Defective chromatin recruitment and retention of NHEJ core components in human tumor cells expressing a Cyclin e fragment

Nucleic Acids Research

Volumn 41, Issue 22, 2013, Pages 10157-10169

  Chatterjee, Payel ^a,b   Plesca, Dragos ^a   Mazumder, Suparna ^a   Boutros, Jean ^a,c   Yannone, Steven M ^d   Almasan, Alexandru ^a,e  

^a LERNER RESEARCH INSTITUTE   (United States)

^b KENT STATE UNIVERSITY   (United States)

^c CLEVELAND STATE UNIVERSITY   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e TAUSSIG CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

53 BINDING PROTEIN 1; ATM PROTEIN; BINDING PROTEIN; CYCLIN E; DNA DEPENDENT PROTEIN KINASE; DOUBLE STRANDED DNA; P18 CYCLIN E; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; COMET ASSAY; CONTROLLED STUDY; DIMERIZATION; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; EPITHELIUM CELL; GENE MUTATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MALE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; STABLE EXPRESSION; TUMOR CELL;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATIN; CYCLIN E; DNA DAMAGE; DNA END-JOINING REPAIR; DNA-ACTIVATED PROTEIN KINASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NUCLEAR PROTEINS; RADIATION, IONIZING; TRANS-ACTIVATORS;

EID: 84890413955     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt812     Document Type: Article

References (34)

1. Bolderson, E., Richard, D.J., Zhou, B.B. and Khanna, K.K. (2009) Recent advances in cancer therapy targeting proteins involved in DNA double-strand break repair. Clin. Cancer Res., 15, 6314-6320.
2. Branzei, D. and Foiani, M. (2008) Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol., 9, 297-308.
3. Mahaney, B.L., Meek, K. and Lees-Miller, S.P. (2009) Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem. J., 417, 639-650.
4. Ahnesorg, P., Smith, P. and Jackson, S.P. (2006) XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell, 124, 301-313.
5. Yoo, S. and Dynan, W.S. (1999) Geometry of a complex formed by double strand break repair proteins at a single DNA end: recruitment of DNA-PKcs induces inward translocation of Ku protein. Nucleic Acids Res., 27, 4679-4686.
6. Noon, A.T. and Goodarzi, A.A. (2011) 53BP1-mediated DNA double strand break repair: insert bad pun here. DNA repair, 10, 1071-1076.
7. Dobbs, T.A., Tainer, J.A. and Lees-Miller, S.P. (2010) A structural model for regulation of NHEJ by DNA-PKcs autophosphorylation. DNA Repair, 9, 1307-1314.
8. Neal, J.A., Dang, V., Douglas, P., Wold, M.S., Lees-Miller, S.P. and Meek, K. (2011) Inhibition of homologous recombination by DNA-dependent protein kinase requires kinase activity, is titratable, and is modulated by autophosphorylation. Mol. Cell. Biol., 31, 1719-1733.
9. Leber, R., Wise, T.W., Mizuta, R. and Meek, K. (1998) The XRCC4 gene product is a target for and interacts with the DNA-dependent protein kinase. J. Biol. Chem., 273, 1794-1801.
10. Povirk, L.F., Zhou, T., Zhou, R., Cowan, M.J. and Yannone, S.M. (2007) Processing of 30-phosphoglycolate-terminated DNA double strand breaks by Artemis nuclease. J. Biol. Chem., 282, 3547-3558.
11. Yu, Y., Wang, W., Ding, Q., Ye, R., Chen, D., Merkle, D., Schriemer, D., Meek, K. and Lees-Miller, S.P. (2003) DNA-PK phosphorylation sites in XRCC4 are not required for survival after radiation or for V(D)J recombination. DNA Repair, 2, 1239-1252.
12. Wang, B., Matsuoka, S., Carpenter, P.B. and Elledge, S.J. (2002) 53BP1, a mediator of the DNA damage checkpoint. Science, 298, 1435-1438.
13. Harding, S.M. and Bristow, R.G. (2012) Discordance between phosphorylation and recruitment of 53BP1 in response to DNA double-strand breaks. Cell Cycle, 11, 1432-1444.
14. Meek, K., Douglas, P., Cui, X., Ding, Q. and Lees-Miller, S.P. (2007) trans Autophosphorylation at DNA-dependent protein kinase's two major autophosphorylation site clusters facilitates end processing but not end joining. Mol. Cell. Biol., 27, 3881-3890.
15. Chan, D.W., Chen, B.P., Prithivirajsingh, S., Kurimasa, A., Story, M.D., Qin, J. and Chen, D.J. (2002) Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev., 16, 2333-2338.
16. Douglas, P., Sapkota, G.P., Morrice, N., Yu, Y., Goodarzi, A.A., Merkle, D., Meek, K., Alessi, D.R. and Lees-Miller, S.P. (2002) Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem. J., 368, 243-251.
17. Chen, B.P., Uematsu, N., Kobayashi, J., Lerenthal, Y., Krempler, A., Yajima, H., Lobrich, M., Shiloh, Y. and Chen, D.J. (2007) Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylations at the Thr-2609 cluster upon DNA double strand break. J. Biol. Chem., 282, 6582-6587.
18. Chen, B.P., Chan, D.W., Kobayashi, J., Burma, S., Asaithamby, A., Morotomi-Yano, K., Botvinick, E., Qin, J. and Chen, D.J. (2005) Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem, 280, 14709-14715.
19. Cui, X., Yu, Y., Gupta, S., Cho, Y.M., Lees-Miller, S.P. and Meek, K. (2005) Autophosphorylation of DNA-dependent protein kinase regulates DNA end processing and may also alter doublestrand break repair pathway choice. Mol. Cell. Biol., 25, 10842-10852.
20. Nagasawa, H., Little, J.B., Lin, Y.F., So, S., Kurimasa, A., Peng, Y., Brogan, J.R., Chen, D.J., Bedford, J.S. and Chen, B.P. (2011) Differential role of DNA-PKcs phosphorylations and kinase activity in radiosensitivity and chromosomal instability. Radiat. Res., 175, 83-89.
21. Mazumder, S., Gong, B., Chen, Q., Drazba, J.A., Buchsbaum, J.C. and Almasan, A. (2002) Proteolytic cleavage of Cyclin E leads to inactivation of associated kinase activity and amplification of apoptosis in hematopoietic cells. Mol. Cell. Biol., 22, 2398-2409.
22. Mazumder, S., Plesca, D. and Almasan, A. (2007) A jekyll and hyde role of Cyclin E in the genotoxic stress response: switching from cell cycle control to apoptosis regulation. Cell Cycle, 6, 1437-1442.
23. Crosby, M.E., Jacobberger, J., Gupta, D., Macklis, R.M. and Almasan, A. (2007) E2F4 regulates a stable G2 arrest response to genotoxic stress in prostate carcinoma. Oncogene, 26, 1897-1909.
24. Plesca, D., Mazumder, S., Gama, V., Matsuyama, S. and Almasan, A. (2008) A C-terminal fragment of Cyclin E, generated by caspase-mediated cleavage, is degraded in the absence of a recognizable phosphodegron. J. Biol. Chem., 283, 30796-30803.
25. Gupta, D., Crosby, M.E., Almasan, A. and Macklis, R.M. (2008) Regulation of CD20 expression by radiation-induced changes in intracellular redox status. Free Radic. Biol. Med., 44, 614-623.
26. Drouet, J., Delteil, C., Lefrancois, J., Concannon, P., Salles, B. and Calsou, P. (2005) DNA-dependent protein kinase and XRCC4-DNA ligase IV mobilization in the cell in response to DNA double strand breaks. J. Biol. Chem., 280, 7060-7069.
27. Singh, K., Matsuyama, S., Drazba, J.A. and Almasan, A. (2012) Autophagy-dependent senescence in response to DNA damage and chronic apoptotic stress. Autophagy, 8, 236-251.
28. Plesca, D., Mazumder, S. and Almasan, A. (2008) DNA damage response and apoptosis. Methods Enzymol., 446, 107-122.
29. Minter-Dykhouse, K., Ward, I., Huen, M.S., Chen, J. and Lou, Z. (2008) Distinct versus overlapping functions of MDC1 and 53BP1 in DNA damage response and tumorigenesis. J. Cell Biol., 181, 727-735.
30. Mazumder, S., Plesca, D., Kinter, M. and Almasan, A. (2007) Interaction of a Cyclin E fragment with Ku70 regulates Baxmediated apoptosis. Mol. Cell. Biol., 27, 3511-3520.
31. Javvadi, P., Makino, H., Das, A.K., Lin, Y.F., Chen, D.J., Chen, B.P. and Nirodi, C.S. (2012) Threonine 2609 phosphorylation of the DNA-dependent protein kinase is a critical prerequisite for epidermal growth factor receptor-mediated radiation resistance. Mol. Cancer Res., 10, 1359-1368.
32. Hammel, M., Yu, Y., Mahaney, B.L., Cai, B., Ye, R., Phipps, B.M., Rambo, R.P., Hura, G.L., Pelikan, M., So, S. et al. (2010) Ku and DNA-dependent protein kinase dynamic conformations and assembly regulate DNA binding and the initial non-homologous end joining complex. J. Biol. Chem., 285, 1414-1423.
33. Hammel, M., Rey, M., Yu, Y., Mani, R.S., Classen, S., Liu, M., Pique, M.E., Fang, S., Mahaney, B.L., Weinfeld, M. et al. (2011) XRCC4 protein interactions with XRCC4-like factor (XLF) create an extended grooved scaffold for DNA ligation and double strand break repair. J. Biol. Chem., 286, 32638-32650.
34. Cottarel, J., Frit, P., Bombarde, O., Salles, B., Negrel, A., Bernard, S., Jeggo, P.A., Lieber, M.R., Modesti, M. and Calsou, P. (2013) A noncatalytic function of the ligation complex during nonhomologous end joining. J. Cell Biol., 200, 173-186.