Embryonic genome instability upon DNA replication timing program emergence.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
28 Aug 2024
28 Aug 2024
Historique:
received:
01
03
2023
accepted:
17
07
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
28
8
2024
Statut:
aheadofprint
Résumé
Faithful DNA replication is essential for genome integrity
Identifiants
pubmed: 39198647
doi: 10.1038/s41586-024-07841-y
pii: 10.1038/s41586-024-07841-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Hu, Y. & Stillman, B. Origins of DNA replication in eukaryotes. Mol. Cell 83, 352–372 (2023).
pubmed: 36640769
doi: 10.1016/j.molcel.2022.12.024
Fragkos, M., Ganier, O., Coulombe, P. & Méchali, M. DNA replication origin activation in space and time. Nat. Rev. Mol. Cell Biol. 16, 360–374 (2015).
pubmed: 25999062
doi: 10.1038/nrm4002
Gilbert, D. M. Making sense of eukaryotic DNA replication origins. Science 294, 96–100 (2001).
pubmed: 11588251
pmcid: 1255916
doi: 10.1126/science.1061724
Alver, R. C., Chadha, G. S. & Blow, J. J. The contribution of dormant origins to genome stability: from cell biology to human genetics. DNA Repair 19, 182–189 (2014).
pubmed: 24767947
pmcid: 4065331
doi: 10.1016/j.dnarep.2014.03.012
Kermi, C., Aze, A. & Maiorano, D. Preserving genome integrity during the early embryonic DNA replication cycles. Genes 10, 398 (2019).
pubmed: 31137726
pmcid: 6563053
doi: 10.3390/genes10050398
Mashiko, D. et al. Chromosome segregation error during early cleavage in mouse pre-implantation embryo does not necessarily cause developmental failure after blastocyst stage. Sci. Rep. 10, 854 (2020).
pubmed: 31965014
pmcid: 6972754
doi: 10.1038/s41598-020-57817-x
Vázquez-Diez, C. & FitzHarris, G. Causes and consequences of chromosome segregation error in preimplantation embryos. Reproduction 155, R63–R76 (2018).
pubmed: 29109119
doi: 10.1530/REP-17-0569
Vanneste, E. et al. Chromosome instability is common in human cleavage-stage embryos. Nat. Med. 15, 577–583 (2009).
pubmed: 19396175
doi: 10.1038/nm.1924
Palmerola, K. L. et al. Replication stress impairs chromosome segregation and preimplantation development in human embryos. Cell 185, 2988–3007.e20 (2022).
pubmed: 35858625
doi: 10.1016/j.cell.2022.06.028
Takahashi, S. et al. Genome-wide stability of the DNA replication program in single mammalian cells. Nat. Genet. 51, 529–540 (2019).
pubmed: 30804559
doi: 10.1038/s41588-019-0347-5
Dileep, V. & Gilbert, D. M. Single-cell replication profiling to measure stochastic variation in mammalian replication timing. Nat. Commun. 9, 427 (2018).
pubmed: 29382831
pmcid: 5789892
doi: 10.1038/s41467-017-02800-w
Vouzas, A. E. & Gilbert, D. M. Mammalian DNA replication timing. Cold Spring Harb. Perspect. Biol. 13, a040162 (2021).
pubmed: 33558366
pmcid: 8247564
doi: 10.1101/cshperspect.a040162
Hiratani, I. & Takahashi, S. DNA replication timing enters the single-cell era. Genes 10, 221 (2019).
pubmed: 30884743
pmcid: 6470765
doi: 10.3390/genes10030221
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
Miura, H. et al. Single-cell DNA replication profiling identifies spatiotemporal developmental dynamics of chromosome organization. Nat. Genet. 51, 1356–1368 (2019).
pubmed: 31406346
doi: 10.1038/s41588-019-0474-z
Miura, H. et al. Mapping replication timing domains genome wide in single mammalian cells with single-cell DNA replication sequencing. Nat. Protoc. 15, 4058–4100 (2020).
pubmed: 33230331
doi: 10.1038/s41596-020-0378-5
Du, Z. et al. Allelic reprogramming of 3D chromatin architecture during early mammalian development. Nature 547, 232–235 (2017).
pubmed: 28703188
doi: 10.1038/nature23263
Ke, Y. et al. 3D Chromatin structures of mature gametes and structural reprogramming during mammalian embryogenesis. Cell 170, 367–381 (2017).
pubmed: 28709003
doi: 10.1016/j.cell.2017.06.029
Flyamer, I. M. et al. Single-cell Hi-C reveals unique chromatin reorganization at oocyte-tozygote transition. Nature 544, 110–114 (2017).
pubmed: 28355183
pmcid: 5639698
doi: 10.1038/nature21711
Dileep, V. et al. Topologically associating domains and their long-range contacts are established during early G1 coincident with the establishment of the replication timing program. Genome Res. 25, 1104–1113 (2015).
pubmed: 25995270
pmcid: 4509995
doi: 10.1101/gr.183699.114
Ladstätter, S. & Tachibana, K. Genomic insights into chromatin reprogramming to totipotency in embryos. J. Cell Biol. 218, 70–82 (2019).
pubmed: 30257850
pmcid: 6314560
doi: 10.1083/jcb.201807044
Fu, X., Zhang, C. & Zhang, Y. Epigenetic regulation of mouse preimplantation embryo development. Curr. Opin. Genet. Dev. 64, 13–20 (2020).
pubmed: 32563750
pmcid: 7641911
doi: 10.1016/j.gde.2020.05.015
Martin, C. et al. Genome restructuring in mouse embryos during reprogramming and early development. Dev. Biol. 292, 317–332 (2006).
pubmed: 16680825
doi: 10.1016/j.ydbio.2006.01.009
Chen, M. et al. Chromatin architecture reorganization in murine somatic cell nuclear transfer embryos. Nat. Commun. 11, 1813 (2020).
pubmed: 32286279
pmcid: 7156422
doi: 10.1038/s41467-020-15607-z
Conti, C. et al. Replication fork velocities at adjacent replication origins are coordinately modified during DNA replication in human cells. Mol. Biol. Cell 18, 3059–3067 (2007).
pubmed: 17522385
pmcid: 1949372
doi: 10.1091/mbc.e06-08-0689
Takebayashi, S.-I. et al. The temporal order of DNA replication shaped by mammalian DNA methyltransferases. Cells 10, 266 (2021).
pubmed: 33572832
pmcid: 7911666
doi: 10.3390/cells10020266
Nakatani, T. et al. DNA replication fork speed underlies cell fate changes and promotes reprogramming. Nat. Genet. 54, 318–327 (2022).
pubmed: 35256805
pmcid: 8920892
doi: 10.1038/s41588-022-01023-0
Cremer, T. & Cremer, C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2, 292–301 (2001).
pubmed: 11283701
doi: 10.1038/35066075
Dimitrova, D. S. & Gilbert, D. M. Temporally coordinated assembly and disassembly of replication factories in the absence of DNA synthesis. Nat. Cell Biol. 2, 686–694 (2000).
pubmed: 11025658
pmcid: 1255923
doi: 10.1038/35036309
Wagner, D. E. & Klein, A. M. Lineage tracing meets single-cell omics: opportunities and challenges. Nat. Rev. Genet. 21, 410–427 (2020).
pubmed: 32235876
pmcid: 7307462
doi: 10.1038/s41576-020-0223-2
Dehé, P.-M. & Gaillard, P.-H. L. Control of structure-specific endonucleases to maintain genome stability. Nat. Rev. Mol. Cell Biol. 18, 315–330 (2017).
pubmed: 28327556
doi: 10.1038/nrm.2016.177
Chagin, V. O. et al. Processive DNA synthesis is associated with localized decompaction of constitutive heterochromatin at the sites of DNA replication and repair. Nucleus 10, 231–253 (2019).
pubmed: 31744372
pmcid: 6949026
doi: 10.1080/19491034.2019.1688932
Bester, A. C. et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435–446 (2011).
pubmed: 21529715
pmcid: 3740329
doi: 10.1016/j.cell.2011.03.044
Halliwell, J. A. et al. Nucleosides rescue replication-mediated genome instability of human pluripotent stem cells. Stem Cell Rep. 14, 1009–1017 (2020).
doi: 10.1016/j.stemcr.2020.04.004
Yuan, K., Seller, C. A., Shermoen, A. W. & O’Farrell, P. H. Timing the Drosophila mid-blastula transition: a cell cycle-centered view. Trends Genet. 32, 496–507 (2016).
pubmed: 27339317
pmcid: 4958567
doi: 10.1016/j.tig.2016.05.006
Hörmanseder, E., Tischer, T. & Mayer, T. U. Modulation of cell cycle control during oocyte-to-embryo transitions. EMBO J. 32, 2191–2203 (2013).
pubmed: 23892458
pmcid: 3746200
doi: 10.1038/emboj.2013.164
Langley, A. R., Smith, J. C., Stemple, D. L. & Harvey, S. A. New insights into the maternal to zygotic transition. Development 141, 3834–3841 (2014).
pubmed: 25294937
doi: 10.1242/dev.102368
Farrell, J. A. & O’Farrell, P. H. From egg to gastrula: how the cell cycle is remodeled during the Drosophila mid-blastula transition. Annu. Rev. Genet. 48, 269–294 (2014).
pubmed: 25195504
pmcid: 4484755
doi: 10.1146/annurev-genet-111212-133531
McCleland, M. L., Shermoen, A. W. & O’Farrell, P. H. DNA replication times the cell cycle and contributes to the mid-blastula transition in Drosophila embryos. J. Cell Biol. 187, 7–14 (2009).
pubmed: 19786576
pmcid: 2762091
doi: 10.1083/jcb.200906191
Hyrien, O. & Méchali, M. Chromosomal replication initiates and terminates at random sequences but at regular intervals in the ribosomal DNA of Xenopus early embryos. EMBO J. 12, 4511–4520 (1993).
pubmed: 8223461
pmcid: 413880
doi: 10.1002/j.1460-2075.1993.tb06140.x
Hyrien, O., Maric, C. & Méchali, M. Transition in specification of embryonic metazoan DNA replication origins. Science 270, 994–997 (1995).
pubmed: 7481806
doi: 10.1126/science.270.5238.994
Sasaki, T., Sawado, T., Yamaguchi, M. & Shinomiya, T. Specification of regions of DNA replication initiation during embryogenesis in the 65-kilobase DNApolα-dE2F locus of Drosophila melanogaster. Mol. Cell. Biol. 19, 547–555 (1999).
pubmed: 9858578
pmcid: 83912
doi: 10.1128/MCB.19.1.547
Vallot, A. & Tachibana, K. The emergence of genome architecture and zygotic genome activation. Curr. Opin. Cell Biol. 64, 50–57 (2020).
pubmed: 32220807
pmcid: 7374442
doi: 10.1016/j.ceb.2020.02.002
Hug, C. B., Grimaldi, A. G., Kruse, K. & Vaquerizas, J. M. Chromatin architecture emerges during zygotic genome activation independent of transcription. Cell 169, 216–228 (2017).
pubmed: 28388407
doi: 10.1016/j.cell.2017.03.024
Cho, C.-Y., Seller, C. A. & O’Farrell, P. H. Temporal control of late replication and coordination of origin firing by self-stabilizing Rif1-PP1 hubs in Drosophila. Proc. Natl Acad. Sci. USA 119, e2200780119 (2022).
pubmed: 35733247
pmcid: 9245680
doi: 10.1073/pnas.2200780119
Seller, C. A. & O’Farrell, P. H. Rif1 prolongs the embryonic S phase at the Drosophila mid-blastula transition. PLoS Biol. 16, e2005687 (2018).
pubmed: 29746464
pmcid: 5963817
doi: 10.1371/journal.pbio.2005687
Niu, L. et al. Three-dimensional folding dynamics of the Xenopus tropicalis genome. Nat. Genet. 53, 1075–1087 (2021).
pubmed: 34099928
pmcid: 8270788
doi: 10.1038/s41588-021-00878-z
Ferreira, J. & Carmo-Fonseca, M. Genome replication in early mouse embryos follows a defined temporal and spatial order. J. Cell Sci. 110, 889–897 (1997).
pubmed: 9133676
doi: 10.1242/jcs.110.7.889
Aoki, E. & Schultz, R. M. DNA replication in the 1-cell mouse embryo: stimulatory effect of histone acetylation. Zygote 7, 165–172 (1999).
pubmed: 10418111
doi: 10.1017/S0967199499000532
Wike, C. L. et al. Chromatin architecture transitions from zebrafish sperm through early embryogenesis. Genome Res. 31, 981–994 (2021).
pubmed: 34006569
pmcid: 8168589
doi: 10.1101/gr.269860.120
Nakamura, R. et al. CTCF looping is established during gastrulation in medaka embryos. Genome Res. 31, 968–980 (2021).
pubmed: 34006570
pmcid: 8168583
doi: 10.1101/gr.269951.120
Siefert, J. C., Georgescu, C., Wren, J. D., Koren, A. & Sansam, C. L. DNA replication timing during development anticipates transcriptional programs and parallels enhancer activation. Genome Res. 27, 1406–1416 (2017).
pubmed: 28512193
pmcid: 5538556
doi: 10.1101/gr.218602.116
Kaaij, L. J. T., van der Weide, R. H., Ketting, R. F. & de Wit, E. Systemic loss and gain of chromatin architecture throughout zebrafish development. Cell Rep. 24, 1–10 (2018).
pubmed: 29972771
pmcid: 6047509
doi: 10.1016/j.celrep.2018.06.003
Ottolini, C. S. et al. Tripolar mitosis and partitioning of the genome arrests human preimplantation development in vitro. Sci. Rep. 7, 9744 (2017).
pubmed: 28851957
pmcid: 5575028
doi: 10.1038/s41598-017-09693-1
Capalbo, A. et al. Sequential comprehensive chromosome analysis on polar bodies, blastomeres and trophoblast: insights into female meiotic errors and chromosomal segregation in the preimplantation window of embryo development. Hum. Reprod. 28, 509–518 (2013).
pubmed: 23148203
doi: 10.1093/humrep/des394
McCoy, R. C. et al. Meiotic and mitotic aneuploidies drive arrest of in vitro fertilized human preimplantation embryos. Genome Med. 15, 77 (2023).
pubmed: 37779206
pmcid: 10544495
doi: 10.1186/s13073-023-01231-1
Borsos, M. et al. Genome-lamina interactions are established de novo in the early mouse embryo. Nature 569, 729–733 (2019).
pubmed: 31118510
pmcid: 6546605
doi: 10.1038/s41586-019-1233-0
Nakatani, T. et al. Emergence of replication timing during early mammalian development. Nature 625, 401–409 (2024).
pubmed: 38123678
doi: 10.1038/s41586-023-06872-1
Bakker, B. et al. Single-cell sequencing reveals karyotype heterogeneity in murine and human malignancies. Genome Biol. 17, 115 (2016).
pubmed: 27246460
pmcid: 4888588
doi: 10.1186/s13059-016-0971-7
Zhang, K. et al. Analysis of genome architecture during SCNT reveals a role of cohesin in impeding minor ZGA. Mol. Cell 79, 234–250 (2020).
pubmed: 32579944
doi: 10.1016/j.molcel.2020.06.001
Kyogoku, H., Wakayama, T., Kitajima, T. S. & Miyano, T. Single nucleolus precursor body formation in the pronucleus of mouse zygotes and SCNT embryos. PLoS ONE 13, e0202663 (2018).
pubmed: 30125305
pmcid: 6101414
doi: 10.1371/journal.pone.0202663
Xu, J. et al. A simple and effective method for the isolation of inner cell mass samples from human blastocysts for gene expression analysis in vitro. Cell. Dev. Biol. Anim. 50, 232–236 (2014).
doi: 10.1007/s11626-013-9713-2
Kaykov, A., Taillefumier, T., Bensimon, A. & Nurse, P. Molecular combing of single DNA molecules on the 10 megabase scale. Sci. Rep. 6, 19636 (2016).
pubmed: 26781994
pmcid: 4726065
doi: 10.1038/srep19636
Jackson, D. A. & Pombo, A. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 140, 1285–1295 (1998).
pubmed: 9508763
pmcid: 2132671
doi: 10.1083/jcb.140.6.1285
Bianco, J. N. et al. Analysis of DNA replication profiles in budding yeast and mammalian cells using DNA combing. Methods 57, 149–157 (2012).
pubmed: 22579803
doi: 10.1016/j.ymeth.2012.04.007
Kyogoku, H. & Kitajima, T. S. Large cytoplasm is linked to the error-prone nature of oocytes. Dev. Cell 41, 287–298 (2017).
pubmed: 28486131
doi: 10.1016/j.devcel.2017.04.009
Rabut, G. & Ellenberg, J. Automatic real-time three-dimensional cell tracking by fluorescence microscopy. J. Microsc. 216, 131–137 (2004).
pubmed: 15516224
doi: 10.1111/j.0022-2720.2004.01404.x
Alavattam, K. G. et al. Attenuated chromatin compartmentalization in meiosis and its maturation in sperm development. Nat. Struct. Mol. Biol. 26, 175–184 (2019).
pubmed: 30778237
pmcid: 6402993
doi: 10.1038/s41594-019-0189-y