The consequences of tetraploidy and aneuploidy

Journal of Cell Science

Volumn 121, Issue 23, 2008, Pages 3859-3866

  Storchova, Zuzana ^a   Kuffer, Christian ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Aneuploidy; Chromosomal instability; Tetraploidy

Indexed keywords

APC PROTEIN; BETA CATENIN; BRCA2 PROTEIN; KINESIN; ONCOPROTEIN; PROTEIN MAD2; PROTEIN MDM2; PROTEIN P16; PROTEIN P21; PROTEIN P53; RETINOBLASTOMA PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ANEUPLOIDY; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DIVISION; CELL FUSION; CELL TRANSFORMATION; CENTROSOME; CHROMOSOMAL INSTABILITY; CHROMOSOME REARRANGEMENT; COLON CANCER; DRUG TARGETING; GENE MUTATION; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; KARYOTYPE; MALIGNANT TRANSFORMATION; MITOSIS; NONHUMAN; PATHOPHYSIOLOGY; POLYPLOIDY; PRIORITY JOURNAL; REVIEW; SUPERNUMERARY CHROMOSOME; TETRAPLOIDY; TISSUE DIFFERENTIATION; UTERINE CERVIX CANCER;

ANEUPLOIDY; ANIMALS; CELL DIVISION; CHROMOSOMAL INSTABILITY; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; POLYPLOIDY;

FUNGI;

EID: 59349098193     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.039537     Document Type: Review

References (87)

1. Andreassen, P. R., Lohez, O. D., Lacroix, F. B. and Margolis, R. L. (2001). Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol. Biol. Cell 12, 1315-1328.
2. Aylon, Y., Michael, D., Shmueli, A., Yabuta, N., Nojima, H. and Oren, M. (2006). A positive feedback loop between the p53 and Lats2 tumor suppressors prevents tetraploidization. Genes Dev. 20, 2687-2700.
3. Azeddine, E., Cunha, M. and Kirsch-Volders, M. (1998). Spindle poisons can induce polyploidy by mitotic slippage and micronucleate mononucleates in the cytokinesis-block assay. Mutagenesis 13, 193-198.
4. Barrett, M. T., Pritchard, D., Palanca-Wessels, C., Anderson, J., Reid, B. J. and Rabinovitch, P. S. (2003). Molecular phenotype of spontaneously arising 4N (G2-Tetraploid) intermediates of neoplastic progression in Barrett's esophagus. Cancer Res. 63, 4211-4217.
5. Basto, R., Brunk, K., Vinadogrova, T., Peel, N., Franz, A., Khodjakov, A. and Raff, J. W. (2008). Centrosome amplification can initiate tumorigenesis in flies. Cell 133, 1032-1042.
6. Biesterfeld, S., Gerres, K., Fischer-Wein, G. and Bocking, A. (1994). Polyploidy in non-neoplastic tissues. J. Clin. Pathol. 47, 38-42.
7. Blagosklonny, M. V. (2006). Prolonged mitosis versus tetraploid checkpoint: how p53 measures the duration of mitosis. Cell Cycle 5, 971-975.
8. Boveri, T. (2008). Concerning the Origin of Malignant Tumours by Theodor Boveri. Translated and annotated by Henry Harris. J. Cell Sci. 121, S1-S84.
9. Brinkley, B. R. and Goepfert, T. M. (1998). Supernumerary centrosomes and cancer: Boveri's hypothesis resurrected. Cell Motil. Cytoskeleton 41, 281-288.
10. Brito, D. A. and Rieder, C. L. (2006). Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr. Biol. 16, 1194-1200.
11. Caldwell, C. M., Green, R. A. and Kaplan, K. B. (2007). APC mutations lead to cytokinetic failures in vitro and tetraploid genotypes in Min mice. J. Cell Biol. 178, 1109-1120.
12. Carr, D. H. and Gedeon, M. M. (1978). Q-banding of chromosomes in human spontaneous abortions. Can. J. Genet. Cytol. 20, 415-425.
13. Castillo, A., Morse, H. C., 3rd, Godfrey, V. L., Naeem, R. and Justice, M. J. (2007). Overexpression of Eg5 causes genomic instability and tumor formation in mice. Cancer Res. 67, 10138-10147.
14. Chi, Y. H. and Jeang, K. T. (2007). Aneuploidy and cancer. J. Cell Biochem. 102, 531-538.
15. Clevers, H. (2006). Wnt/β-Catenin signaling in development and disease. Cell 127, 469-480.
16. Comai, L. (2005). The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836-846.
17. Cowell, J. K. and Wigley, C. B. (1980). Changes in DNA content during in vitro transformation of mouse salivary-gland epithelium. J. Natl. Cancer Inst. 64, 1443-1449.
18. Cross, S. M., Sanchez, C. A., Morgan, C. A., Schimke, M. K., Ramel, S., Idzerda, R. L., Raskind, W. H. and Reid, B. J. (1995). A p53-dependent mouse spindle checkpoint. Science 267, 1353-1356.
19. Dalton, W. B., Nandan, M. O., Moore, R. T. and Yang, V. W. (2007). Human cancer cells commonly acquire DNA damage during mitotic arrest. Cancer Res. 67, 11487-11492.
20. Danes, B. S. (1976). Gardner syndrome-increased tetraploidy in cultured skin fibroblast. J. Med. Genet. 13, 52-56.
21. Daniels, M. J., Wang, Y., Lee, M. and Venkitaraman, A. R. (2004). Abnormal cytokinesis in cells deficient in the breast cancer susceptibility protein BRCA2. Science 306, 876-879.
22. Dikovskaya, D., Schiffmann, D., Newton, I. P., Oakley, A., Kroboth, K., Sansom, O., Jamieson, T. J., Meniel, V., Clarke, A. and Nathke, I. S. (2007). Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J. Cell Biol. 176, 183-195.
23. Duelli, D. M., Hearn, S., Myers, M. P. and Lazebnik, Y. (2005). A primate virus generates transformed human cells by fusion. J. Cell Biol. 171, 493-503.
24. Duelli, D. M., Padilla-Nash, H. M., Berman, D., Murphy, K. M., Ried, T. and Lazebnik, Y. (2007). A virus causes cancer by inducing massive chromosomal instability through cell fusion. Curr. Biol. 17, 431-437.
25. Edgar, B. A. and Orr-Weaver, T. L. (2001). Endoreplication cell cycles: more for less. Cell 105, 297-306.
26. Eiben, B., Bartels, I., Bähr-Porsch, S., Borgmann, S., Gatz, G., Gellert, G., Goebel, R., Hammans, W., Hentemann, M. and Osmers, R. (1990). Cytogenetic analysis of 750 spontaneous abortions with the direct-preparation method of chorionic villi and its implications for studying genetic causes of pregnancy wastage. Am. J. Hum. Genet. 47, 656-663.
27. Fausto, N. and Campbell, J. S. (2003). The role of hepatocytes and oval cells in liver regeneration and repopulation. Mech. Dev. 120, 117-130.
28. Fearon, E. R. and Vogelstein, B. (1990). A genetic model for colorectal tumorigenesis. Cell 61, 759-767.
29. Fuhrken, P. G., Apostolidis, P. A., Lindsey, S., Miller, W. M. and Papoutsakis, E. T. (2008). Tumor suppressor protein p53 regulates megakaryocytic polyploidization and apoptosis. J. Biol. Chem. 283, 15589-15600.
30. Fujiwara, T., Bandi, M., Nitta, M., Ivanova, E. V., Bronson, R. T. and Pellman, D. (2005). Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437, 1043-1047.
31. Galipeau, P. C., Cowan, D. S., Sanchez, C. A., Barrett, M. T., Emond, M. J., Levine, D. S., Rabinovitch, P. S. and Reid, B. J. (1996). 17p (p53) allelic losses, 4N (G2/tetraploid) populations, and progression to aneuploidy in Barrett's esophagus. Proc. Natl. Acad. Sci. USA 93, 7081-7084.
32. Ganem, N. J. and Pellman, D. (2007). Limiting the proliferation of polyploid cells. Cell 131, 437-440.
33. Ghadimi, B. M., Sackett, D. L., Difilippantonio, M. J., Schröck, E., Neumann, T., Jauho, A., Auer, G. and Ried, T. (2000). Centrosome amplification and instability occurs exclusively in aneuploid, but not in diploid colorectal cancer cell lines, and correlates with numerical chromosomal aberrations. Genes Chromosomes Cancer 27, 183-190.
34. Gisselsson, D., Hakanson, U., Stoller, P., Marti, D., Jin, Y., Rosengren, A. H., Stewenius, Y., Kahl, F. and Panagopoulos, I. (2008). When the genome plays dice: circumvention of the spindle assembly checkpoint and near-random chromosome segregation in multipolar cancer cell mitoses. PLoS ONE 3, e1871.
35. Gjoerup, O. V., Wu, J., Chandler-Militello, D., Williams, G. L., Zhao, J., Schaffhausen, B., Jat, P. S. and Roberts, T. M. (2007). Surveillance mechanism linking Bub1 loss to the p53 pathway. Proc. Natl. Acad. Sci. USA 104, 8334-8339.
36. Gottesfeld, J. M. and Forbes, D. J. (1997). Mitotic repression of the transcriptional machinery. Trends Biochem. Sci. 22, 197-202.
37. Guidotti, J. E., Bregerie, O., Robert, A., Debey, P., Brechot, C. and Desdouets, C. (2003). Liver cell polyploidization: a pivotal role for binuclear hepatocytes. J. Biol. Chem. 278, 19095-19101.
38. Ha, G. H., Baek, K. H., Kim, H. S., Jeong, S. J., Kim, C. M., McKeon, F. and Lee, C. W. (2007). p53 activation in response to mitotic spindle damage requires signaling via BubR1-mediated phosphorylation. Cancer Res. 67, 7155-7164.
39. Hassold, T., Chen, N., Funkhouser, J., Jooss, T., Manuel, B., Matsuura, J., Matsuyama, A., Wilson, C., Yamane, J. A. and Jacobs, P. A. (1980). A cytogenetic study of 1000 spontaneous abortions. Ann. Hum. Genet. 44, 151-178.
40. Hau, P. M., Siu, W. Y., Wong, N., Lai, P. B. S. and Poon, R. Y. C. (2006). Polyploidization increases the sensitivity to DNA-damaging agents in mammalian cells. FEBS Lett. 580, 4727-4736.
41. Hernando, E., Nahle, Z., Juan, G., Diaz-Rodriguez, E., Alaminos, M., Hemann, M., Michel, L., Mittal, V., Gerald, W., Benezra, R. et al. (2004). Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 430, 797-802.
42. Hinchcliffe, E. H., Li, C., Thompson, E. A., Maller, J. L. and Sluder, G. (1999). Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283, 851-854.
43. Jannink, G., Duplantier, B. and Sikorav, J. L. (1996). Forces on chromosomal DNA during anaphase. Biophys. J. 71, 451-465.
44. Jeganathan, K., Malureanu, L., Baker, D. J., Abraham, S. C. and van Deursen, J. M. (2007). Bub1 mediates cell death in response to chromosome missegregation and acts to suppress spontaneous tumorigenesis. J. Cell Biol. 179, 255-267.
45. Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Habedanck, R., Stierhof, Y. D. and Nigg, E. A. (2007). Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202.
46. Kops, G. J., Weaver, B. A. and Cleveland, D. W. (2005). On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 5, 773-785.
47. Kuriyama, R., Terada, Y., Lee, K. S. and Wang, C. L. (2007). Centrosome replication in hydroxyurea-arrested CHO cells expressing GFP-tagged centrin2. J. Cell. Sci. 120, 2444-2453.
48. Kwon, M., Godinho, S. A., Chandhok, N. S., Ganem, N. J., Azioune, A., Thery, M. and Pellman, D. (2008). Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev. 22, 2189-2203.
49. Lanni, J. S. and Jacks, T. (1998). Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol. Cell. Biol. 18, 1055-1064.
50. Lengauer, C., Kinzler, K. W. and Vogelstein, B. (1997). Genetic instability in colorectal cancers. Nature 386, 623-627.
51. Livingstone, L. R., White, A., Sprouse, J., Livanos, E., Jacks, T. and Tlsty, T. D. (1992). Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell 70, 923-935.
52. Mable, B. K. and Otto, S. P. (2001). Masking and purging mutations following EMS treatment in haploid, diploid and tetraploid yeast (Saccharomyces cerevisiae). Genet. Res. 77, 9-26.
53. Maley, C. C. (2007). Multistage carcinogenesis in Barrett's esophagus. Cancer Lett. 245, 22-32.
54. Margolis, R. L., Lohez, O. D. and Andreassen, P. R. (2003). G1 tetraploidy checkpoint and the suppression of tumorigenesis. J. Cell. Biochem. 88, 673-683.
55. Mayer, V. W. and Aguilera, A. (1990). High levels of chromosome instability in polyploids of Saccharomyces cerevisiae. Mutat. Res. 231, 177-186.
56. -/- cells. EMBO J. 21, 483-492.
57. Meraldi, P., Honda, R. and Nigg, E. A. (2004). Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr. Opin. Genet. Dev. 14, 29-36.
58. Migeon, B. R., Norum, R. A. and Corsaro, C. M. (1974). Isolation and analysis of somatic hybrids derived from two human diploid cells. Proc. Natl. Acad. Sci. USA 71, 937-941.
59. Mikule, K., Delaval, B., Kaldis, P., Jurcyzk, A., Hergert, P. and Doxsey, S. (2007). Loss of centrosome integrity induces p38-p53-p21-dependent G1-S arrest. Nat. Cell Biol. 9, 160-170.
60. Mullins, J. and Biesele, J. J. (1977). Terminal phase of cytokinesis in D-98S cells. J. Cell Biol. 73, 672-684.
61. Musacchio, A. and Salmon, E. D. (2007). The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell. Biol. 8, 379-393.
62. Neuber, M., Rehder, H., Zuther, C., Lettau, R. and Schwinger, E. (1993). Polyploidies in abortion material decrease with maternal age. Hum. Genet. 91, 563-566.
63. Nicklas, R. B., Waters, J. C., Salmon, E. D. and Ward, S. C. (2001). Checkpoint signals in grasshopper meiosis are sensitive to microtubule attachment, but tension is still essential. J. Cell Sci. 114, 4173-4183.
64. Nigg, E. A. (2002). Centrosome aberrations: cause or consequence of cancer progression? Nat. Rev. Cancer 2, 815-825.
65. Olaharski, A. J., Sotelo, R., Solorza-Luna, G., Gonsebatt, M. E., Guzman, P., Mohar, A. and Eastmond, D. A. (2006). Tetraploidy and chromosomal instability are early events during cervical carcinogenesis. Carcinogenesis 27, 337-343.
66. Ornitz, D. M., Hammer, R. E., Messing, A., Palmiter, R. D. and Brinster, R. L. (1987). Pancreatic neoplasia induced by SV40 T-antigen expression in acinar cells of transgenic mice. Science 238, 188-193.
67. Oshimori, N., Ohsugi, M. and Yamamoto, T. (2006). The Plk1 target Kizuna stabilizes mitotic centrosomes to ensure spindle bipolarity. Nat. Cell Biol. 8, 1095-1101.
68. Otto, S. P. (2007). The Evolutionary consequences of polyploidy. Cell 131, 452-462.
69. Quignon, F., Rozier, L., Lachages, A. M., Bieth, A., Simili, M. and Debatisse, M. (2007). Sustained mitotic block elicits DNA breaks: one-step alteration of ploidy and chromosome integrity in mammalian cells. Oncogene 26, 165-172.
70. Quintyne, N. J., Reing, J. E., Hoffelder, D. R., Gollin, S. M. and Saunders, W. S. (2005). Spindle multipolarity is prevented by centrosomal clustering. Science 307, 127-129.
71. Reverte, C. G., Benware, A., Jones, C. W. and LaFlamme, S. E. (2006). Perturbing integrin function inhibits microtubule growth from centrosomes, spindle assembly, and cytokinesis. J. Cell Biol. 174, 491-497.
72. Rusan, N. M. and Peifer, M. (2008). Original CIN: reviewing roles for APC in chromosome instability. J. Cell Biol. 181, 719-726.
73. Shackney, S. E., Smith, C. A., Miller, B. W., Burholt, D. R., Murtha, K., Giles, H. R., Ketterer, D. M. and Pollice, A. A. (1989). Model for the genetic evolution of human solid tumors. Cancer Res. 49, 3344-3354.
74. Shi, Q. and King, R. W. (2005). Chromosome nondisjunction yields tetraploid rather than aneuploid cells in human cell lines. Nature 437, 1038-1042.
75. Shin, H. J., Baek, K. H., Jeon, A. H., Park, M. T., Lee, S. J., Kang, C. M., Lee, H. S., Yoo, S. H., Chung, D. H., Sung, Y. C. et al. (2003). Dual roles of human BubR1, a mitotic checkpoint kinase, in the monitoring of chromosomal instability. Cancer Cell 4, 483-497.
76. Sjoblom, T., Jones, S., Wood, L. D., Parsons, D. W., Lin, J., Barber, T. D., Mandelker, D., Leary, R. J., Ptak, J., Silliman, N. et al. (2006). The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274.
77. Sotillo, R., Hernando, E., Diaz-Rodriguez, E., Teruya-Feldstein, J., Cordon-Cardo, C., Lowe, S. W. and Benezra, R. (2007). Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 11, 9-23.
78. Storchova, Z. and Pellman, D. (2004). From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell. Biol. 5, 45-54.
79. Storchova, Z., Breneman, A., Cande, J., Dunn, J., Burbank, K., O'Toole, E. and Pellman, D. (2006). Genome-wide genetic analysis of polyploidy in yeast. Nature 443, 541-547.
80. Uetake, Y. and Sluder, G. (2004). Cell cycle progression after cleavage failure: mammalian somatic cells do not possess a 'tetraploidy checkpoint'. J. Cell Biol. 165, 609-615.
81. Uetake, Y. and Sluder, G. (2007). Cell-cycle progression without an intact microtubule cytoskeleton. Curr. Biol. 17, 2081-2086.
82. von Hansemann, D. (1890). Ueber asymmetrische Zellteilung in Epithelkrebsen und deren biologische Bedeutung. Virchows Arch. Path. Anat. Physiol. Klin. Med. 119, 299-326.
83. Wang, X., Zhou, Y. X., Qiao, W., Tominaga, Y., Ouchi, M., Ouchi, T. and Deng, C. X. (2006). Overexpression of aurora kinase A in mouse mammary epithelium induces genetic instability preceding mammary tumor formation. Oncogene 25, 7148-7158.
84. Warburton, D., Kline, J. and Kinney, A. (1994). No maternal age relationship for polyploidy. Hum. Genet. 93, 725-726.
85. Weaver, B. A., Silk, A. D., Montagna, C., Verdier-Pinard, P. and Cleveland, D. W. (2007). Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 11, 25-36.
86. Wong, C. and Stearns, T. (2005). Mammalian cells lack checkpoints for tetraploidy, aberrant centrosome number, and cytokinesis failure. BMC Cell Biol. 6, 6.
87. Yang, Z., Loncarek, J., Khodjakov, A. and Rieder, C. L. (2008). Extra centrosomes and/or chromosomes prolong mitosis in human cells. Nat. Cell Biol. 10, 748-751.