A human XRCC4-XLF complex bridges DNA

Nucleic Acids Research

Volumn 40, Issue 4, 2012, Pages 1868-1878

  Andres, Sara N ^a   Vergnes, Alexandra ^b,d   Ristic, Dejan ^c   Wyman, Claire ^c   Modesti, Mauro ^b   Junop, Murray ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b AIX MARSEILLE UNIVERSITY   (France)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; NUCLEOPROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; XRCC4 PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; HUMAN; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

BINDING SITES; DNA; DNA LIGASES; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; HUMANS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; PROTEIN BINDING;

EUKARYOTA;

EID: 84857820399     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks022     Document Type: Article

References (52)

1. Kuzminov, A. (2001) Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc. Natl Acad. Sci. USA, 98, 8241-8246. (Pubitemid 32678019)
2. Roth, D. B., Nakagima, P. B., Menetski, J. P., Bosma, M. J. and Gellert, M. (1992) V(D)J recombination in mouse thymocytes: double-strand breaks near T cell receptor delta rearrangement signals. Cell, 69, 41-53.
3. Gottlieb, T. M. and Jackson, S. P. (1993) The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell, 72, 131-142. (Pubitemid 23029700)
4. Ding, Q., Reddy, Y. V., Wang, W., Woods, T., Douglas, P., Ramsden, D. A., Lees-Miller, S. P. and Meek, K. (2003) Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol. Cell Biol., 23, 5836-5848. (Pubitemid 36951345)
5. McElhinny, S. A., Havener, J. M., Garcia-Diaz, M., Juärez, R., Bebenek, K., Kee, B. L., Blanco, L., Kunkel, T. A. and Ramsden, D. A. (2005) A gradient of template dependence defines distinct biological roles for family-polymerases in nonhomologous end joining. Mol. Cell, 19, 357-366.
6. 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 double-strand break repair pathway choice. Mol. Cell Biol., 25, 10842-10852. (Pubitemid 41747129)
7. Goodarzi, A. A., Yu, Y., Riballo, E., Douglas, P., Walker, S. A., Ye, R., Härer, C., Marchetti, C., Morrice, N., Jeggo, P. A. et al. (2006) DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J., 25, 3880-3889. (Pubitemid 44300273)
8. 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, 2, 301-313. (Pubitemid 43121979)
9. Grawunder, U., Wilm, M., Wu, X., Kulesza, P., Wilson, T. E., Mann, M. and Lieber, M. R. (1997) Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature, 388, 492-495. (Pubitemid 27328929)
10. Tsai, C. J., Kim, S. A. and Chu, G. (2007) XLF promotes the ligation of mismatched and noncohesive DNA ends. Proc. Natl Acad. Sci. USA, 19, 7851-7856. (Pubitemid 47185840)
11. Giaccia, A. J., Denko, N., MacLaren, R., Mirman, D., Waldren, C., Hart, I. and Stamato, T. D. (1990) Human chromosome 5 complements the DNA double-strand break-repair deficiency and gamma-ray sensitivity of the XR-1 hamster variant. Am. J. Hum. Genet., 47, 459-469.
12. Zha, S., Alt, F. W., Cheng, H. L., Brush, J. W. and Li, G. (2007) Defective DNA repair and increased genomic instability in Cernunnos-XLF- deficient murine ES cells. Proc. Natl Acad. Sci. USA., 104, 4518-4523. (Pubitemid 47186257)
13. Gao, Y., Sun, Y., Frank, K. M., Dikkes, P., Fujiwara, Y., Seidl, K. J., Sekiguchi, J. M., Rathbun, G. A., Swat, W., Wang, J. et al. (1998) A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell, 95, 891-902. (Pubitemid 29019042)
14. Buck, D., Malivert, L., de Chasseval, R., Barraud, A., Fondanèche, M. C., Sanal, O., Plebani, A., Stëhan, J. L., Hufnagel, M., le Deist, F. et al. (2006) Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell, 124, 287-299. (Pubitemid 43121978)
15. Li, Y., Chirgadze, D. Y., Bolanos-Garcia, V. M., Sibanda, V. M., Sibanda, B. L., Davies, O. R., Ahnesorg, P., Jackson, S. P. and Blundell, T. L. (2008) Crystal structure of human XLF/Cernunnos reveals unexpected differences from XRCC4 with implications for NHEJ. EMBO J., 27, 290-300.
16. Zha, S., Guo, C., Boboila, C., Oksenych, V., Cheng, H. L., Zhang, Y., Wesemann, D. R., Yuen, G., Patel, H., Goff, P. H. et al. (2011) ATM damage response and XLF repair factor are functionally redundant in joining DNA breaks. Nature, 469, 250-254.
17. Critchlow, S. E., Bowater, R. P. and Jackson, S. P. (1997) Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Curr. Biol., 7, 588-598. (Pubitemid 27335654)
18. Yano, K., Morotomi-Yano, K., Lee, K. J. and Chen, D. J. (2011) Functional significance of the interaction with Ku in DNAdouble-strand break recognition of XLF. FEBS Lett., 585, 841-846.
19. Yano, K., Morotomi-Yano, K., Wang, S. Y., Uematsu, N., Lee, K. J., Asaithamby, A., Weterings, E. and Chen, D. J. (2008) Ku recruits XLF to DNA double-strand breaks. EMBO Rep., 9, 91-96.
20. Andres, S. N., Modesti, M., Tsai, C. J., Chu, G. and Junop, M. S. (2007) Crystal structure of human XLF: a twist in nonhomologous DNA end-joining. Mol. Cell., 28, 1093-1101. (Pubitemid 350297023)
21. Junop, M. S., Modesti, M., GuarnëA., Ghirlando, R., Gellert, M. and Yang, W. (2000) Crystal structure of the Xrcc4 DNA repair protein and implications for end joining. EMBO J., 22, 5962-5970.
22. Malivert, L., Ropars, V., Nunez, M., Drevet, P., Miron, S., Faure, G., Guerois, R., Mornon, J. P., Revy, P., Charbonnier, J. B. et al. (2010) Delineation of the Xrcc4-interacting region in the globular head domain of cernunnos/XLF. J. Biol. Chem., 285, 26475-26483.
23. Hammel, M., Yu, Y., Fang, S., Lees-Miller, S. P. and Tainer, J. A. (2010) XLF regulates filament architecture of the XRCC4-ligaseIV complex. Structure, 11, 1431-1442.
24. Ropars, V., Drevet, P., Legrand, P., Baconnais, S., Amram, J., Faure, G., Märquez, J. A., Piërement, O., Guerois, R., Callebaut, I. et al. (2011) Structural characterization of filaments formed by human XRCC4-Cernunnos/XLF complex involved in nonhomologous DNA end-joining. Proc. Natl Acad. Sci. USA, 108, 12663-12668.
25. 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 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.
26. Wu, Q., Ochi, T., Matak-Vinkovic, D., Robinson, C. V., Chirgadze, D. Y. and Blundell, T. L. (2011) Non-homologous end-joining partners in a helical dance: structural studies of XLF-XRCC4 interactions. Biochem. Soc. Trans., 39, 1387-1392.
27. Modesti, M., Hesse, J. E. and Gellert, M. (1999) DNA binding of Xrcc4 protein is associated with V(D)J recombination but not with stimulation of DNA ligase IV activity. EMBO J., 18, 2008-2018. (Pubitemid 29158543)
28. Andres, S. N. and Junop, M. S. (2011) Crystallization and preliminary X-ray diffraction analysis of the human XRCC4-XLF complex. Acta Cryst., F67, 1399-1402.
29. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326. (Pubitemid 27085611)
30. Adams, P. D., Afonine, P. V., Bunköczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Cryst., D66, 213-221.
31. Brunger, A. T. (2007) Version 1. 2 of the crystallography and NMR system. Nat. Protoc., 2, 2728-2733.
32. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Cryst., D60, 2126-2132. (Pubitemid 41742764)
33. Schroeder, G. F., Levitt, M. and Brunger, A. T. (2010) Super-resolution biomolecular crystallography with low-resolution data. Nature, 464, 1218-1222.
34. Zhorov, B. S. (1981) Vector method for calculating derivatives of energy of atom-atom interactions of complex molecules according to generalized coordinates. J. Struct. Chem., 22, 4-8.
35. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol., 372, 774-797. (Pubitemid 47321791)
36. Sulek, M., Yarrington, R., McGibbon, G., Boeke, J. D. and Junop, M. (2007) A critical role for the C-terminus of Nej1 protein in Lif1p association, DNA binding and non-homologous end-joining. DNA Repair, 6, 1805-1818. (Pubitemid 350064586)
37. Wu, P. Y., Frit, P., Meesala, S., Dauvillier, S., Modesti, M., Andres, S. N., Huang, Y., Sekiguchi, J., Calsou, P., Salles, B. et al. (2009) Structural and functional interaction between the human DNA repair proteins DNA Ligase IV and XRCC4. Mol. Cell. Biol., 29, 3163-3172.
38. Modesti, M., Junop, M. S., Ghirlando, R., van de Rakt, M., Gellert, M., Yang, W. and Kanaar, R. (2003) Tetramerization and DNA ligase IV interaction of the DNA double-strand break repair protein XRCC4 are mutually exclusive. J. Mol. Biol., 334, 215-228. (Pubitemid 37357262)
39. 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.
40. Di Capua, E., Engel, A., Stasiak, A. and Koller, T. (1982) Characterization of complexes between recA protein and duplex DNA by electron microscopy. J. Mol. Biol., 157, 87-103.
41. Galkin, V. E., Wu, Y., Zhang, X. P., Qian, X., He, Y., Yu, X., Heyer, W. D., Luo, Y. and Egelman, E. H. (2006) The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity. Structure, 14, 983-992. (Pubitemid 43841994)
42. Sandler, S. J., Satin, L. H., Samra, H. S. and Clark, A. J. (1996) RecA-like genes from three archaean species with putative protein products similar to Rad51 and Dmc1 proteins of the yeast Saccharomyces cerevisiae. Nucleic Acids Res., 24, 2125-2132. (Pubitemid 26174556)
43. Chen, L. T., Ko, T. P., Chang, Y. C., Lin, K. A., Chang, C. S., Wang, A. H. and Wang, T. F. (2007) Crystal structure of the left-handed archael RadA helical filament: identification of a functional motif for controlling quaternary structures and enzymatic functions of RecA family proteins. Nucleic Acids Res., 35, 1781-1801.
44. Conway, A. B., Lynch, T. W., Zhang, Y., Fortin, G. S., Fung, C. W., Symington, L. S. and Rice, P. A. (2004) Crystal structure of a Rad51 filament. Nat. Struct. Mol. Biol., 11, 791-796. (Pubitemid 39014506)
45. Datta, S., Prabu, M. M., Vaze, M. B., Ganesh, N., Chandra, N. R., Muniyappa, K. and Vijayan, M. (2000) Crystal structures of Mycobacterium tuberculosis RecA and its complex with ADP-AlF (4): implications for decreased ATPase activity and molecular aggregation. Nucleic Acids Res., 28, 4964-4973. (Pubitemid 32014267)
46. Chen, Z., Yang, H. and Pavletich, N. P. (2008) Mechanism of homologous recombination from RecA-ssDNA/dsDNA structures. Nature, 453, 489-494. (Pubitemid 351733325)
47. Arold, S. T., Leonard, P. G., Parkinson, G. N. and Ladbury, J. E. (2010) H-NS forms a superhelical protein scaffold for DNA condensation. Proc. Natl Acad. Sci. USA, 107, 15728-15732.
48. deFazio, L. G., Stansel, R. M., Griffith, J. D. and Chu, G. (2002) Synapsis of DNA ends by DNA-dependent protein kinase. EMBO J., 21, 3192-3200. (Pubitemid 34670402)
49. Chen, L., Trujillo, K., Ramos, W., Sung, P. and Tomkinson, A. E. (2011) Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol. Cell, 8, 1105-1115.
50. Bredemeyer, A. L., Sharma, G. G., Huang, C. Y., Helmink, B. A., Walker, L. M., Khor, K. C., Nuskey, B., Sullivan, K. E., Pandita, T. K., Bassing, C. H. et al. (2006) ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature, 442, 466-470. (Pubitemid 44264797)
51. Ramsden, D. A. and Gellert, M. (1998) Ku protein stimulates DNA end joining by mammalian DNA ligases: a direct role for Ku in repair of DNA double-strand breaks. EMBO J., 17, 609-614. (Pubitemid 28045500)
52. Roy, S., Andres, S. N., Vergnes, A., Neal, J. A., Xu, Y., Yu, Y., Lees-Miller, S. P., Junop, M., Modesti, M. and Meek, K. (2012) XRCC4's interaction with XLF is required for coding (but not signal) end joining. Nucl. Acids Res., 40, 1684-1694.