Oncogenic c-Myc induces replication stress by increasing cohesins chromatin occupancy in a CTCF-dependent manner.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
21 Feb 2024
21 Feb 2024
Historique:
received:
04
11
2020
accepted:
07
02
2024
medline:
22
2
2024
pubmed:
22
2
2024
entrez:
21
2
2024
Statut:
epublish
Résumé
Oncogene-induced replication stress is a crucial driver of genomic instability and one of the key events contributing to the onset and evolution of cancer. Despite its critical role in cancer, the mechanisms that generate oncogene-induced replication stress remain not fully understood. Here, we report that an oncogenic c-Myc-dependent increase in cohesins on DNA contributes to the induction of replication stress. Accumulation of cohesins on chromatin is not sufficient to cause replication stress, but also requires cohesins to accumulate at specific sites in a CTCF-dependent manner. We propose that the increased accumulation of cohesins at CTCF site interferes with the progression of replication forks, contributing to oncogene-induced replication stress. This is different from, and independent of, previously suggested mechanisms of oncogene-induced replication stress. This, together with the reported protective role of cohesins in preventing replication stress-induced DNA damage, supports a double-edge involvement of cohesins in causing and tolerating oncogene-induced replication stress.
Identifiants
pubmed: 38383676
doi: 10.1038/s41467-024-45955-z
pii: 10.1038/s41467-024-45955-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1579Subventions
Organisme : Cancer Research UK (CRUK)
ID : C37/A18784
Organisme : RCUK | Medical Research Council (MRC)
ID : Ref MC_U12266B
Organisme : Wellcome Trust (Wellcome)
ID : 221978/Z/20/Z
Informations de copyright
© 2024. The Author(s).
Références
Saxena, S. & Zou, L. Hallmarks of DNA replication stress. Mol. Cell 82, 2298–2314 (2022).
doi: 10.1016/j.molcel.2022.05.004
pubmed: 35714587
pmcid: 9219557
Forment, J. V. & O’Connor, M. J. Targeting the replication stress response in cancer. Pharm. Ther. 188, 155–167 (2018).
doi: 10.1016/j.pharmthera.2018.03.005
Burrell, R. A. et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 494, 492–496 (2013).
doi: 10.1038/nature11935
pubmed: 23446422
pmcid: 4636055
Garribba, L. et al. Short-term molecular consequences of chromosome mis-segregation for genome stability. Nat. Commun. 14, 1353 (2023).
doi: 10.1038/s41467-023-37095-7
pubmed: 36906648
pmcid: 10008630
Jones, R. M. et al. Increased replication initiation and conflicts with transcription underlie Cyclin E-induced replication stress. Oncogene 32, 3744–3753 (2013).
doi: 10.1038/onc.2012.387
pubmed: 22945645
Ekholm-Reed, S. et al. Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J. Cell Biol. 165, 789–800 (2004).
doi: 10.1083/jcb.200404092
pubmed: 15197178
pmcid: 2172392
Macheret, M. & Halazonetis, T. D. Intragenic origins due to short G1 phases underlie oncogene-induced DNA replication stress. Nature 555, 112–116 (2018).
doi: 10.1038/nature25507
pubmed: 29466339
pmcid: 5837010
Dominguez-Sola, D. et al. Non-transcriptional control of DNA replication by c-C-Myc. Nature 448, 445–451 (2007).
doi: 10.1038/nature05953
pubmed: 17597761
Srinivasan, S. V., Dominguez-Sola, D., Wang, L. C., Hyrien, O. & Gautier, J. Cdc45 is a critical effector of c-Myc-dependent DNA replication stress. Cell Rep. 3, 1629–1639 (2013).
doi: 10.1016/j.celrep.2013.04.002
pubmed: 23643534
Lin, C. Y. et al. Transcriptional amplification in tumor cells with elevated c-C-Myc. Cell 151, 56–67 (2012).
doi: 10.1016/j.cell.2012.08.026
pubmed: 23021215
pmcid: 3462372
Rohban, S., Cerutti, A., Morelli, M. J., d’Adda di Fagagna, F. & Campaner, S. The cohesin complex prevents C-Myc-induced replication stress. Cell Death Dis. 8, e2956 (2017).
doi: 10.1038/cddis.2017.345
pubmed: 28749464
pmcid: 5550886
Strom, L., Lindroos, H. B., Shirahige, K. & Sjogren, C. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell 16, 1003–1015 (2004).
doi: 10.1016/j.molcel.2004.11.026
pubmed: 15610742
Frattini, C. et al. Cohesin ubiquitylation and mobilization facilitate stalled replication fork dynamics. Mol. Cell 68, 758–772 e754 (2017).
doi: 10.1016/j.molcel.2017.10.012
pubmed: 29129641
Kanke, M., Tahara, E., Huis In’t Veld, P. J. & Nishiyama, T. Cohesin acetylation and Wapl-Pds5 oppositely regulate translocation of cohesin along DNA. EMBO J. 35, 2686–2698 (2016).
doi: 10.15252/embj.201695756
pubmed: 27872142
pmcid: 5167340
Morales, C. et al. PDS5 proteins are required for proper cohesin dynamics and participate in replication fork protection. J. Biol. Chem. 295, 146–157 (2020).
doi: 10.1074/jbc.RA119.011099
pubmed: 31757807
Uhlmann, F. SMC complexes: from DNA to chromosomes. Nat. Rev. Mol. Cell Biol. 17, 399–412 (2016).
doi: 10.1038/nrm.2016.30
pubmed: 27075410
Tedeschi, A. et al. Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 501, 564–568 (2013).
doi: 10.1038/nature12471
pubmed: 23975099
pmcid: 6080692
Gerlich, D., Koch, B., Dupeux, F., Peters, J. M. & Ellenberg, J. Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Curr. Biol. 16, 1571–1578 (2006).
doi: 10.1016/j.cub.2006.06.068
pubmed: 16890534
Zhang, J. et al. Acetylation of SMC3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol. Cell 31, 143–151 (2008).
doi: 10.1016/j.molcel.2008.06.006
pubmed: 18614053
Rowland, B. D. et al. Building sister chromatid cohesion: SMC3 acetylation counteracts an antiestablishment activity. Mol. Cell 33, 763–774 (2009).
doi: 10.1016/j.molcel.2009.02.028
pubmed: 19328069
Lengronne, A. et al. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430, 573–578 (2004).
doi: 10.1038/nature02742
pubmed: 15229615
pmcid: 2610358
Busslinger, G. A. et al. Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl. Nature 544, 503–507 (2017).
doi: 10.1038/nature22063
pubmed: 28424523
pmcid: 6080695
Pope, B. D. et al. Topologically associating domains are stable units of replication-timing regulation. Nature 515, 402–405 (2014).
doi: 10.1038/nature13986
pubmed: 25409831
pmcid: 4251741
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).
doi: 10.1101/gr.183699.114
pubmed: 25995270
pmcid: 4509995
Wendt, K. S. et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451, 796–801 (2008).
doi: 10.1038/nature06634
pubmed: 18235444
Wutz, G. et al. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. EMBO J. 36, 3573–3599 (2017).
doi: 10.15252/embj.201798004
pubmed: 29217591
pmcid: 5730888
Wutz, G. et al. ESCO1 and CTCF enable formation of long chromatin loops by protecting cohesin(STAG1) from WAPL. eLife https://doi.org/10.7554/eLife.52091 . (2020).
Bertoli, C., Herlihy, A. E., Pennycook, B. R., Kriston-Vizi, J. & de Bruin, R. A. M. Sustained E2F-dependent transcription is a key mechanism to prevent replication-stress-induced DNA damage. Cell Rep. 15, 1412–1422 (2016).
doi: 10.1016/j.celrep.2016.04.036
pubmed: 27160911
pmcid: 4893157
Pennycook, B. R. et al. E2F-dependent transcription determines replication capacity and S phase length. Nat. Commun. 11, 3503 (2020).
doi: 10.1038/s41467-020-17146-z
pubmed: 32665547
pmcid: 7360579
Trotter, E. W. & Hagan, I. M. Release from cell cycle arrest with Cdk4/6 inhibitors generates highly synchronized cell cycle progression in human cell culture. Open Biol. 10, 200200 (2020).
doi: 10.1098/rsob.200200
pubmed: 33052073
pmcid: 7653349
Kotsantis, P. et al. Increased global transcription activity as a mechanism of replication stress in cancer. Nat. Commun. 7, 13087 (2016).
doi: 10.1038/ncomms13087
pubmed: 27725641
pmcid: 5062618
Egan, B. et al. An alternative approach to ChIP-Seq normalization enables detection of genome-wide changes in histone H3 lysine 27 trimethylation upon EZH2 inhibition. PLoS ONE 11, e0166438 (2016).
doi: 10.1371/journal.pone.0166438
pubmed: 27875550
pmcid: 5119738
Ciosk, R. et al. Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol. Cell 5, 243–254 (2000).
doi: 10.1016/S1097-2765(00)80420-7
pubmed: 10882066
Watrin, E. et al. Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr. Biol. 16, 863–874 (2006).
doi: 10.1016/j.cub.2006.03.049
pubmed: 16682347
Chao, W. C. et al. Structural studies reveal the functional modularity of the Scc2-Scc4 cohesin loader. Cell Rep. 12, 719–725 (2015).
doi: 10.1016/j.celrep.2015.06.071
pubmed: 26212329
Parenti, I. et al. MAU2 and NIPBL variants impair the heterodimerization of the cohesin loader subunits and cause Cornelia De Lange syndrome. Cell Rep. 31, 107647 (2020).
doi: 10.1016/j.celrep.2020.107647
pubmed: 32433956
Dang, C. V. C.- MYC on the path to cancer. Cell 149, 22–35 (2012).
doi: 10.1016/j.cell.2012.03.003
pubmed: 22464321
pmcid: 3345192
Minchell, N. E., Keszthelyi, A. & Baxter, J. Cohesin causes replicative DNA damage by trapping DNA topological stress. Mol. Cell 78, 739–751 e738 (2020).
doi: 10.1016/j.molcel.2020.03.013
pubmed: 32259483
pmcid: 7242899