A novel mode of nuclease action is revealed by the bacterial Mre11/Rad50 complex

Nucleic Acids Research

Volumn 43, Issue 20, 2015, Pages 9804-9816

  Lim, Chew Theng ^a   Lai, Pey Jiun ^a   Leach, David R F ^b   Maki, Hisaji ^a   Furukohri, Asako ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; MRE11 PROTEIN; NUCLEASE; PHOSPHODIESTERASE I; RAD50 PROTEIN; SPLEEN EXONUCLEASE; CRUCIFORM DNA; DEOXYRIBONUCLEASE; ESCHERICHIA COLI PROTEIN; EXONUCLEASE; SBCC PROTEIN, E COLI; SBCD PROTEIN, E COLI;

ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; DNA HAIRPIN; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; CHEMISTRY; METABOLISM;

DEOXYRIBONUCLEASES; DNA; DNA CLEAVAGE; DNA, CRUCIFORM; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI PROTEINS; EXONUCLEASES;

EID: 84950161308     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv855     Document Type: Article

References (34)

1. 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 (Amst), 9, 1299-1306.
2. Stracker, T. H. and Petrini, J. H. (2011) The MRE11 complex: starting from the ends. Nat. Rev. Mol. Cell Biol. , 12, 90-103.
3. Paull, T. T. (2010) Making the best of the loose ends: Mre11/Rad50 complexes and Sae2 promote DNA double-strand break resection. DNA Repair (Amst), 9, 1283-1291.
4. 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.
5. 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.
6. Connelly, J. C. and Leach, D. R. (1996) The sbcC and sbcD genes of Escherichia coli encode a nuclease involved in palindrome inviability and genetic recombination. Genes Cells, 1, 285-291.
7. Connelly, J. C. , de Leau, E. S. , Okely, E. A. and Leach, D. R. (1997) Overexpression, purification, and characterization of the SbcCD protein from Escherichia coli. J. Biol. Chem. , 272, 19819-19826.
8. Connelly, J. C. , Kirkham, L. A. and Leach, D. R. (1998) The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc. Natl. Acad. Sci. U. S. A. , 95, 7969-7974.
9. Kamble, V. A. and Misra, H. S. (2010) The SbcCD complex of Deinococcus radiodurans contributes to radioresistance and DNA strand break repair in vivo and exhibits Mre11-Rad50 type activity in vitro. DNA Repair (Amst), 9, 488-494.
10. Hopfner, K. P. , Karcher, A. , Shin, D. , 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.
11. 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.
12. 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.
13. Cannavo, E. and Cejka, P. (2014) Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature, 514, 122-125.
14. Leach, D. R. , Okely, E. A. and Pinder, D. J. (1997) Repair by recombination of DNA containing a palindromic sequence. Mol. Microbiol. , 26, 597-606.
15. Eykelenboom, J. K. , Blackwood, J. K. , Okely, E. and Leach, D. R. (2008) SbcCD causes a double-strand break at a DNA palindrome in the Escherichia coli chromosome. Mol. Cell, 29, 644-651.
16. Leach, D. R. (1994) Long DNA palindromes, cruciform structures, genetic instability and secondary structure repair. Bioessays, 16, 893-900.
17. Chalker, A. F. , Leach, D. R. and Lloyd, R. G. (1988) Escherichia coli sbcC mutants permit stable propagation of DNA replicons containing a long palindrome. Gene, 71, 201-205.
18. Bikard, D. , Loot, C. , Baharoglu, Z. and Mazel, D. (2010) Folded DNA in action: Hairpin formation and biological functions in prokaryotes. Microbiol. Mol. Biol. Rev. , 74, 570-588.
19. Farah, J. A. , Cromie, G. , Steiner, W. W. and Smith, G. R. (2005) A novel recombination pathway initiated by theMre11/Rad50/Nbs1 complex eliminates palindromes during meiosis in Schizosaccharomyces pombe. Genetics, 169, 1261-1274.
20. Darmon, E. , Eykelenboom, J. K. , Lincker, F. , Jones, L. H. , White, M. , Okely, E. , Blackwood, J. K. and Leach, D. R. (2010) E. coli SbcCD and RecA control chromosomal rearrangement induced by an interrupted palindrome. Mol. Cell, 39, 59-70.
21. Inagaki, H. , Ohye, T. , Kogo, H. , Tsutsumi, M. , Kato, T. , Tong, M. , Emanuel, B. S. and Kurahashi, H. (2013) Two sequential cleavage reactions on cruciform DNA structures cause palindrome-mediated chromosomal translocations. Nat. Commun. , 4, 1592.
22. Azeroglu, B. , Lincker, F. , White, M. A. , Jain, D. and Leach, D. R. (2014) A perfect palindrome in the Escherichia coli chromosome forms DNA hairpins on both leading- and lagging-strands. Nucleic Acids Res. , 42, 13206-13213.
23. Higuchi, K. , Katayama, T. , Iwai, S. , Hidaka, M. , Horiuchi, T. and Maki, H. (2003) Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro. Genes Cells, 8, 437-449.
24. Pinder, D. J. , Blake, C. E. , Lindsey, J. C. and Leach, D. R. (1998) Replication strand preference for deletions associated with DNA palindromes. Mol. Microbiol. , 28, 719-727.
25. Kurahashi, H. , Inagaki, H. , Yamada, K. , Ohye, T. , Taniguchi, M. , Emanuel, B. S. and Toda, T. (2004) Cruciform DNA structure underlies the etiology for palindrome-mediated human chromosomal translocations. J. Biol. Chem. , 279, 35377-35383.
26. Ausubel, F. M. , Brent, R. , Kingston, R. E. , Moore, D. D. and Seidman, J. G. (1994) Current Protocols in Molecular Biology. John Wiley & Sons, NY.
27. Mizuuchi, K. , Mizuuchi, M. and Gellert, M. (1982) Cruciform structures in palindromic DNA are favored by DNA supercoiling. J. Mol. Biol. , 156, 229-243.
28. Connelly, J. C. , de Leau, E. S. and Leach, D. R. (1999) DNA cleavage and degradation by the SbcCD protein complex from Escherichia coli. Nucleic Acids Res. , 27, 1039-1046.
29. Connelly, J. C. , de Leau, E. S. and Leach, D. R. (2003) Nucleolytic processing of a protein-bound DNA end by the E. coli SbcCD (MR) complex. DNA Repair (Amst), 2, 795-807.
30. Moreau, S. , Ferguson, J. R. and Symington, L. S. (1999) The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. , 19, 556-566.
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. Arthur, L. M. , Gustausson, K. , Hopfner, K. P. , Carson, C. T. , Stracker, T. H. , Karcher, A. , Felton, D. , Weitzman, M. D. , Tainer, J. and Carney, J. P. (2004) Structural and functional analysis of Mre11-3. Nucleic Acids Res. , 32, 1886-1893.
33. 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.
34. 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.