Nbs1 Flexibly Tethers Ctp1 and Mre11-Rad50 to Coordinate DNA Double-Strand Break Processing and Repair

Cell

Volumn 139, Issue 1, 2009, Pages 87-99

  Williams, R Scott ^a   Dodson, Gerald E ^a   Limbo, Oliver ^a   Yamada, Yoshiki ^a   Williams, Jessica S ^a   Guenther, Grant ^a   Classen, Scott ^b   Glover, J N Mark ^c   Iwasaki, Hiroshi ^d   Russell, Paul ^a   Tainer, John A ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

DISEASE; DNA; PROTEINS

Indexed keywords

ATM PROTEIN; CYTIDINE TRIPHOSPHATE; MRE11 PROTEIN; NIBRIN; PROTEIN SUBUNIT; RAD50 PROTEIN;

ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENETIC ANALYSIS; GENOME; HOMOLOGOUS RECOMBINATION; NIJMEGEN BREAKAGE SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

SCHIZOSACCHAROMYCETACEAE;

EID: 70349472553     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.07.033     Document Type: Article

References (54)

1. Akamatsu Y., Murayama Y., Yamada T., Nakazaki T., Tsutsui Y., Ohta K., and Iwasaki H. Molecular characterization of the role 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. Bernstein N.K., Williams R.S., Rakovszky M.L., Cui D., Green R., Karimi-Busheri F., Mani R.S., Galicia S., Koch C.A., Cass C.E., et al. The molecular architecture of the mammalian DNA repair enzyme, polynucleotide kinase. Mol. Cell 17 (2005) 657-670
3. Carney J.P., Maser R.S., Olivares H., Davis E.M., Le Beau M., Yates III 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. Chapados B.R., Hosfield D.J., Han S., Qiu J., Yelent B., Shen B., and Tainer J.A. Structural basis for FEN-1 substrate specificity and PCNA-mediated activation in DNA replication and repair. Cell 116 (2004) 39-50
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., Trujillo K., Ramos W., Sung P., and Tomkinson A.E. Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol. Cell 8 (2001) 1105-1115
7. 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
8. Chen P.L., Liu F., Cai S., Lin X., Li A., Chen Y., Gu B., Lee E.Y., and Lee W.H. Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insufficiency. Mol. Cell. Biol. 25 (2005) 3535-3542
9. Clapperton J.A., Manke I.A., Lowery D.M., Ho T., Haire L.F., Yaffe M.B., and Smerdon S.J. Structure and mechanism of BRCA1 BRCT domain recognition of phosphorylated BACH1 with implications for cancer. Nat. Struct. Mol. Biol. 11 (2004) 512-518
10. DiDonato M., Craig L., Huff M.E., Thayer M.M., Cardoso R.M., Kassmann C.J., Lo T.P., Bruns C.K., Powers E.T., Kelly J.W., et al. ALS mutants of human superoxide dismutase form fibrous aggregates via framework destabilization. J. Mol. Biol. 332 (2003) 601-615
11. Difilippantonio S., Celeste A., Fernandez-Capetillo O., Chen H.T., Reina San Martin B., Van Laethem F., Yang Y.P., Petukhova G.V., Eckhaus M., Feigenbaum L., et al. Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat. Cell Biol. 7 (2005) 675-685
12. Digweed M., and Sperling K. Nijmegen breakage syndrome: clinical manifestation of defective response to DNA double-strand breaks. DNA Repair (Amst.) 3 (2004) 1207-1217
13. Durocher D., Henckel J., Fersht A.R., and Jackson S.P. The FHA domain is a modular phosphopeptide recognition motif. Mol. Cell 4 (1999) 387-394
14. 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
15. Fan L., Fuss J.O., Cheng Q.J., Arvai A.S., Hammel M., Roberts V.A., Cooper P.K., and Tainer J.A. XPD helicase structures and activities: insights into the cancer and aging phenotypes from XPD mutations. Cell 133 (2008) 789-800
16. Glover J.N., Williams R.S., and Lee M.S. Interactions between BRCT repeats and phosphoproteins: tangled up in two. Trends Biochem. Sci. 29 (2004) 579-585
17. Goldberg M., Stucki M., Falck J., D'Amours D., Rahman D., Pappin D., Bartek J., and Jackson S.P. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421 (2003) 952-956
18. Hartsuiker E., Neale M.J., and Carr A.M. Distinct requirements for the Rad32(Mre11) nuclease and Ctp1(CtIP) in the removal of covalently bound topoisomerase I and II from DNA. Mol. Cell 33 (2009) 117-123
19. Heikkinen K., Rapakko K., Karppinen S.M., Erkko H., Knuutila S., Lundan T., Mannermaa A., Borresen-Dale A.L., Borg A., Barkardottir R.B., et al. RAD50 and NBS1 are breast cancer susceptibility genes associated with genomic instability. Carcinogenesis 27 (2006) 1593-1599
20. Hopfner K.P., Karcher A., Shin D.S., Craig L., Arthur L.M., Carney J.P., and Tainer J.A. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101 (2000) 789-800
21. Hopfner K.P., Karcher A., Craig L., Woo T.T., Carney J.P., and Tainer J.A. Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105 (2001) 473-485
22. Hopfner K.P., Craig L., Moncalian G., Zinkel R.A., Usui T., Owen B.A., Karcher A., Henderson B., Bodmer J.L., McMurray C.T., et al. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418 (2002) 562-566
23. Hopkins B.B., and Paull T.T. The P. furiosus Mre11/Rad50 complex promotes 5′ strand resection at a DNA double-strand break. Cell 135 (2008) 250-260
24. Hura G.L., Menon A.L., Hammel M., Rambo R.P., Poole II F.L., Tsutakawa S.E., Jenney Jr. F.E., Classen S., Frankel K.A., Hopkins R.C., et al. Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS). Nat. Methods 6 (2009) 606-612
25. Kruger L., Demuth I., Neitzel H., Varon R., Sperling K., Chrzanowska K.H., Seemanova E., and Digweed M. Cancer incidence in Nijmegen breakage syndrome is modulated by the amount of a variant NBS protein. Carcinogenesis 28 (2007) 107-111
26. Lee J.H., and Paull T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308 (2005) 551-554
27. Lengsfeld B.M., Rattray A.J., Bhaskara V., Ghirlando R., and Paull T.T. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28 (2007) 638-651
28. 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
29. Lloyd J., Chapman J.R., Clapperton J.A., Haire L.F., Hartsuiker E., Li J., Carr A.M., Jackson S.P., and Smerdon S.J. A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 139 (2009) 100-111 this issue
30. Lou Z., Minter-Dykhouse K., Franco S., Gostissa M., Rivera M.A., Celeste A., Manis J.P., van Deursen J., Nussenzweig A., Paull T.T., et al. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 21 (2006) 187-200
31. 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
32. 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
33. 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
34. Mimitou E.P., and Symington L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455 (2008) 770-774
35. Moreno-Herrero F., de Jager M., Dekker N.H., Kanaar R., Wyman C., and Dekker C. Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature 437 (2005) 440-443
36. Neale M.J., Pan J., and Keeney S. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436 (2005) 1053-1057
37. 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
38. Pascal J.M., Tsodikov O.V., Hura G.L., Song W., Cotner E.A., Classen S., Tomkinson A.E., Tainer J.A., and Ellenberger T. A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA. Mol. Cell 24 (2006) 279-291
39. Putnam C.D., Hammel M., Hura G.L., and Tainer J.A. X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q. Rev. Biophys. 40 (2007) 191-285
40. 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
41. Seemanova E., Sperling K., Neitzel H., Varon R., Hadac J., Butova O., Schrock E., Seeman P., and Digweed M. Nijmegen breakage syndrome (NBS) with neurological abnormalities and without chromosomal instability. J. Med. Genet. 43 (2006) 218-224
42. Shima H., Suzuki M., and Shinohara M. Isolation and characterization of novel xrs2 mutations in Saccharomyces cerevisiae. Genetics 170 (2005) 71-85
43. Shin D.S., Pellegrini L., Daniels D.S., Yelent B., Craig L., Bates D., Yu D.S., Shivji M.K., Hitomi C., Arvai A.S., et al. Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. EMBO J. 22 (2003) 4566-4576
44. 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
45. Stewart G.S., Maser R.S., Stankovic T., Bressan D.A., Kaplan M.I., Jaspers N.G., Raams A., Byrd P.J., Petrini J.H., and Taylor A.M. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99 (1999) 577-587
46. 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
47. Stucki M., and Jackson S.P. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst.) 5 (2006) 534-543
48. Williams R.S., Green R., and Glover J.N. Crystal structure of the BRCT repeat region from the breast cancer-associated protein BRCA1. Nat. Struct. Biol. 8 (2001) 838-842
49. Williams R.S., Lee M.S., Hau D.D., and Glover J.N. Structural basis of phosphopeptide recognition by the BRCT domain of BRCA1. Nat. Struct. Mol. Biol. 11 (2004) 519-525
50. 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
51. Williams R.S., Moncalian G., Williams J.S., Yamada Y., Limbo O., Shin D.S., Groocock L.M., Cahill D., Hitomi C., Guenther G., et al. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 135 (2008) 97-109
52. 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
53. 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
54. Zhu Z., Chung W.H., Shim E.Y., Lee S.E., and Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134 (2008) 981-994