A Supramodular FHA/BRCT-Repeat Architecture Mediates Nbs1 Adaptor Function in Response to DNA Damage

Cell

Volumn 139, Issue 1, 2009, Pages 100-111

  Lloyd, Janette ^a   Chapman, J Ross ^b   Clapperton, Julie A ^a   Haire, Lesley F ^a   Hartsuiker, Edgar ^c   Li, Jiejin ^a   Carr, Antony M ^c   Jackson, Stephen P ^b   Smerdon, Stephen J ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

DNA; HUMDISEASE; PROTEINS

Indexed keywords

ADAPTOR PROTEIN; ASPARTIC ACID; MRE11 PROTEIN; MULTIPROTEIN COMPLEX; NIBRIN; NUCLEASE; RAD50 PROTEIN; SCAFFOLD PROTEIN; SERINE; THREONINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; GENETIC CONSERVATION; HUMAN; HUMAN CELL; MOLECULAR DOCKING; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION;

SCHIZOSACCHAROMYCETACEAE;

EID: 70349470626     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.07.043     Document Type: Article

References (44)

1. Akamatsu Y., Murayama Y., Yamada T., Nakazaki T., Tsutsui Y., Ohta K., and Iwasaki H. Molecular characterization of the Schizosaccharomyces pombe nip1+/ctp1+ gene in DNA double strand break repair in association with the Mre11-Rad50-Nbs1 complex. Mol. Cell. Biol. 28 (2008) 3639-3651
2. Becker E., Meyer V., Madaoui H., and Guerois R. Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response. Bioinformatics 22 (2006) 1289-1292
3. Carney J.P., Maser R.S., Olivares H., Davis E.M., Le Beau M., Yates J.R., Hays L., Morgan W.F., and Petrini J.H. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93 (1998) 477-486
4. Cerosaletti K.M., and Concannon P. Nibrin forkhead-associated domain and breast cancer C-terminal domain are both required for nuclear focus formation and phosphorylation. J. Biol. Chem. 278 (2003) 21944-21951
5. Chapman J.R., and Jackson S.P. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. 9 (2008) 795-801
6. Chen L., Nievera C.J., Lee A.Y., and Wu X. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem. 283 (2008) 7713-7720
7. D'Amours D., and Jackson S.P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3 (2002) 317-327
8. Derbyshire D.J., Basu B.P., Serpell L.C., Joo W.S., Date T., Iwabuchi K., and Doherty A.J. Crystal structure of human 53BP1 BRCT domains bound to p53 tumour suppressor. EMBO J. 21 (2002) 3863-3872
9. Desai-Mehta A., Cerosaletti K.M., and Concannon P. Distinct functional domains of nibrin mediate Mre11 binding, focus formation, and nuclear localization. Mol. Cell. Biol. 21 (2001) 2184-2191
10. Difilippantonio S., and Nussenzweig A. The NBS1-ATM connection revisited. Cell Cycle 6 (2007) 2366-2370
11. Durocher D., Taylor I.A., Sarbassova D., Haire L.F., Westcott S.L., Jackson S.P., Smerdon S.J., and Yaffe M.B. The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol. Cell 6 (2000) 1169-1182
12. Falck J., Coates J., and Jackson S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434 (2005) 605-611
13. Gardino A.K., Smerdon S.J., and Yaffe M.B. Structural determinants of 14-3-3 binding specificities and regulation of subcellular localization of 14-3-3-ligand complexes: a comparison of the X-ray crystal structures of all human 14-3-3 isoforms. Semin. Cancer Biol. 16 (2006) 173-182
14. Giglione C., Boularot A., and Meinnel T. Protein N-terminal methionine excision. Cell. Mol. Life Sci. 61 (2004) 1455-1474
15. Joo W.S., Jeffrey P.D., Cantor S.B., Finnin M.S., Livingston D.M., and Pavletich N.P. Structure of the 53BP1 BRCT region bound to p53 and its comparison to the Brca1 BRCT structure. Genes Dev. 16 (2002) 583-593
16. Kobayashi J., Tauchi H., Sakamoto S., Nakamura A., Morishima K., Matsuura S., Kobayashi T., Tamai K., Tanimoto K., and Komatsu K. NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12 (2002) 1846-1851
17. Lee M.S., Edwards R.A., Thede G.L., and Glover J.N. Structure of the BRCT repeat domain of MDC1 and its specificity for the free COOH-terminal end of the gamma-H2AX histone tail. J. Biol. Chem. 280 (2005) 32053-32056
18. Li J., Williams B.L., Haire L.F., Goldberg M., Wilker E., Durocher D., Yaffe M.B., Jackson S.P., and Smerdon S.J. Structural and functional versatility of the FHA domain in DNA-damage signaling by the tumor suppressor kinase Chk2. Mol. Cell 9 (2002) 1045-1054
19. Limbo O., Chahwan C., Yamada Y., de Bruin R.A., Wittenberg C., and Russell P. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 28 (2007) 134-146
20. Lukas C., Melander F., Stucki M., Falck J., Bekker-Jensen S., Goldberg M., Lerenthal Y., Jackson S.P., Bartek J., and Lukas J. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23 (2004) 2674-2683
21. Mahajan A., Yuan C., Lee H., Chen E.S., Wu P.Y., and Tsai M.D. Structure and function of the phosphothreonine-specific FHA domain. Sci. Signal. 1 (2008) re12
22. Manke I.A., Lowery D.M., Nguyen A., and Yaffe M.B. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302 (2003) 636-639
23. Martinez A., Traverso J.A., Valot B., Ferro M., Espagne C., Ephritikhine G., Zivy M., Giglione C., and Meinnel T. Extent of N-terminal modifications in cytosolic proteins from eukaryotes. Proteomics 8 (2008) 2809-2831
24. Maser R.S., Zinkel R., and Petrini J.H. An alternative mode of translation permits production of a variant NBS1 protein from the common Nijmegen breakage syndrome allele. Nat. Genet. 27 (2001) 417-421
25. Matsuura S., Tauchi H., Nakamura A., Kondo N., Sakamoto S., Endo S., Smeets D., Solder B., Belohradsky B.H., Der Kaloustian V.M., et al. Positional cloning of the gene for Nijmegen breakage syndrome. Nat. Genet. 19 (1998) 179-181
26. Matsuzaki K., Shinohara A., and Shinohara M. Forkhead-associated domain of yeast Xrs2, a homolog of human Nbs1, promotes nonhomologous end joining through interaction with a ligase IV partner protein, Lif1. Genetics 179 (2008) 213-225
27. Melander F., Bekker-Jensen S., Falck J., Bartek J., Mailand N., and Lukas J. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J. Cell Biol. 181 (2008) 213-226
28. Nott T.J., Kelly G., Stach L., Li J., Westcott S.L., Patel D., Hunt D.M., Howell S., Buxton R.S., O'Hare H., and Smerdon S.J. An intra-molecular switch regulates phospho-independent FHA domain interactions in Mycobacterium tuberculosis. Sci. Signal. 2 (2009) ra12
29. Palmbos P.L., Wu D., Daley J.M., and Wilson T.E. Recruitment of Saccharomyces cerevisiae Dnl4-Lif1 complex to a double-strand break requires interactions with Yku80 and the Xrs2 FHA domain. Genetics 180 (2008) 1809-1819
30. Riches L.C., Lynch A.M., and Gooderham N.J. Early events in the mammalian response to DNA double-strand breaks. Mutagenesis 23 (2008) 331-339
31. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., Baer R., Lukas J., and Jackson S.P. Human CtIP promotes DNA end resection. Nature 450 (2007) 509-514
32. Spycher C., Miller E.S., Townsend K., Pavic L., Morrice N.A., Janscak P., Stewart G.S., and Stucki M. Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J. Cell Biol. 181 (2008) 227-240
33. Stucki M., Clapperton J.A., Mohammad D., Yaffe M.B., Smerdon S.J., and Jackson S.P. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123 (2005) 1213-1226
34. Suga M., and Hatakeyama T. A rapid and simple procedure for high-efficiency lithium acetate transformation of cryopreserved Schizosaccharomyces pombe cells. Yeast 22 (2005) 799-804
35. Varon R., Vissinga C., Platzer M., Cerosaletti K.M., Chrzanowska K.H., Saar K., Beckmann G., Seemanová E., Cooper P.R., Nowak N.J., et al. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93 (1998) 467-476
36. Watson A.T., Garcia V., Bone N., Carr A.M., and Armstrong J. Gene tagging and gene replacement using recombinase-mediated cassette exchange in Schizosaccharomyces pombe. Gene 407 (2008) 63-74
37. Williams R.S., Williams J.S., and Tainer J.A. Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem. Cell Biol. 85 (2007) 509-520
38. Williams R.S., Dodson G.E., Limbo O., Yamada Y., Williams J.S., Guenther G., Classen S., Glover J.N.M., Iwasaki H., Russell P., and Tainer J.A. Nbs1 Flexibly Tethers Ctp1 and Mre11-Rad50 to Coordinate DNA Double-Strand Break Processing and Repair. Cell 139 (2009) 87-99 this issue
39. Wu L., Luo K., Lou Z., and Chen J. MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 105 (2008) 11200-11205
40. Xu C., Wu L., Cui G., Botuyan M.V., Chen J., and Mer G. Structure of a second BRCT domain identified in the nijmegen breakage syndrome protein Nbs1 and its function in an MDC1-dependent localization of Nbs1 to DNA damage sites. J. Mol. Biol. 381 (2008) 361-372
41. You Z., Chahwan C., Bailis J., Hunter T., and Russell P. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25 (2005) 5363-5379
42. Yu X., Chini C.C., He M., Mer G., and Chen J. The BRCT domain is a phospho-protein binding domain. Science 302 (2003) 639-642
43. Zhao S., Weng Y.C., Yuan S.S., Lin Y.T., Hsu H.C., Lin S.C., Gerbino E., Song M.H., Zdzienicka M.Z., Gatti R.A., et al. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405 (2000) 473-477
44. Zhu J., Petersen S., Tessarollo L., and Nussenzweig A. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 11 (2001) 105-109