ATP driven structural changes of the bacterial Mre11:Rad50 catalytic head complex

Nucleic Acids Research

Volumn 40, Issue 2, 2012, Pages 914-927

  Möckel, Carolin ^a   Lammens, Katja ^a,b   Schele, Alexandra ^a   Hopfner, Karl Peter ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b Munich Center for Integrated Protein Science   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; MRE11 PROTEIN; RAD50 PROTEIN; SINGLE STRANDED DNA;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BINDING SITE; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIMERIZATION; DISULFIDE BOND; DNA PROTEIN COMPLEX; DNA REPAIR; DOUBLE STRANDED DNA BREAK; NONHUMAN; NUCLEOTIDE BINDING DOMAIN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; THERMOTOGA MARITIMA;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; DNA; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; THERMOTOGA MARITIMA;

BACTERIA (MICROORGANISMS); THERMOTOGA MARITIMA;

EID: 84855870632     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr749     Document Type: Article

References (55)

1. Ward, J. F. (1988) DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability. Progr. Nucleic Acid Res. Mol. Biol., 35, 95-125.
2. Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D. and Gautier, J. (2001) Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell, 8, 137-147.
3. Harper, J. W. and Elledge, S. J. (2007) The DNA damage response: ten years after. Mol. Cell, 28, 739-745.
4. Heyer, W. D., Ehmsen, K. T. and Liu, J. (2010) Regulation of homologous recombination in eukaryotes. Ann. Rev. Genet., 44, 113-139.
5. Mladenov, E. and Iliakis, G. (2011) Induction and repair of DNA double strand breaks: The increasing spectrum of non-homologous end joining pathways. Mutat. Res., 711, 61-72.
6. San Filippo, J., Sung, P. and Klein, H. (2008) Mechanism of eukaryotic homologous recombination. Ann. Rev. Biochem., 77, 229-257.
7. 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.= Biochimie et Biologie Cell., 85, 509-520.
8. Stracker, T. H. and Petrini, J. H. (2011) The MRE11 complex: starting from the ends. Nat. Rev. Mo., Cell. Biol., 12, 90-103.
9. Williams, G. J., Lees-Miller, S. P. and Tainer, J. A. (2010) Mre11-Rad50-Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair, 9, 1299-1306.
10. Lee, K., Zhang, Y. and Lee, S. E. (2008) Saccharomyces cerevisiae ATM orthologue suppresses break-induced chromosome translocations. Nature, 454, 543-546.
11. Putnam, C. D., Hayes, T. K. and Kolodner, R. D. (2009) Specific pathways prevent duplication-mediated genome rearrangements. Nature, 460, 984-989.
12. Wang, J. H., Gostissa, M., Yan, C. T., Goff, P., Hickernell, T., Hansen, E., Difilippantonio, S., Wesemann, D. R., Zarrin, A. A., Rajewsky, K. et al. (2009) Mechanisms promoting translocations in editing and switching peripheral B cells. Nature, 460, 231-236.
13. Waltes, R., Kalb, R., Gatei, M., Kijas, A. W., Stumm, M., Sobeck, A., Wieland, B., Varon, R., Lerenthal, Y., Lavin, M. F. et al. (2009) Human RAD50 deficiency in a Nijmegen breakage syndrome-like disorder. Am. J. Hum. Genet., 84, 605-616.
14. Carney, J. P., Maser, R. S., Olivares, H., Davis, E. M., Le Beau, M., Yates, J. R. 3rd, Hays, L., Morgan, W. F. and Petrini, J. H. (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.
15. 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. (1999) The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell, 99, 577-587.
16. Varon, R., Vissinga, C., Platzer, M., Cerosaletti, K. M., Chrzanowska, K. H., Saar, K., Beckmann, G., Seemanova, 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.
17. Petrini, J. H. (2000) The Mre11 complex and ATM: collaborating to navigate S phase. Curr. Opin. Cell Biol., 12, 293-296.
18. Zahradka, K., Buljubasic, M., Petranovic, M. and Zahradka, D. (2009) Roles of ExoI and SbcCD nucleases in 'reckless' DNA degradation in recA mutants of Escherichia coli. J. Bacteriol., 191, 1677-1687.
19. Cromie, G. A., Connelly, J. C. and Leach, D. R. (2001) Recombination at double-strand breaks and DNA ends: conserved mechanisms from phage to humans. Mol. Cell, 8, 1163-1174.
20. Darmon, E., Eykelenboom, J. K., Lincker, F., Jones, L. H., White, M., Okely, E., Blackwood, J. K. and Leach, D. R. E. (2010) coli SbcCD and RecA control chromosomal rearrangement induced by an interrupted palindrome. Mol. Cell, 39, 59-70.
21. Delmas, S., Shunburne, L., Ngo, H. P. and Allers, T. (2009) Mre11-Rad50 promotes rapid repair of DNA damage in the polyploid archaeon Haloferax volcanii by restraining homologous recombination. PLoS Genet., 5, e1000552.
22. Sharples, G. J. and Leach, D. R. (1995) Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol. Microbiol., 17, 1215-1217.
23. Falck, J., Coates, J. and Jackson, S. P. (2005) Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature, 434, 605-611.
24. 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.
25. 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.
26. de Jager, M., van Noort, J., van Gent, D. C., 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.
27. Anderson, D. E., Trujillo, K. M., Sung, P. and Erickson, H. P. (2001) Structure of the Rad50 x Mre11 DNA repair complex from Saccharomyces cerevisiae by electron microscopy. J. Biol. Chem., 276, 37027-37033.
28. 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. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature, 418, 562-566.
29. Wiltzius, J. J., Hohl, M., Fleming, J. C. and Petrini, J. H. (2005) The Rad50 hook domain is a critical determinant of Mre11 complex functions. Nat. Struct. Mol. Biol., 12, 403-407.
30. Paull, T. T. and Gellert, M. (1998) The 3' to 5' exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell, 1, 969-979.
31. Budd, M. E. and Campbell, J. L. (2009) Interplay of Mre11 nuclease with Dna2 plus Sgs1 in Rad51-dependent recombinational repair. PloS One, 4, e4267.
32. Zhu, Z., Chung, W. H., 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.
33. Mimitou, E. P. and Symington, L. S. (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature, 455, 770-774.
34. 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.
35. 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.
36. Raymond, W. E. and Kleckner, N. (1993) RAD50 protein of S.cerevisiae exhibits ATP-dependent DNA-binding. Nucleic Acids Res., 21, 3851-3856.
37. Lammens, K., Bemeleit, D. J., Mockel, C., Clausing, E., Schele, A., Hartung, S., Schiller, C. B., Lucas, M., Angermuller, C., Soding, J. et al. (2011) The Mre11:Rad50 structure shows an ATP-dependent molecular clamp in DNA double-strand break repair. Cell, 145, 54-66.
38. *Mre11 complex. J. Biol. Chem., 276, 35458-35464.
39. Herdendorf, T. J., Albrecht, D. W., Benkovic, S. J. and Nelson, S. W. (2011) Biochemical characterization of bacteriophage T4 Mre11-Rad50 complex. J. Biol. Chem., 286, 2382-2392.
40. 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.
41. Paull, T. T. and Lee, J. H. (2005) The Mre11/Rad50/Nbs1 complex and its role as a DNA double-strand break sensor for ATM. Cell Cycle, 4, 737-740.
42. Williams, G. J., Williams, R. S., Williams, J. S., Moncalian, G., Arvai, A. S., Limbo, O., Guenther, G., SilDas, S., Hammel, M., Russell, P. et al. (2011) ABC ATPase signature helices in Rad50 link nucleotide state to Mre11 interface for DNA repair. Nat. Struct. Mol. Biol., 18, 423-431.
43. Lim, H. S., Kim, J. S., Park, Y. B., Gwon, G. H. and Cho, Y. (2011) Crystal structure of the Mre11-Rad50-ATP{gamma}S complex: understanding the interplay between Mre11 and Rad50. Genes Dev., 25, 1091-1104.
44. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr., 26, 795-800.
45. McCoy, A. J. (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallographica, 63, 32-41.
46. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallographica, 60, 2126-2132.
47. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K. and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallographica, 58, 1948-1954.
48. Honegger, A., Spinelli, S., Cambillau, C. and Pluckthun, A. (2005) A mutation designed to alter crystal packing permits structural analysis of a tight-binding fluorescein-scFv complex. Protein Sci., 14, 2537-2549.
49. 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. (2008) Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell, 135, 97-109.
50. Bhaskara, V., Dupre, A., Lengsfeld, B., Hopkins, B. B., Chan, A., Lee, J. H., Zhang, X., Gautier, J., Zakian, V. and Paull, T. T. (2007) Rad50 adenylate kinase activity regulates DNA tethering by Mre11/Rad50 complexes. Mol. Cell, 25, 647-661.
51. Koroleva, O., Makharashvili, N., Courcelle, C. T., Courcelle, J. and Korolev, S. (2007) Structural conservation of RecF and Rad50: implications for DNA recognition and RecF function. EMBO J., 26, 867-877.
52. Usui, T., Ohta, T., Oshiumi, H., Tomizawa, J., Ogawa, H. and Ogawa, T. (1998) Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell, 95, 705-716.
53. de Jager, M., Trujillo, K. M., Sung, P., Hopfner, K. P., Carney, J. P., Tainer, J. A., Connelly, J. C., Leach, D. R., Kanaar, R. and Wyman, C. (2004) Differential arrangements of conserved building blocks among homologs of the Rad50/Mre11 DNA repair protein complex. J. Mol. Biol., 339, 937-949.
54. 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.
55. Baker, N. A. (2004) Poisson-Boltzmann methods for biomolecular electrostatics. Methods Enzymol., 383, 94-118.