous partial unwrapping and rewrapping of DNA near the entry/ exit site (2, 3), nucleosomes are quite stable and show limited mobility. Fourteen major histone-DNA contacts at 10.5-bp intervals primarily contribute to this stability, and about 14 kCal/mol of energy is required to break these contacts (4, 5). ATP-dependent chromatin remodelers like RSC and SWI/SNF reposition (6) or evict (7,8) nucleosomes by breaking these histone-DNA contacts during the course of remodeling. However, specific point mutations in the core histones can weaken key histone-DNA or histone-histone interactions in the nucleosome and partially alleviate the requirement for SWI/SNF (9). These mutations, termed SIN (SWI/SNF-independent) mutations, when present at the nucleosomal dyad or in the histone dimer-tetramer interface, decrease stability while increasing thermal mobility of nucleosomes and thereby may substitute for SWI/SNF function (10, 11).Incorporation of various posttranslational modifications (PTMs) into histones regulates nucleosome structure and dynamics. While the majority of PTMs reside in the unstructured N-terminal tail domain of histones, many have been identified in the ␣-helical histone fold motif that constrains the DNA superhelix to form the compact nucleosome core (12)(13)(14). Unlike the histone tail PTMs, those in the histone core are often buried and hence are less likely to be accessible for regulatory factor binding. Some of these nucleosome core PTMs are located in the histone-DNA interface (15,16). Several of them colocalize with known SIN mutations (15) and reduce DNA binding affinity (1...

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“…Acetylated H3 K56 is very abundant in the yeast being found on ϳ28% of the total H3 (36). H3 K56 is located near the DNA entry and exit point of the nucleosome and, as such, can influence the wrapping of DNA on the nucleosome (42,43). The level of H3 K56 acetylation has been measured by various labs in biological systems from yeast to human (34, 36, 44 -48).…”

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confidence: 99%

Discovery of Histone Modification Crosstalk Networks by Stable Isotope Labeling of Amino Acids in Cell Culture Mass Spectrometry (SILAC MS)

Guan

Rastogi

Parthun

et al. 2013

Molecular & Cellular Proteomics

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In this paper we describe an approach that combines stable isotope labeling of amino acids in cells culture, high mass accuracy liquid chromatography tandem mass spectrometry and a novel data analysis approach to accurately determine relative peptide post-translational modification levels. This paper describes the application of this approach to the discovery of novel histone modification crosstalk networks in Saccharomyces cerevisiae. Yeast histone mutants were generated to mimic the presence/absence of 44 well-known modifications on core histones H2A, H2B, H3, and H4. In each mutant strain the relative change in H3 K79 methylation and H3 K56 acetylation were determined using stable isotope labeling of amino acids in cells culture. This approach showed relative changes in H3 K79 methylation and H3 K56 acetylation that are consistent with known histone crosstalk networks. More importantly, this study revealed additional histone modification sites that affect H3 K79 methylation and H3 K56 acetylation. Histone post-translational modifications play a crucial role in stabilizing chromosomal structure and regulating gene transcription (1-3). There is mounting evidence that histone modifications communicate via crosstalk (4 -11). Crosstalk can occur between modifications that are present on the same histone molecule (cis) or between modifications on different histones (trans). For example, H2B K123 monoubiquitination regulates H3 K4 and K79 methylation via a direct trans crosstalk interaction that involves the ubiquitin-conjugating enzyme, Rad6, and the methyltransferases, Set1 and Dot1 (4, 12-24). The methylation of histone H3 can also be regulated in trans by elements on the NH 2 -terminal tail of histone H4 and histone H2A (23,25,26). Another example of histone crosstalk is the influence of histone H3 S10 phosphorylation on the acetylation of histone H4 K16, via a trans interaction, and H3 K14, via a cis interaction (27, 28). Histone crosstalk is not strictly limited to post-translational modifications. For example, the isomerization of histone H3 P30, catalyzed by the proline isomerase Fpr4, inhibits the ability of Set2 to methylate H3 K36 (29).In this paper we examined histone crosstalk networks for H3 K79 methylation and H3 K56 acetylation, which are among the most intensively studied histone modifications (14, 30 -36). Van Leeuwen and colleagues first reported that in the budding yeast Saccharomyces cerevisiae lysine 79 of histone H3, located at the surface of the nucleosome, is methylated by the protein Dot1p. H3 K79 methylation is an abundant modification that is found in euchromatic regions of the genome and plays an important role in the discrimination between euchromatin and heterochromatin. The abundance of the mono-, di-and tri-methylation states was quantitated by liquid chromatography (LC) 1 -MS using the doubly charged peptides with different methylation levels whose identity was verified by tandem MS (MS/MS) (35). Using LC-MS, the Henikoff laboratory also quantified the relative abundance of doubly c...

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Histone fold modifications control nucleosome unwrapping and disassembly

Cited by 173 publications

References 53 publications

Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency

Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency

Histone Acetylation near the Nucleosome Dyad Axis Enhances Nucleosome Disassembly by RSC and SWI/SNF

Discovery of Histone Modification Crosstalk Networks by Stable Isotope Labeling of Amino Acids in Cell Culture Mass Spectrometry (SILAC MS)

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