Structural insights into the role of domain flexibility in human DNA ligase IV

Structure

Volumn 20, Issue 7, 2012, Pages 1212-1222

  Ochi, Takashi ^a   Wu, Qian ^a   Chirgadze, Dimitri Y ^a   Grossmann, J Günter ^b   Bolanos Garcia, Victor M ^a   Blundell, Tom L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDYLTRANSFERASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; XRCC4 PROTEIN;

CHROMATOGRAPHY; ENZYME STRUCTURE; ORTHOLOGY; PRIORITY JOURNAL; REVIEW; X RAY CRYSTALLOGRAPHY;

EID: 84863531762     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.04.012     Document Type: Article

References (71)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. P. Ahnesorg, P. Smith, and S.P. Jackson XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining Cell 124 2006 301 313 (Pubitemid 43121979)
3. S.N. Andres, M. Modesti, C.J. Tsai, G. Chu, and M.S. Junop Crystal structure of human XLF: a twist in nonhomologous DNA end-joining Mol. Cell 28 2007 1093 1101 (Pubitemid 350297023)
4. S.N. Andres, A. Vergnes, D. Ristic, C. Wyman, M. Modesti, and M. Junop A human XRCC4-XLF complex bridges DNA Nucleic Acids Res. 40 2012 1868 1878
5. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, and D.J. Lipman Basic local alignment search tool J. Mol. Biol. 215 1990 403 410
6. S. Balaji, and L. Aravind The RAGNYA fold: a novel fold with multiple topological variants found in functionally diverse nucleic acid, nucleotide and peptide-binding proteins Nucleic Acids Res. 35 2007 5658 5671 (Pubitemid 47506285)
7. T.G. Battye, L. Kontogiannis, O. Johnson, H.R. Powell, and A.G. Leslie iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM Acta Crystallogr. D Biol. Crystallogr. 67 2011 271 281
8. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne The protein data bank Nucleic Acids Res. 28 2000 235 242 (Pubitemid 30047768)
9. M. Bryans, M.C. Valenzano, and T.D. Stamato Absence of DNA ligase IV protein in XR-1 cells: evidence for stabilization by XRCC4 Mutat. Res. 433 1999 53 58 (Pubitemid 29073670)
10. D. Buck, D. Moshous, R. de Chasseval, Y. Ma, F. le Deist, M. Cavazzana-Calvo, A. Fischer, J.-L. Casanova, M.R. Lieber, and J.-P. de Villartay Severe combined immunodeficiency and microcephaly in siblings with hypomorphic mutations in DNA ligase IV Eur. J. Immunol. 36 2006 224 235 (Pubitemid 43116409)
11. D. Buck, L. Malivert, R. de Chasseval, A. Barraud, M.-C. Fondanèche, O. Sanal, A. Plebani, J.-L. Stéphan, M. Hufnagel, and F. le Deist Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly Cell 124 2006 287 299 (Pubitemid 43121978)
12. X. Chen, and A.E. Tomkinson Yeast Nej1 is a key participant in the initial end binding and final ligation steps of nonhomologous end joining J. Biol. Chem. 286 2011 4931 4940
13. X. Chen, J.D. Ballin, J. Della-Maria, M.-S. Tsai, E.J. White, A.E. Tomkinson, and G.M. Wilson Distinct kinetics of human DNA ligases I, IIIalpha, IIIbeta, and IV reveal direct DNA sensing ability and differential physiological functions in DNA repair DNA Repair (Amst.) 8 2009 961 968
14. S. Costantini, L. Woodbine, L. Andreoli, P.A. Jeggo, and A. Vindigni Interaction of the Ku heterodimer with the DNA ligase IV/Xrcc4 complex and its regulation by DNA-PK DNA Repair (Amst.) 6 2007 712 722 (Pubitemid 46670084)
15. E. Cotner-Gohara, I.-K. Kim, M. Hammel, J.A. Tainer, A.E. Tomkinson, and T. Ellenberger Human DNA ligase III recognizes DNA ends by dynamic switching between two DNA-bound states Biochemistry 49 2010 6165 6176
16. K. Cowtan "dm": An automated procedure for phase improvement by density modification Joint CCP4 ESF-EACBM Newsl Protein Crystallogr. 31 1994 34 38
17. S.E. Critchlow, R.P. Bowater, and S.P. Jackson Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV Curr. Biol. 7 1997 588 598 (Pubitemid 27335654)
18. R.A. Deshpande, and T.E. Wilson Modes of interaction among yeast Nej1, Lif1 and Dnl4 proteins and comparison to human XLF, XRCC4 and Lig4 DNA Repair (Amst.) 6 2007 1507 1516 (Pubitemid 47386045)
19. A.S. Doré, N. Furnham, O.R. Davies, B.L. Sibanda, D.Y. Chirgadze, S.P. Jackson, L. Pellegrini, and T.L. Blundell Structure of an Xrcc4-DNA ligase IV yeast ortholog complex reveals a novel BRCT interaction mode DNA Repair (Amst.) 5 2006 362 368 (Pubitemid 43247602)
20. R.C. Edgar MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797 (Pubitemid 38832724)
21. M.B. Einarson Detection of protein-protein interactions using the GST fusion protein pull-down technique J. Sambrook, D.W. Russell, Molecular Cloning: A Laboratory Manual 2001 Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York 18.55 18.59
22. T. Ellenberger, and A.E. Tomkinson Eukaryotic DNA ligases: structural and functional insights Annu. Rev. Biochem. 77 2008 313 338
23. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
24. P. Evans Scaling and assessment of data quality Acta Crystallogr. D Biol. Crystallogr. 62 2006 72 82
25. P.-M. Girard, B. Kysela, C.J. Härer, A.J. Doherty, and P.A. Jeggo Analysis of DNA ligase IV mutations found in LIG4 syndrome patients: the impact of two linked polymorphisms Hum. Mol. Genet. 13 2004 2369 2376 (Pubitemid 39377841)
26. M. Gouy, S. Guindon, and O. Gascuel SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building Mol. Biol. Evol. 27 2010 221 224
27. U. Grawunder, M. Wilm, X. Wu, P. Kulesza, T.E. Wilson, M. Mann, and M.R. Lieber Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells Nature 388 1997 492 495 (Pubitemid 27328929)
28. N.V. Grishin Phosphatidylinositol phosphate kinase: a link between protein kinase and glutathione synthase folds J. Mol. Biol. 291 1999 239 247 (Pubitemid 29381425)
29. M. Hammel, Y. Yu, S. Fang, S.P. Lees-Miller, and J.A. Tainer XLF regulates filament architecture of the XRCC4·ligase IV complex Structure 18 2010 1431 1442
30. M. Hammel, M. Rey, Y. Yu, R.S. Mani, S. Classen, M. Liu, M.E. Pique, S. Fang, B.L. Mahaney, and M. Weinfeld 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 2011 32638 32650
31. J. Kim, O. Kim, H.W. Kim, H.S. Kim, S.J. Lee, and S.W. Suh ATP-dependent DNA ligase from Archaeoglobus fulgidus displays a tightly closed conformation Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65 2009 544 550
32. M.R. Lieber The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway Annu. Rev. Biochem. 79 2010 181 211
33. R.S. Mani, Y. Yu, S. Fang, M. Lu, M. Fanta, A.E. Zolner, N. Tahbaz, D.A. Ramsden, D.W. Litchfield, S.P. Lees-Miller, and M. Weinfeld Dual modes of interaction between XRCC4 and polynucleotide kinase/phosphatase: implications for nonhomologous end joining J. Biol. Chem. 285 2010 37619 37629
34. K. Mizuguchi, C.M. Deane, T.L. Blundell, M.S. Johnson, and J.P. Overington JOY: protein sequence-structure representation and analysis Bioinformatics 14 1998 617 623 (Pubitemid 28461583)
35. G.N. Murshudov, P. Skubák, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 67 2011 355 367
36. A.G. Murzin Structural classification of proteins: new superfamilies Curr. Opin. Struct. Biol. 6 1996 386 394 (Pubitemid 26197440)
37. P.A. Nair, J. Nandakumar, P. Smith, M. Odell, C.D. Lima, and S. Shuman Structural basis for nick recognition by a minimal pluripotent DNA ligase Nat. Struct. Mol. Biol. 14 2007 770 778 (Pubitemid 47220053)
38. A. Nijnik, L. Woodbine, C. Marchetti, S. Dawson, T. Lambe, C. Liu, N.P. Rodrigues, T.L. Crockford, E. Cabuy, and A. Vindigni DNA repair is limiting for haematopoietic stem cells during ageing Nature 447 2007 686 690 (Pubitemid 46889732)
39. H. Nishida, S. Kiyonari, Y. Ishino, and K. Morikawa The closed structure of an archaeal DNA ligase from Pyrococcus furiosus J. Mol. Biol. 360 2006 956 967 (Pubitemid 44062514)
40. T. Ochi, B.L. Sibanda, Q. Wu, D.Y. Chirgadze, V.M. Bolanos-Garcia, and T.L. Blundell Structural biology of DNA repair: spatial organisation of the multicomponent complexes of nonhomologous end joining J. Nucleic Acids 2010 2010 1 19
41. M. O'Driscoll, K.M. Cerosaletti, P.-M. Girard, Y. Dai, M. Stumm, B. Kysela, B. Hirsch, A. Gennery, S.E. Palmer, and J. Seidel DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency Mol. Cell 8 2001 1175 1185 (Pubitemid 34084990)
42. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326 (Pubitemid 27085611)
43. J.M. Pascal, P.J. O'Brien, A.E. Tomkinson, and T. Ellenberger Human DNA ligase I completely encircles and partially unwinds nicked DNA Nature 432 2004 473 478 (Pubitemid 39576523)
44. J.M. Pascal, O.V. Tsodikov, G.L. Hura, W. Song, E.A. Cotner, S. Classen, A.E. Tomkinson, J.A. Tainer, and T. Ellenberger A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA Mol. Cell 24 2006 279 291 (Pubitemid 44557121)
45. J. Peränen, M. Rikkonen, M. Hyvönen, and L. Kääriäinen T7 vectors with modified T7lac promoter for expression of proteins in Escherichia coli Anal. Biochem. 236 1996 371 373
46. J.J.P. Perry, E. Cotner-Gohara, T. Ellenberger, and J.A. Tainer Structural dynamics in DNA damage signaling and repair Curr. Opin. Struct. Biol. 20 2010 283 294
47. M.V. Petoukhov, and D.I. Svergun Global rigid body modeling of macromolecular complexes against small-angle scattering data Biophys. J. 89 2005 1237 1250 (Pubitemid 41099005)
48. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
49. M.A. Recuero-Checa, A.S. Doré, E. Arias-Palomo, A. Rivera-Calzada, S.H.W. Scheres, J.D. Maman, L.H. Pearl, and O. Llorca Electron microscopy of Xrcc4 and the DNA ligase IV-Xrcc4 DNA repair complex DNA Repair (Amst.) 8 2009 1380 1389
50. E. Riballo, S.E. Critchlow, S.H. Teo, A.J. Doherty, A. Priestley, B. Broughton, B. Kysela, H. Beamish, N. Plowman, and C.F. Arlett Identification of a defect in DNA ligase IV in a radiosensitive leukaemia patient Curr. Biol. 9 1999 699 702 (Pubitemid 29332352)
51. E. Riballo, A.J. Doherty, Y. Dai, T. Stiff, M.A. Oettinger, P.A. Jeggo, and B. Kysela Cellular and biochemical impact of a mutation in DNA ligase IV conferring clinical radiosensitivity J. Biol. Chem. 276 2001 31124 31132
52. E. Riballo, L. Woodbine, T. Stiff, S.A. Walker, A.A. Goodarzi, and P.A. Jeggo XLF-Cernunnos promotes DNA ligase IV-XRCC4 re-adenylation following ligation Nucleic Acids Res. 37 2009 482 492
53. V. Ropars, P. Drevet, P. Legrand, S. Baconnais, J. Amram, G. Faure, J.A. Márquez, O. Piétrement, R. Guerois, and I. Callebaut Structural characterization of filaments formed by human Xrcc4-Cernunnos/XLF complex involved in nonhomologous DNA end-joining Proc. Natl. Acad. Sci. USA 108 2011 12663 12668
54. A. Sali, and T.L. Blundell Comparative protein modeling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815 (Pubitemid 24007801)
55. J. Shi, T.L. Blundell, and K. Mizuguchi FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties J. Mol. Biol. 310 2001 243 257 (Pubitemid 32619966)
56. S. Shuman, and B. Schwer RNA capping enzyme and DNA ligase: a superfamily of covalent nucleotidyl transferases Mol. Microbiol. 17 1995 405 410
57. S. Shuman, and C.D. Lima The polynucleotide ligase and RNA capping enzyme superfamily of covalent nucleotidyltransferases Curr. Opin. Struct. Biol. 14 2004 757 764 (Pubitemid 39592587)
58. B.L. Sibanda, S.E. Critchlow, J. Begun, X.Y. Pei, S.P. Jackson, T.L. Blundell, and L. Pellegrini Crystal structure of an Xrcc4-DNA ligase IV complex Nat. Struct. Biol. 8 2001 1015 1019 (Pubitemid 33101619)
59. G.C.M. Smith, and S.P. Jackson The DNA-dependent protein kinase Genes Dev. 13 1999 916 934 (Pubitemid 29200976)
60. H.S. Subramanya, A.J. Doherty, S.R. Ashford, and D.B. Wigley Crystal structure of an ATP-dependent DNA ligase from bacteriophage T7 Cell 85 1996 607 615 (Pubitemid 26157198)
61. D.I. Svergun Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25 1992 495 503 (Pubitemid 23564996)
62. D.I. Svergun Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing Biophys. J. 76 1999 2879 2886 (Pubitemid 29269438)
63. D.I. Svergun, and M.H.J. Koch Small-angle scattering studies of biological macromolecules in solution Rep. Prog. Phys. 66 2003 1735 1782 (Pubitemid 37365734)
64. N. Toita, N. Hatano, S. Ono, M. Yamada, R. Kobayashi, I. Kobayashi, N. Kawamura, M. Okano, A. Satoh, and A. Nakagawa Epstein-Barr virus-associated B-cell lymphoma in a patient with DNA ligase IV (LIG4) syndrome Am. J. Med. Genet. A. 143 2007 742 745 (Pubitemid 46606685)
65. A. Vagin, and A. Teplyakov MOLREP: an Automated Program for Molecular Replacement J. Appl. Crystallogr. 30 1997 1022 1025 (Pubitemid 127485985)
66. Y. Wang, B.J. Lamarche, and M.D. Tsai Human DNA ligase IV and the ligase IV/XRCC4 complex: analysis of nick ligation fidelity Biochemistry 46 2007 4962 4976 (Pubitemid 46682995)
67. C.L. Worth, and T.L. Blundell On the evolutionary conservation of hydrogen bonds made by buried polar amino acids: the hidden joists, braces and trusses of protein architecture BMC Evol. Biol. 10 2010 161
68. C.L. Worth, R. Preissner, and T.L. Blundell SDM - a server for predicting effects of mutations on protein stability and malfunction Nucleic Acids Res. 39 Web Server issue 2011 W215-22
69. P.Y. Wu, P. Frit, S. Meesala, S. Dauvillier, M. Modesti, S.N. Andres, Y. Huang, J. Sekiguchi, P. Calsou, B. Salles, and M.S. Junop Structural and functional interaction between the human DNA repair proteins DNA ligase IV and XRCC4 Mol. Cell. Biol. 29 2009 3163 3172
70. Q. Wu, T. Ochi, D. Matak-Vinkovic, C.V. Robinson, D.Y. Chirgadze, and T.L. Blundell Nonhomologous end-joining partners in a helical dance: structural studies of XLF-XRCC4 interactions Biochem. Soc. Trans. 39 2011 1387 1392 2, 1392
71. K.-I. Yano, K. Morotomi-Yano, S.-Y.Y. Wang, N. Uematsu, K.-J.J. Lee, A. Asaithamby, E. Weterings, and D.J. Chen Ku recruits XLF to DNA double-strand breaks EMBO Rep. 9 2008 91 96