Genetic instability from a single S phase after whole-genome duplication.


Journal

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

Informations de publication

Date de publication:
04 2022
Historique:
received: 16 07 2021
accepted: 23 02 2022
pubmed: 1 4 2022
medline: 19 4 2022
entrez: 31 3 2022
Statut: ppublish

Résumé

Diploid and stable karyotypes are associated with health and fitness in animals. By contrast, whole-genome duplications-doublings of the entire complement of chromosomes-are linked to genetic instability and frequently found in human cancers

Identifiants

pubmed: 35355016
doi: 10.1038/s41586-022-04578-4
pii: 10.1038/s41586-022-04578-4
pmc: PMC8986533
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

146-151

Commentaires et corrections

Type : CommentIn
Type : CommentIn
Type : ErratumIn

Informations de copyright

© 2022. The Author(s).

Références

Zack, T. I. et al. Pan-cancer patterns of somatic copy number alteration. Nat. Genet. 45, 1134–1140 (2013).
pubmed: 24071852 pmcid: 3966983 doi: 10.1038/ng.2760
Bielski, C. M. et al. Genome doubling shapes the evolution and prognosis of advanced cancers. Nat. Genet. 50, 1189–1195 (2018).
pubmed: 30013179 pmcid: 6072608 doi: 10.1038/s41588-018-0165-1
López, S. et al. Interplay between whole-genome doubling and the accumulation of deleterious alterations in cancer evolution. Nat. Genet. 52, 283–293 (2020).
pubmed: 32139907 pmcid: 7116784 doi: 10.1038/s41588-020-0584-7
Storchova, Z. & Kuffer, C. The consequences of tetraploidy and aneuploidy. J. Cell Sci. 121, 3859–3866 (2008).
pubmed: 19020304 doi: 10.1242/jcs.039537
Storchova, Z. & Pellman, D. From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell Biol. 5, 45–54 (2004).
pubmed: 14708009 doi: 10.1038/nrm1276
Dewhurst, S. M. et al. Tolerance of whole- genome doubling propagates chromosomal instability and accelerates cancer genome evolution. Cancer Discov. 4, 175–185 (2014).
pubmed: 24436049 pmcid: 4293454 doi: 10.1158/2159-8290.CD-13-0285
Fox, D. T., Gall, J. G. & Spradling, A. C. Error-prone polyploid mitosis during normal Drosophila development. Genes Dev. 24, 2294–2302 (2010).
pubmed: 20952538 pmcid: 2956208 doi: 10.1101/gad.1952710
Goupil, A. et al. Chromosomes function as a barrier to mitotic spindle bipolarity in polyploid cells. J. Cell Biol. 219, e201908006 (2020).
pubmed: 32328633 pmcid: 7147111 doi: 10.1083/jcb.201908006
Fujiwara, T. et al. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437, 1043–1047 (2005).
pubmed: 16222300 doi: 10.1038/nature04217
Pedersen, R. S. et al. Profiling DNA damage response following mitotic perturbations. Nat. Commun. 7, 13887 (2016).
doi: 10.1038/ncomms13887
Orr-Weaver, T. L. When bigger is better: the role of polyploidy in organogenesis. Trends Genet. 31, 307–315 (2015).
pubmed: 25921783 pmcid: 4537166 doi: 10.1016/j.tig.2015.03.011
Gemble, S. & Basto, R. CHRONOCRISIS: when cell cycle asynchrony generates DNA damage in polyploid cells. BioEssays 42, e2000105 (2020).
pubmed: 32885500 doi: 10.1002/bies.202000105
Zeman, M. K. & Cimprich, K. A. Causes and consequences of replication stress. Nat. Cell Biol. 16, 2–9 (2014).
pubmed: 24366029 pmcid: 4354890 doi: 10.1038/ncb2897
Koundrioukoff, S. et al. Stepwise activation of the ATR signaling pathway upon increasing replication stress impacts fragile site integrity. PLoS Genet. 9, e1003643 (2013).
pubmed: 23874235 pmcid: 3715430 doi: 10.1371/journal.pgen.1003643
Panier, S. & Boulton, S. J. Double-strand break repair: 53BP1 comes into focus. Nat. Rev. Mol. Cell Biol. 15, 7–18 (2014).
pubmed: 24326623 doi: 10.1038/nrm3719
Ganem, N. J. et al. Cytokinesis failure triggers hippo tumor suppressor pathway activation. Cell 158, 833–848 (2014).
pubmed: 25126788 pmcid: 4136486 doi: 10.1016/j.cell.2014.06.029
Zhao, B., Rothenberg, E., Ramsden, D. A. & Lieber, M. R. The molecular basis and disease relevance of non-homologous DNA end joining. Nat. Rev. Mol. Cell Biol. 21, 765–781 (2020).
pubmed: 33077885 pmcid: 8063501 doi: 10.1038/s41580-020-00297-8
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
Burgess, A., Lorca, T. & Castro, A. Quantitative live imaging of endogenous DNA replication in mammalian cells. PLoS ONE 7, e45726 (2012).
pubmed: 23029203 pmcid: 3447815 doi: 10.1371/journal.pone.0045726
Michalet, X. et al. Dynamic molecular combing: stretching the whole human genome for high- resolution studies. Science 277, 1518–1523 (1997).
pubmed: 9278517 doi: 10.1126/science.277.5331.1518
Zhong, Y. et al. The level of origin firing inversely affects the rate of replication fork progression. J. Cell Biol. 201, 373–383 (2013).
pubmed: 23629964 pmcid: 3639389 doi: 10.1083/jcb.201208060
Tatsumi, Y., Ohta, S., Kimura, H., Tsurimoto, T. & Obuse, C. The ORC1 cycle in human cells: I. Cell cycle-regulated oscillation of human ORC1. J. Biol. Chem. 278, 41528–41534 (2003).
pubmed: 12909627 doi: 10.1074/jbc.M307534200
Remus, D. et al. Concerted loading of Mcm2–7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719–730 (2009).
pubmed: 19896182 pmcid: 2804858 doi: 10.1016/j.cell.2009.10.015
Siddiqui, K., On, K. F. & Diffley, J. F. X. Regulating DNA replication in Eukarya. Cold Spring Harb. Perspect. Biol. 5, a012930 (2013).
pubmed: 23838438 pmcid: 3753713 doi: 10.1101/cshperspect.a012930
Yan, Z. et al. Cdc6 is regulated by E2F and is essential for DNA replication in mammalian cells. Proc. Natl Acad. Sci. USA 95, 3603–3608 (1998).
pubmed: 9520412 pmcid: 19882 doi: 10.1073/pnas.95.7.3603
Moyer, S. E., Lewis, P. W. & Botchan, M. R. Isolation of the Cdc45/Mcm2–7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc. Natl Acad. Sci. USA 103, 10236–10241 (2006).
pubmed: 16798881 pmcid: 1482467 doi: 10.1073/pnas.0602400103
Kumagai, A., Shevchenko, A., Shevchenko, A. & Dunphy, W. G. Treslin collaborates with TopBP1 in triggering the initiation of DNA replication. Cell 140, 349–359 (2010).
pubmed: 20116089 pmcid: 2857569 doi: 10.1016/j.cell.2009.12.049
DeGregori, J., Kowalik, T. & Nevins, J. R. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol. Cell Biol. 15, 4215–4224 (1995).
pubmed: 7623816 pmcid: 230660 doi: 10.1128/MCB.15.8.4215
Pardee, A. B. G1 events and regulation of cell proliferation. Science 246, 603–608 (1989).
pubmed: 2683075 doi: 10.1126/science.2683075
Cross, F. R., Buchler, N. E. & Skotheim, J. M. Evolution of networks and sequences in eukaryotic cell cycle control. Phil. Trans. R. Soc. B 366, 3532–3544 (2011).
pubmed: 22084380 pmcid: 3203458 doi: 10.1098/rstb.2011.0078
Bertoli, C., Skotheim, J. M. & De Bruin, R. A. M. Control of cell cycle transcription during G1 and S phases. Nat. Rev. Mol. Cell Biol. 14, 518–528 (2013).
pubmed: 23877564 pmcid: 4569015 doi: 10.1038/nrm3629
Cadart, C. et al. Size control in mammalian cells involves modulation of both growth rate and cell cycle duration. Nat. Commun. 9, 3275 (2018).
pubmed: 30115907 pmcid: 6095894 doi: 10.1038/s41467-018-05393-0
Nano, M. et al. Cell-cycle asynchrony generates DNA damage at mitotic entry in polyploid cells. Curr. Biol. 29, 3937–3945.e7 (2019).
pubmed: 31708395 doi: 10.1016/j.cub.2019.09.041
Frawley, L. E. & Orr-Weaver, T. L. Polyploidy. Curr. Biol. 25, R353–R358 (2015).
pubmed: 25942544 doi: 10.1016/j.cub.2015.03.037
Carter, S. L. et al. Absolute quantification of somatic DNA alterations in human cancer. Nat. Biotechnol. 30, 413–421 (2012).
pubmed: 22544022 pmcid: 4383288 doi: 10.1038/nbt.2203
Taylor, A. M. et al. Genomic and functional approaches to understanding cancer aneuploidy. Cancer Cell 33, 676–689.e3 (2018).
pubmed: 29622463 pmcid: 6028190 doi: 10.1016/j.ccell.2018.03.007
Hégarat, N. et al. Cyclin A triggers mitosis either via the greatwall kinase pathway or cyclin B. EMBO J. 39, e104419 (2020).
pubmed: 32350921 pmcid: 7265243 doi: 10.15252/embj.2020104419
SB, K. et al. A quantitative FastFUCCI assay defines cell cycle dynamics at a single-cell level. J. Cell Sci. 130, 512–520 (2017).
KS, Y., RH, K., M, L., R, G. & R, W. Single cell resolution in vivo imaging of DNA damage following PARP inhibition. Sci Rep. 5, 10129 (2015).
doi: 10.1038/srep10129
Karess, R. E. et al. The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65, 1177–1189 (1991).
pubmed: 1905980 doi: 10.1016/0092-8674(91)90013-O
Gemble, S. et al. Centromere dysfunction compromises mitotic spindle pole integrity. Curr. Biol. 29, 3072–3080.e5 (2019).
pubmed: 31495582 doi: 10.1016/j.cub.2019.07.052
J, L., BO, P., K, H., J, B. & K, H. Deregulated expression of E2F family members induces S-phase entry and overcomes p16INK4A-mediated growth suppression. Mol. Cell. Biol. 16, 1047–1057 (1996).
doi: 10.1128/MCB.16.3.1047
Sakaue-Sawano, A. et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487–498 (2008).
pubmed: 18267078 doi: 10.1016/j.cell.2007.12.033
Aknoun, S. et al. Living cell dry mass measurement using quantitative phase imaging with quadriwave lateral shearing interferometry: an accuracy and sensitivity discussion. J. Biomed. Opt. 20, 126009 (2015).
pubmed: 26720876 doi: 10.1117/1.JBO.20.12.126009
Bon, P., Maucort, G., Wattellier, B. & Monneret, S. Quadriwave lateral shearing interferometry for quantitative phase microscopy of living cells. Opt. Express 17, 13080 (2009).
pubmed: 19654713 doi: 10.1364/OE.17.013080
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286 pmcid: 3322381 doi: 10.1038/nmeth.1923
Jun, G., Wing, M. K., Abecasis, G. R. & Kang, H. M. An efficient and scalable analysis framework for variant extraction and refinement from population-scale DNA sequence data. Genome Res. 25, 918–925 (2015).
pubmed: 25883319 pmcid: 4448687 doi: 10.1101/gr.176552.114
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
van den Bos, H. et al. Single-cell whole genome sequencing reveals no evidence for common aneuploidy in normal and Alzheimer’s disease neurons. Genome Biol. 17, 116 (2016)
pubmed: 27246599 pmcid: 4888403 doi: 10.1186/s13059-016-0976-2
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517 pmcid: 1239896 doi: 10.1073/pnas.0506580102
Mootha, V. K. et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267–273 (2003).
pubmed: 12808457 doi: 10.1038/ng1180

Auteurs

Simon Gemble (S)

Institut Curie, PSL Research University, CNRS, UMR144, Biology of Centrosomes and Genetic Instability Laboratory, Paris, France. simon.gemble@curie.fr.

René Wardenaar (R)

European Research Institute for the Biology of Ageing, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.

Kristina Keuper (K)

Department of Molecular Genetics, TU Kaiserslautern, Kaiserslautern, Germany.

Nishit Srivastava (N)

Institut Curie and Institut Pierre Gilles de Gennes, PSL Research University, CNRS, UMR 144, Systems Biology of Cell Polarity and Cell Division, Paris, France.

Maddalena Nano (M)

Institut Curie, PSL Research University, CNRS, UMR144, Biology of Centrosomes and Genetic Instability Laboratory, Paris, France.
Molecular, Cellular, and Developmental Biology Department, University of California, Santa Barbara, CA, USA.

Anne-Sophie Macé (AS)

Cell and Tissue Imaging Facility (PICT-IBiSA), Institut Curie, PSL Research University, Centre National de la Recherche Scientifique, Paris, France.

Andréa E Tijhuis (AE)

European Research Institute for the Biology of Ageing, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.

Sara Vanessa Bernhard (SV)

Department of Molecular Genetics, TU Kaiserslautern, Kaiserslautern, Germany.

Diana C J Spierings (DCJ)

European Research Institute for the Biology of Ageing, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.

Anthony Simon (A)

Institut Curie, PSL Research University, CNRS, UMR144, Biology of Centrosomes and Genetic Instability Laboratory, Paris, France.

Oumou Goundiam (O)

Institut Curie, PSL Research University, CNRS, UMR144, Biology of Centrosomes and Genetic Instability Laboratory, Paris, France.

Helfrid Hochegger (H)

Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Brighton, UK.

Matthieu Piel (M)

Institut Curie and Institut Pierre Gilles de Gennes, PSL Research University, CNRS, UMR 144, Systems Biology of Cell Polarity and Cell Division, Paris, France.

Floris Foijer (F)

European Research Institute for the Biology of Ageing, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.

Zuzana Storchová (Z)

Department of Molecular Genetics, TU Kaiserslautern, Kaiserslautern, Germany.

Renata Basto (R)

Institut Curie, PSL Research University, CNRS, UMR144, Biology of Centrosomes and Genetic Instability Laboratory, Paris, France. renata.basto@curie.fr.

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