Histone H4K20 methylation mediated chromatin compaction threshold ensures genome integrity by limiting DNA replication licensing

The decompaction and re-establishment of chromatin organization immediately after mitosis is essential for genome regulation. Mechanisms underlying chromatin structure control in daughter cells are not fully understood. Here we show that a chromatin compaction threshold in cells exiting mitosis ensu...

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Published inNature communications Vol. 9; no. 1; pp. 3704 - 11
Main Authors Shoaib, Muhammad, Walter, David, Gillespie, Peter J., Izard, Fanny, Fahrenkrog, Birthe, Lleres, David, Lerdrup, Mads, Johansen, Jens Vilstrup, Hansen, Klaus, Julien, Eric, Blow, J. Julian, Sørensen, Claus S.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 12.09.2018
Nature Publishing Group
Nature Portfolio
Subjects
13/1
13/106
13/31
13/89
14/19
14/28
14/33
45/23
631/337/100/101
631/80/458/1648
Biochemistry, Molecular Biology
Cell cycle
Cell Line, Tumor
Chromatin
Chromatin - genetics
Chromatin - metabolism
Compaction
Constraining
Deoxyribonucleic acid
DNA
DNA biosynthesis
DNA Damage
DNA Damage - genetics
DNA Damage - physiology
DNA methylation
DNA Replication
DNA Replication - genetics
DNA Replication - physiology
Flow Cytometry
G1 phase
Gene expression
Genomes
Genomics
Histone H4
Histones
Histones - genetics
Histones - metabolism
Humanities and Social Sciences
Humans
Integrity
Licenses
Licensing
Life Sciences
Lysine
Methylation
Microscopy, Fluorescence
Mitosis
multidisciplinary
Origin recognition complex
Overloading
Replication
RNA, Small Interfering
RNA, Small Interfering - genetics
Science
Science (multidisciplinary)
Single-stranded DNA
Online AccessGet full text

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Abstract The decompaction and re-establishment of chromatin organization immediately after mitosis is essential for genome regulation. Mechanisms underlying chromatin structure control in daughter cells are not fully understood. Here we show that a chromatin compaction threshold in cells exiting mitosis ensures genome integrity by limiting replication licensing in G1 phase. Upon mitotic exit, chromatin relaxation is controlled by SET8-dependent methylation of histone H4 on lysine 20. In the absence of either SET8 or H4K20 residue, substantial genome-wide chromatin decompaction occurs allowing excessive loading of the origin recognition complex (ORC) in the daughter cells. ORC overloading stimulates aberrant recruitment of the MCM2-7 complex that promotes single-stranded DNA formation and DNA damage. Restoring chromatin compaction restrains excess replication licensing and loss of genome integrity. Our findings identify a cell cycle-specific mechanism whereby fine-tuned chromatin relaxation suppresses excessive detrimental replication licensing and maintains genome integrity at the cellular transition from mitosis to G1 phase. Cell cycle and replication need to be tightly regulated to ensure genome stability in mammalian cells. Here the authors provide a link between chromatin structure and DNA replication regulation by showing that chromatin compaction limits replication licensing thereby promoting genome integrity.
AbstractList The decompaction and re-establishment of chromatin organization immediately after mitosis is essential for genome regulation. Mechanisms underlying chromatin structure control in daughter cells are not fully understood. Here we show that a chromatin compaction threshold in cells exiting mitosis ensures genome integrity by limiting replication licensing in G1 phase. Upon mitotic exit, chromatin relaxation is controlled by SET8-dependent methylation of histone H4 on lysine 20. In the absence of either SET8 or H4K20 residue, substantial genome-wide chromatin decompaction occurs allowing excessive loading of the origin recognition complex (ORC) in the daughter cells. ORC overloading stimulates aberrant recruitment of the MCM2-7 complex that promotes single-stranded DNA formation and DNA damage. Restoring chromatin compaction restrains excess replication licensing and loss of genome integrity. Our findings identify a cell cycle-specific mechanism whereby fine-tuned chromatin relaxation suppresses excessive detrimental replication licensing and maintains genome integrity at the cellular transition from mitosis to G1 phase.
The decompaction and re-establishment of chromatin organization immediately after mitosis is essential for genome regulation. Mechanisms underlying chromatin structure control in daughter cells are not fully understood. Here we show that a chromatin compaction threshold in cells exiting mitosis ensures genome integrity by limiting replication licensing in G1 phase. Upon mitotic exit, chromatin relaxation is controlled by SET8-dependent methylation of histone H4 on lysine 20. In the absence of either SET8 or H4K20 residue, substantial genome-wide chromatin decompaction occurs allowing excessive loading of the origin recognition complex (ORC) in the daughter cells. ORC overloading stimulates aberrant recruitment of the MCM2-7 complex that promotes single-stranded DNA formation and DNA damage. Restoring chromatin compaction restrains excess replication licensing and loss of genome integrity. Our findings identify a cell cycle-specific mechanism whereby fine-tuned chromatin relaxation suppresses excessive detrimental replication licensing and maintains genome integrity at the cellular transition from mitosis to G1 phase.The decompaction and re-establishment of chromatin organization immediately after mitosis is essential for genome regulation. Mechanisms underlying chromatin structure control in daughter cells are not fully understood. Here we show that a chromatin compaction threshold in cells exiting mitosis ensures genome integrity by limiting replication licensing in G1 phase. Upon mitotic exit, chromatin relaxation is controlled by SET8-dependent methylation of histone H4 on lysine 20. In the absence of either SET8 or H4K20 residue, substantial genome-wide chromatin decompaction occurs allowing excessive loading of the origin recognition complex (ORC) in the daughter cells. ORC overloading stimulates aberrant recruitment of the MCM2-7 complex that promotes single-stranded DNA formation and DNA damage. Restoring chromatin compaction restrains excess replication licensing and loss of genome integrity. Our findings identify a cell cycle-specific mechanism whereby fine-tuned chromatin relaxation suppresses excessive detrimental replication licensing and maintains genome integrity at the cellular transition from mitosis to G1 phase.
The decompaction and re-establishment of chromatin organization immediately after mitosis is essential for genome regulation. Mechanisms underlying chromatin structure control in daughter cells are not fully understood. Here we show that a chromatin compaction threshold in cells exiting mitosis ensures genome integrity by limiting replication licensing in G1 phase. Upon mitotic exit, chromatin relaxation is controlled by SET8-dependent methylation of histone H4 on lysine 20. In the absence of either SET8 or H4K20 residue, substantial genome-wide chromatin decompaction occurs allowing excessive loading of the origin recognition complex (ORC) in the daughter cells. ORC overloading stimulates aberrant recruitment of the MCM2-7 complex that promotes single-stranded DNA formation and DNA damage. Restoring chromatin compaction restrains excess replication licensing and loss of genome integrity. Our findings identify a cell cycle-specific mechanism whereby fine-tuned chromatin relaxation suppresses excessive detrimental replication licensing and maintains genome integrity at the cellular transition from mitosis to G1 phase. Cell cycle and replication need to be tightly regulated to ensure genome stability in mammalian cells. Here the authors provide a link between chromatin structure and DNA replication regulation by showing that chromatin compaction limits replication licensing thereby promoting genome integrity.
Cell cycle and replication need to be tightly regulated to ensure genome stability in mammalian cells. Here the authors provide a link between chromatin structure and DNA replication regulation by showing that chromatin compaction limits replication licensing thereby promoting genome integrity.
ArticleNumber 3704
Author Fahrenkrog, Birthe
Shoaib, Muhammad
Sørensen, Claus S.
Lleres, David
Lerdrup, Mads
Gillespie, Peter J.
Izard, Fanny
Julien, Eric
Walter, David
Blow, J. Julian
Johansen, Jens Vilstrup
Hansen, Klaus
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30209253$$D View this record in MEDLINE/PubMed
https://hal.umontpellier.fr/hal-02292291$$DView record in HAL
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Issue 1
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Snippet The decompaction and re-establishment of chromatin organization immediately after mitosis is essential for genome regulation. Mechanisms underlying chromatin...
Cell cycle and replication need to be tightly regulated to ensure genome stability in mammalian cells. Here the authors provide a link between chromatin...
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StartPage 3704
SubjectTerms 13/1
13/106
13/31
13/89
14/19
14/28
14/33
45/23
631/337/100/101
631/80/458/1648
Biochemistry, Molecular Biology
Cell cycle
Cell Line, Tumor
Chromatin
Chromatin - genetics
Chromatin - metabolism
Compaction
Constraining
Deoxyribonucleic acid
DNA
DNA biosynthesis
DNA Damage
DNA Damage - genetics
DNA Damage - physiology
DNA methylation
DNA Replication
DNA Replication - genetics
DNA Replication - physiology
Flow Cytometry
G1 phase
Gene expression
Genomes
Genomics
Histone H4
Histones
Histones - genetics
Histones - metabolism
Humanities and Social Sciences
Humans
Integrity
Licenses
Licensing
Life Sciences
Lysine
Methylation
Microscopy, Fluorescence
Mitosis
multidisciplinary
Origin recognition complex
Overloading
Replication
RNA, Small Interfering
RNA, Small Interfering - genetics
Science
Science (multidisciplinary)
Single-stranded DNA
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Title Histone H4K20 methylation mediated chromatin compaction threshold ensures genome integrity by limiting DNA replication licensing
URI https://link.springer.com/article/10.1038/s41467-018-06066-8
https://www.ncbi.nlm.nih.gov/pubmed/30209253
https://www.proquest.com/docview/2102903375
https://www.proquest.com/docview/2103679183
https://hal.umontpellier.fr/hal-02292291
https://pubmed.ncbi.nlm.nih.gov/PMC6135857
https://doaj.org/article/8099256713994c5ea367ade824604648
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