Mre11 Dimers Coordinate DNA End Bridging and Nuclease Processing in Double-Strand-Break Repair

Cell

Volumn 135, Issue 1, 2008, Pages 97-109

  Williams, R Scott ^a   Moncalian, Gabriel ^a   Williams, Jessica S ^a   Yamada, Yoshiki ^a   Limbo, Oliver ^a   Shin, David S ^a   Groocock, Lynda M ^a   Cahill, Dana ^b   Hitomi, Chiharu ^a   Guenther, Grant ^a   Moiani, Davide ^a   Carney, James P ^b   Russell, Paul ^a   Tainer, John A ^a,c  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

DNA

Indexed keywords

ATM PROTEIN; DIMER; DOUBLE STRANDED DNA; NIBRIN; NUCLEASE; PROTEIN CTP1; RAD50 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATAXIA TELANGIECTASIA; CELL SURVIVAL; COMPLEX FORMATION; CRYSTAL STRUCTURE; DIMERIZATION; DNA REPAIR; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE MUTATION; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PYROCOCCUS FURIOSUS; X RAY ANALYSIS; X RAY CRYSTALLOGRAPHY; YEAST;

ATAXIA TELANGIECTASIA; PYROCOCCUS FURIOSUS; SCHIZOSACCHAROMYCETACEAE;

EID: 52949149420     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.08.017     Document Type: Article

References (41)

1. Bressan D.A., Olivares H.A., Nelms B.E., and Petrini J.H. Alteration of N-terminal phosphoesterase signature motifs inactivates Saccharomyces cerevisiae Mre11. Genetics 150 (1998) 591-600
2. Buis J., Wu Y., Deng Y., Leddon J., Westfield G., Eckersdorff M., Sekiguchi J.M., Chang S., and Ferguson D.O. Mre11 Nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135 (2008) 85-96 this issue
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. Chahwan C., Nakamura T.M., Sivakumar S., Russell P., and Rhind N. The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol. Cell. Biol. 23 (2003) 6564-6573
5. 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
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. Costanzo V., Robertson K., Bibikova M., Kim E., Grieco D., Gottesman M., Carroll D., and Gautier J. Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell 8 (2001) 137-147
8. de Jager M., van Noort J., van Gent D.C., Dekker C., Kanaar R., and Wyman C. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell 8 (2001) 1129-1135
9. 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
10. 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 provide insights into cancer and aging phenotypes from XPD mutations. Cell 133 (2008) 789-800
11. Fernet M., Gribaa M., Salih M.A., Seidahmed M.Z., Hall J., and Koenig M. Indentification and functional consequences of a novel Mre11 mutation affecting 10 Saudi Arabian patients with the ataxia telangiectasia-like disorder. Hum. Mol. Genet. 14 (2005) 307-318
12. 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
13. 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
14. Krogh B.O., Llorente B., Lam A., and Symington L.S. Mutations in Mre11 phosphoesterase motif I that impair Saccharomyces cerevisiae Mre11-Rad50-Xrs2 complex stability in addition to nuclease activity. Genetics 171 (2005) 1561-1570
15. Lee J.H., Ghirlando R., Bhaskara V., Hoffmeyer M.R., Gu J., and Paull T.T. Regulation of Mre11/Rad50 by Nbs1: effects on nucleotide-dependent DNA binding and association with ataxia-telangiectasia-like disorder mutant complexes. J. Biol. Chem. 278 (2003) 45171-45181
16. 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
17. 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
18. Lewis L.K., Storici F., Van Komen S., Calero S., Sung P., and Resnick M.A. Role of the nuclease activity of Saccharomyces cerevisiae Mre11 in repair of DNA double-strand breaks in mitotic cells. Genetics 166 (2004) 1701-1713
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. Lisby M., Barlow J.H., Burgess R.C., and Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118 (2004) 699-713
21. Manolis K.G., Nimmo E.R., Hartsuiker E., Carr A.M., Jeggo P.A., and Allshire R.C. Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J. 20 (2001) 210-221
22. Mirzoeva O.K., and Petrini J.H. DNA damage-dependent nuclear dynamics of the Mre11 complex. Mol. Cell. Biol. 21 (2001) 281-288
23. 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
24. Moreau S., Morgan E.A., and Symington L.S. Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism. Genetics 159 (2001) 1423-1433
25. Paull T.T., and Gellert M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1 (1998) 969-979
26. Paull T.T., and Gellert M. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13 (1999) 1276-1288
27. Paull T.T., and Gellert M. A mechanistic basis for Mre11-directed DNA joining at microhomologies. Proc. Natl. Acad. Sci. USA 97 (2000) 6409-6414
28. 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
29. Rattray A.J., McGill C.B., Shafer B.K., and Strathern J.N. Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 158 (2001) 109-122
30. 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
31. Shiloh Y. ATM and related protein kinases: Safeguarding genome integrity. Nat. Rev. Cancer 3 (2003) 155-168
32. 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
33. Tomita K., Matsuura A., Caspari T., Carr A.M., Akamatsu Y., Iwasaki H., Mizuno K., Ohta K., Uritani M., Ushimaru T., et al. Competition between the Rad50 complex and the Ku heterodimer reveals a role for Exo1 in processing double-strand breaks but not telomeres. Mol. Cell. Biol. 23 (2003) 5186-5197
34. Trenz K., Smith E., Smith S., and Costanzo V. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 25 (2006) 1764-1774
35. Trujillo K.M., Yuan S.S., Lee E.Y., and Sung P. Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 273 (1998) 21447-21450
36. Trujillo K.M., and Sung P. DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50/Mre11 complex. J. Biol. Chem. 276 (2001) 35458-35464
37. Wen Q., Scorah J., Phear G., Rodgers G., Rodgers S., and Meuth M. A mutant allele of MRE11 found in mismatch repair deficient tumor cells suppresses the cellular response to DNA replication fork stress in a dominant negative manner. Mol. Biol. Cell 19 (2008) 1693-1705
38. Williams R.S., Lee M.S., Hau D.D., and Glover J.N. Structural basis of phosphopeptide recongnition by the BRCT domain of BRCA1. Nat. Struct. Mol. Biol. 11 (2004) 519-525
39. 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
40. Wyman C., and Kanaar R. DNA double-strand break repair: All's well that ends well. Annu. Rev. Genet. 40 (2006) 363-383
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