Replication stress interferes with histone recycling and predeposition marking of new histones

Zuzana Jasencakova; Annette N D Scharf; Katrine Ask; Armelle Corpet; Axel Imhof; Geneviève Almouzni; Anja Groth

doi:10.1016/j.molcel.2010.01.033

Replication stress interferes with histone recycling and predeposition marking of new histones

Zuzana Jasencakova, Annette N D Scharf, Katrine Ask, Armelle Corpet, Axel Imhof, Geneviève Almouzni, Anja Groth

Research output: Contribution to journal › Journal article › Research › peer-review

225 Citations (Scopus)

Abstract

To restore chromatin on new DNA during replication, recycling of histones evicted ahead of the fork is combined with new histone deposition. The Asf1 histone chaperone, which buffers excess histones under stress, is a key player in this process. Yet how histones handled by human Asf1 are modified remains unclear. Here we identify marks on histones H3-H4 bound to Asf1 and changes induced upon replication stress. In S phase, distinct cytosolic and nuclear Asf1b complexes show ubiquitous H4K5K12diAc and heterogeneous H3 marks, including K9me1, K14ac, K18ac, and K56ac. Upon acute replication arrest, the predeposition mark H3K9me1 and modifications typical of chromatin accumulate in Asf1 complexes. In parallel, ssDNA is generated at replication sites, consistent with evicted histones being trapped with Asf1. During recovery, histones stored with Asf1 are rapidly used as replication resumes. This shows that replication stress interferes with predeposition marking and histone recycling with potential impact on epigenetic stability.

Original language	English
Journal	Molecular Cell
Volume	37
Issue number	5
Pages (from-to)	736-43
Number of pages	8
ISSN	1097-2765
DOIs	https://doi.org/10.1016/j.molcel.2010.01.033
Publication status	Published - 12 Mar 2010

Keywords

Acetylation
Blotting, Western
Cell Cycle Proteins
Cell Nucleus
Chromatin Assembly and Disassembly
Cytosol
DNA Replication
DNA, Single-Stranded
Hela Cells
Histones
Humans
Methylation
Nuclear Proteins
Nucleosomes
Protein Binding
Protein Processing, Post-Translational
S Phase
Stress, Physiological
Tandem Mass Spectrometry
Time Factors
Transfection

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10.1016/j.molcel.2010.01.033

Cite this

@article{dc217830a15411df928f000ea68e967b,

title = "Replication stress interferes with histone recycling and predeposition marking of new histones",

abstract = "To restore chromatin on new DNA during replication, recycling of histones evicted ahead of the fork is combined with new histone deposition. The Asf1 histone chaperone, which buffers excess histones under stress, is a key player in this process. Yet how histones handled by human Asf1 are modified remains unclear. Here we identify marks on histones H3-H4 bound to Asf1 and changes induced upon replication stress. In S phase, distinct cytosolic and nuclear Asf1b complexes show ubiquitous H4K5K12diAc and heterogeneous H3 marks, including K9me1, K14ac, K18ac, and K56ac. Upon acute replication arrest, the predeposition mark H3K9me1 and modifications typical of chromatin accumulate in Asf1 complexes. In parallel, ssDNA is generated at replication sites, consistent with evicted histones being trapped with Asf1. During recovery, histones stored with Asf1 are rapidly used as replication resumes. This shows that replication stress interferes with predeposition marking and histone recycling with potential impact on epigenetic stability.",

keywords = "Acetylation, Blotting, Western, Cell Cycle Proteins, Cell Nucleus, Chromatin Assembly and Disassembly, Cytosol, DNA Replication, DNA, Single-Stranded, Hela Cells, Histones, Humans, Methylation, Nuclear Proteins, Nucleosomes, Protein Binding, Protein Processing, Post-Translational, S Phase, Stress, Physiological, Tandem Mass Spectrometry, Time Factors, Transfection",

author = "Zuzana Jasencakova and Scharf, {Annette N D} and Katrine Ask and Armelle Corpet and Axel Imhof and Genevi{\`e}ve Almouzni and Anja Groth",

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T1 - Replication stress interferes with histone recycling and predeposition marking of new histones

AU - Jasencakova, Zuzana

AU - Scharf, Annette N D

AU - Ask, Katrine

AU - Corpet, Armelle

AU - Imhof, Axel

AU - Almouzni, Geneviève

AU - Groth, Anja

N1 - Paper id:: 10.1016/j.molcel.2010.01.033

PY - 2010/3/12

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N2 - To restore chromatin on new DNA during replication, recycling of histones evicted ahead of the fork is combined with new histone deposition. The Asf1 histone chaperone, which buffers excess histones under stress, is a key player in this process. Yet how histones handled by human Asf1 are modified remains unclear. Here we identify marks on histones H3-H4 bound to Asf1 and changes induced upon replication stress. In S phase, distinct cytosolic and nuclear Asf1b complexes show ubiquitous H4K5K12diAc and heterogeneous H3 marks, including K9me1, K14ac, K18ac, and K56ac. Upon acute replication arrest, the predeposition mark H3K9me1 and modifications typical of chromatin accumulate in Asf1 complexes. In parallel, ssDNA is generated at replication sites, consistent with evicted histones being trapped with Asf1. During recovery, histones stored with Asf1 are rapidly used as replication resumes. This shows that replication stress interferes with predeposition marking and histone recycling with potential impact on epigenetic stability.

AB - To restore chromatin on new DNA during replication, recycling of histones evicted ahead of the fork is combined with new histone deposition. The Asf1 histone chaperone, which buffers excess histones under stress, is a key player in this process. Yet how histones handled by human Asf1 are modified remains unclear. Here we identify marks on histones H3-H4 bound to Asf1 and changes induced upon replication stress. In S phase, distinct cytosolic and nuclear Asf1b complexes show ubiquitous H4K5K12diAc and heterogeneous H3 marks, including K9me1, K14ac, K18ac, and K56ac. Upon acute replication arrest, the predeposition mark H3K9me1 and modifications typical of chromatin accumulate in Asf1 complexes. In parallel, ssDNA is generated at replication sites, consistent with evicted histones being trapped with Asf1. During recovery, histones stored with Asf1 are rapidly used as replication resumes. This shows that replication stress interferes with predeposition marking and histone recycling with potential impact on epigenetic stability.

KW - Acetylation

KW - Blotting, Western

KW - Cell Cycle Proteins

KW - Cell Nucleus

KW - Chromatin Assembly and Disassembly

KW - Cytosol

KW - DNA Replication

KW - DNA, Single-Stranded

KW - Hela Cells

KW - Histones

KW - Humans

KW - Methylation

KW - Nuclear Proteins

KW - Nucleosomes

KW - Protein Binding

KW - Protein Processing, Post-Translational

KW - S Phase

KW - Stress, Physiological

KW - Tandem Mass Spectrometry

KW - Time Factors

KW - Transfection

U2 - 10.1016/j.molcel.2010.01.033

DO - 10.1016/j.molcel.2010.01.033

M3 - Journal article

C2 - 20227376

VL - 37

SP - 736

EP - 743

JO - Molecular Cell

JF - Molecular Cell

SN - 1097-2765

IS - 5

ER -