Tetraploid cells from cytokinesis failure induce aneuploidy and spontaneous transformation of mouse ovarian surface epithelial cells

Cell Cycle

Volumn 11, Issue 15, 2012, Pages 2864-2875

  Lv, Lei ^a   Zhang, Tianwei ^a   Yi, Qiyi ^a   Huang, Yun ^a   Wang, Zheng ^a   Hou, Heli ^a   Zhang, Huan ^a   Zheng, Wei ^a   Hao, Qiaomei ^a   Guo, Zongyou ^b   Cooke, Howard J ^a,c   Shi, Qinghua ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Aneuploidy; Chromosome mis segregation; Cytokinesis failure; Ovarian cancer; Tetraploid cells

Indexed keywords

ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL TRANSFORMATION; CHROMOSOME ANALYSIS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOKINESIS; DIPLOIDY; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; MITOSIS; MOUSE; NONHUMAN; OVARY CANCER; TETRAPLOIDY;

MUS;

EID: 84864540104     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.21196     Document Type: Article

References (49)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009; 59:225-49; PMID:19474385; http://dx.doi.org/10.3322/ caac.20006.
2. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev 2001; 22:255-88; PMID:11294827; http://dx.doi.org/10.1210/er.22.2.255.
3. Riman T, Persson I, Nilsson S. Hormonal aspects of epithelial ovarian cancer: review of epidemiological evidence. Clin Endocrinol (Oxf) 1998; 49:695-707; PMID:10209555; http://dx.doi.org/10.1046/j.1365-2265.1998.00577.x.
4. Fathalla MF. Incessant ovulation--a factor in ovarian neoplasia? Lancet 1971; 2:163; PMID:4104488; http://dx.doi.org/10.1016/S0140-6736(71)92335-X.
5. Godwin AK, Testa JR, Handel LM, Liu Z, Vanderveer LA, Tracey PA, et al. Spontaneous transformation of rat ovarian surface epithelial cells: association with cytogenetic changes and implications of repeated ovulation in the etiology of ovarian cancer. J Natl Cancer Inst 1992; 84:592-601; PMID:1556770; http://dx.doi.org/10.1093/jnci/84.8.592.
6. Testa JR, Getts LA, Salazar H, Liu Z, Handel LM, Godwin AK, et al. Spontaneous transformation of rat ovarian surface epithelial cells results in well to poorly differentiated tumors with a parallel range of cytogenetic complexity. Cancer Res 1994; 54:2778-84; PMID:8168110.
7. Roby KF, Taylor CC, Sweetwood JP, Cheng Y, Pace JL, Tawfik O, et al. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 2000; 21:585-91; PMID:10753190; http://dx.doi.org/10.1093/carcin/ 21.4.585.
8. Roberts PC, Mottillo EP, Baxa AC, Heng HH, Doyon-Reale N, Gregoire L, et al. Sequential molecular and cellular events during neoplastic progression: a mouse syngeneic ovarian cancer model. Neoplasia 2005; 7:944-56; PMID:16242077; http://dx.doi.org/10.1593/neo.05358.
9. Holland AJ, Cleveland DW. Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat Rev Mol Cell Biol 2009; 10:478-87; PMID:19546858; http://dx.doi.org/10.1038/nrm2718.
10. Weaver BA, Cleveland DW. Does aneuploidy cause cancer? Curr Opin Cell Biol 2006; 18:658-67; PMID:17046232; http://dx.doi.org/10.1016/j.ceb.2006.10. 002.
11. Lassus H, Staff S, Leminen A, Isola J, Butzow R. Aurora-A overexpression and aneuploidy predict poor outcome in serous ovarian carcinoma. Gynecol Oncol 2011; 120:11-7; PMID:20937525; http://dx.doi.org/10.1016/j.ygyno.2010.09.003.
12. Kim YT, Zhao M, Kim SH, Lee CS, Kim JH, Kim JW. Prognostic significance of DNA quantification by flow cytometry in ovarian tumors. Int J Gynaecol Obstet 2005; 88:286-91; PMID:15733883; http://dx.doi.org/10.1016/j.ijgo.2004.12.010.
13. Ozalp S, Yalcin OT, Gulbas Z, Tanir HM, Minsin T. Effect of cellular DNA content on the prognosis of epithelial ovarian cancers. Gynecol Obstet Invest 2001; 52:93-7; PMID:11586035; http://dx.doi.org/10.1159/000052950.
14. Pothuri B, Leitao MM, Levine DA, Viale A, Olshen AB, Arroyo C, et al. Genetic analysis of the early natural history of epithelial ovarian carcinoma. PLoS One 2010; 5:e10358; PMID:20436685; http://dx.doi.org/10.1371/journal.pone. 0010358.
15. Compton DA. Mechanisms of aneuploidy. Curr Opin Cell Biol 2011; 23:109-13; PMID:20810265; http://dx.doi.org/10.1016/j.ceb.2010.08.007.
16. Thompson SL, Bakhoum SF, Compton DA. Mechanisms of chromosomal instability. Curr Biol 2010; 20:R285-95; PMID:20334839; http://dx.doi.org/10. 1016/j.cub.2010.01.034.
17. Boveri T, Boveri M. The origin of malignant tumors. Baltimore: The Williams & Wilkins Company, 1929.
18. Shackney SE, Smith CA, Miller BW, Burholt DR, Murtha K, Giles HR, et al. Model for the genetic evolution of human solid tumors. Cancer Res 1989; 49:3344-54; PMID:2720687.
19. Storchova Z, Pellman D. From polyploidy to aneuploidy, genome instability and cancer. Nat Rev Mol Cell Biol 2004; 5:45-54; PMID:14708009; http://dx.doi.org/10.1038/nrm1276.
20. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005; 437:1043-7; PMID:16222300; http://dx.doi.org/10.1038/ nature04217.
21. Shi Q, King RW. Chromosome nondisjunction yields tetraploid rather than aneuploid cells in human cell lines. Nature 2005; 437:1038-42; PMID:16222248; http://dx.doi.org/10.1038/nature03958.
22. Galipeau PC, Cowan DS, Sanchez CA, Barrett MT, Emond MJ, Levine DS, et al. 17p (p53) allelic losses, 4N (G2/tetraploid) populations, and progression to aneuploidy in Barrett's esophagus. Proc Natl Acad Sci USA 1996; 93:7081-4; PMID:8692948; http://dx.doi.org/10.1073/pnas.93.14.7081.
23. Olaharski AJ, Sotelo R, Solorza-Luna G, Gonsebatt ME, Guzman P, Mohar A, et al. Tetraploidy and chromosomal instability are early events during cervical carcinogenesis. Carcinogenesis 2006; 27:337-43; PMID:16123119; http://dx.doi.org/10.1093/carcin/bgi218.
24. Levine DS, Rabinovitch PS, Haggitt RC, Blount PL, Dean PJ, Rubin CE, et al. Distribution of aneuploid cell populations in ulcerative colitis with dysplasia or cancer. Gastroenterology 1991; 101:1198-210; PMID:1936790.
25. Yancik R. Ovarian cancer. Age contrasts in incidence, histology, disease stage at diagnosis, and mortality. Cancer 1993; 71(Suppl):517-23; PMID:8420671; http://dx.doi.org/10.1002/cncr.2820710205.
26. Chuaire-Noack L, Rondón-Lagos S, Ramírez-Corredor A, Ibáñez-Pinilla M, Ramírez-Clavijo S. Cytogenetic aberrations in primary cell cultures of the ovarian surface epithelium. Invest Clin 2010; 51:541-51; PMID:21361148.
27. Bayani J, Paderova J, Murphy J, Rosen B, Zielenska M, Squire JA. Distinct patterns of structural and numerical chromosomal instability characterize sporadic ovarian cancer. Neoplasia 2008; 10:1057-65; PMID:18813350.
28. Yoon BS, Kim YT, Kim S, Lee CS, Kim JW, Kim JH, et al. Prognostic value of nuclear DNA quantification and cyclin A expression in epithelial ovarian carcinoma. Eur J Obstet Gynecol Reprod Biol 2008; 136:110-5; PMID:17157431; http://dx.doi.org/10.1016/j.ejogrb.2006.10.008.
29. Kristensen GB, Kildal W, Abeler VM, Kaern J, Vergote I, Tropé CG, et al. Large-scale genomic instability predicts long-term outcome for women with invasive stage I ovarian cancer. Ann Oncol 2003; 14:1494-500; PMID:14504048; http://dx.doi.org/10.1093/annonc/mdg403.
30. Friedlander ML, Taylor IW, Russell P, Musgrove EA, Hedley DH, Tattersall MH. Ploidy as a prognostic factor in ovarian cancer. Int J Gynecol Pathol 1983; 2:55-63; PMID:6307906; http://dx.doi.org/10.1097/00004347-198301000-00005.
31. Tsao SW, Mok SC, Fey EG, Fletcher JA, Wan TS, Chew EC, et al. Characterization of human ovarian surface epithelial cells immortalized by human papilloma viral oncogenes (HPV-E6E7 ORFs). Exp Cell Res 1995; 218:499-507; PMID:7796885; http://dx.doi.org/10.1006/excr.1995.1184.
32. Davies BR, Steele IA, Edmondson RJ, Zwolinski SA, Saretzki G, von Zglinicki T, et al. Immortalisation of human ovarian surface epithelium with telomerase and temperature-sensitive SV40 large T antigen. Exp Cell Res 2003; 288:390-402; PMID:12915130; http://dx.doi.org/10.1016/S0014-4827(03)00218-0.
33. Caldwell CM, Green RA, Kaplan KB. APC mutations lead to cytokinetic failures in vitro and tetraploid genotypes in Min mice. J Cell Biol 2007; 178:1109-20; PMID:17893240; http://dx.doi.org/10.1083/jcb.200703186.
34. Rosario CO, Ko MA, Haffani YZ, Gladdy RA, Paderova J, Pollett A, et al. Plk4 is required for cytokinesis and maintenance of chromosomal stability. Proc Natl Acad Sci USA 2010; 107:6888-93; PMID:20348415; http://dx.doi.org/10.1073/ pnas.0910941107.
35. Sagona AP, Stenmark H. Cytokinesis and cancer. FEBS Lett 2010; 584:2652-61; PMID:20371245; http://dx.doi.org/10.1016/j.febslet.2010.03.044.
36. Duelli DM, Padilla-Nash HM, Berman D, Murphy KM, Ried T, Lazebnik Y. A virus causes cancer by inducing massive chromosomal instability through cell fusion. Curr Biol 2007; 17:431-7; PMID:17320392; http://dx.doi.org/10.1016/j. cub.2007.01.049.
37. Mazumdar M, Lee JH, Sengupta K, Ried T, Rane S, Misteli T. Tumor formation via loss of a molecular motor protein. Curr Biol 2006; 16:1559-64; PMID:16890532; http://dx.doi.org/10.1016/j.cub.2006.06.029.
38. Ganem NJ, Storchova Z, Pellman D. Tetraploidy, aneuploidy and cancer. Curr Opin Genet Dev 2007; 17:157-62; PMID:17324569; http://dx.doi.org/10.1016/j. gde.2007.02.011.
39. Ganem NJ, Godinho SA, Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009; 460:278-82; PMID:19506557; http://dx.doi.org/10.1038/nature08136.
40. Silkworth WT, Nardi IK, Scholl LM, Cimini D. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome missegregation in cancer cells. PLoS One 2009; 4:e6564; PMID:19668340; http://dx.doi.org/10.1371/journal.pone.0006564.
41. Cimini D, Howell B, Maddox P, Khodjakov A, Degrassi F, Salmon ED. Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J Cell Biol 2001; 153:517-27; PMID:11331303; http://dx.doi.org/10.1083/jcb.153.3.517.
42. Atkin NB. Modal DNA value and chromosome number in ovarian neoplasia. A clinical and histopathologic assessment. Cancer 1971; 27:1064-73; PMID:4325742; http://dx.doi.org/10.1002/1097-0142(197105)27:5〈1064::AID- CNCR2820270510〉3.0.CO;2-K.
43. Kusyk CJ, Seski JC, Medlin WV, Edwards CL. Progressive chromosome changes associated with different sites of one ovarian carcinoma. J Natl Cancer Inst 1981; 66:1021-5; PMID:6941036.
44. Wang X, Allen TD, May RJ, Lightfoot S, Houchen CW, Huycke MM. Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect. Cancer Res 2008; 68:9909-17; PMID:19047172; http://dx.doi.org/10.1158/0008-5472.CAN-08-1551.
45. Umeda M, Murata-Kamiya N, Saito Y, Ohba Y, Takahashi M, Hatakeyama M. Helicobacter pylori CagA causes mitotic impairment and induces chromosomal instability. J Biol Chem 2009; 284:22166-72; PMID:19546211; http://dx.doi.org/ 10.1074/jbc.M109.035766.
46. Shi QH, Adler ID, Yu L, Zhang JX. Detection of numerical chromosomal aberrations in epididymal sperm of mice using three-color FISH with chromosome-specific DNA probes. Yi Chuan Xue Bao 1999; 26:458-67; PMID:10665221.
47. Shi Q, Adler ID, Zhang J, Zhang X, Shan X, Martin R. Incidence of mosaic cell lines in vivo and malsegregation of chromosome 21 in lymphocytes in vitro of trisomy 21 patients: detection by fluorescence in situ hybridization on binucleated lymphocytes. Hum Genet 2000; 106:29-35; PMID:10982178; http://dx.doi.org/10.1007/s004390051005.
48. Takahashi S, Qian J, Brown JA, Alcaraz A, Bostwick DG, Lieber MM, et al. Potential markers of prostate cancer aggressiveness detected by fluorescence in situ hybridization in needle biopsies. Cancer Res 1994; 54:3574-9; PMID:8012984.
49. Rao X, Zhang Y, Yi Q, Hou H, Xu B, Chu L, et al. Multiple origins of spontaneously arising micronuclei in HeLa cells: direct evidence from long-term live cell imaging. Mutat Res 2008; 646:41-9; PMID:18845170; http://dx.doi.org/ 10.1016/j.mrfmmm.2008.09.004.