DNA ligase III acts as a DNA strand break sensor in the cellular orchestration of DNA strand break repair

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages 875-892

  Abdou, Ismail ^a   Poirier, Guy G ^b   Hendzel, Michael J ^a   Weinfeld, Michael ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DNA LIGASE; DNA LIGASE III; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, MOUSE; PHOSPHOTRANSFERASE; PNKP PROTEIN, HUMAN; X-RAY REPAIR CROSS COMPLEMENTING PROTEIN 1;

ANIMAL; CELL CULTURE; CHEMISTRY; DNA REPAIR; DNA STRAND BREAKAGE; HELA CELL LINE; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SINGLE STRANDED DNA BREAK;

ANIMALS; CELLS, CULTURED; DNA BREAKS; DNA BREAKS, SINGLE-STRANDED; DNA LIGASES; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MICE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); POLY(ADP-RIBOSE) POLYMERASES; PROTEIN STRUCTURE, TERTIARY;

EID: 84941095899     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1307     Document Type: Article

References (42)

1. Hoeijmakers, J.H. (2001) Genome maintenance mechanisms for preventing cancer. Nature, 411, 366-374.
2. Caldecott, K. (2008) Single-strand break repair and genetic disease. Nat. Rev. Genet., 9, 619-631.
3. Rouleau, M., Patel, A., Hendzel, M.J., Kaufmann, S.H., Poirier, G.G. (2010) PARP inhibition: PARP1 and beyond. Nat. Rev. Cancer, 10, 293-301.
4. Weinfeld, M., Mani, R.S., Abdou, I., Aceytuno, R.D., Glover, J.N.M. (2011) Tidying up loose ends: the role of polynucleotide kinase/phosphatase in DNA strand break repair. Trends Biochem. Sci., 36, 262-271.
5. Wilson, S.H., Beard, W.A, Shock, D.D., Batra, V.K., Cavanaugh, N.A, Prasad, R., Hou, E.W., Liu, Y., Asagoshi, K., Horton, J.K. et al. (2010) Base excision repair and design of small molecule inhibitors of human DNA polymerase-. Cell. Mol. Life Sci., 67, 3633-3647.
6. Cappelli, E., Taylor, R., Cevasco, M., Abbondandolo, A., Caldecott, K., Frosina, G. (1997) Involvement of XRCC1 and DNA ligase III gene products in DNA base excision repair. J. Biol. Chem., 272, 23970-23975.
7. Horton, J., Watson, M., Stefanick, D. (2008) XRCC1 and DNA polymerase-in cellular protection against cytotoxic DNA single-strand breaks. Cell Res., 18, 48-63.
8. El-Khamisy, S.F., Masutani, M., Suzuki, H., Caldecott, K.W. (2003) A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res., 31, 5526-5533.
9. Mortusewicz, O., Amé, J.-C., Schreiber, V., Leonhardt, H. (2007) Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res., 35, 7665-7675.
10. Godon, C., Cordelières, F.P., Biard, D., Giocanti, N., Mégnin-Chanet, F., Hall, J., Favaudon, V. (2008) PARP inhibition versus PARP-1 silencing: different outcomes in terms of single-strand break repair and radiation susceptibility. Nucleic Acids Res., 36, 4454-4464.
11. Campalans, A., Kortulewski, T., Amouroux, R., Menoni, H., Vermeulen, W., Radicella, J.P. (2013) Distinct spatiotemporal patterns and PARP dependence of XRCC1 recruitment to single-strand break and base excision repair. Nucleic Acids Res., 41, 3115-3129.
12. Hanssen-Bauer, A., Solvang-Garten, K., Sundheim, O., Pe ña-Diaz, J., Andersen, S., Slupphaug, G., Krokan, H.E., Wilson, D.M., Akbari, M., Otterlei, M. (2011) XRCC1 coordinates disparate responses and multiprotein repair complexes depending on the nature and context of the DNA damage. Environ. Mol. Mutagen., 52, 623-635.
13. Vodenicharov, M.D., Sallmann, F.R., Satoh, M.S., Poirier, G.G. (2000) Base excision repair is efficient in cells lacking poly(ADP-ribose) polymerase 1. Nucleic Acids Res., 28, 3887-3896.
14. Str öm, C.E., Johansson, F., Uhlén, M., Szigyarto, C.A.-K., Erixon, K., Helleday, T. (2011) Poly (ADP-ribose) polymerase (PARP) is not involved in base excision repair but PARP inhibition traps a single-strand intermediate. Nucleic Acids Res., 39, 3166-3175.
15. Petrucco, S. (2003) Sensing DNA damage by PARP-like fingers. Nucleic Acids Res., 31, 6689-6699.
16. Eustermann, S., Videler, H., Yang, J.-C., Cole, P.T., Gruszka, D., Veprintsev, D., Neuhaus, D. (2011) The DNA-binding domain of human PARP-1 interacts with DNA single-strand breaks as a monomer through its second zinc finger. J. Mol. Biol., 407, 149-170.
17. Mackey, Z.B., Niedergang, C., Murcia, J.M., Leppard, J., Au, K., Chen, J., de Murcia, G., Tomkinson, A.E. (1999) DNA ligase III is recruited to DNA strand breaks by a zinc finger motif homologous to that of poly(ADP-ribose) polymerase. Identification of two functionally distinct DNA binding regions within DNA ligase III. J. Biol. Chem., 274, 21679-21687.
18. Cotner-Gohara, E., Kim, I.-K., Tomkinson, A.E., Ellenberger, T. (2008) Two DNA-binding and nick recognition modules in human DNA ligase III. J. Biol. Chem., 283, 10764-10772.
19. Caldecott, K.W., McKeown, C.K., Tucker, J.D., Ljungquist, S., Thompson, L.H. (1994) An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. 14, 68-76.
20. Caldecott, K.W., Tucker, J.D., Stanker, L.H., Thompson, L.H. (1995) Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res., 23, 4836-4843.
21. Caldecott, K.W., Aoufouchi, S., Johnson, P., Shall, S. (1996) XRCC1 polypeptide interacts with DNA polymerase and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res., 24, 4387-4394.
22. Mortusewicz, O., Rothbauer, U., Cardoso, M.C., Leonhardt, H. (2006) Differential recruitment of DNA Ligase I and III to DNA repair sites. Nucleic Acids Res., 34, 3523-3532.
23. Haince, J.-F., McDonald, D., Rodrigue, A., Déry, U., Masson, J.-Y., Hendzel, M.J., 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.
24. Vallejo, A.N., Pogulis, R.J., Pease, L.R. (2008) PCR mutagenesis by overlap extension and gene SOE. CSH Protoc., 3, 1-7.
25. Carrero, G., McDonald, D., Crawford, E., de Vries, G., Hendzel, M.J. (2003) Using FRAP and mathematical modeling to determine the in vivo kinetics of nuclear proteins. Methods, 29, 14-28.
26. Dinant, C., de Jager, M., Essers, J., van Cappellen, W.A., Kanaar, R., Houtsmuller, A.B., Vermeulen, W. (2007) Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J. Cell Sci., 120, 2731-2740.
27. Kong, X., Mohanty, S.K., Stephens, J., Heale, J.T., Gomez-Godinez, V., Shi, L.Z., Kim, J.-S., Yokomori, K., Berns, M.W. (2009) Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells. Nucleic Acids Res., 37, e68.
28. Van der Schans, G.P., Paterson, M.C., Cross, W.G. (1983) DNA strand break and rejoining in cultured human fibroblasts exposed to fast neutrons or gamma rays. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 44, 75-85.
29. Della-Maria, J., Hegde, M.L., McNeill, D.R., Matsumoto, Y., Tsai, M.-S., Ellenberger, T., Wilson, D.M., Mitra, S., Tomkinson, A.E. (2012) The interaction between polynucleotide kinase phosphatase and the DNA repair protein XRCC1 is critical for repair of DNA alkylation damage and stable association at DNA damage sites. J. Biol. Chem., 287, 39233-39244.
30. Jakob, B., Splinter, J., Conrad, S., Voss, K.-O., Zink, D., Durante, M., Löbrich, M., Taucher-Scholz, G. (2011) DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res., 39, 6489-6499.
31. Malanga, M., Althaus, F.R. (2005) The role of poly (ADP-ribose) in the DNA damage signaling network. Biochem. Cell Biol., 83, 354-364.
32. Veuger, S.J., Curtin, N.J., Smith, G.C.M., Durkacz, B.W. (2004) Effects of novel inhibitors of poly(ADP-ribose) polymerase-1 and the DNA-dependent protein kinase on enzyme activities and DNA repair. Oncogene, 23, 7322-7329.
33. Mabley, J.G., Jagtap, P., Perretti, M., Getting, S.J., Salzman, A.L., Virág, L., Szab o, E., Soriano, F.G., Liaudet, L., Abdelkarim, G.E. et al. (2001) Anti-inflammatory effects of a novel, potent inhibitor of poly (ADP-ribose) polymerase. Inflamm. Res., 50, 561-569.
34. Simsek, D., Brunet, E., Wong, S.Y.-W., Katyal, S., Gao, Y., McKinnon, P.J., Lou, J., Zhang, L., Li, J., Rebar, E.J. et al. (2011) DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet., 7, e1002080.
35. Taylor, R.M., Wickstead, B., Cronin, S., Caldecott, K.W. (1998) Role of a BRCT domain in the interaction of DNA ligase III-alpha with the DNA repair protein XRCC1. Curr. Biol., 8, 877-880.
36. Taylor, R.M., Whitehouse, C.J., Caldecott, K.W. (2000) The DNA ligase III zinc finger stimulates binding to DNA secondary structure and promotes end joining. Nucleic Acids Res., 28, 3558-3563.
37. Pommier, Y. (2009) DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem. Rev., 109, 2894-2902.
38. Caldecott, K.W. (2014) Protein ADP-ribosylation and the cellular response to DNA strand breaks. DNA Repair, 19, 108-113.
39. Katyal, S., McKinnon, P.J. (2011) Disconnecting XRCC1 and DNA ligase III. Cell Cycle, 10, 2269-2275.
40. Zhang, Y.-W., Regairaz, M., Seiler, J.A., Agama, K.K., Doroshow, J.H., Pommier, Y. (2011) Poly(ADP-ribose) polymerase and XPF-ERCC1 participate in distinct pathways for the repair of topoisomerase I-induced DNA damage in mammalian cells. Nucleic Acids Res., 39, 3607-3620.
41. Pommier, Y., Barcelo, J., Rao, V.A., Sordet, O., Jobson, A.G., Miao, Z., Seiler, J., Zhang, H., Marchand, C., Redon, C. (2006) Repair of topoisomerase I-mediaed DNA damage. Prog. Nucleic Acid Res. Mol. Biol., 81, 179-229.
42. Odell, I.D., Barbour, J.-E., Murphy, D.L., Della-Maria, J.A., Sweasy, J.B., Tomkinson, A.E., Wallace, S.S., Pederson, D.S. (2011) Nucleosome disruption by DNA ligase III-XRCC1 promotes efficient base excision repair. Mol. Cell. Biol., 31, 4623-4632.