Embryonic Stem Cell Specific "master" Replication Origins at the Heart of the Loss of Pluripotency

Overview

Journal PLoS Comput Biol

Specialty Biology

Date 2015 Feb 7

PMID 25658386

Citations 11

Authors

Hanna Julienne

Benjamin Audit

Alain Arneodo

Affiliations

Soon will be listed here.

Abstract

Epigenetic regulation of the replication program during mammalian cell differentiation remains poorly understood. We performed an integrative analysis of eleven genome-wide epigenetic profiles at 100 kb resolution of Mean Replication Timing (MRT) data in six human cell lines. Compared to the organization in four chromatin states shared by the five somatic cell lines, embryonic stem cell (ESC) line H1 displays (i) a gene-poor but highly dynamic chromatin state (EC4) associated to histone variant H2AZ rather than a HP1-associated heterochromatin state (C4) and (ii) a mid-S accessible chromatin state with bivalent gene marks instead of a polycomb-repressed heterochromatin state. Plastic MRT regions (≲ 20% of the genome) are predominantly localized at the borders of U-shaped timing domains. Whereas somatic-specific U-domain borders are gene-dense GC-rich regions, 31.6% of H1-specific U-domain borders are early EC4 regions enriched in pluripotency transcription factors NANOG and OCT4 despite being GC poor and gene deserts. Silencing of these ESC-specific "master" replication initiation zones during differentiation corresponds to a loss of H2AZ and an enrichment in H3K9me3 mark characteristic of late replicating C4 heterochromatin. These results shed a new light on the epigenetically regulated global chromatin reorganization that underlies the loss of pluripotency and lineage commitment.

Citing Articles

The Role of the Histone Variant H2A.Z in Metazoan Development.

Dijkwel Y, Tremethick D J Dev Biol. 2022; 10(3).

PMID: 35893123 PMC: 9326617. DOI: 10.3390/jdb10030028.

Nuclear-localized, iron-bound superoxide dismutase-2 antagonizes epithelial lineage programs to promote stemness of breast cancer cells via a histone demethylase activity.

Coelho D, Palma F, Paviani V, He C, Danes J, Huang Y Proc Natl Acad Sci U S A. 2022; 119(29):e2110348119.

PMID: 35858297 PMC: 9303987. DOI: 10.1073/pnas.2110348119.

Low Replicative Stress Triggers Cell-Type Specific Inheritable Advanced Replication Timing.

Courtot L, Bournique E, Maric C, Guitton-Sert L, Madrid-Mencia M, Pancaldi V Int J Mol Sci. 2021; 22(9).

PMID: 34066960 PMC: 8125030. DOI: 10.3390/ijms22094959.

Evolution of replication origins in vertebrate genomes: rapid turnover despite selective constraints.

Massip F, Laurent M, Brossas C, Fernandez-Justel J, Gomez M, Prioleau M Nucleic Acids Res. 2019; 47(10):5114-5125.

PMID: 30916335 PMC: 6547456. DOI: 10.1093/nar/gkz182.

Developmental and cancer-associated plasticity of DNA replication preferentially targets GC-poor, lowly expressed and late-replicating regions.

Wu X, Kabalane H, Kahli M, Petryk N, Laperrousaz B, Jaszczyszyn Y Nucleic Acids Res. 2018; 46(19):10157-10172.

PMID: 30189101 PMC: 6212843. DOI: 10.1093/nar/gky797.

References

Lemaitre C, Zaghloul L, Sagot M, Gautier C, Arneodo A, Tannier E . Analysis of fine-scale mammalian evolutionary breakpoints provides new insight into their relation to genome organisation. BMC Genomics. 2009; 10:335. PMC: 2722678. DOI: 10.1186/1471-2164-10-335. View

Audit B, Baker A, Chen C, Rappailles A, Guilbaud G, Julienne H . Multiscale analysis of genome-wide replication timing profiles using a wavelet-based signal-processing algorithm. Nat Protoc. 2012; 8(1):98-110. DOI: 10.1038/nprot.2012.145. View

Karnani N, Taylor C, Malhotra A, Dutta A . Pan-S replication patterns and chromosomal domains defined by genome-tiling arrays of ENCODE genomic areas. Genome Res. 2007; 17(6):865-76. PMC: 1891345. DOI: 10.1101/gr.5427007. View

Huvet M, Nicolay S, Touchon M, Audit B, dAubenton-Carafa Y, Arneodo A . Human gene organization driven by the coordination of replication and transcription. Genome Res. 2007; 17(9):1278-85. PMC: 1950896. DOI: 10.1101/gr.6533407. View

Sexton T, Schober H, Fraser P, Gasser S . Gene regulation through nuclear organization. Nat Struct Mol Biol. 2007; 14(11):1049-55. DOI: 10.1038/nsmb1324. View

Boyer L, Lee T, Cole M, Johnstone S, Levine S, Zucker J . Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005; 122(6):947-56. PMC: 3006442. DOI: 10.1016/j.cell.2005.08.020. View

Zink D, BORNFLETH H, Visser A, Cremer C, Cremer T . Organization of early and late replicating DNA in human chromosome territories. Exp Cell Res. 1999; 247(1):176-88. DOI: 10.1006/excr.1998.4311. View

Liu T, Rechtsteiner A, Egelhofer T, Vielle A, Latorre I, Cheung M . Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res. 2010; 21(2):227-36. PMC: 3032926. DOI: 10.1101/gr.115519.110. View

Cayrou C, Coulombe P, Puy A, Rialle S, Kaplan N, Segal E . New insights into replication origin characteristics in metazoans. Cell Cycle. 2012; 11(4):658-67. PMC: 3318102. DOI: 10.4161/cc.11.4.19097. View

10.

Bickmore W, van Steensel B . Genome architecture: domain organization of interphase chromosomes. Cell. 2013; 152(6):1270-84. DOI: 10.1016/j.cell.2013.02.001. View

11.

Tardat M, Brustel J, Kirsh O, Lefevbre C, Callanan M, Sardet C . The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat Cell Biol. 2010; 12(11):1086-93. DOI: 10.1038/ncb2113. View

12.

Chakalova L, Debrand E, Mitchell J, Osborne C, Fraser P . Replication and transcription: shaping the landscape of the genome. Nat Rev Genet. 2005; 6(9):669-77. DOI: 10.1038/nrg1673. View

13.

Ryba T, Hiratani I, Sasaki T, Battaglia D, Kulik M, Zhang J . Replication timing: a fingerprint for cell identity and pluripotency. PLoS Comput Biol. 2011; 7(10):e1002225. PMC: 3197641. DOI: 10.1371/journal.pcbi.1002225. View

14.

Schwaiger M, Stadler M, Bell O, Kohler H, Oakeley E, Schubeler D . Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev. 2009; 23(5):589-601. PMC: 2658520. DOI: 10.1101/gad.511809. View

15.

Moindrot B, Audit B, Klous P, Baker A, Thermes C, de Laat W . 3D chromatin conformation correlates with replication timing and is conserved in resting cells. Nucleic Acids Res. 2012; 40(19):9470-81. PMC: 3479194. DOI: 10.1093/nar/gks736. View

16.

Raghuraman M, Winzeler E, Collingwood D, Hunt S, Wodicka L, Conway A . Replication dynamics of the yeast genome. Science. 2001; 294(5540):115-21. DOI: 10.1126/science.294.5540.115. View

17.

Vaillant C, Audit B, Arneodo A . Experiments confirm the influence of genome long-range correlations on nucleosome positioning. Phys Rev Lett. 2008; 99(21):218103. DOI: 10.1103/PhysRevLett.99.218103. View

18.

Schoenherr C, Anderson D . The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science. 1995; 267(5202):1360-3. DOI: 10.1126/science.7871435. View

19.

Audit B, Zaghloul L, Vaillant C, Chevereau G, dAubenton-Carafa Y, Thermes C . Open chromatin encoded in DNA sequence is the signature of 'master' replication origins in human cells. Nucleic Acids Res. 2009; 37(18):6064-75. PMC: 2764438. DOI: 10.1093/nar/gkp631. View

20.

Ho L, Crabtree G . Chromatin remodelling during development. Nature. 2010; 463(7280):474-84. PMC: 3060774. DOI: 10.1038/nature08911. View