Cohesin-mediated loop anchors confine the locations of human replication origins.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
06 2022
Historique:
received: 31 12 2020
accepted: 26 04 2022
pubmed: 9 6 2022
medline: 25 6 2022
entrez: 8 6 2022
Statut: ppublish

Résumé

DNA replication occurs through an intricately regulated series of molecular events and is fundamental for genome stability

Identifiants

pubmed: 35676475
doi: 10.1038/s41586-022-04803-0
pii: 10.1038/s41586-022-04803-0
pmc: PMC9217744
doi:

Substances chimiques

Cell Cycle Proteins 0
Chromatin 0
Chromosomal Proteins, Non-Histone 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

812-819

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH120269
Pays : United States
Organisme : NHGRI NIH HHS
ID : UM1 HG011536
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG010658
Pays : United States
Organisme : NIMH NIH HHS
ID : DP1 MH129957
Pays : United States
Organisme : NIDA NIH HHS
ID : U01 DA052715
Pays : United States
Organisme : NIDDK NIH HHS
ID : U54 DK107965
Pays : United States
Organisme : NIDDK NIH HHS
ID : U01 DK127405
Pays : United States
Organisme : NHLBI NIH HHS
ID : U01 HL129998
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NIDDK NIH HHS
ID : U54 DK107980
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Bellush, J. M. & Whitehouse, I. DNA replication through a chromatin environment. Philos. Trans. R. Soc. B 372, 20160287 (2017).
doi: 10.1098/rstb.2016.0287
Mechali, M. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 11, 728–738 (2010).
pubmed: 20861881 doi: 10.1038/nrm2976
Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376–380 (2012).
pubmed: 22495300 pmcid: 3356448 doi: 10.1038/nature11082
Nora, E. P. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381–385 (2012).
pubmed: 22495304 pmcid: 3555144 doi: 10.1038/nature11049
Hou, C., Li, L., Qin, Z. S. & Corces, V. G. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol. Cell 48, 471–484 (2012).
pubmed: 23041285 pmcid: 3496039 doi: 10.1016/j.molcel.2012.08.031
Sexton, T. et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458–472 (2012).
pubmed: 22265598 doi: 10.1016/j.cell.2012.01.010
Phillips-Cremins, J. E. et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153, 1281–1295 (2013).
pubmed: 23706625 pmcid: 3712340 doi: 10.1016/j.cell.2013.04.053
Rao, S. S. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014).
pubmed: 25497547 pmcid: 5635824 doi: 10.1016/j.cell.2014.11.021
Krietenstein, N. et al. Ultrastructural details of mammalian chromosome architecture. Mol. Cell 78, 554–565 (2020).
pubmed: 32213324 pmcid: 7222625 doi: 10.1016/j.molcel.2020.03.003
Hsieh, T. S. et al. Resolving the 3D landscape of transcription-linked mammalian chromatin folding. Mol. Cell 78, 539–553 (2020).
pubmed: 32213323 pmcid: 7703524 doi: 10.1016/j.molcel.2020.03.002
Akgol Oksuz, B. et al. Systematic evaluation of chromosome conformation capture assays. Nat. Methods 18, 1046–1055 (2021).
pubmed: 34480151 pmcid: 8446342 doi: 10.1038/s41592-021-01248-7
Fudenberg, G. et al. Formation of chromosomal domains by loop extrusion. Cell Rep. 15, 2038–2049 (2016).
pubmed: 27210764 pmcid: 4889513 doi: 10.1016/j.celrep.2016.04.085
Vian, L. et al. The energetics and physiological impact of cohesin extrusion. Cell 173, 1165–1178 (2018).
pubmed: 29706548 pmcid: 6065110 doi: 10.1016/j.cell.2018.03.072
Sanborn, A. L. et al. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc. Natl Acad. Sci. USA 112, E6456 (2015).
pubmed: 26499245 pmcid: 4664323
Petryk, N. et al. Replication landscape of the human genome. Nat. Commun. 7, 10208 (2016).
pubmed: 26751768 pmcid: 4729899 doi: 10.1038/ncomms10208
Zhao, P. A., Sasaki, T. & Gilbert, D. M. High-resolution Repli-Seq defines the temporal choreography of initiation, elongation and termination of replication in mammalian cells. Genome Biol. 21, 76 (2020).
pubmed: 32209126 pmcid: 7092589 doi: 10.1186/s13059-020-01983-8
Wang, W. et al. Genome-wide mapping of human DNA replication by optical replication mapping supports a stochastic model of eukaryotic replication. Mol. Cell 81, 2975–2988 (2021).
pubmed: 34157308 doi: 10.1016/j.molcel.2021.05.024
Ryba, T. et al. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 20, 761–770 (2010).
pubmed: 20430782 pmcid: 2877573 doi: 10.1101/gr.099655.109
Pope, B. D. et al. Topologically associating domains are stable units of replication-timing regulation. Nature 515, 402–405 (2014).
pubmed: 25409831 pmcid: 4251741 doi: 10.1038/nature13986
Norton, H. K. et al. Detecting hierarchical genome folding with network modularity. Nat. Methods 15, 119–122 (2018).
pubmed: 29334377 pmcid: 6029251 doi: 10.1038/nmeth.4560
Gilgenast, T. G. & Phillips-Cremins, J. E. Systematic evaluation of statistical methods for identifying looping interactions in 5C data. Cell Syst. 8, 197–211 (2019).
pubmed: 30904376 pmcid: 6696950 doi: 10.1016/j.cels.2019.02.006
Fernandez, L. R., Gilgenast, T. G. & Phillips-Cremins, J. E. 3DeFDR: statistical methods for identifying cell type-specific looping interactions in 5C and Hi-C data. Genome Biol. 21, 219 (2020).
pubmed: 32859248 pmcid: 7496221 doi: 10.1186/s13059-020-02061-9
Rao, S. S. P. et al. Cohesin loss eliminates all loop domains. Cell 171, 305–320 (2017).
pubmed: 28985562 pmcid: 5846482 doi: 10.1016/j.cell.2017.09.026
Schwarzer, W. et al. Two independent modes of chromatin organization revealed by cohesin removal. Nature 551, 51–56 (2017).
pubmed: 29094699 pmcid: 5687303 doi: 10.1038/nature24281
Davidson, I. F. et al. Rapid movement and transcriptional re-localization of human cohesin on DNA. EMBO J. 35, 2671–2685 (2016).
pubmed: 27799150 pmcid: 5167347 doi: 10.15252/embj.201695402
Pherson, M., Misulovin, Z., Gause, M. & Dorsett, D. Cohesin occupancy and composition at enhancers and promoters are linked to DNA replication origin proximity in Drosophila. Genome Res. 29, 602–612 (2019).
pubmed: 30796039 pmcid: 6442380 doi: 10.1101/gr.243832.118
Guillou, E. et al. Cohesin organizes chromatin loops at DNA replication factories. Genes Dev. 24, 2812–2822 (2010).
pubmed: 21159821 pmcid: 3003199 doi: 10.1101/gad.608210
de Wit, E. et al. CTCF binding polarity determines chromatin looping. Mol. Cell 60, 676–684 (2015).
pubmed: 26527277 doi: 10.1016/j.molcel.2015.09.023
Tang, Z. et al. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163, 1611–1627 (2015).
pubmed: 26686651 pmcid: 4734140 doi: 10.1016/j.cell.2015.11.024
Besnard, E. et al. Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat. Struct. Mol. Biol. 19, 837–844 (2012).
pubmed: 22751019 doi: 10.1038/nsmb.2339
Li, Y. et al. Transcription-coupled structural dynamics of topologically associating domains regulate replication origin efficiency. Genome Biol. 22, 206 (2021).
pubmed: 34253239 pmcid: 8276456 doi: 10.1186/s13059-021-02424-w
Sequeira-Mendes, J. et al. Transcription initiation activity sets replication origin efficiency in mammalian cells. PLoS Genet. 5, e1000446 (2009).
pubmed: 19360092 pmcid: 2661365 doi: 10.1371/journal.pgen.1000446
Chen, Y. H. et al. Transcription shapes DNA replication initiation and termination in human cells. Nat. Struct. Mol. Biol. 26, 67–77 (2019).
pubmed: 30598550 doi: 10.1038/s41594-018-0171-0
Cayrou, C. et al. The chromatin environment shapes DNA replication origin organization and defines origin classes. Genome Res. 25, 1873–1885 (2015).
pubmed: 26560631 pmcid: 4665008 doi: 10.1101/gr.192799.115
Liu, Y. et al. Transcription shapes DNA replication initiation to preserve genome integrity. Genome Biol. 22, 176 (2021).
pubmed: 34108027 pmcid: 8188667 doi: 10.1186/s13059-021-02390-3
Cadoret, J. C. et al. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc. Natl Acad. Sci. USA 105, 15837–15842 (2008).
pubmed: 18838675 pmcid: 2572913 doi: 10.1073/pnas.0805208105
Oldach, P. & Nieduszynski, C. A. Cohesin-mediated genome architecture does not define DNA replication timing domains. Genes 10, 196 (2019).
pmcid: 6471042 doi: 10.3390/genes10030196
Cremer, M. et al. Cohesin depleted cells rebuild functional nuclear compartments after endomitosis. Nat. Commun. 11, 6146 (2020).
pubmed: 33262376 pmcid: 7708632 doi: 10.1038/s41467-020-19876-6
Sima, J. et al. Identifying cis elements for spatiotemporal control of mammalian DNA replication. Cell 176, 816–830(2019).
pubmed: 30595451 doi: 10.1016/j.cell.2018.11.036
Hiratani, I. et al. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6, e245 (2008).
pubmed: 18842067 pmcid: 2561079 doi: 10.1371/journal.pbio.0060245
Haarhuis, J. H. I. et al. The cohesin release factor WAPL restricts chromatin loop extension. Cell 169, 693–707 (2017).
pubmed: 28475897 pmcid: 5422210 doi: 10.1016/j.cell.2017.04.013
Yesbolatova, A. et al. The auxin-inducible degron 2 technology provides sharp degradation control in yeast, mammalian cells, and mice. Nat. Commun. 11, 5701 (2020).
pubmed: 33177522 pmcid: 7659001 doi: 10.1038/s41467-020-19532-z
Zhang, D. et al. Alteration of genome folding via contact domain boundary insertion. Nat. Genet. 52, 1076–1087 (2020).
pubmed: 32868908 pmcid: 7541666 doi: 10.1038/s41588-020-0680-8
Dimitrova, D. S., Prokhorova, T. A., Blow, J. J., Todorov, I. T. & Gilbert, D. M. Mammalian nuclei become licensed for DNA replication during late telophase. J. Cell Sci. 115, 51–59 (2002).
pubmed: 11801723 doi: 10.1242/jcs.115.1.51
Ryu, M. J. et al. Direct interaction between cohesin complex and DNA replication machinery. Biochem. Biophys. Res. Commun. 341, 770–775 (2006).
pubmed: 16438930 doi: 10.1016/j.bbrc.2006.01.029
Gros, J. et al. Post-licensing specification of eukaryotic replication origins by facilitated Mcm2-7 sliding along DNA. Mol. Cell 60, 797–807 (2015).
pubmed: 26656162 pmcid: 4680849 doi: 10.1016/j.molcel.2015.10.022
Powell, S. K. et al. Dynamic loading and redistribution of the Mcm2-7 helicase complex through the cell cycle. EMBO J. 34, 531–543 (2015).
pubmed: 25555795 pmcid: 4331006 doi: 10.15252/embj.201488307
Sasaki, T. et al. The Chinese hamster dihydrofolate reductase replication origin decision point follows activation of transcription and suppresses initiation of replication within transcription units. Mol. Cell. Biol. 26, 1051–1062 (2006).
pubmed: 16428457 pmcid: 1347040 doi: 10.1128/MCB.26.3.1051-1062.2006
Dequeker, B. J. H. et al. MCM complexes are barriers that restrict cohesin-mediated loop extrusion. Nature https://doi.org/10.1038/s41586-022-04730-0 (2022).
Nagano, T. et al. Cell-cycle dynamics of chromosomal organization at single-cell resolution. Nature 547, 61–67 (2017).
pubmed: 28682332 pmcid: 5567812 doi: 10.1038/nature23001

Auteurs

Daniel J Emerson (DJ)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Peiyao A Zhao (PA)

Department of Biological Science, Florida State University, Tallahassee, FL, USA.

Ashley L Cook (AL)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

R Jordan Barnett (RJ)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Kyle N Klein (KN)

Department of Biological Science, Florida State University, Tallahassee, FL, USA.

Dalila Saulebekova (D)

Institut Curie, PSL Research University, CNRS UMR3244, Dynamics of Genetic Information, Sorbonne Université, Paris, France.

Chunmin Ge (C)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Linda Zhou (L)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Zoltan Simandi (Z)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Miriam K Minsk (MK)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Katelyn R Titus (KR)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Weitao Wang (W)

Institut Curie, PSL Research University, CNRS UMR3244, Dynamics of Genetic Information, Sorbonne Université, Paris, France.

Wanfeng Gong (W)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Di Zhang (D)

Children's Hospital of Pennsylvania, Philadelphia, PA, USA.

Liyan Yang (L)

University of Massachusetts Chan Medical School, Worcester, MA, USA.

Sergey V Venev (SV)

University of Massachusetts Chan Medical School, Worcester, MA, USA.

Johan H Gibcus (JH)

University of Massachusetts Chan Medical School, Worcester, MA, USA.

Hongbo Yang (H)

Department of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA.

Takayo Sasaki (T)

San Diego Biomedical Research Institute, San Diego, CA, USA.

Masato T Kanemaki (MT)

Department of Chromosome Science, National Institute of Genetics, Research Organization of Information and Systems (ROIS), Mishima, Japan.
Department of Genetics, The Graduate University for Advanced Studies (Sokendai), Mishima, Japan.

Feng Yue (F)

Department of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA.

Job Dekker (J)

University of Massachusetts Chan Medical School, Worcester, MA, USA.
Howard Hughes Medical Institute, Chevy Chase, MD, USA.

Chun-Long Chen (CL)

Institut Curie, PSL Research University, CNRS UMR3244, Dynamics of Genetic Information, Sorbonne Université, Paris, France.

David M Gilbert (DM)

Department of Biological Science, Florida State University, Tallahassee, FL, USA.
San Diego Biomedical Research Institute, San Diego, CA, USA.

Jennifer E Phillips-Cremins (JE)

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA. jcremins@seas.upenn.edu.
Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. jcremins@seas.upenn.edu.
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. jcremins@seas.upenn.edu.
New York Stem Cell Foundation Robertson Investigator, New York, NY, USA. jcremins@seas.upenn.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH