Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 195162, 14 pages
http://dx.doi.org/10.1155/2014/195162
Review Article

Structural Insight into the DNA-Binding Mode of the Primosomal Proteins PriA, PriB, and DnaT

1School of Biomedical Sciences, Chung Shan Medical University, No. 110, Section 1, Chien-Kuo N. Road, Taichung City 40201, Taiwan
2Department of Medical Research, Chung Shan Medical University Hospital, No. 110, Section 1, Chien-Kuo N. Road, Taichung City 40201, Taiwan

Received 18 April 2014; Revised 20 June 2014; Accepted 1 July 2014; Published 21 July 2014

Academic Editor: Yoshito Abe

Copyright © 2014 Yen-Hua Huang and Cheng-Yang Huang. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Smeenk and H. van Attikum, “The chromatin response to DNA breaks: leaving a mark on genome integrity,” Annual Review of Biochemistry, vol. 82, pp. 55–80, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Panier and D. Durocher, “Push back to respond better: regulatory inhibition of the DNA double-strand break response,” Nature Reviews Molecular Cell Biology, vol. 14, pp. 661–672, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. R. C. Heller and K. J. Marians, “Replisome assembly and the direct restart of stalled replication forks,” Nature Reviews Molecular Cell Biology, vol. 7, no. 12, pp. 932–943, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. R. L. Maher, A. M. Branagan, and S. W. Morrical, “Coordination of DNA replication and recombination activities in the maintenance of genome stability,” Journal of Cellular Biochemistry, vol. 112, no. 10, pp. 2672–2682, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. P. McGlynn and R. G. Lloyd, “Recombinational repair and restart of damaged replication forks,” Nature Reviews Molecular Cell Biology, vol. 3, no. 11, pp. 859–870, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. M. M. Cox, M. F. Goodman, K. N. Kreuzer, D. J. Sherratt, S. J. Sandler, and K. J. Marians, “The importance of repairing stalled replication forks,” Nature, vol. 404, no. 6773, pp. 37–41, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Masai, T. Tanaka, and D. Kohda, “Stalled replication forks: making ends meet for recognition and stabilization,” BioEssays, vol. 32, no. 8, pp. 687–697, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. C. B. Gabbai and K. J. Marians, “Recruitment to stalled replication forks of the PriA DNA helicase and replisome-loading activities is essential for survival,” DNA Repair, vol. 9, no. 3, pp. 202–209, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. K. J. Marians, “Prokaryotic DNA replication,” Annual Review of Biochemistry, vol. 61, pp. 673–719, 1992. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Schekman, A. Weiner, and A. Kornberg, “Multienzyme systems of DNA replication: proteins required for chromosome replication are resolved with the aid of a simple viral DNA template,” Science, vol. 186, no. 4168, pp. 987–993, 1974. View at Publisher · View at Google Scholar · View at Scopus
  11. S. J. Sandler and K. J. Marians, “Role of PriA in replication fork reactivation in Escherichia coli,” Journal of Bacteriology, vol. 182, no. 1, pp. 9–13, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. S. J. Sandler, “Multiple genetic pathways for restarting DNA replication forks in Escherichia coli K-12,” Genetics, vol. 155, no. 2, pp. 487–497, 2000. View at Google Scholar · View at Scopus
  13. K. J. Marians, “PriA-directed replication fork restart in Escherichia coli,” Trends in Biochemical Sciences, vol. 25, no. 4, pp. 185–189, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. S. S. Patel, M. Pandey, and D. Nandakumar, “Dynamic coupling between the motors of DNA replication: hexameric helicase, DNA polymerase, and primase,” Current Opinion in Chemical Biology, vol. 15, no. 5, pp. 595–605, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Lopper, R. Boonsombat, S. J. Sandler, and J. L. Keck, “A hand-off mechanism for primosome assembly in replication restart,” Molecular Cell, vol. 26, no. 6, pp. 781–793, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Boonsombat, S. Yeh, A. Milne, and S. J. Sandler, “A novel dnaC mutation that suppresses priB rep mutant phenotypes in Escherichia coli K-12,” Molecular Microbiology, vol. 60, no. 4, pp. 973–983, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. S. J. Sandler, “Requirements for replication restart proteins during constitutive stable DNA replication in Escherichia coli K-12,” Genetics, vol. 169, no. 4, pp. 1799–1806, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. J. D. McCool, C. C. Ford, and S. J. Sandler, “A dnaT mutant with phenotypes similar to those of a priA2::kan mutant in Escherichia coli K-12,” Genetics, vol. 167, no. 2, pp. 569–578, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Hinds and S. J. Sandler, “Allele specific synthetic lethality between priC and dnaAts alleles at the permissive temperature of 30°C in E. coli K-12,” BMC Microbiology, vol. 4, article 47, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. S. J. Sandler, J. D. McCool, T. T. Do, and R. U. Johansen, “PriA mutations that affect PriA-PriC function during replication restart,” Molecular Microbiology, vol. 41, no. 3, pp. 697–704, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Liu, L. Xu, S. J. Sandler, and K. J. Marians, “Replication fork assembly at recombination intermediates is required for bacterial growth,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 7, pp. 3552–3555, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. A. H. Marceau, D. A. Bernstein, B. W. Walsh, W. Shapiro, L. A. Simmons, and J. L. Keck, “Protein interactions in genome maintenance as novel antibacterial targets,” PLoS ONE, vol. 8, no. 3, Article ID e58765, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Lu, D. A. Bernstein, K. A. Satyshur, and J. L. Keck, “Small-molecule tools for dissecting the roles of SSB/protein interactions in genome maintenance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 2, pp. 633–638, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Bush, “Alarming β-lactamase-mediated resistance in multidrug-resistant Enterobacteriaceae,” Current Opinion in Microbiology, vol. 13, no. 5, pp. 558–564, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. H. W. Boucher, G. H. Talbot, J. S. Bradley et al., “Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America,” Clinical Infectious Diseases, vol. 48, no. 1, pp. 1–12, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Sunchu, L. Berg, H. E. Ward, and M. E. Lopper, “Identification of a small molecule PriA helicase inhibitor,” Biochemistry, vol. 51, no. 51, pp. 10137–10146, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Arai and A. Kornberg, “Unique primed start of phage phi X174 DNA replication and mobility of the primosome in a direction opposite chain synthesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 78, no. 1, pp. 69–73, 1981. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Masai, T. Asai, Y. Kubota, K. Arai, and T. Kogoma, “Escherichia coli PriA protein is essential for inducible and constitutive stable DNA replication,” EMBO Journal, vol. 13, no. 22, pp. 5338–5345, 1994. View at Google Scholar · View at Scopus
  29. P. Nurse, K. H. Zavitz, and K. J. Marians, “Inactivation of the Escherichia coli PriA DNA replication protein induces the SOS response,” Journal of Bacteriology, vol. 173, no. 21, pp. 6686–6693, 1991. View at Google Scholar · View at Scopus
  30. A. Kornberg, “Replication deficiencies in priA mutants of Escherichia coli lacking the primosomal replication n' protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 8, pp. 3029–3032, 1991. View at Publisher · View at Google Scholar · View at Scopus
  31. M. R. Szymanski, P. J. Bujalowski, M. J. Jezewska, A. M. Gmyrek, and W. Bujalowski, “The N-terminal domain of the Escherichia coli pria helicase contains both the DNA- and nucleotide-binding sites. Energetics of domain-DNA interactions and allosteric effect of the nucleotide cofactors,” Biochemistry, vol. 50, no. 43, pp. 9167–9183, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Chen, S. H. North, and H. Nakai, “Properties of the PriA helicase domain and its role in binding PriA to specific DNA structures,” Journal of Biological Chemistry, vol. 279, no. 37, pp. 38503–38512, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Tanaka, T. Mizukoshi, C. Taniyama, D. Kohda, K. Arai, and H. Masai, “DNA binding of PriA protein requires cooperation of the N-terminal D-loop/arrested-fork binding and C-terminal helicase domains,” Journal of Biological Chemistry, vol. 277, no. 41, pp. 38062–38071, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. C. A. Ouzounis and B. J. Blencowe, “Bacterial DNA replication initiation factor priA is related to proteins belonging to the “DEAD-box” family,” Nucleic Acids Research, vol. 19, no. 24, article 6953, 1991. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Y. Ng and K. J. Marians, “The ordered assembly of the phiX174-type primosome. I. Isolation and identification of intermediate protein-DNA complexes,” Journal of Biological Chemistry, vol. 271, no. 26, pp. 15642–15648, 1996. View at Google Scholar
  36. P. Nurse, J. Liu, and K. J. Marians, “Two modes of PriA binding to DNA,” Journal of Biological Chemistry, vol. 274, no. 35, pp. 25026–25032, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. P. McGlynn, A. A. Al-Deib, J. Liu, K. J. Marians, and R. G. Lloyd, “The DNA replication protein PriA and the recombination protein RecG bind D-loops,” Journal of Molecular Biology, vol. 270, no. 2, pp. 212–221, 1997. View at Publisher · View at Google Scholar · View at Scopus
  38. C. J. Cadman and P. McGlynn, “PriA helicase and SSB interact physically and functionally,” Nucleic Acids Research, vol. 32, no. 21, pp. 6378–6387, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Dong, N. P. George, K. L. Duckett, M. A. P. DeBeer, and M. E. Lopper, “The crystal structure of Neisseria gonorrhoeae PriB reveals mechanistic differences among bacterial DNA replication restart pathways,” Nucleic Acids Research, vol. 38, no. 2, Article ID gkp1031, pp. 499–509, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. C. J. Cadman, M. Lopper, P. B. Moon, J. L. Keck, and P. McGlynn, “PriB stimulates PriA helicase via an interaction with single-stranded DNA,” The Journal of Biological Chemistry, vol. 280, no. 48, pp. 39693–39700, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. R. C. Heller and K. J. Marians, “Unwinding of the nascent lagging strand by Rep and PriA enables the direct restart of stalled replication forks,” Journal of Biological Chemistry, vol. 280, no. 40, pp. 34143–34151, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. R. C. Heller and K. J. Marians, “The disposition of nascent strands at stalled replication forks dictates the pathway of replisome loading during restart,” Molecular Cell, vol. 17, no. 5, pp. 733–743, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Sasaki, T. Ose, N. Okamoto et al., “Structural basis of the 3′-end recognition of a leading strand in stalled replication forks by PriA,” EMBO Journal, vol. 26, no. 10, pp. 2584–2593, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Landau, I. Mayrose, Y. Rosenberg et al., “ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures,” Nucleic Acids Research, vol. 33, no. 2, pp. W299–W302, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Bhattacharyya, N. P. George, T. M. Thurmes et al., “Structural mechanisms of PriA-mediated DNA replication restart,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 4, pp. 1373–1378, 2014. View at Publisher · View at Google Scholar
  46. A. Vindigni, F. Marino, and O. Gileadi, “Probing the structural basis of RecQ helicase function,” Biophysical Chemistry, vol. 149, no. 3, pp. 67–77, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. A. C. W. Pike, B. Shrestha, V. Popuri et al., “Structure of the human RECQ1 helicase reveals a putative strand-separation pin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 4, pp. 1039–1044, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Büttner, S. Nehring, and K. Hopfner, “Structural basis for DNA duplex separation by a superfamily-2 helicase,” Nature Structural and Molecular Biology, vol. 14, no. 7, pp. 647–652, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. B. Lucic, Y. Zhang, O. King et al., “A prominent β-hairpin structure in the winged-helix domain of RECQ1 is required for DNA unwinding and oligomer formation,” Nucleic Acids Research, vol. 39, no. 5, pp. 1703–1717, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. S. S. Velankar, P. Soultanas, M. S. Dillingham, H. S. Subramanya, and D. B. Wigley, “Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism,” Cell, vol. 97, no. 1, pp. 75–84, 1999. View at Publisher · View at Google Scholar · View at Scopus
  51. M. R. Singleton, S. Scaife, and D. B. Wigley, “Structural analysis of DNA replication fork reversal by RecG,” Cell, vol. 107, no. 1, pp. 79–89, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. S. S. Patel and I. Donmez, “Mechanisms of helicases,” Journal of Biological Chemistry, vol. 281, no. 27, pp. 18265–18268, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. S. J. Sandler, K. J. Marians, K. H. Zavitz, J. Coutu, M. A. Parent, and A. J. Clark, “dnaC mutations suppress defects in DNA replication- and recombination-associated functions in priB and priC double mutants in Escherichia coli K-12,” Molecular Microbiology, vol. 34, no. 1, pp. 91–101, 1999. View at Publisher · View at Google Scholar · View at Scopus
  54. R. L. Low, J. Shlomai, and A. Kornberg, “Protein n, a primosomal DNA replication protein of Escherichia coli: purification and characterization,” Journal of Biological Chemistry, vol. 257, no. 11, pp. 6242–6250, 1982. View at Google Scholar · View at Scopus
  55. G. C. Allen Jr. and A. Kornberg, “Assembly of the primosome of DNA replication in Escherichia coli,” Journal of Biological Chemistry, vol. 268, no. 26, pp. 19204–19209, 1993. View at Google Scholar · View at Scopus
  56. C. Feng, B. Sunchu, M. E. Greenwood, and M. E. Lopper, “A bacterial PriB with weak single-stranded DNA binding activity can stimulate the DNA unwinding activity of its cognate PriA helicase,” BMC Microbiology, vol. 11, article 189, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Liu, P. Nurse, and K. J. Marians, “The ordered assembly of the φX174-type primosome. III. PriB facilitates complex formation between PriA and DnaT,” Journal of Biological Chemistry, vol. 271, no. 26, pp. 15656–15661, 1996. View at Publisher · View at Google Scholar · View at Scopus
  58. M. R. Szymanski, M. J. Jezewska, and W. Bujalowski, “Binding of two PriA-PriB complexes to the primosome assembly site initiates primosome formation,” Journal of Molecular Biology, vol. 411, no. 1, pp. 123–142, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. H. Huang and C. Y. Huang, “The N-terminal domain of DnaT, a primosomal DNA replication protein, is crucial for PriB binding and self-trimerization,” Biochemical and Biophysical Research Communications, vol. 442, pp. 147–152, 2013. View at Publisher · View at Google Scholar
  60. J. Y. Ng and K. J. Marians, “The ordered assembly of the φX174-type primosome. II. Preservation of primosome composition from assembly through replication,” The Journal of Biological Chemistry, vol. 271, no. 26, pp. 15649–15655, 1996. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. H. Huang, M. J. Lin, and C. Y. Huang, “Yeast two-hybrid analysis of PriB-interacting proteins in replication restart primosome: a proposed PriB-SSB interaction model,” The Protein Journal, vol. 32, no. 6, pp. 477–483, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. H. Huang, H. H. Lin, and C. Y. Huang, “A single residue determines the cooperative binding property of a primosomal DNA replication protein, PriB, to single-stranded DNA,” Bioscience, Biotechnology and Biochemistry, vol. 76, no. 6, pp. 1110–1115, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Shioi, T. Ose, K. Maenaka et al., “Crystal structure of a biologically functional form of PriB from Escherichia coli reveals a potential single-stranded DNA-binding site,” Biochemical and Biophysical Research Communications, vol. 326, no. 4, pp. 766–776, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Lopper, J. M. Holton, and J. L. Keck, “Crystal structure of PriB, a component of the Escherichia coli replication restart primosome,” Structure, vol. 12, no. 11, pp. 1967–1975, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. J. H. Liu, T. W. Chang, C. Y. Huang et al., “Crystal structure of PriB, a primosomal DNA replication protein of Escherichia coli,” The Journal of Biological Chemistry, vol. 279, no. 48, pp. 50465–50471, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. M. P. Horvath, “Structural anatomy of telomere OB proteins,” Critical Reviews in Biochemistry and Molecular Biology, vol. 46, no. 5, pp. 409–435, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. R. L. Flynn and L. Zou, “Oligonucleotide/oligosaccharide-binding fold proteins: a growing family of genome guardians,” Critical Reviews in Biochemistry and Molecular Biology, vol. 45, no. 4, pp. 266–275, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. I. D. Kerr, R. I. M. Wadsworth, L. Cubeddu, W. Blankenfeldt, J. H. Naismith, and M. F. White, “Insights into ssDNA recognition by the OB fold from a structural and thermodynamic study of SulfolobusSSB protein,” The EMBO Journal, vol. 22, no. 11, pp. 2561–2570, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. A. G. Murzin, “OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences,” The EMBO Journal, vol. 12, no. 3, pp. 861–867, 1993. View at Google Scholar · View at Scopus
  70. Y. H. Huang, Y. H. Lo, W. Huang, and C. Y. Huang, “Crystal structure and DNA-binding mode of Klebsiella pneumoniae primosomal PriB protein,” Genes to Cells, vol. 17, no. 10, pp. 837–849, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. H. C. Hsieh and C. Y. Huang, “Identification of a novel protein, PriB, in Klebsiella pneumoniae,” Biochemical and Biophysical Research Communications, vol. 404, no. 1, pp. 546–551, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. M. R. Szymanski, M. J. Jezewska, and W. Bujalowski, “Interactions of the Escherichia coli Primosomal PriB Protein with the Single-stranded DNA. Stoichiometries, Intrinsic Affinities, Cooperativities, and Base Specificities,” Journal of Molecular Biology, vol. 398, no. 1, pp. 8–25, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Y. Huang, C. H. Hsu, Y. J. Sun, H. N. Wu, and C. D. Hsiao, “Complexed crystal structure of replication restart primosome protein PriB reveals a novel single-stranded DNA-binding mode,” Nucleic Acids Research, vol. 34, no. 14, pp. 3878–3886, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. K. W. Chan, Y. J. Lee, C. H. Wang, H. Huang, and Y. J. Sun, “Single-stranded DNA-binding protein complex from Helicobacter pylori suggests an ssDNA-binding surface,” Journal of Molecular Biology, vol. 388, no. 3, pp. 508–519, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Raghunathan, A. G. Kozlov, T. M. Lohman, and G. Waksman, “Structure of the DNA binding domain of E. coli SSB bound to ssDNA,” Nature Structural Biology, vol. 7, no. 8, pp. 648–652, 2000. View at Publisher · View at Google Scholar · View at Scopus
  76. V. A. Ponomarev, K. S. Makarova, L. Aravind, and E. V. Koonin, “Gene duplication with displacement and rearrangement: origin of the bacterial replication protein PriB from the single-stranded DNA-binding protein Ssb,” Journal of Molecular Microbiology and Biotechnology, vol. 5, no. 4, pp. 225–229, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Fujiyama, Y. Abe, T. Takenawa et al., “Involvement of histidine in complex formation of PriB and single-stranded DNA,” Biochimica et Biophysica Acta, vol. 184, pp. 299–307, 2014. View at Google Scholar
  78. R. R. Meyer and P. S. Laine, “The single-stranded DNA-binding protein of Escherichia coli,” Microbiological Reviews, vol. 54, no. 4, pp. 342–380, 1990. View at Google Scholar · View at Scopus
  79. J. A. Wilce, J. P. Vivian, A. F. Hastings et al., “Structure of the RTP-DNA complex and the mechanism of polar replication fork arrest,” Nature Structural Biology, vol. 8, no. 3, pp. 206–210, 2001. View at Publisher · View at Google Scholar · View at Scopus
  80. K. L. Tsai, Y. J. Sun, C. Y. Huang, J. Y. Yang, M. C. Hung, and C. D. Hsiao, “Crystal structure of the human FOXO3a-DBD/DNA complex suggests the effects of post-translational modification,” Nucleic Acids Research, vol. 35, no. 20, pp. 6984–6994, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. K. L. Tsai, C. Y. Huang, C. H. Chang, Y. J. Sun, W. J. Chuang, and C. D. Hsiao, “Crystal structure of the human FOXK1a-DNA complex and its implications on the diverse binding specificity of winged helix/forkhead proteins,” Journal of Biological Chemistry, vol. 281, no. 25, pp. 17400–17409, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. D. Kamashev, A. Balandina, A. K. Mazur, P. B. Arimondo, and J. Rouviere-Yaniv, “HU binds and folds single-stranded DNA,” Nucleic Acids Research, vol. 36, no. 3, pp. 1026–1036, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. K. K. Swinger, K. M. Lemberg, Y. Zhang, and P. A. Rice, “Flexible DNA bending in HU-DNA cocrystal structures,” The EMBO Journal, vol. 22, no. 14, pp. 3749–3760, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. H. Masai and K. Arai, “Initiation of lagging-strand synthesis for pBR322 plasmid DNA replication in vitro is dependent on primosomal protein i encoded by dnaT,” The Journal of Biological Chemistry, vol. 263, no. 29, pp. 15016–15023, 1988. View at Google Scholar · View at Scopus
  85. H. Masai, M. W. Bond, and K. Arai, “Cloning of the Escherichia coli gene for primosomal protein i: the relationship to dnaT, essential for chromosomal DNA replication,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 5, pp. 1256–1260, 1986. View at Publisher · View at Google Scholar · View at Scopus
  86. K. Arai, R. McMacken, S. Yasuda, and A. Kornberg, “Purification and properties of Escherichia coli protein i, a prepriming protein in X174 DNA replication,” The Journal of Biological Chemistry, vol. 256, no. 10, pp. 5281–5286, 1981. View at Google Scholar · View at Scopus
  87. H. Masai and K. Arai, “Escherichia coli dnaT gene function is required for pBR322 plasmid replication but not for R1 plasmid replication,” Journal of Bacteriology, vol. 171, no. 6, pp. 2975–2980, 1989. View at Google Scholar · View at Scopus
  88. S. L. Black, A. Dawson, F. B. Ward, and R. J. Allen, “Genes required for growth at high hydrostatic pressure in Escherichia coli K-12 identified by genome-wide screening,” PLoS One, vol. 8, Article ID e73995, 2013. View at Google Scholar
  89. S. Jang, S. J. Sandler, and R. M. Harshey, “Mu insertions are repaired by the double-strand break repair pathway of Escherichia coli,” PLoS Genetics, vol. 8, no. 4, Article ID e1002642, 2012. View at Publisher · View at Google Scholar · View at Scopus
  90. Y. H. Huang, M. J. Lin, and C. Y. Huang, “DnaT is a single-stranded DNA binding protein,” Genes Cells, vol. 18, pp. 1007–1019, 2013. View at Google Scholar
  91. M. R. Szymanski, M. J. Jezewska, and W. Bujalowski, “The Escherichia coli primosomal dnat protein exists in solution as a monomer-trimer equilibrium system,” Biochemistry, vol. 52, no. 11, pp. 1845–1857, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. Y. H. Lo, K. L. Tsai, Y. J. Sun, W. T. Chen, C. Y. Huang, and C. D. Hsiao, “The crystal structure of a replicative hexameric helicase DnaC and its complex with single-stranded DNA,” Nucleic Acids Research, vol. 37, no. 3, pp. 804–814, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. D. L. Theobald, R. M. Mitton-Fry, and D. S. Wuttke, “Nucleic acid recognition by OB-fold proteins,” Annual Review of Biophysics and Biomolecular Structure, vol. 32, pp. 115–133, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. C. Yang, U. Curth, C. Urbanke, and C. H. Kang, “Crystal structure of human mitochondrial single-stranded DNA binding protein at 2.4 A resolution,” Nature Structural Biology, vol. 4, no. 2, pp. 153–157, 1997. View at Publisher · View at Google Scholar · View at Scopus
  95. K. Arnold, L. Bordoli, J. Kopp, and T. Schwede, “The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling,” Bioinformatics, vol. 22, no. 2, pp. 195–201, 2006. View at Publisher · View at Google Scholar · View at Scopus
  96. C.-C. Chen, J.-K. Hwang, and J.-M. Yang, “(PS)2-v2: template-based protein structure prediction server,” BMC Bioinformatics, vol. 10, article 366, 2009. View at Publisher · View at Google Scholar · View at Scopus
  97. C. C. Chen, J. K. Hwang, and J. M. Yang, “(PS)2: protein structure prediction server,” Nucleic Acids Research, vol. 34, pp. W152–W157, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. T. M. Lohman, E. J. Tomko, and C. G. Wu, “Non-hexameric DNA helicases and translocases: mechanisms and regulation,” Nature Reviews Molecular Cell Biology, vol. 9, no. 5, pp. 391–401, 2008. View at Publisher · View at Google Scholar · View at Scopus
  99. W. Zhang, M. S. Dillingham, C. D. Thomas, S. Allen, C. J. Roberts, and P. Soultanas, “Directional loading and stimulation of PcrA helicase by the replication initiator protein RepD,” Journal of Molecular Biology, vol. 371, no. 2, pp. 336–348, 2007. View at Publisher · View at Google Scholar · View at Scopus
  100. R. D. Shereda, D. A. Bernstein, and J. L. Keck, “A central role for SSB in Escherichia coli RecQ DNA helicase function,” Journal of Biological Chemistry, vol. 282, no. 26, pp. 19247–19258, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. S. W. Matson and A. B. Robertson, “The UvrD helicase and its modulation by the mismatch repair protein MutL,” Nucleic Acids Research, vol. 34, no. 15, pp. 4089–4097, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. R. Roy, A. G. Kozlov, T. M. Lohman, and T. Ha, “SSB protein diffusion on single-stranded DNA stimulates RecA filament formation,” Nature, vol. 461, pp. 1092–1097, 2009. View at Publisher · View at Google Scholar