Crystal structure of DnaT84-153-dT10 ssDNA complex reveals a novel single-stranded DNA binding mode

Nucleic Acids Research

Volumn 42, Issue 14, 2014, Pages 9470-9483

  Liu, Zheng ^a,b   Chen, Peng ^a,b   Wang, Xuejuan ^a,b   Cai, Gang ^a,b   Niu, Liwen ^a,b   Teng, Maikun ^a,b   Li, Xu ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA B; DNA C; GENOMIC DNA; HELICASE; NUCLEOPROTEIN; PRIMER RNA; RNA; SCAFFOLD PROTEIN; SINGLE STRANDED DNA; DNA BINDING PROTEIN; DNAT PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN;

AGAR GEL ELECTROPHORESIS; ARTICLE; BINDING ASSAY; CHEMICAL ANALYSIS; CHROMOSOME REPLICATION; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; DNA BINDING; DNA REPLICATION; ELECTRON MICROSCOPY; ESCHERICHIA COLI; FLUORESCENCE ANALYSIS; GEL PERMEATION CHROMATOGRAPHY; MOLECULAR CLONING; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; RNA SYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; NUCLEOPROTEINS; PROTEIN BINDING;

EID: 84906277074     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku633     Document Type: Article

References (47)

1. Mott, M.L. and Berger, J.M. (2007) DNA replication initiation: mechanisms and regulation in bacteria. Nat. Rev. Microbiol., 5, 343-354.
2. Arias-Palomo, E., O'Shea, V.L., Hood, I.V. and Berger, J.M. (2013) The bacterial DnaC helicase loader is a DnaB ring breaker. Cell, 153, 438-448.
3. Masai, H. and Arai, K. (1996) DnaA- and PriA-dependent primosomes: two distinct replication complexes for replication of Escherichia coli chromosome. Front Biosci., 1, d48-d58.
4. Allen, G.C. Jr and Kornberg, A. (1993) Assembly of the primosome of DNA replication in Escherichia coli. J. Biol. Chem., 268, 19204-19209.
5. Lopper, M., Boonsombat, R., Sandler, S.J. and Keck, J.L. (2007) A hand-off mechanism for primosome assembly in replication restart. Mol. Cell, 26, 781-793.
6. Heller, R.C. and Marians, K.J. (2006) Replication fork reactivation downstream of a blocked nascent leading strand. Nature, 439, 557-562.
7. Gabbai, C.B. and Marians, K.J. (2010) Recruitment to stalled replication forks of the PriA DNA helicase and replisome-loading activities is essential for survival. DNA Repair (Amst), 9, 202-209.
8. Heller, R.C. and Marians, K.J. (2005) The disposition of nascent strands at stalled replication forks dictates the pathway of replisome loading during restart. Mol. Cell, 17, 733-743.
9. Erzberger, J.P., Pirruccello, M.M. and Berger, J.M. (2002) The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J., 21, 4763-4773.
10. Liu, B., Eliason, W.K. and Steitz, T.A. (2013) Structure of a helicase-helicase loader complex reveals insights into the mechanism of bacterial primosome assembly. Nat. Commun., 4, 2495.
11. Makowska-Grzyska, M. and Kaguni, J.M. (2010) Primase directs the release of DnaC from DnaB. Mol. Cell, 37, 90-101.
12. Lo, Y.H., Tsai, K.L., Sun, Y.J., Chen, W.T., Huang, C.Y. and Hsiao, C.D. (2009) The crystal structure of a replicative hexameric helicase DnaC and its complex with single-stranded DNA. Nucleic Acids Res., 37, 804-814.
13. Naue, N., Beerbaum, M., Bogutzki, A., Schmieder, P. and Curth, U. (2013) The helicase-binding domain of Escherichia coli DnaG primase interacts with the highly conserved C-terminal region of single-stranded DNA-binding protein. Nucleic Acids Res., 41, 4507-4517.
14. Bailey, S., Eliason, W.K. and Steitz, T.A. (2007) Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase. Science, 318, 459-463.
15. Bhattacharyya, B., George, N.P., Thurmes, T.M., Zhou, R., Jani, N., Wessel, S.R., Sandler, S.J., Ha, T. and Keck, J.L. (2014) Structural mechanisms of PriA-mediated DNA replication restart. Proc. Natl. Acad. Sci. U.S.A., 111, 1373-1378.
16. Sasaki, K., Ose, T., Okamoto, N., Maenaka, K., Tanaka, T., Masai, H., Saito, M., Shirai, T. and Kohda, D. (2007) Structural basis of the 3′-end recognition of a leading strand in stalled replication forks by PriA. EMBO J., 26, 2584-2593.
17. Szymanski, M.R., Jezewska, M.J. and Bujalowski, W. (2011) Binding of two PriA-PriB complexes to the primosome assembly site initiates primosome formation. J. Mol. Biol., 411, 123-142.
18. Cadman, C.J., Lopper, M., Moon, P.B., Keck, J.L. and McGlynn, P. (2005) PriB stimulates PriA helicase via an interaction with single-stranded DNA. J. Biol. Chem., 280, 39693-39700.
19. Liu, J., Nurse, P. and Marians, K.J. (1996) The ordered assembly of the phiX174-type primosome. III. PriB facilitates complex formation between PriA and DnaT. J. Biol. Chem., 271, 15656-15661.
20. Dong, J., George, N.P., Duckett, K.L., DeBeer, M.A. and Lopper, M.E. (2010) The crystal structure of Neisseria gonorrhoeae PriB reveals mechanistic differences among bacterial DNA replication restart pathways. Nucleic Acids Res., 38, 499-509.
21. Huang, C.Y., Hsu, C.H., Sun, Y.J., Wu, H.N. and Hsiao, C.D. (2006) Complexed crystal structure of replication restart primosome protein PriB reveals a novel single-stranded DNA-binding mode. Nucleic Acids Res., 34, 3878-3886.
22. Lopper, M., Holton, J.M. and Keck, J.L. (2004) Crystal structure of PriB, a component of the Escherichia coli replication restart primosome. Structure, 12, 1967-1975.
23. Liu, J.H., Chang, T.W., Huang, C.Y., Chen, S.U., Wu, H.N., Chang, M.C. and Hsiao, C.D. (2004) Crystal structure of PriB, a primosomal DNA replication protein of Escherichia coli. J. Biol. Chem., 279, 50465-50471.
24. Masai, H. and Arai, K. (1989) Escherichia coli dnaT gene function is required for pBR322 plasmid replication but not for R1 plasmid replication. J. Bacteriol., 171, 2975-2980.
25. McCool, J.D., Ford, C.C. and Sandler, S.J. (2004) A dnaT mutant with phenotypes similar to those of a priA2::kan mutant in Escherichia coli K-12. Genetics, 167, 569-578.
26. Black, S.L., Dawson, A., Ward, F.B. and Allen, R.J. (2013) Genes required for growth at high hydrostatic pressure in Escherichia coli K-12 identified by genome-wide screening. PLoS One, 8, e73995.
27. Huang, Y.H. and Huang, C.Y. (2013) The N-terminal domain of DnaT, a primosomal DNA replication protein, is crucial for PriB binding and self-trimerization. Biochem. Biophys. Res. Commun., 442, 147-152.
28. Huang, Y.H., Lin, M.J. and Huang, C.Y. (2013) DnaT is a single-stranded DNA binding protein. Genes Cells, 18, 1007-1019.
29. Szymanski, M.R., Jezewska, M.J. and Bujalowski, W. (2013) Energetics of the Escherichia coli DnaT protein trimerization reaction. Biochemistry, 52, 1858-1873.
30. Szymanski, M.R., Jezewska, M.J. and Bujalowski, W. (2013) The Escherichia coli primosomal DnaT protein exists in solution as a monomer-trimer equilibrium system. Biochemistry, 52, 1845-1857.
31. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr., Pt A, 276, 307-326.
32. Collaborative Coputational Protject Number, 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr., 50, 760-763.
33. 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 Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
34. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
35. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr., 53, 240-255.
36. Vagin, A. and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr., 30, 1022-1025.
37. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. 3rd, Snoeyink, J., Richardson, J.S. et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res., 35, W375-W383.
38. Wiedemann, C., Bellstedt, P. and Gorlach, M. (2013) CAPITO-a web server-based analysis and plotting tool for circular dichroism data. Bioinformatics, 29, 1750-1757.
39. Bocquet, N., Bizard, A.H., Abdulrahman, W., Larsen, N.B., Faty, M., Cavadini, S., Bunker, R.D., Kowalczykowski, S.C., Cejka, P., Hickson, I.D. et al. (2014) Structural and mechanistic insight into Holliday-junction dissolution by topoisomerase IIIalpha and RMI1. Nat. Struct. Mol. Biol., 21, 261-268.
40. Arai, K., McMacken, R., Yasuda, S. and Kornberg, A. (1981) Purification and properties of Escherichia coli protein i, a prepriming protein in phi X174 DNA replication. J. Biol. Chem., 256, 5281-5286.
41. Shamoo, Y., Friedman, A.M., Parsons, M.R., Konigsberg, W.H. and Steitz, T.A. (1995) Crystal structure of a replication fork single-stranded DNA binding protein (T4 gp32) complexed to DNA. Nature, 376, 362-366.
42. Brenner, S.L., Zlotnick, A. and Griffith, J.D. (1988) RecA protein self-assembly. Multiple discrete aggregation states. J. Mol. Biol., 204, 959-972.
43. Dickey, T.H., Altschuler, S.E. and Wuttke, D.S. (2013) Single-stranded DNA-binding proteins: multiple domains for multiple functions. Structure, 21, 1074-1084.
44. Wang, W., Ding, J., Zhang, Y., Hu, Y. and Wang, D.C. (2014) Structural insights into the unique single-stranded DNA-binding mode of Helicobacter pylori DprA. Nucleic Acids Res., 42, 3478-3491.
45. Lunde, B.M., Moore, C. and Varani, G. (2007) RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol., 8, 479-490.
46. Duderstadt, K.E., Chuang, K. and Berger, J.M. (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature, 478, 209-213.
47. Chen, Z., Yang, H. and Pavletich, N.P. (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature, 453, 489-484.