Developmental signals control chromosome segregation fidelity during pluripotency and neurogenesis by modulating replicative stress.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
28 Aug 2024
28 Aug 2024
Historique:
received:
10
11
2023
accepted:
09
08
2024
medline:
28
8
2024
pubmed:
28
8
2024
entrez:
27
8
2024
Statut:
epublish
Résumé
Human development relies on the correct replication, maintenance and segregation of our genetic blueprints. How these processes are monitored across embryonic lineages, and why genomic mosaicism varies during development remain unknown. Using pluripotent stem cells, we identify that several patterning signals-including WNT, BMP, and FGF-converge into the modulation of DNA replication stress and damage during S-phase, which in turn controls chromosome segregation fidelity in mitosis. We show that the WNT and BMP signals protect from excessive origin firing, DNA damage and chromosome missegregation derived from stalled forks in pluripotency. Cell signalling control of chromosome segregation declines during lineage specification into the three germ layers, but re-emerges in neural progenitors. In particular, we find that the neurogenic factor FGF2 induces DNA replication stress-mediated chromosome missegregation during the onset of neurogenesis, which could provide a rationale for the elevated chromosomal mosaicism of the developing brain. Our results highlight roles for morphogens and cellular identity in genome maintenance that contribute to somatic mosaicism during mammalian development.
Identifiants
pubmed: 39191776
doi: 10.1038/s41467-024-51821-9
pii: 10.1038/s41467-024-51821-9
doi:
Substances chimiques
Bone Morphogenetic Proteins
0
Fibroblast Growth Factor 2
103107-01-3
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7404Informations de copyright
© 2024. The Author(s).
Références
Musacchio, A. The molecular biology of spindle assembly checkpoint signaling dynamics. Curr. Biol. 25, R1002–R1018 (2015).
pubmed: 26485365
doi: 10.1016/j.cub.2015.08.051
Saxena, S. & Zou, L. Hallmarks of DNA replication stress. Mol. Cell 82, 2298–2314 (2022).
pubmed: 35714587
pmcid: 9219557
doi: 10.1016/j.molcel.2022.05.004
Malumbres, M. & Barbacid, M. Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer 9, 153–166 (2009).
pubmed: 19238148
doi: 10.1038/nrc2602
Baris, Y., Taylor, M. R. G., Aria, V. & Yeeles, J. T. P. Fast and efficient DNA replication with purified human proteins. Nature 606, 204–210 (2022).
pubmed: 35585232
pmcid: 7613936
doi: 10.1038/s41586-022-04759-1
Bae, T. et al. Different mutational rates and mechanisms in human cells at pregastrulation and neurogenesis. Science 359, 550–555 (2018).
pubmed: 29217587
doi: 10.1126/science.aan8690
Bizzotto, S. et al. Landmarks of human embryonic development inscribed in somatic mutations. Science 371, 1249–1253 (2021).
pubmed: 33737485
pmcid: 8170505
doi: 10.1126/science.abe1544
Bolton, H. et al. Mouse model of chromosome mosaicism reveals lineage-specific depletion of aneuploid cells and normal developmental potential. Nat. Commun. 7, 11165 (2016).
pubmed: 27021558
pmcid: 4820631
doi: 10.1038/ncomms11165
Breuss, M. W. et al. Somatic mosaicism reveals clonal distributions of neocortical development. Nature 604, 689–696 (2022).
pubmed: 35444276
pmcid: 9436791
doi: 10.1038/s41586-022-04602-7
van Echten-Arends, J. et al. Chromosomal mosaicism in human preimplantation embryos: a systematic review. Hum. Reprod. Update 17, 620–627 (2011).
pubmed: 21531753
doi: 10.1093/humupd/dmr014
Yang, A. H. et al. Chromosome segregation defects contribute to aneuploidy in normal neural progenitor cells. J. Neurosci. 23, 10454–10462 (2003).
pubmed: 14614104
pmcid: 6740997
doi: 10.1523/JNEUROSCI.23-32-10454.2003
Yurov, Y. B. et al. Aneuploidy and confined chromosomal mosaicism in the developing human brain. PLoS One 2, e558 (2007).
pubmed: 17593959
pmcid: 1891435
doi: 10.1371/journal.pone.0000558
McConnell, M. J. et al. Mosaic copy number variation in human neurons. Science 342, 632–637 (2013).
pubmed: 24179226
pmcid: 3975283
doi: 10.1126/science.1243472
Ertych, N. et al. Increased microtubule assembly rates influence chromosomal instability in colorectal cancer cells. Nat. Cell Biol. 16, 779–791 (2014).
pubmed: 24976383
pmcid: 4389786
doi: 10.1038/ncb2994
Burrell, R. A. et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 494, 492–496 (2013).
pubmed: 23446422
pmcid: 4636055
doi: 10.1038/nature11935
Fernandez-Casanas, M. & Chan, K. L. The unresolved problem of DNA bridging. Genes. https://doi.org/10.3390/genes9120623 (2018)
Bakhoum, S. F., Kabeche, L., Compton, D. A., Powell, S. N. & Bastians, H. Mitotic DNA damage response: at the crossroads of structural and numerical cancer chromosome instabilities. Trends Cancer 3, 225–234 (2017).
pubmed: 28718433
pmcid: 5518619
doi: 10.1016/j.trecan.2017.02.001
Bohly, N. et al. Increased replication origin firing links replication stress to whole chromosomal instability in human cancer. Cell Rep. 41, 111836 (2022).
pubmed: 36516748
doi: 10.1016/j.celrep.2022.111836
Gilmour, D., Rembold, M. & Leptin, M. From morphogen to morphogenesis and back. Nature 541, 311–320 (2017).
pubmed: 28102269
doi: 10.1038/nature21348
De Robertis, E. M. & Moriyama, Y. The chordin morphogenetic pathway. Curr. Top. Dev. Biol. 116, 231–245 (2016).
pubmed: 26970622
doi: 10.1016/bs.ctdb.2015.10.003
Bier, E. & De Robertis, E. M. EMBRYO DEVELOPMENT. BMP gradients: a paradigm for morphogen-mediated developmental patterning. Science 348, aaa5838 (2015).
pubmed: 26113727
doi: 10.1126/science.aaa5838
Clevers, H., Loh, K. M. & Nusse, R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346, 1248012 (2014).
pubmed: 25278615
doi: 10.1126/science.1248012
Niehrs, C. On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137, 845–857 (2010).
pubmed: 20179091
doi: 10.1242/dev.039651
Li, R. & Zhu, J. Effects of aneuploidy on cell behaviour and function. Nat. Rev. Mol. Cell Biol. 23, 250–265 (2022).
pubmed: 34987171
doi: 10.1038/s41580-021-00436-9
Su, J. et al. Genomic integrity safeguards self-renewal in embryonic stem cells. Cell Rep. 28, 1400–1409 e1404 (2019).
pubmed: 31390555
pmcid: 6708277
doi: 10.1016/j.celrep.2019.07.011
Shi, L., Qalieh, A., Lam, M. M., Keil, J. M. & Kwan, K. Y. Robust elimination of genome-damaged cells safeguards against brain somatic aneuploidy following Knl1 deletion. Nat. Commun. 10, 2588 (2019).
pubmed: 31197172
pmcid: 6565622
doi: 10.1038/s41467-019-10411-w
Pfau, S. J., Silberman, R. E., Knouse, K. A. & Amon, A. Aneuploidy impairs hematopoietic stem cell fitness and is selected against in regenerating tissues in vivo. Genes Dev. 30, 1395–1408 (2016).
pubmed: 27313317
pmcid: 4926863
doi: 10.1101/gad.278820.116
Lin, Y. C. et al. Wnt10b-GSK3beta-dependent Wnt/STOP signaling prevents aneuploidy in human somatic cells. Life Sci. Alliance. https://doi.org/10.26508/lsa.202000855 (2021).
Stolz, A., Neufeld, K., Ertych, N. & Bastians, H. Wnt-mediated protein stabilization ensures proper mitotic microtubule assembly and chromosome segregation. EMBO Rep. 16, 490–499 (2015).
pubmed: 25656539
pmcid: 4388615
doi: 10.15252/embr.201439410
Habib, S. J. & Acebron, S. P. Wnt signalling in cell division: from mechanisms to tissue engineering. Trends Cell Biol. https://doi.org/10.1016/j.tcb.2022.05.006 (2022).
Moris, N. et al. An in vitro model of early anteroposterior organization during human development. Nature 582, 410–415 (2020).
pubmed: 32528178
doi: 10.1038/s41586-020-2383-9
Kunath, T. et al. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134, 2895–2902 (2007).
pubmed: 17660198
doi: 10.1242/dev.02880
Loh, K. M. et al. Mapping the pairwise choices leading from pluripotency to human bone, heart, and other mesoderm cell types. Cell 166, 451–467 (2016).
pubmed: 27419872
pmcid: 5474394
doi: 10.1016/j.cell.2016.06.011
Tchieu, J. et al. A modular platform for differentiation of human PSCs into all major ectodermal lineages. Cell Stem Cell 21, 399–410 e397 (2017).
pubmed: 28886367
pmcid: 5737635
doi: 10.1016/j.stem.2017.08.015
Martyn, I., Kanno, T. Y., Ruzo, A., Siggia, E. D. & Brivanlou, A. H. Self-organization of a human organizer by combined Wnt and nodal signalling. Nature 558, 132–135 (2018).
pubmed: 29795348
pmcid: 6077985
doi: 10.1038/s41586-018-0150-y
Bachiller, D. et al. The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 403, 658–661 (2000).
pubmed: 10688202
doi: 10.1038/35001072
Fuentealba, L. C. et al. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131, 980–993 (2007).
pubmed: 18045539
pmcid: 2200633
doi: 10.1016/j.cell.2007.09.027
Piccolo, S., Sasai, Y., Lu, B. & De Robertis, E. M. Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589–598 (1996).
pubmed: 8752213
pmcid: 3070603
doi: 10.1016/S0092-8674(00)80132-4
Iwata, T. & Hevner, R. F. Fibroblast growth factor signaling in development of the cerebral cortex. Dev. Growth Differ. 51, 299–323 (2009).
pubmed: 19379279
doi: 10.1111/j.1440-169X.2009.01104.x
Acebron, S. P. & Niehrs, C. beta-catenin-independent roles of Wnt/LRP6 signaling. Trends Cell Biol. 26, 956–967 (2016).
pubmed: 27568239
doi: 10.1016/j.tcb.2016.07.009
Dailey, L., Ambrosetti, D., Mansukhani, A. & Basilico, C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev. 16, 233–247 (2005).
pubmed: 15863038
doi: 10.1016/j.cytogfr.2005.01.007
Acebron, S. P., Karaulanov, E., Berger, B. S., Huang, Y.-L. & Niehrs, C. Mitotic wnt signaling promotes protein stabilization and regulates cell size. Mol. cell 54, 663–674 (2014).
pubmed: 24837680
doi: 10.1016/j.molcel.2014.04.014
Bufe, A. et al. Wnt signaling recruits KIF2A to the spindle to ensure chromosome congression and alignment during mitosis. Proc. Natl. Acad. Sci. USA. https://doi.org/10.1073/pnas.2108145118 (2021).
Petruk, S. et al. TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150, 922–933 (2012).
pubmed: 22921915
pmcid: 3432699
doi: 10.1016/j.cell.2012.06.046
Chong, S. Y. et al. H3K4 methylation at active genes mitigates transcription-replication conflicts during replication stress. Nat. Commun. 11, 809 (2020).
pubmed: 32041946
pmcid: 7010754
doi: 10.1038/s41467-020-14595-4
Lamm, N. et al. Genomic instability in human pluripotent stem cells arises from replicative stress and chromosome condensation defects. Cell Stem Cell 18, 253–261 (2016).
pubmed: 26669899
doi: 10.1016/j.stem.2015.11.003
Blakemore, D. et al. MYBL2 and ATM suppress replication stress in pluripotent stem cells. EMBO Rep. 22, e51120 (2021).
pubmed: 33779025
pmcid: 8097389
doi: 10.15252/embr.202051120
Courbet, S. et al. Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455, 557–560 (2008).
pubmed: 18716622
doi: 10.1038/nature07233
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
Maya-Mendoza, A., Olivares-Chauvet, P., Shaw, A. & Jackson, D. A. S phase progression in human cells is dictated by the genetic continuity of DNA foci. PLoS Genet. 6, e1000900 (2010).
pubmed: 20386742
pmcid: 2851568
doi: 10.1371/journal.pgen.1000900
van den Berg, J. et al. Quantifying DNA replication speeds in single cells by scEdU-seq. Nat. Methods. https://doi.org/10.1038/s41592-024-02308-4 (2024).
Cox, J. et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell Proteom. 13, 2513–2526 (2014).
doi: 10.1074/mcp.M113.031591
Mukherjee, C. et al. RIF1 promotes replication fork protection and efficient restart to maintain genome stability. Nat. Commun. 10, 3287 (2019).
pubmed: 31337767
pmcid: 6650494
doi: 10.1038/s41467-019-11246-1
Garzon, J., Ursich, S., Lopes, M., Hiraga, S. I. & Donaldson, A. D. Human RIF1-protein phosphatase 1 prevents degradation and breakage of nascent DNA on replication stalling. Cell Rep. 27, 2558–2566 e2554 (2019).
pubmed: 31141682
pmcid: 6547018
doi: 10.1016/j.celrep.2019.05.002
Balasubramanian, S. et al. Protection of nascent DNA at stalled replication forks is mediated by phosphorylation of RIF1 intrinsically disordered region. Elife. https://doi.org/10.7554/eLife.75047 (2022).
Luo, M. L. et al. Inactivation of the prolyl isomerase Pin1 sensitizes BRCA1-proficient breast cancer to PARP inhibition. Cancer Res. 80, 3033–3045 (2020).
pubmed: 32193285
pmcid: 7755124
doi: 10.1158/0008-5472.CAN-19-2739
Przetocka, S. et al. CtIP-mediated fork protection synergizes with BRCA1 to suppress genomic instability upon DNA replication stress. Mol. Cell 72, 568–582 e566 (2018).
pubmed: 30344097
doi: 10.1016/j.molcel.2018.09.014
Cho, W. H., Lee, Y. J., Kong, S. I., Hurwitz, J. & Lee, J. K. CDC7 kinase phosphorylates serine residues adjacent to acidic amino acids in the minichromosome maintenance 2 protein. Proc. Natl. Acad. Sci. USA 103, 11521–11526 (2006).
pubmed: 16864800
pmcid: 1544202
doi: 10.1073/pnas.0604990103
Liu, Y. EEPD1: breaking and rescuing the replication fork. PLoS Genet. 12, e1005742 (2016).
pubmed: 26844887
pmcid: 4742060
doi: 10.1371/journal.pgen.1005742
Yu, H. et al. Chaperoning HMGA2 protein protects stalled replication forks in stem and cancer cells. Cell Rep. 6, 684–697 (2014).
pubmed: 24508460
doi: 10.1016/j.celrep.2014.01.014
Morales, J. C. et al. XRN2 links transcription termination to DNA damage and replication stress. PLoS Genet. 12, e1006107 (2016).
pubmed: 27437695
pmcid: 4954731
doi: 10.1371/journal.pgen.1006107
Singh, S. et al. SF3B1 mutations induce R-loop accumulation and DNA damage in MDS and leukemia cells with therapeutic implications. Leukemia 34, 2525–2530 (2020).
pubmed: 32076118
pmcid: 7449882
doi: 10.1038/s41375-020-0753-9
Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. & Bonner, W. M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858–5868 (1998).
pubmed: 9488723
doi: 10.1074/jbc.273.10.5858
Burma, S., Chen, B. P., Murphy, M., Kurimasa, A. & Chen, D. J. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276, 42462–42467 (2001).
pubmed: 11571274
doi: 10.1074/jbc.C100466200
Ahuja, A. K. et al. A short G1 phase imposes constitutive replication stress and fork remodelling in mouse embryonic stem cells. Nat. Commun. 7, 10660 (2016).
pubmed: 26876348
pmcid: 4756311
doi: 10.1038/ncomms10660
Ruff, P., Donnianni, R. A., Glancy, E., Oh, J. & Symington, L. S. RPA Stabilization of single-stranded DNA is critical for break-induced replication. Cell Rep. 17, 3359–3368 (2016).
pubmed: 28009302
pmcid: 5218512
doi: 10.1016/j.celrep.2016.12.003
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
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
Beck, H. et al. Cyclin-dependent kinase suppression by WEE1 kinase protects the genome through control of replication initiation and nucleotide consumption. Mol. Cell Biol. 32, 4226–4236 (2012).
pubmed: 22907750
pmcid: 3457333
doi: 10.1128/MCB.00412-12
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
Bohly, N., Kistner, M. & Bastians, H. Mild replication stress causes aneuploidy by deregulating microtubule dynamics in mitosis. Cell Cycle 18, 2770–2783 (2019).
pubmed: 31448675
pmcid: 6773245
doi: 10.1080/15384101.2019.1658477
Niehrs, C. & Acebron, S. P. Mitotic and mitogenic Wnt signalling. EMBO J. 31, 2705–2713 (2012).
pubmed: 22617425
pmcid: 3380213
doi: 10.1038/emboj.2012.124
Madan, B. et al. Temporal dynamics of Wnt-dependent transcriptome reveal an oncogenic Wnt/MYC/ribosome axis. J. Clin. Invest 128, 5620–5633 (2018).
pubmed: 30300142
pmcid: 6264740
doi: 10.1172/JCI122383
Chambers, S. M. et al. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275–280 (2009).
pubmed: 19252484
pmcid: 2756723
doi: 10.1038/nbt.1529
Menendez, L., Yatskievych, T. A., Antin, P. B. & Dalton, S. Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. Proc. Natl. Acad. Sci. USA 108, 19240–19245 (2011).
pubmed: 22084120
pmcid: 3228464
doi: 10.1073/pnas.1113746108
Kafer, G. R. Replication stress tolerance and management differs between naïve and primed pluripotent cells. Preprint at https://doi.org/10.1101/2022.05.12.491744 (2022).
Rohrback, S. et al. Submegabase copy number variations arise during cerebral cortical neurogenesis as revealed by single-cell whole-genome sequencing. Proc. Natl. Acad. Sci. USA 115, 10804–10809 (2018).
pubmed: 30262650
pmcid: 6196524
doi: 10.1073/pnas.1812702115
Duncan, A. W. et al. Frequent aneuploidy among normal human hepatocytes. Gastroenterology 142, 25–28 (2012).
pubmed: 22057114
doi: 10.1053/j.gastro.2011.10.029
Zhu, J., Tsai, H. J., Gordon, M. R. & Li, R. Cellular stress associated with aneuploidy. Dev. Cell 44, 420–431 (2018).
pubmed: 29486194
pmcid: 6529225
doi: 10.1016/j.devcel.2018.02.002
Rehen, S. K. et al. Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proc. Natl. Acad. Sci. USA 98, 13361–13366 (2001).
pubmed: 11698687
pmcid: 60876
doi: 10.1073/pnas.231487398
Liu, Y. et al. Directed differentiation of forebrain GABA interneurons from human pluripotent stem cells. Nat. Protoc. 8, 1670–1679 (2013).
pubmed: 23928500
pmcid: 4121169
doi: 10.1038/nprot.2013.106
Yuan, F. et al. Efficient generation of region-specific forebrain neurons from human pluripotent stem cells under highly defined condition. Sci. Rep. 5, 18550 (2015).
pubmed: 26670131
pmcid: 4680876
doi: 10.1038/srep18550
Taverna, E., Götz, M. & Huttner, W. B. The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu. Rev. Cell Dev. Biol. 30, 465–502 (2014).
pubmed: 25000993
doi: 10.1146/annurev-cellbio-101011-155801
Raballo, R. et al. Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J. Neurosci. 20, 5012–5023 (2000).
pubmed: 10864959
pmcid: 6772267
doi: 10.1523/JNEUROSCI.20-13-05012.2000
Hirabayashi, Y. et al. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131, 2791–2801 (2004).
pubmed: 15142975
doi: 10.1242/dev.01165
Israsena, N., Hu, M., Fu, W., Kan, L. & Kessler, J. A. The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev. Biol. 268, 220–231 (2004).
pubmed: 15031118
doi: 10.1016/j.ydbio.2003.12.024
Da Silva, F. et al. Mitotic WNT signalling orchestrates neurogenesis in the developing neocortex. EMBO J. 40, e108041 (2021).
pubmed: 34431536
pmcid: 8488556
doi: 10.15252/embj.2021108041
Arai, Y. et al. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2, 154 (2011).
pubmed: 21224845
doi: 10.1038/ncomms1155
Gotz, M. & Huttner, W. B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777–788 (2005).
pubmed: 16314867
doi: 10.1038/nrm1739
Vaccarino, F. M. et al. Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat. Neurosci. 2, 246–253 (1999).
pubmed: 10195217
doi: 10.1038/6350
Rohrback, S., Siddoway, B., Liu, C. S. & Chun, J. Genomic mosaicism in the developing and adult brain. Dev. Neurobiol. 78, 1026–1048 (2018).
pubmed: 30027562
pmcid: 6214721
doi: 10.1002/dneu.22626
Albert, O. et al. Chromosome instability and aneuploidy in the mammalian brain. Chromosome Res. 31, 32 (2023).
pubmed: 37910282
pmcid: 10833588
doi: 10.1007/s10577-023-09740-w
Ma, T. C., Vong, K. I. & Kwan, K. M. Spatiotemporal decline of BMP signaling activity in neural progenitors mediates fate transition and safeguards neurogenesis. Cell Rep. 30, 3616–3624 e3614 (2020).
pubmed: 32187534
doi: 10.1016/j.celrep.2020.02.089
Yi, J. J., Barnes, A. P., Hand, R., Polleux, F. & Ehlers, M. D. TGF-beta signaling specifies axons during brain development. Cell 142, 144–157 (2010).
pubmed: 20603020
pmcid: 2933408
doi: 10.1016/j.cell.2010.06.010
Augustin, I. et al. Autocrine Wnt regulates the survival and genomic stability of embryonic stem cells. Sci. Signal. https://doi.org/10.1126/scisignal.aah6829 (2017).
Hadjihannas, M. V. et al. Aberrant Wnt/beta-catenin signaling can induce chromosomal instability in colon cancer. Proc. Natl. Acad. Sci. USA 103, 10747–10752 (2006).
pubmed: 16815967
pmcid: 1502302
doi: 10.1073/pnas.0604206103
Fodde, R. et al. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat. Cell Biol. 3, 433–438 (2001).
pubmed: 11283620
doi: 10.1038/35070129
Kikuchi, K., Niikura, Y., Kitagawa, K. & Kikuchi, A. Dishevelled, a Wnt signalling component, is involved in mitotic progression in cooperation with Plk1. EMBO J. 29, 3470–3483 (2010).
pubmed: 20823832
pmcid: 2964169
doi: 10.1038/emboj.2010.221
Alberici, P. & Fodde, R. The role of the APC tumor suppressor in chromosomal instability. Genome Dyn. 1, 149–170 (2006).
pubmed: 18724059
doi: 10.1159/000092506
Rusan, N. M. & Peifer, M. Original CIN: reviewing roles for APC in chromosome instability. J. Cell Biol. 181, 719–726 (2008).
pubmed: 18519734
pmcid: 2396796
doi: 10.1083/jcb.200802107
Tighe, A., Ray-Sinha, A., Staples, O. D. & Taylor, S. S. GSK-3 inhibitors induce chromosome instability. BMC Cell Biol. 8, 34 (2007).
pubmed: 17697341
pmcid: 1976608
doi: 10.1186/1471-2121-8-34
Rashid, M. S., Mazur, T., Ji, W., Liu, S. T. & Taylor, W. R. Analysis of the role of GSK3 in the mitotic checkpoint. Sci. Rep. 8, 14259 (2018).
pubmed: 30250048
pmcid: 6155330
doi: 10.1038/s41598-018-32435-w
Ross, J. et al. A rare human syndrome provides genetic evidence that WNT signaling is required for reprogramming of fibroblasts to induced pluripotent stem cells. Cell Rep. 9, 1770–1780 (2014).
pubmed: 25464842
pmcid: 4335800
doi: 10.1016/j.celrep.2014.10.049
Huang, P., Senga, T. & Hamaguchi, M. A novel role of phospho-beta-catenin in microtubule regrowth at centrosome. Oncogene 26, 4357–4371 (2007).
pubmed: 17260019
doi: 10.1038/sj.onc.1210217
Maya-Mendoza, A. et al. High speed of fork progression induces DNA replication stress and genomic instability. Nature 559, 279–284 (2018).
pubmed: 29950726
doi: 10.1038/s41586-018-0261-5
Barlow, C. et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86, 159–171 (1996).
pubmed: 8689683
doi: 10.1016/S0092-8674(00)80086-0
Elson, A. et al. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 93, 13084–13089 (1996).
pubmed: 8917548
pmcid: 24050
doi: 10.1073/pnas.93.23.13084
Gurley, K. E. & Kemp, C. J. Synthetic lethality between mutation in Atm and DNA-PK(cs) during murine embryogenesis. Curr. Biol. 11, 191–194 (2001).
pubmed: 11231155
doi: 10.1016/S0960-9822(01)00048-3
Enriquez-Rios, V. et al. DNA-PKcs, ATM, and ATR interplay maintains genome integrity during neurogenesis. J. Neurosci. 37, 893–905 (2017).
pubmed: 28123024
pmcid: 5296783
doi: 10.1523/JNEUROSCI.4213-15.2016
Kafer, G. R. & Cesare, A. J. A survey of essential genome stability genes reveals that replication stress mitigation is critical for peri-implantation embryogenesis. Front. Cell Dev. Biol. 8, 416 (2020).
pubmed: 32548123
pmcid: 7274024
doi: 10.3389/fcell.2020.00416
Charlier, C. F. & Martins, R. A. P. Protective mechanisms against DNA replication stress in the nervous system. Genes. https://doi.org/10.3390/genes11070730 (2020).
McKinnon, P. J. Genome integrity and disease prevention in the nervous system. Genes Dev. 31, 1180–1194 (2017).
pubmed: 28765160
pmcid: 5558921
doi: 10.1101/gad.301325.117
Matson, J. P. et al. Rapid DNA replication origin licensing protects stem cell pluripotency. Elife. https://doi.org/10.7554/eLife.30473 (2017).
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
Ruiz, S. et al. Limiting replication stress during somatic cell reprogramming reduces genomic instability in induced pluripotent stem cells. Nat. Commun. 6, 8036 (2015).
pubmed: 26292731
doi: 10.1038/ncomms9036
Orlando, L. et al. Phosphorylation state of the histone variant H2A.X controls human stem and progenitor cell fate decisions. Cell Rep. 34, 108818 (2021).
pubmed: 33691101
doi: 10.1016/j.celrep.2021.108818
Starostik, M. R., Sosina, O. A. & McCoy, R. C. Single-cell analysis of human embryos reveals diverse patterns of aneuploidy and mosaicism. Genome Res. 30, 814–825 (2020).
pubmed: 32641298
pmcid: 7370883
doi: 10.1101/gr.262774.120
Yang, M. et al. Depletion of aneuploid cells in human embryos and gastruloids. Nat. Cell Biol. 23, 314–321 (2021).
pubmed: 33837289
doi: 10.1038/s41556-021-00660-7
Wei, P. C. et al. Long neural genes harbor recurrent DNA break clusters in neural stem/progenitor cells. Cell 164, 644–655 (2016).
pubmed: 26871630
pmcid: 4752721
doi: 10.1016/j.cell.2015.12.039
Wu, W. et al. Neuronal enhancers are hotspots for DNA single-strand break repair. Nature 593, 440–444 (2021).
pubmed: 33767446
pmcid: 9827709
doi: 10.1038/s41586-021-03468-5
Mora-Bermudez, F. et al. Longer metaphase and fewer chromosome segregation errors in modern human than Neanderthal brain development. Sci. Adv. 8, eabn7702 (2022).
pubmed: 35905187
pmcid: 9337762
doi: 10.1126/sciadv.abn7702
Pellegrini, L. et al. Human CNS barrier-forming organoids with cerebrospinal fluid production. Science. https://doi.org/10.1126/science.aaz5626 (2020).
Lancaster, M. A. et al. Cerebral organoids model human brain development and microcephaly. Nature. https://doi.org/10.1038/nature12517 (2013).
Tamayo-Orrego, L. et al. Sonic hedgehog accelerates DNA replication to cause replication stress promoting cancer initiation in medulloblastoma. Nat. Cancer 1, 840–854 (2020).
pubmed: 35122047
doi: 10.1038/s43018-020-0094-7
Foskolou, I. P. et al. Ribonucleotide reductase requires subunit switching in hypoxia to maintain DNA replication. Mol. Cell 66, 206–220 e209 (2017).
pubmed: 28416140
pmcid: 5405111
doi: 10.1016/j.molcel.2017.03.005
Ibler, A. E. M. et al. Typhoid toxin exhausts the RPA response to DNA replication stress driving senescence and Salmonella infection. Nat. Commun. 10, 4040 (2019).
pubmed: 31492859
pmcid: 6731267
doi: 10.1038/s41467-019-12064-1
Knouse, K. A., Lopez, K. E., Bachofner, M. & Amon, A. Chromosome segregation fidelity in epithelia requires tissue architecture. Cell 175, 200–211 e213 (2018).
pubmed: 30146160
pmcid: 6151153
doi: 10.1016/j.cell.2018.07.042
Glinka, A. et al. LGR4 and LGR5 are R-spondin receptors mediating Wnt/beta-catenin and Wnt/PCP signalling. EMBO Rep. 12, 1055–1061 (2011).
pubmed: 21909076
pmcid: 3185347
doi: 10.1038/embor.2011.175
Giebel, N. et al. USP42 protects ZNRF3/RNF43 from R-spondin-dependent clearance and inhibits Wnt signalling. EMBO Rep. 22, e51415 (2021).
pubmed: 33786993
pmcid: 8097334
doi: 10.15252/embr.202051415
Hayashi, K., Ohta, H., Kurimoto, K., Aramaki, S. & Saitou, M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146, 519–532 (2011).
pubmed: 21820164
doi: 10.1016/j.cell.2011.06.052
Kinoshita, M. et al. Capture of mouse and human stem cells with features of formative pluripotency. Cell Stem Cell 28, 453–471 e458 (2021).
pubmed: 33271069
pmcid: 7939546
doi: 10.1016/j.stem.2020.11.005
Boon, R. et al. Amino acid levels determine metabolism and CYP450 function of hepatocytes and hepatoma cell lines. Nat. Commun. 11, 1393 (2020).
pubmed: 32170132
pmcid: 7069944
doi: 10.1038/s41467-020-15058-6
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 e2976 (2021).
pubmed: 34157308
pmcid: 8286344
doi: 10.1016/j.molcel.2021.05.024
Geigl, J. B., Uhrig, S. & Speicher, M. R. Multiplex-fluorescence in situ hybridization for chromosome karyotyping. Nat. Protoc. 1, 1172–1184 (2006).
pubmed: 17406400
doi: 10.1038/nprot.2006.160
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F. & Regev, A. Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33, 495–502 (2015).
pubmed: 25867923
pmcid: 4430369
doi: 10.1038/nbt.3192
Ruprecht, B. et al. Comprehensive and reproducible phosphopeptide enrichment using iron immobilized metal ion affinity chromatography (Fe-IMAC) columns. Mol. Cell Proteom. 14, 205–215 (2015).
doi: 10.1074/mcp.M114.043109
Schwanhausser, B. et al. Global quantification of mammalian gene expression control. Nature 473, 337–342 (2011).
pubmed: 21593866
doi: 10.1038/nature10098
Das, B., Mishra, P., Pandey, P., Sharma, S. & Chabes, A. dNTP concentrations do not increase in mammalian cells in response to DNA damage. Cell Metab. 34, 1895–1896 (2022).
pubmed: 36476929
doi: 10.1016/j.cmet.2022.11.002
Jia, S., Marjavaara, L., Buckland, R., Sharma, S. & Chabes, A. Determination of deoxyribonucleoside triphosphate concentrations in yeast cells by strong anion-exchange high-performance liquid chromatography coupled with ultraviolet detection. Methods Mol. Biol. 1300, 113–121 (2015).
pubmed: 25916709
doi: 10.1007/978-1-4939-2596-4_8
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