The PARP3-and ATM-dependent phosphorylation of APLF facilitates DNA double-strand break repair

Nucleic Acids Research

Volumn 41, Issue 7, 2013, Pages 4080-4092

  Fenton, Amanda L ^a,b   Shirodkar, Purnata ^a,b   MacRae, Chloe J ^a,b   Meng, Li ^a   Anne Koch, C ^a,b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; APLF PROTEIN; ATM PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 3; POLY(ADENOSINE DIPHOSPHATE RIBOSE); SERINE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; IONIZING RADIATION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

CELL CYCLE PROTEINS; CELL LINE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; DNA-BINDING PROTEINS; LASERS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RADIATION TOLERANCE; RADIATION, IONIZING; SERINE; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 84876528414     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt134     Document Type: Article

References (41)

1. Dery, U. and Masson, J.Y. (2007) Twists and turns in the function of DNA damage signaling and repair proteins by post-translational modifications. DNA Repair, 6, 561-577. (Pubitemid 46518334)
2. Vilenchik, M.M. and Knudson, A.G. (2003) Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc. Natl Acad. Sci. USA, 100, 12871-12876. (Pubitemid 37339992)
3. Shrivastav, M., De Haro, L.P. and Nickoloff, J.A. (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res., 18, 134-147.
4. Helleday, T., Lo, J., van Gent, D.C. and Engelward, B.P. (2007) DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair, 6, 923-935. (Pubitemid 46880473)
5. Hakem, R. (2008) DNA-damage repair; the good, the bad, and the ugly. EMBO J., 27, 589-605. (Pubitemid 351273123)
6. Durocher, D. and Jackson, S.P. (2001) DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme Curr. Opin. Cell Biol., 13, 225-231. (Pubitemid 32209224)
7. Canman, C.E. and Lim, D.S. (1998) The role of ATM in DNA damage responses and cancer. Oncogene, 17, 3301-3308. (Pubitemid 29043982)
8. Chan, D.W., Mody, C.H., Ting, N.S. and Lees-Miller, S.P. (1996) Purification and characterization of the double-stranded DNA-activated protein kinase, DNA-PK, from human placenta. Biochem. Cell Biol., 74, 67-73. (Pubitemid 126733696)
9. Zolner, A.E., Abdou, I., Ye, R., Mani, R.S., Fanta, M., Yu, Y., Douglas, P., Tahbaz, N., Fang, S., Dobbs, T. et al. (2011) Phosphorylation of polynucleotide kinase/phosphatase by DNA-dependent protein kinase and ataxia-telangiectasia mutated regulates its association with sites of DNA damage. Nucleic Acids Res., 39, 9224-9237.
10. Urquhart, A.J., Gatei, M., Richard, D.J. and Khanna, K.K. (2011) ATM mediated phosphorylation of CHD4 contributes to genome maintenance. Genome Integr., 2, 1.
11. Woodhouse, B.C., Dianova, I.I., Parsons, J.L. and Dianov, G.L. (2008) Poly(ADP-ribose) polymerase-1 modulates DNA repair capacity and prevents formation of DNA double strand breaks. DNA Repair, 7, 932-940.
12. Lindahl, T., Satoh, M.S., Poirier, G.G. and Klungland, A. (1995) Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem. Sci., 20, 405-411.
13. Yelamos, J., Farres, J., Llacuna, L., Ampurdanes, C. and Martin-Caballero, J. (2011) PARP-1 and PARP-2: New players in tumour development. Am. J. Cancer Res., 1, 328-346.
14. Schreiber, V., Dantzer, F., Ame, J.C. and de Murcia, G. (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol., 7, 517-528. (Pubitemid 44036457)
15. Rulten, S.L., Fisher, A.E., Robert, I., Zuma, M.C., Rouleau, M., Ju, L., Poirier, G., Reina-San-Martin, B. and Caldecott, K.W. (2011) PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell, 41, 33-45.
16. Rouleau, M., McDonald, D., Gagne, P., Ouellet, M.E., Droit, A., Hunter, J.M., Dutertre, S., Prigent, C., Hendzel, M.J. and Poirier, G.G. (2007) PARP-3 associates with polycomb group bodies and with components of the DNA damage repair machinery. J. Cell. Biochem., 100, 385-401. (Pubitemid 46146088)
17. Boehler, C., Gauthier, L.R., Mortusewicz, O., Biard, D.S., Saliou, J.M., Bresson, A., Sanglier-Cianferani, S., Smith, S., Schreiber, V., Boussin, F. et al. (2011) Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc. Natl Acad. Sci. USA, 108, 2783-2788.
18. Macrae, C.J., McCulloch, R.D., Ylanko, J., Durocher, D. and Koch, C.A. (2008) APLF (C2orf13) facilitates nonhomologous end-joining and undergoes ATM-dependent hyperphosphorylation following ionizing radiation. DNA Repair, 7, 292-302.
19. Rulten, S.L., Cortes-Ledesma, F., Guo, L., Iles, N.J. and Caldecott, K.W. (2008) APLF (C2orf13) is a novel component of poly(ADP-ribose) signaling in mammalian cells. Mol. Cell Biol., 28, 4620-4628. (Pubitemid 351977759)
20. Li, G.Y., McCulloch, R.D., Fenton, A.L., Cheung, M., Meng, L., Ikura, M. and Koch, C.A. (2010) Structure and identification of ADP-ribose recognition motifs of APLF and role in the DNA damage response. Proc. Natl Acad. Sci. USA, 107, 9129-9134.
21. Mehrotra, P.V., Ahel, D., Ryan, D.P., Weston, R., Wiechens, N., Kraehenbuehl, R., Owen-Hughes, T. and Ahel, I. DNA repair factor APLF is a histone chaperone. Mol. Cell, 41, 46-55.
22. Iles, N., Rulten, S., El-Khamisy, S.F. and Caldecott, K.W. (2007) APLF (C2orf13) is a novel human protein involved in the cellular response to chromosomal DNA strand breaks. Mol. Cell Biol., 27, 3793-3803. (Pubitemid 46726186)
23. Koch, C.A., Agyei, R., Galicia, S., Metalnikov, P., O'Donnell, P., Starostine, A., Weinfeld, M. and Durocher, D. (2004) Xrcc4 physically links DNA end processing by polynucleotide kinase to DNA ligation by DNA ligase IV. EMBO J., 23, 3874-3885. (Pubitemid 39389718)
24. Franken, N.A., Rodermond, H.M., Stap, J., Haveman, J. and van Bree, C. (2006) Clonogenic assay of cells in vitro. Nat. Protoc., 1, 2315-2319.
25. 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. (Pubitemid 43121979)
26. Bekker-Jensen, S., Fugger, K., Danielsen, J.R., Gromova, I., Sehested, M., Celis, J., Bartek, J., Lukas, J. and Mailand, N. (2007) Human Xip1 (C2orf13) is a novel regulator of cellular responses to DNA strand breaks. J. Biol. Chem., 282, 19638-19643. (Pubitemid 47100052)
27. Kurz, E.U. and Lees-Miller, S.P. (2004) DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair (Amst.), 3, 889-900. (Pubitemid 38997931)
28. Loseva, O., Jemth, A.S., Bryant, H.E., Schuler, H., Lehtio, L., Karlberg, T. and Helleday, T. (2010) PARP-3 is a mono-ADP-ribosylase that activates PARP-1 in the absence of DNA. J. Biol. Chem., 285, 8054-8060.
29. Bekker-Jensen, S., Lukas, C., Kitagawa, R., Melander, F., Kastan, M.B., Bartek, J. and Lukas, J. (2006) Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol., 173, 195-206.
30. Kanno, S., Kuzuoka, H., Sasao, S., Hong, Z., Lan, L., Nakajima, S. and Yasui, A. (2007) A novel human AP endonuclease with conserved zinc-finger-like motifs involved in DNA strand break responses. EMBO J., 26, 2094-2103. (Pubitemid 46625798)
31. Bakkenist, C.J. and Kastan, M.B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature, 421, 499-506. (Pubitemid 36168436)
32. Burma, S., Chen, B.P., Murphy, M., Kurimasa, A. and Chen, D.J. (2001) ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem., 276, 42462-42467.
33. Polo, S.E., Kaidi, A., Baskcomb, L., Galanty, Y. and Jackson, S.P. (2010) Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J., 29, 3130-3139.
34. Segal-Raz, H., Mass, G., Baranes-Bachar, K., Lerenthal, Y., Wang, S.Y., Chung, Y.M., Ziv-Lehrman, S., Strom, C.E., Helleday, T., Hu, M.C. et al. (2011) ATM-mediated phosphorylation of polynucleotide kinase/phosphatase is required for effective DNA double-strand break repair. EMBO Rep., 12, 713-719.
35. Das, B.B., Antony, S., Gupta, S., Dexheimer, T.S., Redon, C.E., Garfield, S., Shiloh, Y. and Pommier, Y. (2009) Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA-PK. EMBO J., 28, 3667-3680.
36. Haince, J.F., Kozlov, S., Dawson, V.L., Dawson, T.M., Hendzel, M.J., Lavin, M.F. and Poirier, G.G. (2007) Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J. Biol. Chem., 282, 16441-16453. (Pubitemid 47100334)
37. Smith, S. (2001) The world according to PARP. Trends Biochem. Sci., 26, 174-179. (Pubitemid 32197577)
38. Haince, J.F., McDonald, D., Rodrigue, A., Dery, U., Masson, J.Y., Hendzel, M.J. and Poirier, G.G. (2008) PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem., 283, 1197-1208.
39. Bryant, H.E. and Helleday, T. (2006) Inhibition of poly (ADP-ribose) polymerase activates ATM which is required for subsequent homologous recombination repair. Nucleic Acids Res., 34, 1685-1691.
40. McCabe, N., Turner, N.C., Lord, C.J., Kluzek, K., Bialkowska, A., Swift, S., Giavara, S., O'Connor, M.J., Tutt, A.N., Zdzienicka, M.Z. et al. (2006) Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res., 66, 8109-8115. (Pubitemid 44299177)
41. Rouleau, M., Patel, A., Hendzel, M.J., Kaufmann, S.H. and Poirier, G.G. (2010) PARP inhibition: PARP1 and beyond. Nat. Rev., Cancer, 10, 293-301.