RAD50 and NBS1 form a stable complex functional in DNA binding and tethering

Nucleic Acids Research

Volumn 37, Issue 5, 2009, Pages 1580-1588

  Van der linden, Eddy ^a   Sanchez, Humberto ^a   Kinoshita, Eri ^a   Kanaar, Roland ^a   Wyman, Claire ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

NIBRIN; RAD50 PROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA PROTEIN COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; SCANNING FORCE MICROSCOPY; STOICHIOMETRY;

CELL CYCLE PROTEINS; DNA; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; HUMANS; MICROSCOPY, ATOMIC FORCE; NUCLEAR PROTEINS; PROTEIN BINDING;

EID: 63249083853     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn1072     Document Type: Article

References (52)

1. Su,T.T. (2006) Cellular responses to DNA damage: One signal, multiple choices. Ann. Rev. Genetics, 40, 187-208.
2. Khanna,K.K. and Jackson,S.P. (2001) DNA double-strand breaks: signalling, repair and the cancer connection. Nat. Gen., 27, 247-254.
3. Valerie,K. and Povirk,L.F. (2003) Regulation and mechanisms of mammalian double-strand break repair. Oncogene, 22, 5792-5812.
4. Van Gent,D.C., Hoeijmakers,J.H.J. and Kanaar,R. (2001) Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet., 2, 196-206.
5. Borde,V., Lin,W., Novikov,E., Petrini,J.H., Lichten,M. and Nicolas,A. (2004) Association of Mre11p with double-strand break sites during yeast meiosis. Mol. Cell, 13, 389-401.
6. Lisby,M., Barlow,J.H., Burgess,R.C. and Rothstein,R. (2004) Choreography of the DNA damage response: Spatiotemporal relationships among checkpoint and repair proteins. Cell, 118, 666-668.
7. Luo,G., Yao,M.S., Bender,C.F., Mills,M., Bladl,A.R., Bradley,A. and Petrini,J.H.J. (1999) Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl Acad. Sci. USA, 96, 7376-7381.
8. Xiao,Y. and Weaver,D.T. (1997) Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res., 25, 2985-2991.
9. Zhu,J., Petersen,S., Tessarollo,L. and Nussenzweig,A. (2001) Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol., 11, 105-109.
10. Chahwan,C., Nakamura,T.M., Sivakumar,S., Russell,P. and Rhind,N. (2003) The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol. Cell. Biol., 23, 6564-6573.
11. D'Amours,D. and Jackson,S.P. (2002) The MRE11 complex: At the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3, 317-327.
12. Pâques,F. and Haber,J.E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 63, 349-404.
13. Varon,R., Viussinga,C., Platzer,M., Cerosaletti,K.M., Chrzanowska,K.H., Saar,K., Beckmann,G., Seemanová,E., Cooper,P.R., Nowak,N.J. et al. (1998) Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell, 93, 467-476.
14. Stewart,G.S., Maser,R.S., Stankovic,T., Bressan,D.A., Kaplan,M.I., Jaspers,N.G.J., Raams,A., Byrd,P.J., Petrini,J.H.J. and Taylor,A.M. (1999) The DNA double-strand break repair gene hMRE11 is mutated in individuals with an Ataxia-Telangiectasia-like disorder. Cell, 99, 577-587.
15. de Jager,M., van Noort,J., van Gent,D., Dekker,C., Kanaar,R. and Wyman,C. (2001) Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell, 8, 1129-1135.
16. Hopfner,K.P., Karcher,A., Craig,L., Woo,T.T., Carney,J.P. and Tainer,J.A. (2001) Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell, 105, 473-485.
17. Hopfner,K.P., Karcher,A., Shin,D.S., Craig,L., Arthur,L.M., Carney,J.P. and Tainer,J.A. (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell, 101, 789-800.
18. Hopfner,K.P., Craig,L., Moncalian,G., Zinkel,R.A., Usui,T., Owen,B.A.L., Karcher,A., Henderson,B., Bodmer,J.L., McMurray,C.T. et al. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature, 418, 562-566.
19. Van Noort,J., Van der Heijden,T., De Jager,M., Wyman,C., Kanaar,R. and Dekker,C. (2003) The coiled-coil of the human Rad50 DNA repair protein contains specific segments of increased flexibility. Proc. Natl Acad. Sci. USA, 100, 7581-7586.
20. Wiltzius,J.J.W., Hohl,M., Fleming,J.C. and Petrini,J.H.J. (2005) The Rad50 hook domain is a critical determinant of Mre11 complex functions. Nat. Struct. Mol. Biol., 12, 403-407.
21. Cahill,D. and Carney,J.P. (2007) Dimerization of the Rad50 protein is independent of the conserved hook domain. Mutagenesis, 22, 269-274.
22. Carney,J.P., Maser,R.S., Olivares,H., Davis,E.M., Le Beau,M., Yates,J.R. III, Hays,L., Morgan,W.F. and Petrini,J.H.J. (1998) The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: Linkage of double-strand break repair to the cellular DNA damage response. Cell, 93, 477-486.
23. Moncalian,G., Lengsfeld,B., Bhaskara,V., Hopfner,K.P., Karcher,A., Alden,E., Tainer,J.A. and Paull,T.T. (2004) The Rad50 signature motif: Essential to ATP binding and biological function. J. Mol. Biol., 335, 937-951.
24. Paull,T.T. and Gellert,M. (1998) The 3′ to 5′ exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell 1, 969-979.
25. Paull,T.T. and Gellert,M. (1999) Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev., 13, 1276-1288.
26. de Jager,M., Dronkert,M.L.G., Modesti,M., Beerens,C.E.M.T., Kanaar,R. and van Gent,D.C. (2001) DNA-binding and strand-annealing activities of human Mre11: Implications for its roles in DNA double-strand break repair pathways. Nucleic Acids Res., 29, 1317-1325.
27. Hopfner,K.P., Karcher,A., Shin,D.S., Fairley,C., Tainer,J.A. and Carney,J.P. (2000) Mre11 and Rad50 from Pyrococcus furiosus: Cloning and biochemical characterization reveal an evolutionarily conserved multiprotein machine. J. Bacteriol., 182, 6036-6041.
28. Furuse,M., Nagase,Y., Tsubouchi,H., Murakami-Murofushi,K., Shibata,T. and Ohta,K. (1998) Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J., 17, 6412-6425.
29. Trujillo,K.M., Yuan,S.F., Lee,E.Y.H.P. and Sung,P. (1998) Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem., 273, 21447-21450.
30. Williams,R.S., Moncalian,G., Williams,J.S., Yamada,Y., Limbo,O., Shin,D.S., Groocock,L.N., Cahill,D., Hitomi,C., Guenther,G. et al. (2008) Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell, 135, 97-109.
31. Buis,J., Wu,Y., Deng,Y., Leddon,J., Westfield,G., Eckersdorff,M., Sekiguchi,J.M., Chang,S. and Ferguson,D.O. (2008) Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell, 135, 85-96.
32. Hopkins,B.B. and Paull,T.T. (2008) The P. furiosus Mre11/Rad50 complex promotes 5′ strand resection at a DNA double-strand break. Cell, 135, 250-260.
33. Zhu,Z., Chung,W., Shim,E.Y., Lee,S.E. and Ira,G. (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell, 134, 981-994.
34. Mimitou,E.P. and Symington,L.S. (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature, 455, 770-774.
35. Lee,J.H., Ghirlando,R., Bhaskara,V., Hoffmeyer,M.R., Gu,J. and Paull,T.T. (2003) Regulation of Mre11/Rad50 by Nbs1. J. Biol. Chem. 278, 45171-45181.
36. Assenmacher,N. and Hopfner,K.P. (2004) MRE11/RAD50/NBS1: Complex activities. Chromosoma, 113, 157-166.
37. Van den Bosch,M., Bree,R.T. and Lowndes,N.F. (2003) The MRN complex: coordinating and mediating the response to broken chromosomes. EMBO Rep., 4, 844-849.
38. You,Z., Chahwan,C., Bailis,J., Hunter,T. and Russell,P. (2005) ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol., 25, 5363-5379.
39. Lee,J.L. and Paull,T.T. (2004) Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science, 304, 93-96.
40. Lee,J.H. and Paull,T.T. (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science, 308, 551-554.
41. Berkovich,E., Monnat,R.J. Jr. and Kastan,M.B. (2007) Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol., 9, 683-690.
42. Stracker,T.H., Morales,M., Couto,S.S., Hussein,H. and Petrini,J.H.J. (2007) The carboxy terminus of NBS1 is required for induction of apoptosis by the MRE11 complex. Nature, 447, 218-221.
43. Matsuoka,S., Ballif,B.A., Smogorzewska,A., McDonald,E.R. III, Hurov,K.E., Corey,J.L., Bakalarski,C.E., Zhao,Z., Solimini,N., Lerenthal,Y. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to the DNA damage. Science, 316, 1160-1166.
44. Wyman,C. and Kanaar,R. (2002) Chromosome orginization: Reaching out to embrace new models. Curr. Biol., 12, R446-R448.
45. Moreno-Herrero,F., de Jager,M., Dekker,N.H., Kanaar,R., Wyman,C. and Dekker,C. (2005). Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature, 437, 440-443.
46. Williams,R.S., Williams,J.S. and Tainer,J.A. (2007) Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem. Cell. Biol., 85 509-520.
47. Raymond,W.E. and Kleckner,N. (1993) RAD50 protein of S. cerevisiae exhibits ATP-dependent DNA binding. Nucleic Acids Res., 21, 3851-3856.
48. Lee,J.H. and Paull,T.T. (2006) Purification and biochemical characterization of ataxia-telangiectasia mutated and Mre11/Rad5/Nbs1. Methods Enzymol., 408, 529-539.
49. Bradford,M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principles of protein-dye-binding. Anal. Biochem., 72, 248-254.
50. Wyman,C., Rombel,I., North,A.K., Bustamente,C. and Kustu,S. (1997) Unusual oligomerization required for activity of NtrC, a bacterial enhancer-binding protein. Science, 275, 1658-1661.
51. Verhoeven,E.E.A., Wyman,C., Moolenaar,G.F. and Goosen,N. (2002) The presence of two UvrB subunits in the UvrAB complex ensures damage detection in both DNA strands. EMBO J., 21, 4196-4205.
52. Zhu,X.-D., Küster,B., Mann,M., Petrini,J.H.J. and de Lange,T. (2000) Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet., 25, 347-352.