Structure and cellular dynamics of deinococcus radiodurans single-stranded DNA (ssDNA)-binding protein (SSB)-DNA complexes

Journal of Biological Chemistry

Volumn 287, Issue 26, 2012, Pages 22123-22132

  George, Nicholas P ^a   Ngo, Khanh V ^b   Chitteni Pattu, Sindhu ^b   Norais, Cédric A ^b,d   Battista, John R ^c   Cox, Michael M ^b   Keck, James L ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c LOUISIANA STATE UNIVERSITY   (United States)

^d LABORATOIRE DE BIOCHIMIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEINS; BIOLOGICAL FUNCTIONS; CELLULAR DYNAMICS; DEINOCOCCUS RADIODURANS; DNA BINDING; DNA COMPLEX; DNA REPAIR; HOMODIMERS; HOMOTETRAMERS; IN-VIVO; POSTIRRADIATION; RADIATION RESISTANCE; RADIATION-RESISTANT BACTERIUM; SINGLE-STRANDED DNA (SS-DNA); TIME-DEPENDENT; X RAY CRYSTAL STRUCTURES;

BINDING ENERGY; COMPLEXATION; DYNAMICS; ELECTRON MICROSCOPY; ESCHERICHIA COLI; IONIZING RADIATION; IRRADIATION; OLIGONUCLEOTIDES;

DNA;

SINGLE STRANDED DNA; SINGLE STRANDED DNA BINDING PROTEIN;

ARTICLE; BACTERIAL GENOME; CELL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; DEINOCOCCUS RADIODURANS; DNA DAMAGE; DNA REPAIR; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ESCHERICHIA COLI; IN VIVO STUDY; IONIZING RADIATION; MOLECULAR DYNAMICS; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE;

CRYSTALLOGRAPHY, X-RAY; DEINOCOCCUS; DNA DAMAGE; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI; KINETICS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; OLIGONUCLEOTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RADIATION, IONIZING; RECOMBINATION, GENETIC; SALTS;

EID: 84862702956     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.367573     Document Type: Article

References (49)

1. Bauermeister, A., Moeller, R., Reitz, G., Sommer, S., and Rettberg, P. (2011) Effect of relative humidity on Deinococcus radiodurans' resistance to prolonged desiccation, heat, ionizing, germicidal, and environmentally relevant UV radiation. Microb. Ecol. 61, 715-722
2. Moseley, B. E., and Mattingly, A. (1971) Repair of irradiation transforming deoxyribonucleic acid in wild type and a radiation-sensitive mutant of Micrococcus radiodurans. J. Bacteriol. 105, 976-983
3. Kitayama, S. (1982) Adaptive repair of cross-links in DNA of Micrococcus radiodurans. Biochim. Biophys. Acta 697, 381-384
4. Blasius, M., Sommer, S., and Hübscher, U. (2008) Deinococcus radiodurans. What belongs to the survival kit? Crit. Rev. Biochem. Mol. Biol. 43, 221-238
5. Mattimore, V., and Battista, J. R. (1996) Radioresistance of Deinococcus radiodurans. Functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J. Bacteriol. 178, 633-637
6. Battista, J. R. (1997) Against all odds. The survival strategies of Deinococcus radiodurans. Annu. Rev. Microbiol. 51, 203-224
7. 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
8. White, O., Eisen, J. A., Heidelberg, J. F., Hickey, E. K., Peterson, J. D., Dodson, R. J., Haft, D. H., Gwinn, M. L., Nelson, W. C., Richardson, D. L., Moffat, K. S., Qin, H., Jiang, L., Pamphile, W., Crosby, M., Shen, M., Vamathevan, J. J., Lam, P., McDonald, L., Utterback, T., Zalewski, C., Makarova, K. S., Aravind, L., Daly, M. J., Minton, K. W., Fleischmann, R. D., Ketchum, K. A., Nelson, K. E., Salzberg, S., Smith, H. O., Venter, J. C., and Fraser, C. M. (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286, 1571-1577
9. Makarova, K. S., Aravind, L., Wolf, Y. I., Tatusov, R. L., Minton, K. W., Koonin, E. V., and Daly, M. J. (2001) Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol. Mol. Biol. Rev. 65, 44-79
10. Cox, M. M., and Battista, J. R. (2005) Deinococcus radiodurans. the consummate survivor. Nat. Rev. Microbiol. 3, 882-892
11. Slade, D., and Radman, M. (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol. Mol. Biol. Rev. 75, 133-191
12. Daly, M. J., and Minton, K. W. (1996) An alternative pathway of recombination of chromosomal fragments precedes recA-dependent recombination in the radioresistant bacterium Deinococcus radiodurans. J. Bacteriol. 178, 4461-4471
13. 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
14. Eggington, J. M., Haruta, N., Wood, E. A., and Cox, M. M. (2004) The single-stranded DNA-binding protein of Deinococcus radiodurans. BMC Microbiol. 4, 2
15. Bernstein, D. A., Eggington, J. M., Killoran, M. P., Misic, A. M., Cox, M. M., and Keck, J. L. (2004) Crystal structure of the Deinococcus radiodurans single-stranded DNA-binding protein suggests a mechanism for coping with DNA damage. Proc. Natl. Acad. Sci. U.S.A. 101, 8575-8580
16. Dabrowski, S., Olszewski, M., Piatek, R., Brillowska-Dabrowska, A., Konopa, G., and Kur, J. (2002) Identification and characterization of single- stranded DNA-binding proteins from Thermus thermophilus and Thermus aquaticus. New arrangement of binding domains. Microbiology 148, 3307-3315
17. Fedorov, R., Witte, G., Urbanke, C., Manstein, D. J., and Curth, U. (2006) 3D structure of Thermus aquaticus single-stranded DNA-binding protein gives insight into the functioning of SSB proteins. Nucleic Acids Res. 34, 6708-6717
18. Jedrzejczak, R., Dauter, M., Dauter, Z., Olszewski, M., Długołecka, A., and Kur, J. (2006) Structure of the single-stranded DNA-binding protein SSB from Thermus aquaticus. Acta Crystallogr. D Biol. Crystallogr. 62, 1407-1412
19. Raghunathan, S., Kozlov, A. G., Lohman, T. M., and Waksman, G. (2000) Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat. Struct. Biol. 7, 648-652
20. Chan, K. W., Lee, Y. J., Wang, C. H., Huang, H., and Sun, Y. J. (2009) Single-stranded DNA-binding protein complex from Helicobacter pylori suggests an ssDNA-binding surface. J. Mol. Biol. 388, 508-519
21. Yadav, T., Carrasco, B., Myers, A. R., George, N. P., Keck, J. L., and Alonso, J. C. (2012) Genetic recombination in Bacillus subtilis. A division of labor between two single-strand DNA-binding proteins. Nucleic Acids Res., in press
22. Matsumoto, T., Morimoto, Y., Shibata, N., Kinebuchi, T., Shimamoto, N., Tsukihara, T., and Yasuoka, N. (2000) Roles of functional loops and the C-terminal segment of a single-stranded DNA-binding protein elucidated by x-ray structure analysis. J. Biochem. 127, 329-335
23. Witte, G., Urbanke, C., and Curth, U. (2005) Single-stranded DNA-binding protein of Deinococcus radiodurans. A biophysical characterization. Nucleic Acids Res. 33, 1662-1670
24. Witte, G., Fedorov, R., and Curth, U. (2008) Biophysical analysis of Thermus aquaticus single-stranded DNA binding protein. Biophys. J. 94, 2269-2279
25. Kozlov, A. G., Eggington, J. M., Cox, M. M., and Lohman, T. M. (2010) Binding of the dimeric Deinococcus radiodurans single-stranded DNA-binding protein to single-stranded DNA. Biochemistry 49, 8266-8275
26. Dabrowski, S., Olszewski, M., Piatek, R., and Kur, J. (2002) Novel thermostable ssDNA-binding proteins from Thermus thermophilus and T. aquaticus expression and purification. Protein Expr. Purif. 26, 131-138
27. Griffith, J. D., Harris, L. D., and Register, J., 3rd (1984) Visualization of SSB-ssDNA complexes active in the assembly of stable RecA-DNA filaments. Cold Spring Harb. Symp. Quant. Biol. 49, 553-559
28. Bujalowski, W., and Lohman, T. M. (1986) Escherichia coli single-strand binding protein forms multiple, distinct complexes with single-stranded DNA. Biochemistry 25, 7799-7802
29. Lohman, T. M., Overman, L. B., and Datta, S. (1986) Salt-dependent changes in the DNA binding co-operativity of Escherichia coli single strand binding protein. J. Mol. Biol. 187, 603-615
30. Chrysogelos, S., and Griffith, J. (1982) Escherichia coli single-strand binding protein organizes single-stranded DNA in nucleosome-like units. Proc. Natl. Acad. Sci. U.S.A. 79, 5803-5807
31. Lohman, T. M., Green, J. M., and Beyer, R. S. (1986) Large-scale overproduction and rapid purification of the Escherichia coli ssb gene product. Expression of the ssb gene under λ PL control. Biochemistry 25, 21-25
32. Shereda, R. D., Kozlov, A. G., Lohman, T. M., Cox, M. M., and Keck, J. L. (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol. 43, 289-318
33. Haruta, N., Yu, X., Yang, S., Egelman, E. H., and Cox, M. M. (2003) A DNA pairing-enhanced conformation of bacterial RecA proteins. J. Biol. Chem. 278, 52710-52723
34. Neuendorf, S. K., and Cox, M. M. (1986) Exchange of recA protein between adjacent recA protein-single-stranded DNA complexes. J. Biol. Chem. 261, 8276-8282
35. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
36. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
37. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
38. Dodson, E. J., Winn, M., and Ralph, A. (1997) Collaborative Computational Project, number 4. Providing programs for protein crystallography. Methods Enzymol. 277, 620-633
39. Grassucci, R. A., Taylor, D. J., and Frank, J. (2007) Preparation of macromolecular complexes for cryo-electron microscopy. Nat. Protoc. 2, 3239-3246
40. Nguyen, H. H., de la Tour, C. B., Toueille, M., Vannier, F., Sommer, S., and Servant, P. (2009) The essential histone-like protein HU plays a major role in Deinococcus radiodurans nucleoid compaction. Mol. Microbiol. 73, 240-252
41. Curth, U., Greipel, J., Urbanke, C., and Maass, G. (1993) Multiple binding modes of the single-stranded DNA binding protein from Escherichia coli as detected by tryptophan fluorescence and site-directed mutagenesis. Biochemistry 32, 2585-2591
42. 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
43. Ujaoney, A. K., Potnis, A. A., Kane, P., Mukhopadhyaya, R., and Apte, S. K. (2010) Radiation desiccation response motif-like sequences are involved in transcriptional activation of the Deinococcal ssb gene by ionizing radiation but not by desiccation. J. Bacteriol. 192, 5637-5644
44. Levin-Zaidman, S., Englander, J., Shimoni, E., Sharma, A. K., Minton, K. W., and Minsky, A. (2003) Ringlike structure of the Deinococcus radiodurans genome. A key to radioresistance? Science 299, 254-256
45. Reyes-Lamothe, R., Sherratt, D. J., and Leake, M. C. (2010) Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328, 498-501
46. Slade, D., Lindner, A. B., Paul, G., and Radman, M. (2009) Recombination and replication in DNA repair of heavily irradiated Deinococcus radio-durans. Cell 136, 1044-1055
47. 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 10, 1223-1231
48. 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
49. 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