The cancer biology of whole-chromosome instability

Oncogene

Volumn 32, Issue 40, 2013, Pages 4727-4736

  Duijf, P H G ^a,b   Benezra, R ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

aneuploidy; cancer biology; non cell autonomous; oncogene induced mitotic stress; tumor microenvironment; whole chromosome instability

Indexed keywords

PROTEIN P53; SECURIN; SEPARASE; TUMOR ANTIGEN; TUMOR SUPPRESSOR PROTEIN;

ANEUPLOIDY; CANCER INHIBITION; CARCINOGENESIS; CELL POPULATION; CELL TRANSFORMATION; CHROMOSOMAL INSTABILITY; CHROMOSOME; CHROMOSOME SEGREGATION; CLINICAL FEATURE; GENE MUTATION; HUMAN; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SYSTEMIC DISEASE;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CHROMOSOMAL INSTABILITY; HUMANS; MITOSIS; NEOPLASMS; ONCOGENES;

EID: 84885158978     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.616     Document Type: Review

References (155)

1. Holland AJ, Cleveland DW. Boveri revisited: Chromosomal instability, aneuploidy and tumorigenesis. Nat Rev Mol Cell Biol 2009; 10: 478-487.
2. Schvartzman JM, Sotillo R, Benezra R. Mitotic chromosomal instability and cancer: Mouse modelling of the human disease. Nat Rev Cancer 2010; 10: 102-115.
3. Thompson SL, Bakhoum SF, Compton DA. Mechanisms of chromosomal instability. Curr Biol 2010; 20: R285-R295.
4. Ricke RM, Van Ree JH, Van De Ursen JM. Whole chromosome instability and cancer: A complex relationship. Trends Genet 2008; 24: 457-466.
5. Gordon DJ, Resio B, Pellman D. Causes and consequences of aneuploidy in cancer. Nat Rev Genet 2012; 13: 189-203.
6. Duensing A, Duensing S. Centrosomes, polyploidy and cancer. Adv Exp Med Biol 2010; 676: 93-103.
7. Oliveira RA, Nasmyth K. Getting through anaphase: Splitting the sisters and beyond. Biochem Soc Trans 2010; 38: 1639-1644.
8. Solomon DA, Kim T, Diaz-Martinez LA, Fair J, Elkahloun AG, Harris BT et al. Mutational inactivation of STAG2 causes aneuploidy in human cancer. Science 2011; 333: 1039-1043.
9. Malumbres M. Oncogene-induced mitotic stress: P53 and pRb get mad too. Cancer Cell 2011; 19: 691-692.
10. Sherr CJ, McCormick F. The RB and p53 pathways in cancer. Cancer Cell 2002; 2: 103-112.
11. Saavedra HI, Fukasawa K, Conn CW, Stambrook PJ. MAPK mediates RAS-induced chromosome instability. J Biol Chem 1999; 274: 38083-38090.
12. Nelsen CJ, Kuriyama R, Hirsch B, Negron VC, Lingle WL, Goggin MM et al. Short term cyclin D1 overexpression induces centrosome amplification, mitotic spindle abnormalities, and aneuploidy. J Biol Chem 2005; 280: 768-776.
13. Kamata T, Hussain J, Giblett S, Hayward R, Marais R, Pritchard C. BRAF inactivation drives aneuploidy by de regulating CRAF. Cancer Res 2010; 70: 8475-8486.
14. Cui Y, Borysova MK, Johnson JO, Guadagno TM. Oncogenic B-Raf(V600E) induces spindle abnormalities, supernumerary centrosomes, and aneuploidy in human melanocytic cells. Cancer Res 2010; 70: 675-684.
15. Coschi CH, Martens AL, Ritchie K, Francis SM, Chakrabarti S, Berube NG et al. Mitotic chromosome condensation mediated by the retinoblastoma protein is tumor-suppressive. Genes Dev 2010; 24: 1351-1363.
16. Van Harn T, Foijer F, Van Vugt M, Banerjee R, Yang F, Oostra A et al. Loss of Rb proteins causes genomic instability in the absence of mitogenic signaling. Genes Dev 2010; 24: 1377-1388.
17. Manning AL, Longworth MS, Dyson NJ. Loss of pRB causes centromere dysfunction and chromosomal instability. Genes Dev 2010; 24: 1364-1376.
18. Fukasawa K, Choi T, Kuriyama R, Rulong S, Vande Woude GF. Abnormal centrosome amplification in the absence of p53. Science 1996; 271: 1744-1747.
19. Hernando E, Nahle Z, Juan G, Diaz-Rodriguez E, Alaminos M, Hemann M et al. Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 2004; 430: 797-802.
20. Sotillo R, Hernando E, Diaz-Rodriguez E, Teruya-Feldstein J, Cordon-Cardo C, Lowe SW et al. Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 2007; 11: 9-23.
21. Schvartzman JM, Duijf PH, Sotillo R, Coker C, Benezra R. Mad2 is a critical mediator of the chromosome instability observed upon Rb and p53 pathway inhibition. Cancer Cell 2011; 19: 701-714.
22. Kabeche L, Compton DA. Checkpoint-Independent Stabilization of Kinetochore-Microtubule Attachments by Mad2 in Human Cells. Curr Biol 2012; 22: 638-644.
23. Liu G, Parant JM, Lang G, Chau P, Chavez-Reyes A, El-Naggar AK et al. Chromosome stability, in the absence of apoptosis, is critical for suppression of tumorigenesis in Trp53 mutant mice. Nat Genet 2004; 36: 63-68.
24. Barboza JA, Liu G, Ju Z, El-Naggar AK, Lozano G. p21 de lays tumor onset by preservation of chromosomal stability. Proc Natl Acad Sci USA 2006; 103: 19842-19847.
25. Mukherjee M, Ge G, Zhang N, Huang E, Nakamura LV, Minor M et al. Separase loss of function cooperates with the loss of p53 in the initiation and progression of T-and B-cell lymphoma, leukemia and aneuploidy in mice. PLoS One 2011; 6: E22167.
26. Celton-Morizur S, de sdouets C. Polyploidization of liver cells. Adv Exp Med Biol 2010; 676: 123-135.
27. Duncan AW, Taylor MH, Hickey RD, Hanlon Newell AE, Lenzi ML, Olson SB et al. The ploidy conveyor of mature hepatocytes as a source of genetic variation. Nature 2010; 467: 707-710.
28. Weaver BA, Silk AD, Montagna C, Verdier-Pinard P, Cleveland DW. Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 2007; 11: 25-36.
29. Duijf PH, Schultz N, Benezra R. Cancer cells preferentially lose small chromosomes. Int J Cancer (e-pub ahead of print 5 November 2012; doi:10.1002/ijc.27924).
30. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-674.
31. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature 1998; 396: 643-649.
32. Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A, Florens L et al. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 2010; 468: 321-325.
33. Rodriguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med 2011; 17: 330-339.
34. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128: 683-692.
35. Visconti R, Grieco D. New insights on oxidative stress in cancer. Curr Opin Drug Discov Devel 2009; 12: 240-245.
36. Li M, Fang X, Baker DJ, Guo L, Gao X, Wei Z et al. The ATM-p53 pathway suppresses aneuploidy-induced tumorigenesis. Proc Natl Acad Sci USA 2010; 107: 14188-14193.
37. Wang Z, Yu R, Melmed S. Mice lacking pituitary tumor transforming gene show testicular and splenic hypoplasia, thymic hyperplasia, thrombocytopenia, aberrant cell cycle progression, and premature centromere division. Mol Endocrinol 2001; 15: 1870-1879.
38. Garcia-Higuera I, Manchado E, Dubus P, Canamero M, Mendez J, Moreno S et al. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat Cell Biol 2008; 10: 802-811.
39. Nguyen HG, Makitalo M, Yang D, Chinnappan St D, Hilaire C, Ravid K. de regulated Aurora-B induced tetraploidy promotes tumorigenesis. FASEB J 2009; 23: 2741-2748.
40. Loeb LA. A mutator phenotype in cancer. Cancer Res 2001; 61: 3230-3239.
41. Sheltzer JM, Blank HM, Pfau SJ, Tange Y, George BM, Humpton TJ et al. Aneuploidy drives genomic instability in yeast. Science 2011; 333: 1026-1030.
42. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, Dunham MJ et al. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 2007; 317: 916-924.
43. Williams BR, Prabhu VR, Hunter KE, Glazier CM, Whittaker CA, Housman De et al. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 2008; 322: 703-709.
44. Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria in cancer cells: What is so special about them? Trends Cell Biol 2008; 18: 165-173.
45. Hayashi MT, Cesare AJ, Fitzpatrick JA, Lazzerini-Denchi E, Karlseder J. A telomeredependent DNA damage checkpoint induced by prolonged mitotic arrest. Nat Struct Mol Biol 2012; 19: 387-394.
46. Janssen A, Van Der Burg M, Szuhai K, Kops GJ, Medema RH. Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 2011; 333: 1895-1898.
47. Guerrero AA, Gamero MC, Trachana V, Futterer A, Pacios-Bras C, Diaz-Concha NP et al. Centromere-localized breaks indicate the generation of DNA damage by the mitotic spindle. Proc Natl Acad Sci USA 2010; 107: 4159-4164.
48. Crasta K, Ganem NJ, Dagher R, Lantermann AB, Ivanova EV, Pan Y et al. DNA breaks and chromosome pulverization from errors in mitosis. Nature 2012; 482: 53-58.
49. Stephens PJ, Greenman CD, Fu B, Yang F, Bignell GR, Mudie LJ et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer Development. Cell 2011; 144: 27-40.
50. Liu P, Erez A, Nagamani SC, Dhar SU, Kolodziejska KE, Dharmadhikari AV et al. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 2011; 146: 889-903.
51. Molenaar JJ, Koster J, Zwijnenburg DA, Van Sluis P, Valentijn LJ, Van Der Ploeg I et al. Sequencing of neuroblastoma identifies chromothripsis and de fects in neuritogenesis genes. Nature 2012; 483: 589-593.
52. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010; 463: 899-905.
53. TCGARN. Integrated genomic analyses of ovarian carcinoma. Nature 2011; 474: 609-615.
54. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012; 486: 346-352.
55. Puente XS, Pinyol M, Quesada V, Conde L, Ordonez GR, Villamor N et al. Wholegenome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature 2011; 475: 101-105.
56. Baker DJ, Jeganathan KB, Malureanu L, Perez-Terzic C, Terzic A, Van De Ursen JM. Early aging-associated phenotypes in Bub3/Rae1 haploinsufficient mice. J Cell Biol 2006; 172: 529-540.
57. Schliekelman M, Cowley DO, O?Quinn R, Oliver TG, Lu L, Salmon ED et al. Impaired Bub1 function in vivo compromises tension-dependent checkpoint function leading to aneuploidy and tumorigenesis. Cancer Res 2009; 69: 45-54.
58. Hasle H, Clemmensen IH, Mikkelsen M. Risks of leukaemia and solid tumours in individuals with Down's syndrome. Lancet 2000; 355: 165-169.
59. Satge D, Sasco AJ, Carlsen NL, Stiller CA, Rubie H, Hero B et al. A lack of neuroblastoma in Down syndrome: A study from 11 European countries. Cancer Res 1998; 58: 448-452.
60. Yang Q, Rasmussen SA, Friedman JM. Mortality associated with Down's syndrome in the USA from 1983 to 1997: A population-based study. Lancet 2002; 359: 1019-1025.
61. Swerdlow AJ, Schoemaker MJ, Higgins CD, Wright AF, Jacobs PA. Cancer incidence and mortality in men with Klinefelter syndrome: A cohort study. J Natl Cancer Inst 2005; 97: 1204-1210.
62. Hasle H, Mellemgaard A, Nielsen J, Hansen J. Cancer incidence in men with Klinefelter syndrome. Br J Cancer 1995; 71: 416-420.
63. Torres EM, de phoure N, Panneerselvam A, Tucker CM, Whittaker CA, Gygi SP et al. Identification of aneuploidy-tolerating mutations. Cell 2010; 143: 71-83.
64. Lakovschek IC, Streubel B, Ulm B. Natural outcome of trisomy 13, trisomy 18, and triploidy after prenatal diagnosis. Am J Med Genet A 2011; 155A: 2626-2633.
65. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140: 883-899.
66. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: From immunosurveillance to tumor escape. Nat Immunol 2002; 3: 991-998.
67. Chang CC, Ogino T, Mullins DW, Oliver JL, Yamshchikov GV, Bandoh N et al. Defective human leukocyte antigen class I-associated antigen presentation caused by a novel beta2-microglobulin loss-of-function in melanoma cells. J Biol Chem 2006; 281: 18763-18773.
68. Sanda MG, Restifo NP, Walsh JC, Kawakami Y, Nelson WG, Pardoll DM et al. Molecular characterization of Defective antigen processing in human prostate cancer. J Natl Cancer Inst 1995; 87: 280-285.
69. Khong HT, Restifo NP. Natural selection of tumor variants in the generation of ?tumor escape? phenotypes. Nat Immunol 2002; 3: 999-1005.
70. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: Integrating immunity's roles in cancer suppression and promotion. Science 2011; 331: 1565-1570.
71. DuPage M, Mazumdar C, Schmidt LM, Cheung AF, Jacks T. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 2012; 482: 405-409.
72. Yamada HY, Yao Y, Wang X, Zhang Y, Huang Y, Dai W et al. Haploinsufficiency of SGO1 results in de regulated centrosome dynamics, enhanced chromosomal instability and colon tumorigenesis. Cell Cycle 2012; 11: 479-488.
73. Oshima M, Dinchuk JE, Kargman SL, Oshima H, Hancock B, Kwong E et al. Suppression of intestinal polyposis in Apc de lta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 1996; 87: 803-809.
74. Chulada PC, Thompson MB, Mahler JF, Doyle CM, Gaul BW, Lee C et al. Genetic disruption of Ptgs-1, as well as Ptgs-2, reduces intestinal tumorigenesis in Min mice. Cancer Res 2000; 60: 4705-4708.
75. Rodier F, Coppe JP, Patil CK, Hoeijmakers WA, Munoz DP, Raza SR et al. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 2009; 11: 973-979.
76. Zheng L, Dai H, Zhou M, Li M, Singh P, Qiu J et al. Fen1 mutations result in autoimmunity, chronic inflammation and cancers. Nat Med 2007; 13: 812-819.
77. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009; 9: 239-252.
78. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: Links to genetic instability. Carcinogenesis 2009; 30: 1073-1081.
79. Lonkar P, de don PC. Reactive species and DNA damage in chronic inflammation: Reconciling chemical mechanisms and biological fates. Int J Cancer 2011; 128: 1999-2009.
80. Aivaliotis IL, Pateras IS, Papaioannou M, Glytsou C, Kontzoglou K, Johnson EO et al. How do cytokines trigger genomic instability? J Biomed Biotechnol 2012; 2012: 536761.
81. Sotillo R, Schvartzman JM, Socci ND, Benezra R. Mad2-induced chromosome instability leads to lung tumour relapse after oncogene withdrawal. Nature 2010; 464: 436-440.
82. Galluzzi L, Vanden Berghe T, Vanlangenakker N, Buettner S, Eisenberg T, Vandenabeele P et al. Programmed necrosis from molecules to health and disease. Int Rev Cell Mol Biol 2011; 289: 1-35.
83. Kimmelman AC. The dynamic nature of autophagy in cancer. Genes Dev 2011; 25: 1999-2010.
84. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12: 401-410.
85. Baker DJ, Jeganathan KB, Cameron JD, Thompson M, Juneja S, Kopecka A et al. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 2004; 36: 744-749.
86. Babu JR, Jeganathan KB, Baker DJ, Wu X, Kang-Decker N, Van De Ursen JM. Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J Cell Biol 2003; 160: 341-353.
87. Chesnokova V, Kovacs K, Castro AV, Zonis S, Melmed S. Pituitary hypoplasia in Pttg-/-mice is protective for Rb?/-pituitary tumorigenesis. Mol Endocrinol 2005; 19: 2371-2379.
88. Li M, Fang X, Wei Z, York JP, Zhang P. Loss of spindle assembly checkpointmediated inhibition of Cdc20 promotes tumorigenesis in mice. J Cell Biol 2009; 185: 983-994.
89. Andreassen PR, Lohez OD, Lacroix FB, Margolis RL. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol Biol Cell 2001; 12: 1315-1328.
90. Rieder CL, Maiato H. Stuck in division or passing through: What happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell 2004; 7: 637-651.
91. Zhang D, Shimizu T, Araki N, Hirota T, Yoshie M, Ogawa K et al. Aurora A overexpression induces cellular senescence in mammary gland hyperplastic tumors Developed in p53-deficient mice. Oncogene 2008; 27: 4305-4314.
92. Bitomsky N, Hofmann TG. Apoptosis and autophagy: Regulation of apoptosis by DNA damage signalling-roles of p53, p73 and HIPK2. FEBS J 2009; 276: 6074-6083.
93. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434: 864-870.
94. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: Mitotic catastrophe. Cell Death Differ 2008; 15: 1153-1162.
95. Manchado E, Guillamot M, Malumbres M. Killing cells by targeting mitosis. Cell Death Differ 2012; 19: 369-377.
96. Gascoigne KE, Taylor SS. Cancer cells display profound intra-and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 2008; 14: 111-122.
97. Terrano DT, Upreti M, Chambers TC. Cyclin-dependent kinase 1-mediated Bcl-xL/Bcl-2 phosphorylation acts as a functional link coupling mitotic arrest and apoptosis. Mol Cell Biol 2010; 30: 640-656.
98. Thompson SL, Compton DA. Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J Cell Biol 2010; 188: 369-381.
99. Mikule K, de laval B, Kaldis P, Jurcyzk A, Hergert P, Doxsey S. Loss of centrosome integrity induces p38-p53-p21-dependent G1-S arrest. Nat Cell Biol 2007; 9: 160-170.
100. Lanni JS, Jacks T. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol Cell Biol 1998; 18: 1055-1064.
101. Minn AJ, Boise LH, Thompson CB. Expression of Bcl-xL and loss of p53 can cooperate to overcome a cell cycle checkpoint induced by mitotic spindle damage. Genes Dev 1996; 10: 2621-2631.
102. Reinhardt HC, Schumacher B. The p53 network: Cellular and systemic DNA damage responses in aging and cancer. Trends Genet 2012; 28: 128-136.
103. de ng Y, Chan SS, Chang S. Telomere dysfunction and tumour suppression: The senescence connection. Nat Rev Cancer 2008; 8: 450-458.
104. Burds AA, Lutum AS, Sorger PK. Generating chromosome instability through the simultaneous de letion of Mad2 and p53. Proc Natl Acad Sci USA 2005; 102: 11296-11301.
105. Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012; 481: 306-313.
106. Hanahan D, Coussens LM. Accessories to the crime: Functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21: 309-322.
107. Ostrand-Rosenberg S. Immune surveillance: A balance between protumor and antitumor immunity. Curr Opin Genet Dev 2008; 18: 11-18.
108. Mason SD, Joyce JA. Proteolytic networks in cancer. Trends Cell Biol 2011; 21: 228-237.
109. Lewis CE, de palma M, Naldini L. Tie2-expressing monocytes and tumor angiogenesis: Regulation by hypoxia and angiopoietin-2. Cancer Res 2007; 67: 8429-8432.
110. Seremet T, Brasseur F, Coulie PG. Tumor-specific antigens and immunologic adjuvants in cancer immunotherapy. Cancer J 2011; 17: 325-330.
111. Granot Z, Henke E, Comen EA, King TA, Norton L, Benezra R. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 2011; 20: 300-314.
112. Png KJ, Halberg N, Yoshida M, Tavazoie SF. A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature 2012; 481: 190-194.
113. Carter SL, Eklund AC, Kohane IS, Harris LN, Szallasi Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat Genet 2006; 38: 1043-1048.
114. Gutenberg A, Gerdes JS, Jung K, Sander B, Gunawan B, Bock HC et al. High chromosomal instability in brain metastases of colorectal carcinoma. Cancer Genet Cytogenet 2010; 198: 47-51.
115. Bhattacharya A, Roy R, Snijders AM, Hamilton G, Paquette J, Tokuyasu T et al. Two distinct routes to oral cancer differing in genome instability and risk for cervical node metastasis. Clin Cancer Res 2011; 17: 7024-7034.
116. Kreike B, Halfwerk H, Armstrong N, Bult P, Foekens JA, Veltkamp SC et al. Local recurrence after breast-conserving therapy in relation to gene expression patterns in a large series of patients. Clin Cancer Res 2009; 15: 4181-4190.
117. Smid M, Hoes M, Sieuwerts AM, Sleijfer S, Zhang Y, Wang Y et al. Patterns and incidence of chromosomal instability and their prognostic relevance in breast cancer subtypes. Breast Cancer Res Treat 2011; 128: 23-30.
118. Skirnisdottir I, Sorbe B, Karlsson M, Seidal T. Prognostic importance of DNA ploidy and p53 in early stages of epithelial ovarian carcinoma. Int J Oncol 2001; 19: 1295-1302.
119. Warth A, Herpel E, Krysa S, Hoffmann H, Schnabel PA, Schirmacher P et al. Chromosomal instability is more frequent in metastasized than in non-metastasized pulmonary carcinoids but is not a reliable predictor of metastatic potential. Exp Mol Med 2009; 41: 349-353.
120. Schardt JA, Meyer M, Hartmann CH, Schubert F, Schmidt-Kittler O, Fuhrmann C et al. Genomic analysis of single cytokeratin-positive cells from bone marrow reveals early mutational events in breast cancer. Cancer Cell 2005; 8: 227-239.
121. Schmidt-Kittler O, Ragg T, Daskalakis A, Granzow M, Ahr A, Blankenstein TJ et al. From latent disseminated cells to overt metastasis: Genetic analysis of systemic breast cancer progression. Proc Natl Acad Sci USA 2003; 100: 7737-7742.
122. Stoecklein NH, Hosch SB, Bezler M, Stern F, Hartmann CH, Vay C et al. Direct genetic analysis of single disseminated cancer cells for prediction of outcome and therapy selection in esophageal cancer. Cancer Cell 2008; 13: 441-453.
123. Weckermann D, Polzer B, Ragg T, Blana A, Schlimok G, Arnholdt H et al. Perioperative activation of disseminated tumor cells in bone marrow of patients with prostate cancer. J Clin Oncol 2009; 27: 1549-1556.
124. McClelland SE, Burrell RA, Swanton C. Chromosomal instability: A composite phenotype that influences sensitivity to chemotherapy. Cell Cycle 2009; 8: 3262-3266.
125. Duesberg P, Stindl R, Hehlmann R. Explaining the high mutation rates of cancer cells to drug and multidrug resistance by chromosome reassortments that are catalyzed by aneuploidy. Proc Natl Acad Sci USA 2000; 97: 14295-14300.
126. Swanton C, Nicke B, Schuett M, Eklund AC, Ng C, Li Q et al. Chromosomal instability de termines taxane response. Proc Natl Acad Sci USA 2009; 106: 8671-8676.
127. Bedard PL, Di Leo A, Piccart-Gebhart MJ. Taxanes: Optimizing adjuvant chemotherapy for early-stage breast cancer. Nat Rev Clin Oncol 2010; 7: 22-36.
128. Janssen A, Kops GJ, Medema RH. Elevating the frequency of chromosome missegregation as a strategy to kill tumor cells. Proc Natl Acad Sci USA 2009; 106: 19108-19113.
129. Rebacz B, Larsen TO, Clausen MH, Ronnest MH, Loffler H, Ho AD et al. Identification of griseofulvin as an inhibitor of centrosomal clustering in a phenotypebased screen. Cancer Res 2007; 67: 6342-6350.
130. Karna P, Rida PC, Pannu V, Gupta KK, Dalton WB, Joshi H et al. A novel microtubule-modulating noscapinoid triggers apoptosis by inducing spindle multipolarity via centrosome amplification and de clustering. Cell Death Differ 2011; 18: 632-644.
131. Kwon M, Godinho SA, Chandhok NS, Ganem NJ, Azioune A, Thery M et al. Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev 2008; 22: 2189-2203.
132. Wu G, Qiu XL, Zhou L, Zhu J, Chamberlin R, Lau J et al. Small molecule targeting the Hec1/Nek2 mitotic pathway suppresses tumor cell growth in culture and in animal. Cancer Res 2008; 68: 8393-8399.
133. Tang YC, Williams BR, Siegel JJ, Amon A. Identification of aneuploidy-selective antiproliferation compounds. Cell 2011; 144: 499-512.
134. Ishida S, Huang E, Zuzan H, Spang R, Leone G, West M et al. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cell Biol 2001; 21: 4684-4699.
135. Polager S, Kalma Y, Berkovich E, Ginsberg D. E2Fs up-regulate expression of genes involved in DNA replication, DNA repair and mitosis. Oncogene 2002; 21: 437-446.
136. Ren B, Cam H, Takahashi Y, Volkert T, Terragni J, Young RA et al. E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. Genes Dev 2002; 16: 245-256.
137. Zhou Y, Mehta KR, Choi AP, Scolavino S, Zhang X. DNA damage-induced inhibition of securin expression is mediated by p53. J Biol Chem 2003; 278: 462-470.
138. Oikawa T, Okuda M, Ma Z, Goorha R, Tsujimoto H, Inokuma H et al. Transcriptional control of BubR1 by p53 and suppression of centrosome amplification by BubR1. Mol Cell Biol 2005; 25: 4046-4061.
139. Lu LY, Wood JL, Ye L, Minter-Dykhouse K, Saunders TL, Yu X et al. Aurora A is essential for early embryonic Development and tumor suppression. J Biol Chem 2008; 283: 31785-31790.
140. Iwanaga Y, Chi YH, Miyazato A, Sheleg S, Haller K, Peloponese Jr JM et al. Heterozygous de letion of mitotic arrest-deficient protein 1 (MAD1) increases the incidence of tumors in mice. Cancer Res 2007; 67: 160-166.
141. Michel LS, Liberal V, Chatterjee A, Kirchwegger R, Pasche B, Gerald W et al. MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 2001; 409: 355-359.
142. Lu LY, Wood JL, Minter-Dykhouse K, Ye L, Saunders TL, Yu X et al. Polo-like kinase 1 is essential for early embryonic Development and tumor suppression. Mol Cell Biol 2008; 28: 6870-6876.
143. Ko MA, Rosario CO, Hudson JW, Kulkarni S, Pollett A, de nnis JW et al. Plk4 haploinsufficiency causes mitotic infidelity and carcinogenesis. Nat Genet 2005; 37: 883-888.
144. Jeganathan K, Malureanu L, Baker DJ, Abraham SC, Van De Ursen JM. Bub1 mediates cell Death in response to chromosome missegregation and acts to suppress spontaneous tumorigenesis. J Cell Biol 2007; 179: 255-267.
145. Ricke RM, Jeganathan KB, Van De Ursen JM. Bub1 overexpression induces aneuploidy and tumor formation through Aurora B kinase hyperactivation. J Cell Biol 2011; 193: 1049-1064.
146. Diaz-Rodriguez E, Sotillo R, Schvartzman JM, Benezra R. Hec1 overexpression hyperactivates the mitotic checkpoint and induces tumor formation in vivo. Proc Natl Acad Sci USA 2008; 105: 16719-16724.
147. Van Ree JH, Jeganathan KB, Malureanu L, Van De Ursen JM. Overexpression of the E2 ubiquitin-conjugating enzyme UbcH10 causes chromosome missegregation and tumor formation. J Cell Biol 2010; 188: 83-100.
148. Janisson-Dargaud D, Durlach A, Lorenzato M, Grange F, Bernard P, Birembaut P. Aneuploidy, but not Ki-67 or EGFR expression, is associated with recurrences in basal cell carcinoma. J Cutan Pathol 2008; 35: 916-921.
149. Susini T, Olivieri S, Molino C, Amunni G, Rapi S, Taddei G et al. DNA ploidy is stronger than lymph node metastasis as prognostic factor in cervical carcinoma: 10-year results of a prospective study. Int J Gynecol Cancer 2011; 21: 678-684.
150. Walther A, Houlston R, Tomlinson I. Association between chromosomal instability and prognosis in colorectal cancer: A meta-analysis. Gut 2008; 57: 941-950.
151. Lagarde P, Perot G, Kauffmann A, Brulard C, Dapremont V, Hostein I et al. Mitotic checkpoints and chromosome instability are strong predictors of clinical outcome in gastrointestinal stromal tumors. Clin Cancer Res 2012; 18: 826-838.
152. Choi CM, Seo KW, Jang SJ, Oh YM, Shim TS, Kim WS et al. Chromosomal instability is a risk factor for poor prognosis of adenocarcinoma of the lung: Fluorescence in situ hybridization analysis of paraffin-embedded tissue from Korean patients. Lung Cancer 2009; 64: 66-70.
153. Ehlers JP, Worley L, Onken MD, Harbour JW. Integrative genomic analysis of aneuploidy in uveal melanoma. Clin Cancer Res 2008; 14: 115-122.
154. Sato H, Uzawa N, Takahashi K, Myo K, Ohyama Y, Amagasa T. Prognostic utility of chromosomal instability de tected by fluorescence in situ hybridization in fineneedle aspirates from oral squamous cell carcinomas. BMC Cancer 2010; 10: 182.
155. Pinto AE, Silva GL, Pereira T, Cabrera RA, Santos JR, Leite V. S-phase fraction and ploidy as predictive markers in primary disease and recurrence of papillary thyroid carcinoma. Clin Endocrinol (Oxf) 2012; 77: 302-309.