Unrepairable DNA double-strand breaks that are generated by ionising radiation determine the fate of normal human cells

Journal of Cell Science

Volumn 125, Issue 22, 2012, Pages 5280-5287

  Noda, Asao ^a   Hirai, Yuko ^a   Hamasaki, Kanya ^a   Mitani, Hiroshi ^b   Nakamura, Nori ^a   Kodama, Yoshiaki ^a  

^a RADIATION EFFECTS RESEARCH FOUNDATION   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

H2AX; Cell senescence; DNA double strand break repair; Ionising radiation; Unrepairable DSBs

Indexed keywords

DOUBLE STRANDED DNA;

ARTICLE; CELL FATE; CELL SURVIVAL; CHEMICAL STRUCTURE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IONIZING RADIATION; IRRADIATION; PRIORITY JOURNAL; RADIATION EXPOSURE;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL AGING; CELL CYCLE PROTEINS; CELL LINEAGE; CELL NUCLEUS; CELL SURVIVAL; DIPLOIDY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, RADIATION; ENZYME ACTIVATION; FIBROBLASTS; HUMANS; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING; TUMOR SUPPRESSOR PROTEINS; UBIQUITINATION;

EID: 84873555201     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.101006     Document Type: Article

References (36)

1. Atwood, K. C. and Norman, A. (1949). On the interpretation of multi-hit survival curves. Proc. Natl. Acad. Sci. USA 35, 696-709.
2. Bandyopadhyay, D., Curry, J. L., Lin, Q., Richards, H. W., Chen, D., Hornsby, P. J., Timchenko, N. A. and Medrano, E. E. (2007). Dynamic assembly of chromatin complexes during cellular senescence: implications for the growth arrest of human melanocytic nevi. Aging Cell 6, 577-591.
3. Bartkova, J., Rezaei, N., Liontos, M., Karakaidos, P., Kletsas, D., Issaeva, N., Vassiliou, L.-V. F., Kolettas, E., Niforou, K., Zoumpourlis, V. C. et al. (2006). Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444, 633-637.
4. Benson, E. K., Lee, S. W. and Aaronson, S. A. (2010). Role of progerin-induced telomere dysfunction in HGPS premature cellular senescence. J. Cell Sci. 123, 2605- 2612.
5. Brugat, T., Nguyen-Khac, F., Grelier, A., Merle-Béral, H. and Delic, J. (2010). Telomere dysfunction-induced foci arise with the onset of telomeric deletions and complex chromosomal aberrations in resistant chronic lymphocytic leukemia cells. Blood 116, 239-249.
6. Cesare, A. J., Kaul, Z., Cohen, S. B., Napier, C. E., Pickett, H. A., Neumann, A. A. and Reddel, R. R. (2009). Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat. Struct. Mol. Biol. 16, 1244- 1251.
7. Chen, X., Zhong, S., Zhu, X., Dziegielewska, B., Ellenberger, T., Wilson, G. M., MacKerell, A. D., Jr and Tomkinson, A. E. (2008). Rational design of human DNA ligase inhibitors that target cellular DNA replication and repair. Cancer Res. 68, 3169-3177.
8. Crowther, J. A. (1926). The action of X-rays on Colpidium Colpoda. Proc. R. Soc. B 100, 390-404.
9. Di Micco, R., Fumagalli, M., Cicalese, A., Piccinin, S., Gasparini, P., Luise, C., Schurra, C., Garre', M., Nuciforo, P. G., Bensimon, A. et al. (2006). Oncogeneinduced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444, 638-642.
10. Dinant, C. and Luijsterburg, M. S. (2009). The emerging role of HP1 in the DNA damage response. Mol. Cell. Biol. 29, 6335-6340.
11. Goodarzi, A. A., Noon, A. T., Deckbar, D., Ziv, Y., Shiloh, Y., Löbrich, M. and Jeggo, P. A. (2008). ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 31, 167-177.
12. Grudzenski, S., Raths, A., Conrad, S., Rü be, C. E. and Löbrich, M. (2010). Inducible response required for repair of low-dose radiation damage in human fibroblasts. Proc. Natl. Acad. Sci. USA 107, 14205-14210.
13. Harrigan, J. A., Belotserkovskaya, R., Coates, J., Dimitrova, D. S., Polo, S. E., Bradshaw, C. R., Fraser, P. and Jackson, S. P. (2011). Replication stress induces 53BP1-containing OPT domains in G1 cells. J. Cell Biol. 193, 97-108.
14. 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.
15. Ksiazek, K., Passos, J. F., Olijslagers, S., Saretzki, G., Martin-Ruiz, C. and von Zglinicki, T. (2007). Premature senescence of mesothelial cells is associated with non-telomeric DNA damage. Biochem. Biophys. Res. Commun. 362, 707-711.
16. Lammens, K., Bemeleit, D. J., Möckel, C., Clausing, E., Schele, A., Hartung, S., Schiller, C. B., Lucas, M., Angermü ller, C., Söding, J. et al. (2011). The Mre11:Rad50 structure shows an ATP-dependent molecular clamp in DNA doublestrand break repair. Cell 145, 54-66.
17. Lukas, C., Savic, V., Bekker-Jensen, S., Doil, C., Neumann, B., Pedersen, R. S., Grøfte, M., Chan, K. L., Hickson, I. D., Bartek, J. et al. (2011). 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13, 243-253.
18. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C. and Lukas, J. (2007). RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887-900.
19. Mayer, P. J., Bradley, M. O. and Nichols, W. W. (1986). No change in DNA damage or repair of single- and double-strand breaks as human diploid fibroblasts age in vitro. Exp. Cell Res. 166, 497-509.
20. Messick, T. E. and Greenberg, R. A. (2009). The ubiquitin landscape at DNA doublestrand breaks. J. Cell Biol. 187, 319-326.
21. Murakawa, Y., Sonoda, E., Barber, L. J., Zeng, W., Yokomori, K., Kimura, H., Niimi, A., Lehmann, A., Zhao, G. Y., Hochegger, H. et al. (2007). Inhibitors of the proteasome suppress homologous DNA recombination in mammalian cells. Cancer Res. 67, 8536-8543.
22. Nakamura, A. J., Chiang, Y. J., Hathcock, K. S., Horikawa, I., Sedelnikova, O. A., Hodes, R. J. and Bonner, W. M. (2008). Both telomeric and non-telomeric DNA damage are determinants of mammalian cellular senescence. Epigenetics Chromatin 1, 6.
23. Narita, M., Nũnez, S., Heard, E., Narita, M., Lin, A. W., Hearn, S. A., Spector, D. L., Hannon, G. J. and Lowe, S. W. (2003). Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113, 703-716.
24. Noda, A., Ning, Y., Venable, S. F., Pereira-Smith, O. M. and Smith, J. R. (1994). Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211, 90-98.
25. Rai, P., Onder, T. T., Young, J. J., McFaline, J. L., Pang, B., Dedon, P. C. and Weinberg, R. A. (2009). Continuous elimination of oxidized nucleotides is necessary to prevent rapid onset of cellular senescence. Proc. Natl. Acad. Sci. USA 106, 169- 174.
26. Rogakou, E. P., Boon, C., Redon, C. and Bonner, W. M. (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146, 905-916.
27. Royou, A., Gagou, M. E., Karess, R. and Sullivan, W. (2010). BubR1- and Polocoated DNA tethers facilitate poleward segregation of acentric chromatids. Cell 140, 235-245.
28. Sedelnikova, O. A., Horikawa, I., Zimonjic, D. B., Popescu, N. C., Bonner, W. M. and Barrett, J. C. (2004). Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell Biol. 6, 168-170.
29. Sedivy, J. M., Banumathy, G. and Adams, P. D. (2008). Aging by epigenetics-A consequence of chromatin damage. Exp. Cell Res. 314, 1909-1917.
30. Shanbhag, N. M., Rafalska-Metcalf, I. U., Balane-Bolivar, C., Janicki, S. M. and Greenberg, R. A. (2010). ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141, 970-981.
31. Shao, G., Lilli, D. R., Patterson-Fortin, J., Coleman, K. A., Morrissey, D. E. and Greenberg, R. A. (2009). The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc. Natl. Acad. Sci. USA 106, 3166-3171.
32. Stewart, G. S., Panier, S., Townsend, K., Al-Hakim, A. K., Kolas, N. K., Miller, E. S., Nakada, S., Ylanko, J., Olivarius, S., Mendez, M. et al. (2009). The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420-434.
33. Turner, J. M. A. (2007). Meiotic sex chromosome inactivation. Development 134, 1823-1831.
34. van Gent, D. C., Hoeijmakers, J. H. J. and Kanaar, R. (2001). Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2, 196-206.
35. Wiktor-Brown, D. M., Kwon, H. S., Nam, Y. S., So, P. T. and Engelward, B. P. (2008). Integrated one- and two-photon imaging platform reveals clonal expansion as a major driver of mutation load. Proc. Natl. Acad. Sci. USA 105, 10314-10319.
36. Zhang, R., Chen, W. and Adams, P. D. (2007). Molecular dissection of formation of senescence-associated heterochromatin foci. Mol. Cell. Biol. 27, 2343-2358.