Origins and Formation of Histone Methylation across the Human Cell Cycle

Zee, Barry M.; Britton, Laura Mae P.; Wolle, Daniel; Haberman, Devorah; Garcia, Benjamin A.

doi:10.1128/mcb.06673-11

Cited by 80 publications

(77 citation statements)

References 55 publications

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“…1B). The slight overrepresentation of old histones likely reflects a contribution of recycled light amino acids during histone biosynthesis (Scharf et al 2009;Xu et al 2012;Zee et al 2012). Thus, chromatin is reassembled by a combination of recycled parental histones and newly synthesized ones.…”

Section: Resultsmentioning

confidence: 99%

“…Previous analysis using SILAC labeling to differentiate new and old histones as well as methylation kinetics in total chromatin found that modification of new histones is a slow process extending into the next cell cycle (Pesavento et al 2008;Scharf et al 2009;Sweet et al 2010;Xu et al 2012;Zee et al 2012). However, full restoration of the prereplication chromatin state could not be monitored, most likely due to limitations associated with analyzing total chromatin.…”

Section: H2az Domains Are Challenged By the Passage Of Replication Fmentioning

confidence: 98%

“…Histone PTM levels are restored by two distinct modes Histone PTM levels must be maintained across the cell cycle (Probst et al 2009;Margueron and Reinberg 2010;Alabert and Groth 2012;Zee et al 2012). Previous analysis using SILAC labeling to differentiate new and old histones as well as methylation kinetics in total chromatin found that modification of new histones is a slow process extending into the next cell cycle (Pesavento et al 2008;Scharf et al 2009;Sweet et al 2010;Xu et al 2012;Zee et al 2012).…”

Section: H2az Domains Are Challenged By the Passage Of Replication Fmentioning

confidence: 99%

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Two distinct modes for propagation of histone PTMs across the cell cycle

et al. 2015

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Epigenetic states defined by chromatin can be maintained through mitotic cell division. However, it remains unknown how histone-based information is transmitted. Here we combine nascent chromatin capture (NCC) and triple-SILAC (stable isotope labeling with amino acids in cell culture) labeling to track histone modifications and histone variants during DNA replication and across the cell cycle. We show that post-translational modifications (PTMs) are transmitted with parental histones to newly replicated DNA. Di-and trimethylation marks are diluted twofold upon DNA replication, as a consequence of new histone deposition. Importantly, within one cell cycle, all PTMs are restored. In general, new histones are modified to mirror the parental histones. However, H3K9 trimethylation (H3K9me3) and H3K27me3 are propagated by continuous modification of parental and new histones because the establishment of these marks extends over several cell generations. Together, our results reveal how histone marks propagate and demonstrate that chromatin states oscillate within the cell cycle.

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Section: Resultsmentioning

confidence: 99%

Section: H2az Domains Are Challenged By the Passage Of Replication Fmentioning

confidence: 98%

Section: H2az Domains Are Challenged By the Passage Of Replication Fmentioning

confidence: 99%

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Two distinct modes for propagation of histone PTMs across the cell cycle

et al. 2015

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“…Methionine can be converted into S-adenosylmethionine (AdoMet), the only methyl donor in the cell (29). Therefore, heavy-labeled methionine can mark both new methylation events as well as new proteins (9). Incorporation of the supplemented heavylabeled amino acids may not happen immediately because they take time to enter the cell and get incorporated into proteins.…”

Section: Systematic Analysis Of the Distribution Of Histone Ptms Inmentioning

confidence: 99%

“…We and others have reported histone lysine methylation kinetics throughout the human cell cycle (9,10). Although histone PTM inheritance is completed after one cell cycle, important repressive marks like H3K9me3 and H3K27me3 are not fully replenished until the next G 1 phase (9).…”

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confidence: 99%

Preferential Phosphorylation on Old Histones during Early Mitosis in Human Cells

Lin

Yuan

Han

et al. 2016

Journal of Biological Chemistry

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How histone post-translational modifications (PTMs) are inherited through the cell cycle remains poorly understood. Canonical histones are made in the S phase of the cell cycle. Combining mass spectrometry-based technologies and stable isotope labeling by amino acids in cell culture, we question the distribution of multiple histone PTMs on old versus new histones in synchronized human cells. We show that histone PTMs can be grouped into three categories according to their distributions. Most lysine mono-methylation and acetylation PTMs are either symmetrically distributed on old and new histones or are enriched on new histones. In contrast, most di-and tri-methylation PTMs are enriched on old histones, suggesting that the inheritance of different PTMs is regulated distinctly. Intriguingly, old and new histones are distinct in their phosphorylation status during early mitosis in the following three human cell types: HeLa, 293T, and human foreskin fibroblast cells. The mitotic hallmark H3S10ph is predominantly associated with old H3 at early mitosis and becomes symmetric with the progression of mitosis. This same distribution was observed with other mitotic phosphorylation marks, including H3T3/T6ph, H3.1/ 2S28ph, and H1.4S26ph but not S28/S31ph on the H3 variant H3.3. Although H3S10ph often associates with the neighboring Lys-9 di-or tri-methylations, they are not required for the asymmetric distribution of Ser-10 phosphorylation on the same H3 tail. Inhibition of the kinase Aurora B does not change the distribution despite significant reduction of H3S10ph levels. However, K9me2 abundance on the new H3 is significantly reduced after Aurora B inhibition, suggesting a cross-talk between H3S10ph and H3K9me2.In eukaryotes, histone proteins facilitate the packaging of DNA molecules. The DNA double helix wraps around histone octamers to form nucleosomes. A histone octamer contains two copies of each core histone H3, H4, H2A, and H2B. A 5th histone, histone H1, is associated with the linker DNA which lies between the nucleosomes. Canonical histone proteins are cell cycle-dependent and are produced in S phase (1, 2), whereas cell cycle-independent histone variants (e.g. H3.3) are synthesized throughout the cell cycle (3). Histone proteins carry numerous post-translational modifications (PTMs) 3 that are involved in multiple functions such as epigenetic regulation of transcription, DNA damage repair, and cell cycle progression (4, 5). To maintain lineage identity and to guide proper transcription, cells must replicate PTMs from old histones onto new histones at each cell division. Major efforts have been devoted to understanding how histones themselves are transmitted through the DNA replication fork in S phase (6). In principle, the newly deposited nucleosomes could contain entirely old or newly synthesized histone proteins, or a mixture of both. Accumulating evidence suggests that most H3/H4 tetramers remain intact, with the exception of some H3.3/H4 tetramers, indicating that nucleosomes should contain either new or ...

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Site‐specific human histone H3 methylation stability: fast K4me3 turnover

et al. 2014

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We employ stable isotope labelling and quantitative mass spectrometry to track histone methylation stability. We show that H3 trimethyl K9 and K27 are slow to be established on new histones and slow to disappear from old histones, with half-lives of multiple cell divisions. By contrast the transcription-associated marks K4me3 and K36me3 turn over far more rapidly, with half-lives of 6.8 h and 57 h, respectively. Inhibition of demethylases increases K9 and K36 methylation, with K9 showing the largest and most robust increase. We interpret different turnover rates in light of genome-wide localization data and transcription-dependent nucleosome rearrangements proximal to the transcription start site.

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Origins and Formation of Histone Methylation across the Human Cell Cycle

Cited by 80 publications

References 55 publications

Two distinct modes for propagation of histone PTMs across the cell cycle

Two distinct modes for propagation of histone PTMs across the cell cycle

Preferential Phosphorylation on Old Histones during Early Mitosis in Human Cells

Site‐specific human histone H3 methylation stability: fast K4me3 turnover

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