The presence of extra chromosomes leads to genomic instability

Nature Communications

Volumn 7, Issue , 2016, Pages

  Passerini, Verena ^a,d   Ozeri Galai, Efrat ^b   De Pagter, Mirjam S ^c   Donnelly, Neysan ^a   Schmalbrock, Sarah ^a   Kloosterman, Wigard P ^c   Kerem, Batsheva ^b   Storchová, Zuzana ^a,d,e  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d Munich Center for Integrated Protein Science   (Germany)

^e University of Koblenz Landau   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER; CELLS AND CELL COMPONENTS; CHROMOSOME; ECOPHYSIOLOGY; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; PHENOTYPE; PHYSIOLOGY; TUMOR;

ANEUPLOIDY; ARTICLE; CHROMOSOME BREAKAGE; CHROMOSOME REARRANGEMENT; CHROMOSOME REPLICATION; DNA DAMAGE; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; NEXT GENERATION SEQUENCING; SINGLE NUCLEOTIDE POLYMORPHISM; SUPERNUMERARY CHROMOSOME; TETRASOMY; TRISOMY; BIOSYNTHESIS; CELL CYCLE; CELL LINE; CHROMOSOME 21; CHROMOSOME 3; CHROMOSOME 5; CHROMOSOME 8; COMPARATIVE GENOMIC HYBRIDIZATION; CONFOCAL MICROSCOPY; DNA MICROARRAY; DNA SEQUENCE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HCT 116 CELL LINE; HIGH THROUGHPUT SEQUENCING; METABOLISM; METAPHASE; NEOPLASM;

DNA; MINICHROMOSOME MAINTENANCE PROTEIN;

ANEUPLOIDY; CELL CYCLE; CELL LINE; CHROMOSOMES, HUMAN, PAIR 21; CHROMOSOMES, HUMAN, PAIR 3; CHROMOSOMES, HUMAN, PAIR 5; CHROMOSOMES, HUMAN, PAIR 8; COMPARATIVE GENOMIC HYBRIDIZATION; DNA; FLUORESCENT ANTIBODY TECHNIQUE; GENOMIC INSTABILITY; HCT116 CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; METAPHASE; MICROSCOPY, CONFOCAL; MINICHROMOSOME MAINTENANCE PROTEINS; NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; TETRASOMY; TRISOMY;

EID: 84958206574     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10754     Document Type: Article

References (55)

1. Williams, B. R. et al. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 322, 703-709 (2008).
2. Thompson, S. L. & Compton, D. A. Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J. Cell Biol. 188, 369-381 (2010).
3. Tang, Y. C., Williams, B. R., Siegel, J. J. & Amon, A. Identification of aneuploidy-selective antiproliferation compounds. Cell 144, 499-512 (2011).
4. 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).
5. Mitelman Database of Chromosome Aberrations and Gene Fusions in Cancer (2016). (eds Mitelman, F., Johansson, B., Mertens, F.), http://cgap.nci.nih.gov/Chromosomes/Mitelman.
6. McGranahan, N., Burrell, R. A., Endesfelder, D., Novelli, M. R. & Swanton, C. Cancer chromosomal instability: therapeutic and diagnostic challenges. EMBO Rep. 13, 528-538 (2012).
7. Gordon, D. J., Resio, B. & Pellman, D. Causes and consequences of aneuploidy in cancer. Nat. Rev. Genet. 13, 189-203 (2012).
8. Schvartzman, J.-M., Sotillo, R. & Benezra, R. Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat. Rev. Cancer. 10, 102-115 (2010).
9. Bartkova, J. et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444, 633-637 (2006).
10. Di Micco, R. et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444, 638-642 (2006).
11. Bester, A. C. et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435-446 (2011).
12. 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).
13. Crasta, K. et al. DNA breaks and chromosome pulverization from errors in mitosis. Nature 482, 53-58 (2012).
14. Burrell, R. A. et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 494, 492-496 (2013).
15. Li, R. et al. Aneuploidy correlated 100% with chemical transformation of Chinese hamster cells. Proc. Natl Acad. Sci. USA 94, 14506-14511 (1997).
16. Upender, M. B. et al. Chromosome transfer induced aneuploidy results in complex dysregulation of the cellular transcriptome in immortalized and cancer cells. Cancer Res. 64, 6941-6949 (2004).
17. Niwa, O., Tange, Y. & Kurabayashi, A. Growth arrest and chromosome instability in aneuploid yeast. Yeast 23, 937-950 (2006).
18. Torres, E. M. et al. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317, 916-924 (2007).
19. Pavelka, N. et al. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468, 321-325 (2010).
20. Sheltzer, J. M., Torres, E. M., Dunham, M. J. & Amon, A. Transcriptional consequences of aneuploidy. Proc. Natl Acad. Sci. USA 109, 12644-12649 (2012).
21. Durrbaum, M. et al. Unique features of the transcriptional response to model aneuploidy in human cells. BMC Genomics 15, 139 (2014).
22. Oromendia, A. B., Dodgson, S. E. & Amon, A. Aneuploidy causes proteotoxic stress in yeast. Genes Dev. 26, 2696-2708 (2012).
23. Donnelly, N., Passerini, V., Durrbaum, M., Stingele, S. & Storchova, Z. HSF1 deficiency and impaired HSP90-dependent protein folding are hallmarks of aneuploid human cells. EMBO J. 33, 2374-2387 (2014).
24. Sheltzer, J. M. et al. Aneuploidy drives genomic instability in yeast. Science 333, 1026-1030 (2011).
25. Zhu, J., Pavelka, N., Bradford, W. D., Rancati, G. & Li, R. Karyotypic determinants of chromosome instability in aneuploid budding yeast. PLoS Genet. 8, e1002719 (2012).
26. Blank, H. M., Sheltzer, J. M., Meehl, C. M. & Amon, A. Mitotic entry in the presence of DNA damage is a widespread property of aneuploidy in yeast. Mol. Biol. Cell 26, 1440-1451 (2015).
27. Nicholson, J. M., Macedo, J. C., Mattingly, A. J., Wangsa, D., Camps, J. & Lima, V. et al. Chromosome mis-segregation and cytokinesis failure in trisomic human cells. eLife 4 (2015).
28. Chan, K. L. & Hickson, I. D. New insights into the formation and resolution of ultra-fine anaphase bridges. Semin. Cell Dev. Biol. 22, 906-912 (2011).
29. Lukas, C. et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13, 243-253 (2011).
30. Chan, K. L., Palmai-Pallag, T., Ying, S. & Hickson, I. D. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 11, 753-760 (2009).
31. Hastings, P. J., Ira, G. & Lupski, J. R. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet. 5, e1000327 (2009).
32. Le Tallec, B. et al. Common fragile site profiling in epithelial and erythroid cells reveals that most recurrent cancer deletions lie in fragile sites hosting large genes. Cell Rep. 4, 420-428 (2013).
33. Debacker, K. & Kooy, R. F. Fragile sites and human disease. Hum. Mol. Genet. 2, R150-R158 (2007).
34. Ge, X. Q., Jackson, D. A. & Blow, J. J. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 21, 3331-3341 (2007).
35. Ibarra, A., Schwob, E. & Méndez, J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl Acad. Sci. USA 105, 8956-8961 (2008).
36. Chuang, L. C. et al. Phosphorylation of Mcm2 by Cdc7 promotes prereplication complex assembly during cell-cycle re-entry. Mol. Cell 35, 206-216 (2009).
37. Noguchi, K., Vassilev, A., Ghosh, S., Yates, J. L. & DePamphilis, M. L. The BAH domain facilitates the ability of human Orc1 protein to activate replication origins in vivo. EMBO J. 25, 5372-5382 (2006).
38. Hass, C. S., Gakhar, L. & Wold, M. S. Functional characterization of a cancer causing mutation in human replication protein A. Mol. Cancer Res. 8, 1017-1026 (2010).
39. Ozeri-Galai, E. et al. Failure of origin activation in response to fork stalling leads to chromosomal instability at fragile sites. Mol. Cell 43, 122-131 (2011).
40. Letessier, A. et al. Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 470, 120-123 (2011).
41. Shima, N. et al. A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat. Genet. 39, 93-98 (2007).
42. Pruitt, S. C., Bailey, K. J. & Freeland, A. Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem Cells 25, 3121-3132 (2007).
43. Chuang, C. H., Wallace, M. D., Abratte, C., Southard, T. & Schimenti, J. C. Incremental genetic perturbations to MCM2-7 expression and subcellular distribution reveal exquisite sensitivity of mice to DNA replication stress. PLoS Genet. 6, e1001110 (2010).
44. Jiang, J. et al. Translating dosage compensation to trisomy 21. Nature 500, 296-300 (2013).
45. Li, L. B. et al. Trisomy correction in Down syndrome induced pluripotent stem cells. Cell Stem Cell 11, 615-619 (2012).
46. Oda, T., Hayano, T., Miyaso, H., Takahashi, N. & Yamashita, T. Hsp90 regulates the Fanconi anemia DNA damage response pathway. Blood 109, 5016-5026 (2007).
47. Dyson, N. The regulation of E2F by pRB-family proteins. Genes Dev. 12, 2245-2262 (1998).
48. Flach, J. et al. Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells. Nature 512, 198-202 (2014).
49. Nizetic, D. & Groet, J. Tumorigenesis in Down's syndrome: big lessons from a small chromosome. Nat. Rev. Cancer. 12, 721-732 (2012).
50. Ishimi, Y. et al. Enhanced expression of Mcm proteins in cancer cells derived from uterine cervix. Eur. J. Biochem. 270, 1089-1101 (2003).
51. Toyokawa, G. et al. Minichromosome Maintenance Protein 7 is a potential therapeutic target in human cancer and a novel prognostic marker of non-small cell lung cancer. Mol. Cancer 10, 65 (2011).
52. Das, M. et al. Over expression of minichromosome maintenance genes is clinically correlated to cervical carcinogenesis. PloS ONE 8, e69607 (2013).
53. 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).
54. Kloosterman, W. P. et al. Chromothripsis as a mechanism driving complex de novo structural rearrangements in the germline. Hum. Mol. Genet. 20, 1916-1924 (2011).
55. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).