Epigenetic dysregulation from chromosomal transit in micronuclei.


Journal

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

Informations de publication

Date de publication:
Jul 2023
Historique:
received: 15 11 2021
accepted: 14 04 2023
medline: 7 7 2023
pubmed: 8 6 2023
entrez: 7 6 2023
Statut: ppublish

Résumé

Chromosomal instability (CIN) and epigenetic alterations are characteristics of advanced and metastatic cancers

Identifiants

pubmed: 37286593
doi: 10.1038/s41586-023-06084-7
pii: 10.1038/s41586-023-06084-7
pmc: PMC10322720
doi:

Substances chimiques

Chromatin 0
Histones 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

176-183

Subventions

Organisme : NCI NIH HHS
ID : T32 CA009207
Pays : United States
Organisme : NIH HHS
ID : DP5 OD026395
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA192937
Pays : United States
Organisme : NCI NIH HHS
ID : R37 CA261183
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM138386
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM114362
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA256188
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA270102
Pays : United States
Organisme : NCI NIH HHS
ID : U24 CA264379
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA247749
Pays : United States
Organisme : NIH HHS
ID : S10 OD030286
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA016359
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007739
Pays : United States
Organisme : NCI NIH HHS
ID : R00 CA212290
Pays : United States
Organisme : NIMHD NIH HHS
ID : L32 MD017781
Pays : United States

Informations de copyright

© 2023. The Author(s).

Références

Jones, P. A. & Baylin, S. B. The epigenomics of cancer. Cell 128, 683–692 (2007).
pubmed: 17320506 pmcid: 3894624 doi: 10.1016/j.cell.2007.01.029
Bakhoum, S. F. & Cantley, L. C. The multifaceted role of chromosomal instability in cancer and its microenvironment. Cell 174, 1347–1360 (2018).
pubmed: 30193109 pmcid: 6136429 doi: 10.1016/j.cell.2018.08.027
Timp, W. & Feinberg, A. P. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat. Rev. Cancer 13, 497–510 (2013).
pubmed: 23760024 pmcid: 4636434 doi: 10.1038/nrc3486
Watkins, T. B. K. et al. Pervasive chromosomal instability and karyotype order in tumour evolution. Nature 587, 126–132 (2020).
pubmed: 32879494 pmcid: 7611706 doi: 10.1038/s41586-020-2698-6
Kato, H. & Sandberg, A. A. Chromosome pulverization in human cells with micronuclei. J. Natl Cancer Inst. 40, 165–179 (1968).
pubmed: 5635016
Crasta, K. et al. DNA breaks and chromosome pulverization from errors in mitosis. Nature 482, 53–58 (2012).
pubmed: 22258507 pmcid: 3271137 doi: 10.1038/nature10802
Hatch, E. M., Fischer, A. H., Deerinck, T. J. & Hetzer, M. W. Catastrophic nuclear envelope collapse in cancer cell micronuclei. Cell 154, 47–60 (2013).
pubmed: 23827674 pmcid: 3749778 doi: 10.1016/j.cell.2013.06.007
Lengauer, C., Kinzler, K. W. & Vogelstein, B. Genetic instability in colorectal cancers. Nature 386, 623–627 (1997).
pubmed: 9121588 doi: 10.1038/386623a0
Lengauer, C., Kinzler, K. W. & Vogelstein, B. Genetic instabilities in human cancers. Nature 396, 643–649 (1998).
pubmed: 9872311 doi: 10.1038/25292
Burrell, R. A., McGranahan, N., Bartek, J. & Swanton, C. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501, 338–345 (2013).
pubmed: 24048066 doi: 10.1038/nature12625
Bakhoum, S. F. et al. Chromosomal instability drives metastasis through a cytosolic DNA response. Nature 553, 467–472 (2018).
pubmed: 29342134 pmcid: 5785464 doi: 10.1038/nature25432
Lee, A. J. X. et al. Chromosomal instability confers intrinsic multidrug resistance. Cancer Res. 71, 1858–1870 (2011).
pubmed: 21363922 pmcid: 3059493 doi: 10.1158/0008-5472.CAN-10-3604
Davoli, T., Uno, H., Wooten, E. C. & Elledge, S. J. Tumor aneuploidy correlates with markers of immune evasion and with reduced response to immunotherapy. Science 355, eaaf8399 (2017).
pubmed: 28104840 pmcid: 5592794 doi: 10.1126/science.aaf8399
McGranahan, N. et al. Allele-specific HLA loss and immune escape in lung cancer evolution. Cell 171, 1259–1271 (2017).
pubmed: 29107330 pmcid: 5720478 doi: 10.1016/j.cell.2017.10.001
Thompson, S. L. & Compton, D. A. Examining the link between chromosomal instability and aneuploidy in human cells. J. Cell Biol. 180, 665–672 (2008).
pubmed: 18283116 pmcid: 2265570 doi: 10.1083/jcb.200712029
Mackenzie, K. J. et al. cGAS surveillance of micronuclei links genome instability to innate immunity. Nature 548, 461–465 (2017).
pubmed: 28738408 pmcid: 5870830 doi: 10.1038/nature23449
Harding, S. M. et al. Mitotic progression following DNA damage enables pattern recognition within micronuclei. Nature 548, 466–470 (2017).
pubmed: 28759889 pmcid: 5857357 doi: 10.1038/nature23470
Ly, P. et al. Chromosome segregation errors generate a diverse spectrum of simple and complex genomic rearrangements. Nat. Genet. 51, 705–715 (2019).
pubmed: 30833795 pmcid: 6441390 doi: 10.1038/s41588-019-0360-8
Zhang, C.-Z. et al. Chromothripsis from DNA damage in micronuclei. Nature 522, 179–184 (2015).
pubmed: 26017310 pmcid: 4742237 doi: 10.1038/nature14493
Mohr, L. et al. ER-directed TREX1 limits cGAS activation at micronuclei. Mol. Cell 81, 724–738 (2021).
pubmed: 33476576 pmcid: 7897315 doi: 10.1016/j.molcel.2020.12.037
Yang, H., Wang, H., Ren, J., Chen, Q. & Chen, Z. J. cGAS is essential for cellular senescence. Proc. Natl Acad. Sci. USA 114, E4612–E4620 (2017).
pubmed: 28533362 pmcid: 5468617 doi: 10.1073/pnas.1705499114
Wang, F. & Higgins, J. M. G. Histone modifications and mitosis: countermarks, landmarks, and bookmarks. Trends Cell Biol. 23, 175–184 (2013).
pubmed: 23246430 doi: 10.1016/j.tcb.2012.11.005
Duan, Y. et al. Ubiquitin ligase RNF20/40 facilitates spindle assembly and promotes breast carcinogenesis through stabilizing motor protein Eg5. Nat. Commun. 7, 12648 (2016).
pubmed: 27557628 pmcid: 5007379 doi: 10.1038/ncomms12648
Kapoor, T. M. et al. Chromosomes can congress to the metaphase plate before biorientation. Science 311, 388–391 (2006).
pubmed: 16424343 pmcid: 4768465 doi: 10.1126/science.1122142
Bennett, A. et al. Cenp-E inhibitor GSK923295: novel synthetic route and use as a tool to generate aneuploidy. Oncotarget 6, 20921–20932 (2015).
pubmed: 26320186 pmcid: 4673239 doi: 10.18632/oncotarget.4879
Ly, P. et al. Selective Y centromere inactivation triggers chromosome shattering in micronuclei and repair by non-homologous end joining. Nat. Cell Biol. 19, 68–75 (2017).
pubmed: 27918550 doi: 10.1038/ncb3450
Abdollahi, E., Taucher-Scholz, G. & Jakob, B. Application of fluorescence lifetime imaging microscopy of DNA binding dyes to assess radiation-induced chromatin compaction changes. Int. J. Mol. Sci. 19, 2399 (2018).
pubmed: 30110966 pmcid: 6121443 doi: 10.3390/ijms19082399
Chen, X. et al. ATAC-see reveals the accessible genome by transposase-mediated imaging and sequencing. Nat. Methods 13, 1013–1020 (2016).
pubmed: 27749837 pmcid: 5509561 doi: 10.1038/nmeth.4031
Bakhoum, S. F., Thompson, S. L., Manning, A. L. & Compton, D. A. Genome stability is ensured by temporal control of kinetochore–microtubule dynamics. Nat. Cell Biol. 11, 27–35 (2009).
pubmed: 19060894 doi: 10.1038/ncb1809
Santaguida, S., Tighe, A., D’Alise, A. M., Taylor, S. S. & Musacchio, A. Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J. Cell Biol. 190, 73–87 (2010).
pubmed: 20624901 pmcid: 2911657 doi: 10.1083/jcb.201001036
Hintzsche, H. et al. Fate of micronuclei and micronucleated cells. Mutat. Res. Rev. Mutat. Res. 771, 85–98 (2017).
pubmed: 28342454 doi: 10.1016/j.mrrev.2017.02.002
Kneissig, M. et al. Micronuclei-based model system reveals functional consequences of chromothripsis in human cells. eLife 8, e50292 (2019).
pubmed: 31778112 pmcid: 6910827 doi: 10.7554/eLife.50292
Umbreit, N. T. et al. Mechanisms generating cancer genome complexity from a single cell division error. Science 368, eaba0712 (2020).
pubmed: 32299917 pmcid: 7347108 doi: 10.1126/science.aba0712
Hose, J. et al. Dosage compensation can buffer copy-number variation in wild yeast. eLife 4, e05462 (2015).
pubmed: 25955966 pmcid: 4448642 doi: 10.7554/eLife.05462
Stingele, S. et al. Global analysis of genome, transcriptome and proteome reveals the response to aneuploidy in human cells. Mol. Syst. Biol. 8, 608 (2012).
pubmed: 22968442 pmcid: 3472693 doi: 10.1038/msb.2012.40
Brennan, C. M. et al. Protein aggregation mediates stoichiometry of protein complexes in aneuploid cells. Genes Dev. 33, 1031–1047 (2019).
pubmed: 31196865 pmcid: 6672052 doi: 10.1101/gad.327494.119
Wu, S. et al. Circular ecDNA promotes accessible chromatin and high oncogene expression. Nature 575, 699–703 (2019).
pubmed: 31748743 pmcid: 7094777 doi: 10.1038/s41586-019-1763-5
Turner, K. M. et al. Extrachromosomal oncogene amplification drives tumour evolution and genetic heterogeneity. Nature 543, 122–125 (2017).
pubmed: 28178237 pmcid: 5334176 doi: 10.1038/nature21356
Shoshani, O. et al. Chromothripsis drives the evolution of gene amplification in cancer. Nature 591, 137–141 (2021).
pubmed: 33361815 doi: 10.1038/s41586-020-03064-z
Vázquez-García, I. et al. Ovarian cancer mutational processes drive site-specificimmune evasion.Nature 612, 778–786 (2022).
pubmed: 36517593 pmcid: 9771812 doi: 10.1038/s41586-022-05496-1
Toufektchan, E. & Maciejowski, J. Purification of micronuclei from cultured cells by flow cytometry. STAR Protoc. 2, 100378 (2021).
pubmed: 33778777 pmcid: 7982749 doi: 10.1016/j.xpro.2021.100378
Lai, D., Ha, G. & Shah, S. Hmmcopy: copy-number prediction with correction for GC and mappability bias for HTS data. Bioconductor package v.1.38 https://git.bioconductor.org/packages/HMMcopy (2022).
Lange, S. et al. Analysis pipelines for cancer genome sequencing in mice. Nat. Protoc. 15, 266–315 (2020).
pubmed: 31907453 doi: 10.1038/s41596-019-0234-7
Sarsani, V. K. et al. The genome of C57BL/6J “Eve”, the mother of the laboratory mouse genome reference strain. G3 9, 1795–1805 (2019).
pubmed: 30996023 pmcid: 6553538 doi: 10.1534/g3.119.400071
Shah, R. N. et al. Examining the roles of H3K4 methylation states with systematically characterized antibodies. Mol. Cell 72, 162–177 (2018).
pubmed: 30244833 pmcid: 6173622 doi: 10.1016/j.molcel.2018.08.015
Yusufova, N. et al. Histone H1 loss drives lymphoma by disrupting 3D chromatin architecture. Nature 589, 299–305 (2021).
pubmed: 33299181 doi: 10.1038/s41586-020-3017-y
Cerami, E. et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2, 401–404 (2012).
pubmed: 22588877 doi: 10.1158/2159-8290.CD-12-0095
Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 21.29.1–21.29.9 (2015).
pubmed: 25559105
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
Sidoli, S., Bhanu, N. V., Karch, K. R., Wang, X. & Garcia, B. A. Complete workflow for analysis of histone post-translational modifications using bottom-up mass spectrometry: from histone extraction to data analysis. J. Vis. Exp. 111, e54112 (2016).
Yuan, Z.-F. et al. EpiProfile 2.0: a computational platform for processing epi-proteomics mass spectrometry data. J. Proteome Res. 17, 2533–2541 (2018).
pubmed: 29790754 pmcid: 6387837 doi: 10.1021/acs.jproteome.8b00133

Auteurs

Albert S Agustinus (AS)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Pharmacology Graduate Program, Weill Cornell Medicine, New York, NY, USA.

Duaa Al-Rawi (D)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Bhargavi Dameracharla (B)

Department of Computer Science, University of California, San Diego, La Jolla, CA, USA.

Ramya Raviram (R)

New York Genome Center, New York, NY, USA.

Bailey S C L Jones (BSCL)

Department of Ophthalmology and Visual Science, Yale University School of Medicine, New Haven, CT, USA.

Stephanie Stransky (S)

Department of Biochemistry, Albert Einstein College of Medicine, New York, NY, USA.

Lorenzo Scipioni (L)

School of Engineering, University of California, Irvine, Irvine, CA, USA.

Jens Luebeck (J)

Department of Computer Science, University of California, San Diego, La Jolla, CA, USA.

Melody Di Bona (M)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Danguole Norkunaite (D)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Robert M Myers (RM)

New York Genome Center, New York, NY, USA.
Tri-institutional MD-PhD Program, New York, NY, USA.

Mercedes Duran (M)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Seongmin Choi (S)

Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Britta Weigelt (B)

Department of Pathology and Laboratory Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Shira Yomtoubian (S)

Department of Cell and Developmental Biology, Weill Cornell Medicine, New York, NY, USA.

Andrew McPherson (A)

Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Eléonore Toufektchan (E)

Molecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Kristina Keuper (K)

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

Paul S Mischel (PS)

Department of Pathology, School of Medicine, Stanford University, Stanford, CA, USA.

Vivek Mittal (V)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Cell and Developmental Biology, Weill Cornell Medicine, New York, NY, USA.

Sohrab P Shah (SP)

Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

John Maciejowski (J)

Molecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Zuzana Storchova (Z)

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

Enrico Gratton (E)

School of Engineering, University of California, Irvine, Irvine, CA, USA.

Peter Ly (P)

Department of Pathology, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Dan Landau (D)

New York Genome Center, New York, NY, USA.
Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.

Mathieu F Bakhoum (MF)

Department of Ophthalmology and Visual Science, Yale University School of Medicine, New Haven, CT, USA.
Department of Pathology, Yale University School of Medicine, New Haven, CT, USA.
Yale Cancer Center, Yale University, New Haven, CT, USA.

Richard P Koche (RP)

Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Simone Sidoli (S)

Department of Biochemistry, Albert Einstein College of Medicine, New York, NY, USA.

Vineet Bafna (V)

Department of Computer Science, University of California, San Diego, La Jolla, CA, USA.

Yael David (Y)

Pharmacology Graduate Program, Weill Cornell Medicine, New York, NY, USA. davidshy@mskcc.org.
Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA. davidshy@mskcc.org.
Tri-institutional PhD Program in Chemical Biology, New York, NY, USA. davidshy@mskcc.org.

Samuel F Bakhoum (SF)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA. samuel.bakhoum@gmail.com.
Department of Radiation Oncology, Memorial Sloan Kettering Cancer Center, New York, NY, USA. samuel.bakhoum@gmail.com.

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