Chromothripsis from DNA damage in micronuclei

Nature

Volumn 522, Issue 7555, 2015, Pages 179-184

  Zhang, Cheng Zhong ^a,b,c   Spektor, Alexander ^a,c   Cornils, Hauke ^a,c   Francis, Joshua M ^a,b   Jackson, Emily K ^a,c,d   Liu, Shiwei ^a,c   Meyerson, Matthew ^a,b,c   Pellman, David ^a,b,c,d  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

CANCER; CHROMOSOME; DNA; GENOME;

ARTICLE; CELL CYCLE S PHASE; CELL DIVISION; CHROMATID; CHROMOSOME FRAGMENTATION; CHROMOSOME REARRANGEMENT; CHROMOSOME STRUCTURE; CHROMOTHRIPSIS; DNA DAMAGE; GENE MUTATION; GENE SEQUENCE; GENETIC PARAMETERS; HUMAN; IMAGING; MICRONUCLEUS; PRIORITY JOURNAL; CELL LINE; CELL SURVIVAL; CHROMOSOME BREAKAGE; CHROMOSOME SEGREGATION; COPY NUMBER VARIATION; GENE REARRANGEMENT; GENETICS; GENOMIC INSTABILITY; MUTATION; NEOPLASM; SINGLE CELL ANALYSIS;

CELL LINE; CELL SURVIVAL; CHROMOSOME BREAKAGE; CHROMOSOME SEGREGATION; DNA COPY NUMBER VARIATIONS; DNA DAMAGE; GENE REARRANGEMENT; GENOMIC INSTABILITY; HUMANS; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MUTATION; NEOPLASMS; S PHASE; SINGLE-CELL ANALYSIS;

EID: 84930941966     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14493     Document Type: Article

References (47)

1. Yates, L. R. and Campbell, P. J. Evolution of the cancer genome. Nature Rev. Genet. 13, 795-806 (2012).
2. Helleday, T., Eshtad, S. , Nik-Zainal, S. Mechanisms underlying mutational signatures in human cancers. Nature Rev. Genet. 15, 585-598 (2014).
3. Zhang, C. Z., Leibowitz, M. L. , Pellman, D. Chromothripsis and beyond: rapid genome evolution from complex chromosomal rearrangements. Genes Dev. 27, 2513-2530 (2013).
4. Stephens, P. J. et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144, 27-40 (2011).
5. Rausch, T. et al. Genome sequencing of pediatric medulloblastoma links catastrophic DNA rearrangements with TP53 mutations. Cell 148, 59-71 (2012).
6. Kloosterman, W. P. et al. Constitutional chromothripsis rearrangements involve clustered double-stranded DNA breaks and nonhomologous repairmechanisms. Cell Rep. 1, 648-655 (2012).
7. Korbel, J. O. , Campbell, P. J. Criteria for inference of chromothripsis in cancer genomes. Cell 152, 1226-1236 (2013).
8. Liu, P., Carvalho, C. M., Hastings, P. J. , Lupski, J. R.Mechanisms for recurrent and complex human genomic rearrangements. Curr. Opin. Genet. Dev. 22, 211-220 (2012).
9. Liu, P. et al. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 146, 889-903 (2011).
10. Kinsella, M., Patel, A. , Bafna, V. The elusive evidence for chromothripsis. Nucleic Acids Res. 42, 8231-8242 (2014).
11. Crasta, K. et al. DNA breaks and chromosome pulverization from errors in mitosis. Nature 482, 53-58 (2012).
12. Terradas, M., Martin, M., Tusell, L.& Genesca, A.Genetic activities in micronuclei: is the DNA entrapped in micronuclei lost for the cell?Mutat. Res. 705, 60-67 (2010).
13. Hoffelder, D. R. et al. Resolution of anaphase bridges in cancer cells. Chromosoma 112, 389-397 (2004).
14. 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).
15. Shee, C. et al. Engineered proteins detect spontaneous DNA breakage in human and bacterial cells. Elife 2, e01222 (2013).
16. Ganem, N. J. , Pellman, D. Linking abnormal mitosis to the acquisition of DNA damage. J. Cell Biol. 199, 871-881 (2012).
17. Uetake, Y.& Sluder, G. Prolonged prometaphase blocks daughter cell proliferation despite normal completion of mitosis. Curr. Biol. 20, 1666-1671 (2010).
18. Francis, J. M. et al. EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing. Cancer Discov. 4, 956-971 (2014).
19. Hayashi, M. T., Cesare, A. J., Fitzpatrick, J. A., Lazzerini-Denchi, E. , Karlseder, J. A telomere-dependent DNA damage checkpoint induced by prolonged mitotic arrest. Nature Struct. Mol. Biol. 19, 387-394 (2012).
20. Zhang, C.-Z. A. et al. Calibrating genomic and allelic coverage bias in single-cell sequencing. Nature Commun. 6, 6822 (2015).
21. Simsek, D. et al. DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet. 7, e1002080 (2011).
22. Chiang, C. et al. Complex reorganization and predominant non-homologous repair following chromosomal breakage in karyotypically balanced germline rearrangements and transgenic integration. Nature Genet. 44, 390-397 (2012).
23. Storlazzi, C. T. et al. Gene amplification as double minutes or homogeneously staining regions in solid tumors: origin and structure. Genome Res. 20, 1198-1206 (2010).
24. Carroll, S.M. et al. Double minute chromosomes can be produced fromprecursors derived from a chromosomal deletion. Mol. Cell. Biol. 8, 1525-1533 (1988).
25. Misteli, T. , Soutoglou, E. The emerging role of nuclear architecture in DNA repair and genome maintenance. Nature Rev. Mol. Cell Biol. 10, 243-254 (2009).
26. Garsed, D. W. et al. The architecture and evolution of cancer neochromosomes. Cancer Cell 26, 653-667 (2014).
27. Haber, J. E. Genome stability: DNA repair and recombination (Garland Science, 2014).
28. Sen, S., Hittelman, W. N., Teeter, L. D.and Kuo, M. T.Model for the formation of double minutes fromprematurely condensed chromosomes of replicating micronuclei in drug-treated Chinese hamster ovary cells undergoing DNA amplification. Cancer Res. 49, 6731-6737 (1989).
29. El Achkar, E., Gerbault-Seureau, M., Muleris, M., Dutrillaux, B. , Debatisse, M. Premature condensation induces breaks at the interface of early and late replicating chromosome bands bearing common fragile sites. Proc. Natl Acad. Sci. USA 102, 18069-18074 (2005).
30. Sheltzer, J. M. et al. Aneuploidy drives genomic instability in yeast. Science 333, 1026-1030 (2011).
31. Janssen, A., van der Burg, M., Szuhai, K., Kops, G. J. , Medema, R. H. Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 333, 1895-1898 (2011).
32. Knouse, K. A., Wu, J., Whittaker, C. A. , Amon, A. Single cell sequencing reveals low levels of aneuploidy across mammalian tissues. Proc. Natl Acad. Sci. USA 111, 13409-13414 (2014).
33. Zack, T. I. et al. Pan-cancer patterns of somatic copy number alteration. Nature Genet. 45, 1134-1140 (2013).
34. Malhotra, A. et al. Breakpoint profiling of 64 cancer genomes reveals numerous complex rearrangements spawned by homology-independent mechanisms. Genome Res. 23, 762-776 (2013).
35. Dean, F. B. et al. Comprehensive human genome amplification using multiple displacement amplification. Proc. Natl Acad. Sci. USA 99, 5261-5266 (2002).
36. Voet, T. et al. Single-cell paired-end genome sequencing reveals structural variation per cell cycle. Nucleic Acids Res. 41, 6119-6138 (2013).
37. De Bourcy, C. F. A. et al. A quantitative comparison of single-cell whole-genome amplification methods. PLoS ONE 9, e105585 (2014).
38. Wang, Y. et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 512, 155-160 (2014).
39. Evrony, G. D. et al. Cell lineage analysis in human brain using endogeneous retroelements. Neuron 85, 49-59 (2015).
40. Zong, C. et al. Genome-wide detection of single-nucleotide and copy-number variations of a single human cell. Science 338, 1622-1626 (2012).
41. Pinard, R. et al. Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing. BMC Genomics 7, 216 (2006).
42. Lage, J. M. et al. Whole genome analysis of genetic alterations in small DNA samples using hyperbranched strand displacementamplification and array-CGH. Genome Res. 13, 294-307 (2003).
43. Evrony, G. D. et al. Single-neuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain. Cell 151, 483-496 (2012).
44. Benjamini, Y. , Speed, T. P. Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Res. 40, e72 (2012).
45. Lasken, R. S. , Stockwell, T. B. Mechanism of chimera formation during the Multiple Displacement Amplification reaction. BMC Biotechnol. 7, 19 (2007).
46. Beroukhim, R. et al. The landscape of somatic copy-number alteration across human cancers. Nature 463, 899-905 (2010).
47. Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 (2009).