Chromosomal breaks during mitotic catastrophe trigger γH2AX-ATM-p53-mediated apoptosis

Journal of Cell Science

Volumn 124, Issue 17, 2011, Pages 2951-2963

  Imreh, Gabriela ^a   Norberg, Helin Vakifahmetoglu ^b   Imreh, Stefan ^a   Zhivotovsky, Boris ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Apoptosis; Cell death; Checkpoint; Genomic instability; Mitotic catastrophe

Indexed keywords

ATM PROTEIN; ATR PROTEIN; DNA; DOXORUBICIN; HISTONE H2AX; PROTEIN P21; PROTEIN P53; STRATIFIN; SYNAPSIN I;

ANAPHASE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE G1 PHASE; CELL DEATH; CELL DESTRUCTION; CHROMOSOME BREAKAGE; CHROMOSOME DAMAGE; CONTROLLED STUDY; DNA DAMAGE; EPITHELIUM CELL; MITOSIS; MITOTIC CATASTROPHE; MOUSE; MULTINUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

14-3-3 PROTEINS; APOPTOSIS; CASPASES; CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOME ABERRATIONS; CHROMOSOME BREAKAGE; DNA DAMAGE; DNA-BINDING PROTEINS; DOXORUBICIN; EXONUCLEASES; G1 PHASE; GENE KNOCKOUT TECHNIQUES; GENOMIC INSTABILITY; HCT116 CELLS; HISTONES; HUMANS; MITOSIS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; S PHASE; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 80053966362     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.081612     Document Type: Article

References (44)

1. Brown, E. J. and Baltimore, D. (2000). ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14, 397-402.
2. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J. P., Sedivy, J. M., Kinzler, K. W. and Vogelstein, B. (1998). Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497-1501.
3. Carrassa, L., Sanchez, Y., Erba, E. and Damia, G. (2009). U2OS cells lacking Chk1 undergo aberrant mitosis and fail to activate the spindle checkpoint. J. Cell. Mol. Med. 13, 1565-1576.
4. Castedo, M., Coquelle, A., Vivet, S., Vitale, I., Kauffmann, A., Dessen, P., Pequignot, M. O., Casares, N., Valent, A., Mouhamad, S., Schmitt, E., Modjtahedi, N., Vainchenker, W., Zitvogel, L., Lazar, V., Garrido, C. and Kroemer, G. (2006). Apoptosis regulation in tetraploid cancer cells. EMBO J. 25, 2584-2595.
5. Castedo, M., Perfettini, J. L., Roumier, T., Valent, A., Raslova, H., Yakushijin, K., Horne, D., Feunteun, J., Lenoir, G., Medema, R. et al. (2004a). Mitotic catastrophe constitutes a special case of apoptosis whose suppression entails aneuploidy. Oncogene 23, 4362-4370.
6. Castedo, M., Perfettini, J. L., Roumier, T., Yakushijin, K., Horne, D., Medema, R. and Kroemer, G. (2004b). The cell cycle checkpoint kinase Chk2 is a negative regulator of mitotic catastrophe. Oncogene 23, 4353-4361.
7. Chan, T. A., Hermeking, H., Lengauer, C., Kinzler, K. W. and Vogelstein, B. (1999). 14-3-3Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 401, 616-620. de Klein, A., Muijtjens, M., van Os, R., Verhoeven, Y., Smit, B., Carr, A. M.,
8. Lehmann, A. R. and Hoeijmakers, J. H. (2000). Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10, 479-482.
9. Eom, Y. W., Kim, M. A., Park, S. S., Goo, M. J., Kwon, H. J., Sohn, S., Kim, W. H., Yoon, G. and Choi, K. S. (2005). Two distinct modes of cell death induced by doxorubicin: apoptosis and cell death through mitotic catastrophe accompanied by senescence-like phenotype. Oncogene 24, 4765-4777.
10. Erenpreisa, J., Kalejs, M. and Cragg, M. S. (2005). Mitotic catastrophe and endomitosis in tumour cells: an evolutionary key to a molecular solution. Cell Biol. Int. 29, 1012-1018.
11. Fernandez-Capetillo, O., Mahadevaiah, S. K., Celeste, A., Romanienko, P. J., Camerini-Otero, R. D., Bonner, W. M., Manova, K., Burgoyne, P. and Nussenzweig, A. (2003). H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 4, 497-508.
12. Gewirtz, D. A. (1999). A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol. 57, 727-741.
13. Giunta, S., Belotserkovskaya, R. and Jackson, S. P. (2010). DNA damage signaling in response to double-strand breaks during mitosis. J. Cell Biol. 190, 197-207.
14. Green, P. S. and Leeuwenburgh, C. (2002). Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim. Biophys. Acta 1588, 94-101.
15. Ha, G. H., Kim, H. S., Lee, C. G., Park, H. Y., Kim, E. J., Shin, H. J., Lee, J. C., Lee, K. W. and Lee, C. W. (2009). Mitotic catastrophe is the predominant response to histone acetyltransferase depletion. Cell Death Differ. 16, 483-497.
16. Hekmat-Nejad, M., You, Z., Yee, M. C., Newport, J. W. and Cimprich, K. A. (2000). Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Curr. Biol. 10, 1565-1573.
17. Huang, X., Tran, T., Zhang, L., Hatcher, R. and Zhang, P. (2005). DNA damage-induced mitotic catastrophe is mediated by the Chk1-dependent mitotic exit DNA damage checkpoint. Proc. Natl. Acad. Sci. USA 102, 1065-1070.
18. Ichijima, Y., Sakasai, R., Okita, N., Asahina, K., Mizutani, S. and Teraoka, H. (2005). Phosphorylation of histone H2AX at M phase in human cells without DNA damage response. Biochem. Biophys. Res. Commun. 336, 807-812.
19. Kastan, M. B. and Lim, D. S. (2000). The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol. 1, 179-186.
20. Kil, W. J., Cerna, D., Burgan, W. E., Beam, K., Carter, D., Steeg, P. S., Tofilon, P. J. and Camphausen, K. (2008). In vitro and in vivo radiosensitization induced by the DNA methylating agent temozolomide. Clin. Cancer Res. 14, 931-938.
21. Kodym, E., Kodym, R., Choy, H. and Saha, D. (2008). Sustained metaphase arrest in response to ionizing radiation in a non-small cell lung cancer cell line. Radiat. Res. 169, 46-58.
22. Loffler, H., Lukas, J., Bartek, J. and Kramer, A. (2006). Structure meets function-centrosomes, genome maintenance and the DNA damage response. Exp. Cell Res. 312, 2633-2640.
23. Momparler, R. L., Karon, M., Siegel, S. E. and Avila, F. (1976). Effect of adriamycin on DNA, RNA, and protein synthesis in cell-free systems and intact cells. Cancer Res. 36, 2891-2895.
24. Nabha, S. M., Mohammad, R. M., Dandashi, M. H., Coupaye-Gerard, B., Aboukameel, A., Pettit, G. R. and Al-Katib, A. M. (2002). Combretastatin-A4 prodrug induces mitotic catastrophe in chronic lymphocytic leukemia cell line independent of caspase activation and poly(ADP-ribose) polymerase cleavage. Clin. Cancer Res. 8, 2735-2741.
25. Niida, H., Tsuge, S., Katsuno, Y., Konishi, A., Takeda, N. and Nakanishi, M. (2005). Depletion of Chk1 leads to premature activation of Cdc2-cyclin B and mitotic catastrophe. J. Biol. Chem. 280, 39246-39252.
26. Niikura, Y., Dixit, A., Scott, R., Perkins, G. and Kitagawa, K. (2007). BUB1 mediation of caspase-independent mitotic death determines cell fate. J. Cell Biol. 178, 283-296.
27. Olsson, M., Vakifahmetoglu, H., Abruzzo, P. M., Hogstrand, K., Grandien, A. and Zhivotovsky, B. (2009). DISC-mediated activation of caspase-2 in DNA damage-induced apoptosis. Oncogene 28, 1949-1959.
28. Park, S. S., Eom, Y. W. and Choi, K. S. (2005). Cdc2 and Cdk2 play critical roles in low dose doxorubicin-induced cell death through mitotic catastrophe but not in high dose doxorubicin-induced apoptosis. Biochem. Biophys. Res. Commun. 334, 1014-1021.
29. Park, S. S., Kim, M. A., Eom, Y. W. and Choi, K. S. (2007). Bcl-xL blocks high dose doxorubicin-induced apoptosis but not low dose doxorubicin-induced cell death through mitotic catastrophe. Biochem. Biophys. Res. Commun. 363, 1044-1049.
30. Radford, I. R. and Murphy, T. K. (1994). Radiation response of mouse lymphoid and myeloid cell lines. Part III. Different signals can lead to apoptosis and may influence sensitivity to killing by DNA double-strand breakage. Int. J. Radiat. Biol. 65, 229-239.
31. Roninson, I. B., Broude, E. V. and Chang, B. D. (2001). If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist. Updat. 4, 303-313.
32. Roschke, A. V., Stover, K., Tonon, G., Schaffer, A. A. and Kirsch, I. R. (2002). Stable karyotypes in epithelial cancer cell lines despite high rates of ongoing structural and numerical chromosomal instability. Neoplasia 4, 19-31.
33. Sasaki, Y. F., Saga, A., Akasaka, M., Yoshida, K., Nishidate, E., Su, Y. Q., Matsusaka, N. and Tsuda, S. (1997). In vivo genotoxicity of ortho-phenylphenol, biphenyl, and thiabendazole detected in multiple mouse organs by the alkaline single cell gel electrophoresis assay. Mutat. Res. 395, 189-198.
34. Spallarossa, P., Garibaldi, S., Altieri, P., Fabbi, P., Manca, V., Nasti, S., Rossettin, P., Ghigliotti, G., Ballestrero, A., Patrone, F. et al. (2004). Carvedilol prevents doxorubicin-induced free radical release and apoptosis in cardiomyocytes in vitro. J. Mol. Cell. Cardiol. 37, 837-846.
35. Tinel, A. and Tschopp, J. (2004). The PIDDosome, a protein complex implicated in activation of caspase-2 in response to genotoxic stress. Science 304, 843-846.
36. Toh, W. H., Nam, S. Y. and Sabapathy, K. (2010). An essential role for p73 in regulating mitotic cell death. Cell Death Differ. 17, 787-800.
37. Tsang, W. P., Chau, S. P., Kong, S. K., Fung, K. P. and Kwok, T. T. (2003). Reactive oxygen species mediate doxorubicin induced p53-independent apoptosis. Life Sci. 73, 2047-2058.
38. Vakifahmetoglu, H., Olsson, M., Orrenius, S. and Zhivotovsky, B. (2006). Functional connection between p53 and caspase-2 is essential for apoptosis induced by DNA damage. Oncogene 25, 5683-5692.
39. Vakifahmetoglu, H., Olsson, M., Tamm, C., Heidari, N., Orrenius, S. and Zhivotovsky, B. (2008). DNA damage induces two distinct modes of cell death in ovarian carcinomas. Cell Death Differ. 15, 555-566.
40. Vitale, I., Antoccia, A., Crateri, P., Leone, S., Arancia, G. and Tanzarella, C. (2005). Caspase-independent apoptosis is activated by diazepam-induced mitotic failure in HeLa cells, but not in human primary fibroblasts. Apoptosis 10, 909-920.
41. Waldman, T., Lengauer, C., Kinzler, K. W. and Vogelstein, B. (1996). Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature 381, 713-716.
42. Wang, G. W., Klein, J. B. and Kang, Y. J. (2001). Metallothionein inhibits doxorubicin-induced mitochondrial cytochrome c release and caspase-3 activation in cardiomyocytes. J. Pharmacol. Exp. Ther. 298, 461-468.
43. Woods, C. M., Zhu, J., McQueney, P. A., Bollag, D. and Lazarides, E. (1995). Taxol-induced mitotic block triggers rapid onset of a p53-independent apoptotic pathway. Mol. Med. 1, 506-526.
44. Yu, C. K. (1964). Chromosomes of X-ray-induced giant cells in chinese hamster in vitro. Nature 204, 1334-1335.