Persistent Telomere Damage Induces Bypass of Mitosis and Tetraploidy

Cell

Volumn 141, Issue 1, 2010, Pages 81-93

  Davoli, Teresa ^a   Denchi, Eros Lazzerini ^a   de Lange, Titia ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Cellcycle; DNA; Humdisease

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN B; GEMININ; PROTEIN P53; REPLICATION LICENSING FACTOR CDT1;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL CYCLE G2 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL PROLIFERATION; CHROMOSOME DAMAGE; CHROMOSOME DUPLICATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; MALIGNANT NEOPLASTIC DISEASE; MITOSIS; MOLECULAR IMAGING; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TELOMERE; TETRAPLOIDY;

EID: 77950932096     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.01.031     Document Type: Article

References (54)

1. Andreassen P.R., Lohez O.D., Lacroix F.B., Margolis R.L. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol. Biol. Cell 2001, 12:1315-1328.
2. Artandi S.E., Chang S., Lee S.L., Alson S., Gottlieb G.J., Chin L., DePinho R.A. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 2000, 406:641-645.
3. Ballabeni A., Melixetian M., Zamponi R., Masiero L., Marinoni F., Helin K. Human geminin promotes pre-RC formation and DNA replication by stabilizing CDT1 in mitosis. EMBO J. 2004, 23:3122-3132.
4. Barlow C., Hirotsune S., Paylor R., Liyanage M., Eckhaus M., Collins F., Shiloh Y., Crawley J.N., Ried T., Tagle D., Wynshaw-Boris A. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 1996, 86:159-171.
5. Bassermann F., Frescas D., Guardavaccaro D., Busino L., Peschiaroli A., Pagano M. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 2008, 134:256-267.
6. Blow J.J., Dutta A. Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 2005, 6:476-486.
7. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., Wright W.E. Extension of life-span by introduction of telomerase into normal human cells. Science 1998, 279:349-352.
8. Caldwell C.M., Green R.A., Kaplan K.B. APC mutations lead to cytokinetic failures in vitro and tetraploid genotypes in Min mice. J. Cell Biol. 2007, 178:1109-1120.
9. Carder P., Wyllie A.H., Purdie C.A., Morris R.G., White S., Piris J., Bird C.C. Stabilised p53 facilitates aneuploid clonal divergence in colorectal cancer. Oncogene 1993, 8:1397-1401.
10. Celli G.B., de Lange T. DNA processing not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 2005, 7:712-718.
11. Chin K., De Solorzano C.O., Knowles D., Jones A., Chou W., Rodriguez E.G., Kuo W.L., Ljung B.M., Chew K., Myambo K., et al. In situ analyses of genome instability in breast cancer. Nat. Genet. 2004, 36:984-988.
12. Chin L., Artandi S.E., Shen Q., Tam A., Lee S.L., Gottlieb G.J., Greider C.W., DePinho R.A. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 1999, 97:527-538.
13. d'Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., Saretzki G., Carter N.P., Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003, 426:194-198.
14. Danes B.S. Increased in vitro tetraploidy: tissue specific within the heritable colorectal cancer syndromes with polyposis coli. Cancer 1978, 41:2330-2334.
15. de Lange T., Jacks T. For better or worse? Telomerase inhibition and cancer. Cell 1999, 98:273-275.
16. de Lange T., Shiue L., Myers R.M., Cox D.R., Naylor S.L., Killery A.M., Varmus H.E. Structure and variability of human chromosome ends. Mol. Cell. Biol. 1990, 10:518-527.
17. Denchi E.L., de Lange T. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 2007, 448:1068-1071.
18. Diffley J.F. Regulation of early events in chromosome replication. Curr. Biol. 2004, 14:R778-R786.
19. Dikovskaya D., Schiffmann D., Newton I.P., Oakley A., Kroboth K., Sansom O., Jamieson T.J., Meniel V., Clarke A., Nathke I.S. Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J. Cell Biol. 2007, 176:183-195.
20. Duelli D.M., Padilla-Nash H.M., Berman D., Murphy K.M., Ried T., Lazebnik Y. A virus causes cancer by inducing massive chromosomal instability through cell fusion. Curr. Biol. 2007, 17:431-437.
21. Dutrillaux B., Gerbault-Seureau M., Remvikos Y., Zafrani B., Prieur M. Breast cancer genetic evolution: I. Data from cytogenetics and DNA content. Breast Cancer Res. Treat. 1991, 19:245-255.
22. Fujiwara T., Bandi M., Nitta M., Ivanova E.V., Bronson R.T., Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005, 437:1043-1047.
23. Galipeau P.C., Cowan D.S., Sanchez C.A., Barrett M.T., Emond M.J., Levine D.S., Rabinovitch P.S., Reid B.J. 17p (p53) allelic losses, 4N (G2/tetraploid) populations, and progression to aneuploidy in Barrett's esophagus. Proc. Natl. Acad. Sci. USA 1996, 93:7081-7084.
24. Ganem N.J., Storchova Z., Pellman D. Tetraploidy, aneuploidy and cancer. Curr. Opin. Genet. Dev. 2007, 17:157-162.
25. Garcia-Higuera I., Manchado E., Dubus P., Canamero M., Mendez J., Moreno S., Malumbres M. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat. Cell Biol. 2008, 10:802-811.
26. Hastie N.D., Dempster M., Dunlop M.G., Thompson A.M., Green D.K., Allshire R.C. Telomere reduction in human colorectal carcinoma and with ageing. Nature 1990, 346:866-868.
27. Hayles J., Fisher D., Woollard A., Nurse P. Temporal order of S phase and mitosis in fission yeast is determined by the state of the p34cdc2-mitotic B cyclin complex. Cell 1994, 78:813-822.
28. Hockemeyer D., Daniels J.P., Takai H., de Lange T. Recent expansion of the telomeric complex in rodents: Two distinct POT1 proteins protect mouse telomeres. Cell 2006, 126:63-77.
29. Itzhaki J.E., Gilbert C.S., Porter A.C. Construction by gene targeting in human cells of a " conditional" CDC2 mutant that rereplicates its DNA. Nat. Genet. 1997, 15:258-265.
30. Kiang L., Heichinger C., Watt S., Bahler J., Nurse P. Cyclin-dependent kinase inhibits reinitiation of a normal S-phase program during G2 in fission yeast. Mol. Cell. Biol. 2009, 29:4025-4032.
31. Kim N.W., Piatyszek M.A., Prowse K.R., Harley C.B., West M.D., Ho P.L., Coviello G.M., Wright W.E., Weinrich S.L., Shay J.W. Specific association of human telomerase activity with immortal cells and cancer. Science 1994, 266:2011-2015.
32. Kops G.J., Weaver B.A., Cleveland D.W. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 2005, 5:773-785.
33. Lanni J.S., Jacks T. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol. Cell. Biol. 1998, 18:1055-1064.
34. Lee H.W., Blasco M.A., Gottlieb G.J., Horner J.W., Greider C.W., DePinho R.A. Essential role of mouse telomerase in highly proliferative organs. Nature 1998, 392:569-574.
35. Levine D.S., Rabinovitch P.S., Haggitt R.C., Blount P.L., Dean P.J., Rubin C.E., Reid B.J. Distribution of aneuploid cell populations in ulcerative colitis with dysplasia or cancer. Gastroenterology 1991, 101:1198-1210.
36. Li M., Shin Y.H., Hou L., Huang X., Wei Z., Klann E., Zhang P. The adaptor protein of the anaphase promoting complex Cdh1 is essential in maintaining replicative lifespan and in learning and memory. Nat. Cell Biol. 2008, 10:1083-1089.
37. Maser R.S., DePinho R.A. Connecting chromosomes, crisis, and cancer. Science 2002, 297:565-569.
38. Narbonne-Reveau K., Senger S., Pal M., Herr A., Richardson H.E., Asano M., Deak P., Lilly M.A. APC/CFzr/Cdh1 promotes cell cycle progression during the Drosophila endocycle. Development 2008, 135:1451-1461.
39. Olaharski A.J., Sotelo R., Solorza-Luna G., Gonsebatt M.E., Guzman P., Mohar A., Eastmond D.A. Tetraploidy and chromosomal instability are early events during cervical carcinogenesis. Carcinogenesis 2006, 27:337-343.
40. Pantic M., Zimmermann S., El Daly H., Opitz O.G., Popp S., Boukamp P., Martens U.M. Telomere dysfunction and loss of p53 cooperate in defective mitotic segregation of chromosomes in cancer cells. Oncogene 2006, 25:4413-4420.
41. Peters J.M. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 2002, 9:931-943.
42. Rabinovitch P.S., Reid B.J., Haggitt R.C., Norwood T.H., Rubin C.E. Progression to cancer in Barrett's esophagus is associated with genomic instability. Lab. Invest. 1989, 60:65-71.
43. Reina-San-Martin B., Nussenzweig M.C., Nussenzweig A., Difilippantonio S. Genomic instability, endoreduplication, and diminished Ig class-switch recombination in B cells lacking Nbs1. Proc. Natl. Acad. Sci. USA 2005, 102:1590-1595.
44. Sakaue-Sawano A., Kurokawa H., Morimura T., Hanyu A., Hama H., Osawa H., Kashiwagi S., Fukami K., Miyata T., Miyoshi H., et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 2008, 132:487-498.
45. Shi Q., King R.W. Chromosome nondisjunction yields tetraploid rather than aneuploid cells in human cell lines. Nature 2005, 437:1038-1042.
46. Sotillo R., Hernando E., Diaz-Rodriguez E., Teruya-Feldstein J., Cordon-Cardo C., Lowe S.W., Benezra R. Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 2007, 11:9-23.
47. Storchova Z., Kuffer C. The consequences of tetraploidy and aneuploidy. J. Cell Sci. 2008, 121:3859-3866.
48. Toledo L.I., Murga M., Gutierrez-Martinez P., Soria R., Fernandez-Capetillo O. ATR signaling can drive cells into senescence in the absence of DNA breaks. Genes Dev. 2008, 22:297-302.
49. van Steensel B., Smogorzewska A., de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell 1998, 92:401-413.
50. Waldman T., Lengauer C., Kinzler K.W., Vogelstein B. Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature 1996, 381:713-716.
51. Wang X., Zou L., Zheng H., Wei Q., Elledge S.J., Li L. Genomic instability and endoreduplication triggered by RAD17 deletion. Genes Dev. 2003, 17:965-970.
52. Weaver B.A., Silk A.D., Cleveland D.W. Cell biology: nondisjunction, aneuploidy and tetraploidy. Nature 2006, 442:E9-E10.
53. Yoshihara T., Ishida M., Kinomura A., Katsura M., Tsuruga T., Tashiro S., Asahara T., Miyagawa K. XRCC3 deficiency results in a defect in recombination and increased endoreduplication in human cells. EMBO J. 2004, 23:670-680.
54. Zielke N., Querings S., Rottig C., Lehner C., Sprenger F. The anaphase-promoting complex/cyclosome (APC/C) is required for rereplication control in endoreplication cycles. Genes Dev. 2008, 22:1690-1703.