Disruption of the bacteriophage T4 Mre11 dimer interface reveals a two-state mechanism for exonuclease activity

Journal of Biological Chemistry

Volumn 287, Issue 37, 2012, Pages 31371-31381

  Albrecht, Dustin W ^a   Herdendorf, Timothy J ^a   Nelson, Scott W ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC COMMUNICATION; ATP HYDROLYSIS; ATP-HYDROLYSIS ACTIVITY; BACTERIOPHAGE T4; DIMER DISRUPTION; DIMER INTERFACE; DNA REPAIR; DOUBLE STRAND BREAKS; EXONUCLEASE; EXONUCLEASE ACTIVITY; NUCLEASE ACTIVITY; RATE DETERMINING STEP; STEADY STATE; STEADY-STATE CONDITION; TWO-STATE; WILD TYPES; WILD-TYPE ENZYMES;

DIMERS; HYDROLYSIS;

INTERFACE STATES;

DOUBLE STRANDED DNA; EXONUCLEASE; NUCLEASE; RAD50 PROTEIN;

ALLOSTERISM; ARTICLE; BACTERIOPHAGE T4; BACTERIOPHAGE T4 MRE11; BINDING AFFINITY; CATALYSIS; CELL COMMUNICATION; CELL CYCLE; CELL DISRUPTION; CELL FUNCTION; CELL INTERACTION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME SYNTHESIS; GENE MUTATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; STEADY STATE;

ALLOSTERIC REGULATION; BACTERIOPHAGE T4; DNA, VIRAL; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; PROTEIN MULTIMERIZATION; VIRAL PROTEINS;

EID: 84866066311     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.392316     Document Type: Article

References (40)

1. Povirk, L. F. (2006) Biochemical mechanisms of chromosomal translocations resulting from DNA double strand breaks. DNA Repair 5, 1199-1212
2. Bassing, C. H., and Alt, F. W. (2004) The cellular response to general and programmed DNA double strand breaks. DNA Repair 3, 781-796
3. McVey, M., and Lee, S. E. (2008) MMEJ repair of double strand breaks (director's cut). Deleted sequences and alternative endings. Trends Genet. 24, 529-538
4. Connelly, J. C., and Leach, D. R. (2002) Tethering on the brink. The evolutionarily conserved Mre11-Rad50 complex. Trends Biochem. Sci. 27, 410-418
5. San Filippo, J., Sung, P., and Klein, H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257
6. Mimitou, E. P., and Symington, L. S. (2008) Sae2, Exo1, and Sgs1 collaborate in DNA double strand break processing. Nature 455, 770-774
7. Cejka, P., Cannavo, E., Polaczek, P., Masuda-Sasa, T., Pokharel, S., Campbell, J. L., and Kowalczykowski, S. C. (2010) DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467, 112-116
8. 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
9. Symington, L. S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double strand break repair. Microbiol. Mol. Biol. Rev. 66, 630-670
10. Krogh, B. O., and Symington, L. S. (2004) Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271
11. Dillingham, M. S., and Kowalczykowski, S. C. (2008) RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 72, 642-671
12. Kreuzer, K. N., Yap, W. Y., Menkens, A. E., and Engman, H. W. (1988) Recombination-dependent replication of plasmids during bacteriophage T4 infection. J. Biol. Chem. 263, 11366-11373
13. Mosig, G. (1998) Recombination and recombination-dependent DNA replication in bacteriophage T4. Annu. Rev. Genet. 32, 379-413
14. Nossal, N. G. (1992) Protein-protein interactions at a DNA replication fork. Bacteriophage T4 as a model. FASEB J. 6, 871-878
15. Hopfner, K. (2003) Rad50/SMC proteins and ABC transporters. Unifying concepts from high resolution structures. Curr. Opin. Struct. Biol. 13, 249-255
16. Jones, P. M., O'Mara, M.L., and George, A.M.(2009) ABC transporters. A riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci. 34, 520-531
17. Davidson, A. L., Dassa, E., Orelle, C., and Chen, J. (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364
18. 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
19. 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 inDNAdouble strand break repair and the ABC-ATPase superfamily. Cell 101, 789-800
20. Barford, D., Das, A. K., and Egloff, M. P. (1998) The structure and mechanism of protein phosphatases. Insights into catalysis and regulation. Annu. Rev. Biophys. Biomol. Struct. 27, 133-164
21. Bressan, D. A., Baxter, B. K., and Petrini, J. H. (1999) The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 7681-7687
22. 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
23. Taylor, A. M., Groom, A., and Byrd, P. J. (2004) Ataxia telangiectasia-like disorder (ATLD). Its clinical presentation and molecular basis. DNA Repair 3, 1219-1225
24. Wyman, C., Lebbink, J., and Kanaar, R. (2011) Mre11-Rad50 complex crystals suggest molecular calisthenics. DNA Repair 10, 1066-1070
25. Möckel, C., Lammens, K., Schele, A., and Hopfner, K. P. (2012) ATP-driven structural changes of the bacterial Mre11-Rad50 catalytic head complex. Nucleic Acids Res. 40, 914-927
26. Williams, G. J., Williams, R. S., Williams, J. S., Moncalian, G., Arvai, A. S., Limbo, O., Guenther, G., SilDas, S., Hammel, M., Russell, P., and Tainer, J. A. (2011) ABC ATPase signature helices in Rad50 link nucleotide state to Mre11 interface for DNA repair. Nat. Struct. Mol. Biol. 18, 423-431
27. Lammens, K., Bemeleit, D. J., Möckel, C., Clausing, E., Schele, A., Hartung, S., Schiller, C. B., Lucas, M., Angermüller, C., Söding, J., Strässer, K., and Hopfner, K. P. (2011) The Mre11:Rad50 structure shows an ATP-dependent molecular clamp in DNA double strand break repair. Cell 145, 54-66
28. Lim, H. S., Kim, J. S., Park, Y. B., Gwon, G. H., and Cho, Y. (2011) Crystal structure of the Mre11-Rad50-ATPγS complex. Understanding the interplay between Mre11 and Rad50. Genes Dev. 25, 1091-1104
29. 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., Carney, J. P., Petrini, J. H., and Tainer, J. A. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418, 562-566
30. 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
31. Herdendorf, T. J., and Nelson, S. W. (2011) Functional evaluation of bacteriophage T4 Rad50 signature motif residues. Biochemistry 50, 6030-6040
32. Gilbert, S. P., and Mackey, A. T. (2000) Kinetics. A tool to study molecular motors. Methods 22, 337-354
33. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace. A web-based environment for protein structure homology modeling. Bioinformatics 22, 195-201
34. Williams, R. S., Moncalian, G., Williams, J. S., Yamada, Y., Limbo, O., Shin, D. S., Groocock, L. M., Cahill, D., Hitomi, C., Guenther, G., Moiani, D., Carney, J. P., Russell, P., and Tainer, J. A. (2008) Mre11 dimers coordinate DNA end bridging and nuclease processing in double strand-break repair. Cell 135, 97-109
35. Schiller, C. B., Lammens, K., Guerini, I., Coordes, B., Feldmann, H., Schlauderer, F., Möckel, C., Schele, A., Strässer, K., Jackson, S. P., and Hopfner, K. P. (2012) Structure of Mre11-Nbs1 complex yields insights into ataxia telangiectasia-like disease mutations and DNA damage signaling. Nat. Struct. Mol. Biol. 19, 693-700
36. Park, Y. B., Chae, J., Kim, Y. C., and Cho, Y. (2011) Crystal structure of human Mre11. Understanding tumorigenic mutations. Structure 19, 1591-1602
37. Das, D., Moiani, D., Axelrod, H. L., Miller, M. D., McMullan, D., Jin, K. K., Abdubek, P., Astakhova, T., Burra, P., Carlton, D., Chiu, H. J., Clayton, T., Deller, M. C., Duan, L., Ernst, D., Feuerhelm, J., Grant, J. C., Grzechnik, A., Grzechnik, S. K., Han, G. W., Jaroszewski, L., Klock, H. E., Knuth, M. W., Kozbial, P., Krishna, S. S., Kumar, A., Marciano, D., Morse, A. T., Nigoghossian, E., Okach, L., Paulsen, J., Reyes, R., Rife, C. L., Sefcovic, N., Tien, H. J., Trame, C. B., van den Bedem, H., Weekes, D., Xu, Q., Hodgson, K. O., Wooley, J., Elsliger, M. A., Deacon, A. M., Godzik, A., Lesley, S. A., Tainer, J. A., and Wilson, I. A. (2010) Crystal structure of the first eubacterial Mre11 nuclease reveals novel features that may discriminate substrates during DNA repair. J. Mol. Biol. 397, 647-663
38. De la Rosa, M. B., and Nelson, S. W. (2011) An interaction between the Walker A and D-loop motifs is critical to ATP hydrolysis and cooperativity in bacteriophage T4 Rad50. J. Biol. Chem. 286, 26258-26266
39. Majka, J., Alford, B., Ausio, J., Finn, R. M., and McMurray, C. T. (2012) ATP hydrolysis by RAD50 protein switches MRE11 enzyme from endonuclease to exonuclease. J. Biol. Chem. 287, 2328-2341
40. Lohman, T. M., Tomko, E. J., and Wu, C. G. (2008) Nonhexameric DNA helicases and translocases. Mechanisms and regulation. Nat. Rev. Mol. Cell Biol. 9, 391-401