Crystal structure of the DdrB/ssDNA complex from Deinococcus radiodurans reveals a DNA binding surface involving higher-order oligomeric states

Nucleic Acids Research

Volumn 41, Issue 21, 2013, Pages 9934-9944

  Sugiman Marangos, Seiji N ^a   Peel, John K ^a   Weiss, Yoni M ^a   Ghirlando, Rodolfo ^b   Junop, Murray S ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; DDRB PROTEIN; MUTANT PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DEINOCOCCUS RADIODURANS; DNA REPAIR; DNA SYNTHESIS; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION; SURFACE PROPERTY;

BACTERIAL PROTEINS; BINDING SITES; DEINOCOCCUS; DNA REPAIR; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY;

EID: 84890053138     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt759     Document Type: Article

References (32)

1. Daly, M.J., Gaidamakova, E.K., Matrosova, V.Y., Vasilenko, A., Zhai, M., Venkateswaran, A., Hess, M., Omelchenko, M.V., Kostandarithes, H.M., Makarova, K.S. et al. (2004) Accumulation of mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science, 306, 1025-1028.
2. Zahradka, K., Slade, D., Bailone, A., Sommer, S., Averbeck, D., Petranovic, M., Lindner, A.B. and Radman, M. (2006) Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature, 443, 569-573.
3. Daly, M.J., Gaidamakova, E.K., Matrosova, V.Y., Vasilenko, A., Zhai, M., Leapman, R.D., Lai, B., Ravel, B., Li, S.M., Kemner, K.M. et al. (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol., 5, e92.
4. Tanaka, M., Earl, A.M., Howell, H.A., Park, M.J., Eisen, J.A., Peterson, S.N. and Battista, J.R. (2004) Analysis of Deinococcus radiodurans's transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance. Genetics, 168, 21-33.
5. Makarova, K.S., Omelchenko, M.V., Gaidamakova, E.K., Matrosova, V.Y., Vasilenko, A., Zhai, M., Lapidus, A., Copeland, A., Kim, E., Land, M. et al. (2007) Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS One, 2, e955.
6. Slade, D., Lindner, A.B., Paul, G. and Radman, M. (2009) Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell, 136, 1044-1055.
7. Liu, Y., Zhou, J., Omelchenko, M.V., Beliaev, A.S., Venkateswaran, A., Stair, J., Wu, L., Thompson, D.K., Xu, D., Rogozin, I.B. et al. (2003) Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl Acad. Sci. USA, 100, 4191-4196.
8. Basu, B. and Apte, S.K. (2012) Gamma radiation-induced proteome of Deinococcus radiodurans primarily targets DNA repair and oxidative stress alleviation. Mol. Cell. Proteomics, 11, M111.011734.
9. Bouthier de la Tour, C., Boisnard, S., Norais, C., Toueille, M., Bentchikou, E., Vannier, F., Cox, M.M., Sommer, S. and Servant, P. (2011) The deinococcal DdrB protein is involved in an early step of DNA double strand break repair and in plasmid transformation through its single-strand annealing activity. DNA Repair (Amst.), 10, 1223-1231.
10. Norais, C.A., Chitteni-Pattu, S., Wood, E.A., Inman, R.B. and Cox, M.M. (2009) DdrB protein, an alternative Deinococcus radiodurans SSB induced by ionizing radiation. J. Biol. Chem., 284, 21402-21411.
11. Sugiman-Marangos, S. and Junop, M.S. (2010) The structure of DdrB from Deinococcus: a new fold for single-stranded DNA binding proteins. Nucleic Acids Res., 38, 3432-3440.
12. Xu, G., Lu, H., Wang, L., Chen, H., Xu, Z., Hu, Y., Tian, B. and Hua, Y. (2010) DdrB stimulates single-stranded DNA annealing and facilitates RecA-independent DNA repair in Deinococcus radiodurans. DNA Repair (Amst.), 9, 805-812.
13. Jiao, J., Wang, L., Xia, W., Li, M., Sun, H., Xu, G., Tian, B. and Hua, Y. (2012) Function and biochemical characterization of RecJ in Deinococcus radiodurans. DNA Repair (Amst.), 11, 349-356.
14. Sugiman-Marangos, S. and Junop, M. (2012) Crystallization of the DdrB-DNA complex from Deinococcus radiodurans. Acta Crystallogr. F Struct. Biol. Cryst. Commun., 68, 1534-1537.
15. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. In: Carter, C.W.J. and Sweet, R.M. (eds), Methods in Enzymology: Macromolecular Crystallography, Part A, Vol. 276. Academic Press, New York, pp. 307-326.
16. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive pythonbased system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
17. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
18. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol., 372, 774-797.
19. Luscombe, N.M., Laskowski, R.A. and Thornton, J.M. (1997) NUCPLOT: a program to generate schematic diagrams of proteinnucleic acid interactions. Nucleic Acids Res., 25, 4940-4945.
20. Durrant, J.D. and McCammon, J.A. (2011) BINANA: a novel algorithm for ligand-binding characterization. J. Mol. Graph. Model., 29, 888-893.
21. Morris, G.M., Huey, R., Lindstrom, W., Sanner, M.F., Belew, R.K., Goodsell, D.S. and Olson, A.J. (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem., 30, 2785-2791.
22. Zhao, H. and Shuck, P. (2012) Global multi-method analysis of affinities and cooperativity in complex systems of macromolecular interactions. Anal. Chem., 84, 9513-9519.
23. Zhao, H., Ghirlando, R., Piszczek, G., Curth, U., Brautigam, C.A. and Schuck, P. (2013) Recorded scan times can limit the accuracy of sedimentation coefficients in analytical ultracentrifugation. Anal. Biochem., 437, 104-108.
24. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J., 78, 1606-1619.
25. Laue, T.M., Shah, B.D., Ridgeway, T.M. and Pelletier, S.L. (1992) Computer-aided interpretation of analytical sedimentation data for proteins. In: Harding, S. and Rowe, A. (eds), Analytical Ultracentrifugation in Biochemistry and Polymer Science. Royal Society of Chemistry, Cambridge, pp. 90-125.
26. Cole, J.L., Lary, J.W., P Moody, T. and Laue, T.M. (2008) Analytical ultracentrifugation: sedimentation velocity and sedimentation equilibrium. Methods Cell Biol., 84, 143-179.
27. Schuck, P. (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem., 320, 104-124.
28. Singleton, M.R., Wentzell, L.M., Liu, Y., West, S.C. and Wigley, D.B. (2002) Structure of the single-strand annealing domain of human RAD52 protein. Proc. Natl Acad. Sci. USA, 99, 13492-13497.
29. Kagawa, W., Kurumizaka, H., Ishitani, R., Fukai, S., Nureki, O., Shibata, T. and Yokoyama, S. (2002) Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol. Cell, 10, 359-371.
30. Roberts, V.A., Pique, M.E., Hsu, S., Li, S., Siupphaug, G., Rambo, R.P., Jamison, J.W., Liu, T., Lee, J.H., Tainer, J.A. et al. (2012) Combining H/D exchange mass spectroscopy and computational docking reveals extended DNA-binding surface on uracil-DNA glycosylase. Nucleic Acids Res., 40, 6070-6081.
31. Tolun, G., Makhov, A.M., Ludtke, S.J. and Griffith, J.D. (2013) Details of ssDNA annealing revealed by an HSV-1 ICP8-ssDNA binary complex. Nucleic Acids Res., 41, 5927-5937.
32. Gutsche, I., Vujicic-Zagar, A., Siebert, X., Servant, P., Vannier, F., Castaing, B., Gallet, B., Heulin, T., de Groot, A., Sommer, S. et al. (2008) Complex oligomeric structure of a truncated form of DdrA: a protein required for the extreme radiotolerance of Deinococcus. Biochim. Biophys. Acta, 1784, 1050-1058.