The hexameric helicase DnaB adopts a nonplanar conformation during translocation

Cell

Volumn 151, Issue 2, 2012, Pages 267-277

  Itsathitphaisarn, Ornchuma ^a   Wing, Richard A ^a   Eliason, William K ^a   Wang, Jimin ^a   Steitz, Thomas A ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNAB HELICASE; SINGLE STRANDED DNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE;

EID: 84867538324     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.09.014     Document Type: Article

References (52)

1. J.P. Abrahams, A.G. Leslie, R. Lutter, and J.E. Walker Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria Nature 370 1994 621 628
2. S. Ayora, F. Weise, P. Mesa, A. Stasiak, and J.C. Alonso Bacillus subtilis bacteriophage SPP1 hexameric DNA helicase, G40P, interacts with forked DNA Nucleic Acids Res. 30 2002 2280 2289
3. S. Bailey, W.K. Eliason, and T.A. Steitz Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase Science 318 2007 459 463
4. S. Bailey, W.K. Eliason, and T.A. Steitz The crystal structure of the Thermus aquaticus DnaB helicase monomer Nucleic Acids Res. 35 2007 4728 4736
5. J.M. Berger SnapShot: nucleic acid helicases and translocases Cell 134 2008 888
6. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
7. Y.R. Chemla, K. Aathavan, J. Michaelis, S. Grimes, P.J. Jardine, D.L. Anderson, and C. Bustamante Mechanism of force generation of a viral DNA packaging motor Cell 122 2005 683 692
8. Z. Chen, H. Yang, and N.P. Pavletich Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures Nature 453 2008 489 494
9. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
10. D.J. Crampton, S. Guo, D.E. Johnson, and C.C. Richardson The arginine finger of bacteriophage T7 gene 4 helicase: role in energy coupling Proc. Natl. Acad. Sci. USA 101 2004 4373 4378
11. D.J. Crampton, S. Mukherjee, and C.C. Richardson DNA-induced switch from independent to sequential dTTP hydrolysis in the bacteriophage T7 DNA helicase Mol. Cell 21 2006 165 174
12. E.J. Enemark, and L. Joshua-Tor Mechanism of DNA translocation in a replicative hexameric helicase Nature 442 2006 270 275
13. E.J. Enemark, and L. Joshua-Tor On helicases and other motor proteins Curr. Opin. Struct. Biol. 18 2008 243 257
14. R. Galletto, M.J. Jezewska, and W. Bujalowski Unzipping mechanism of the double-stranded DNA unwinding by a hexameric helicase: quantitative analysis of the rate of the dsDNA unwinding, processivity and kinetic step-size of the Escherichia coli DnaB helicase using rapid quench-flow method J. Mol. Biol. 343 2004 83 99
15. M.M. Hingorani, and S.S. Patel Interactions of bacteriophage T7 DNA primase/helicase protein with single-stranded and double-stranded DNAs Biochemistry 32 1993 12478 12487
16. M.J. Jezewska, S. Rajendran, and W. Bujalowski Complex of Escherichia coli primary replicative helicase DnaB protein with a replication fork: recognition and structure Biochemistry 37 1998 3116 3136
17. M.J. Jezewska, S. Rajendran, and W. Bujalowski Functional and structural heterogeneity of the DNA binding site of the Escherichia coli primary replicative helicase DnaB protein J. Biol. Chem. 273 1998 9058 9069
18. D.L. Kaplan The 3′-tail of a forked-duplex sterically determines whether one or two DNA strands pass through the central channel of a replication-fork helicase J. Mol. Biol. 301 2000 285 299
19. D.L. Kaplan, and T.A. Steitz DnaB from Thermus aquaticus unwinds forked duplex DNA with an asymmetric tail length dependence J. Biol. Chem. 274 1999 6889 6897
20. D.L. Kaplan, and M. O'Donnell DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands Mol. Cell 10 2002 647 657
21. B.A. Kelch, D.L. Makino, M. O'Donnell, and J. Kuriyan How a DNA polymerase clamp loader opens a sliding clamp Science 334 2011 1675 1680
22. J.L. Kim, K.A. Morgenstern, J.P. Griffith, M.D. Dwyer, J.A. Thomson, M.A. Murcko, C. Lin, and P.R. Caron Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding Structure 6 1998 89 100
23. T. Kitani, K. Yoda, T. Ogawa, and T. Okazaki Evidence that discontinuous DNA replication in Escherichia coli is primed by approximately 10 to 12 residues of RNA starting with a purine J. Mol. Biol. 184 1985 45 52
24. J.H. LeBowitz, and R. McMacken The Escherichia coli dnaB replication protein is a DNA helicase J. Biol. Chem. 261 1986 4738 4748
25. D.D. Leipe, E.V. Koonin, and L. Aravind Evolution and classification of P-loop kinases and related proteins J. Mol. Biol. 333 2003 781 815
26. A.Y. Lyubimov, M. Strycharska, and J.M. Berger The nuts and bolts of ring-translocase structure and mechanism Curr. Opin. Struct. Biol. 21 2011 240 248
27. M. Manosas, M.M. Spiering, Z. Zhuang, S.J. Benkovic, and V. Croquette Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome Nat. Chem. Biol. 5 2009 904 912
28. A. Martin, T.A. Baker, and R.T. Sauer Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines Nature 437 2005 1115 1120
29. P. Mesa, J.C. Alonso, and S. Ayora Bacillus subtilis bacteriophage SPP1 G40P helicase lacking the n-terminal domain unwinds DNA bidirectionally J. Mol. Biol. 357 2006 1077 1088
30. J.R. Moffitt, Y.R. Chemla, K. Aathavan, S. Grimes, P.J. Jardine, D.L. Anderson, and C. Bustamante Intersubunit coordination in a homomeric ring ATPase Nature 457 2009 446 450
31. M.J. Moreau, A.T. McGeoch, A.R. Lowe, L.S. Itzhaki, and S.D. Bell ATPase site architecture and helicase mechanism of an archaeal MCM Mol. Cell 28 2007 304 314
32. Otwinowski, Z. (1991). Isomorphous replacement and anomalous scattering. W. Wolf, P.R. Evans, and A.G.W. Leslie, eds. Proceedings of the CCP4 Study Weekend 25-26 January 1991, 80-85.
33. Z.M.W. Otwinowski Processing of X-Ray Diffraction Data Collected in Oscillation Mode 1997 Academic Press New York
34. R. Reyes-Lamothe, C. Possoz, O. Danilova, and D.J. Sherratt Independent positioning and action of Escherichia coli replisomes in live cells Cell 133 2008 90 102
35. N. Ribeck, D.L. Kaplan, I. Bruck, and O.A. Saleh DnaB helicase activity is modulated by DNA geometry and force Biophys. J. 99 2010 2170 2179
36. K. Saikrishnan, B. Powell, N.J. Cook, M.R. Webb, and D.B. Wigley Mechanistic basis of 5′-3′ translocation in SF1B helicases Cell 137 2009 849 859
37. P.M. Schaeffer, M.J. Headlam, and N.E. Dixon Protein - protein interactions in the eubacterial replisome IUBMB Life 57 2005 5 12
38. K. Scheffzek, M.R. Ahmadian, W. Kabsch, L. Wiesmüller, A. Lautwein, F. Schmitz, and A. Wittinghofer The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants Science 277 1997 333 338
39. G.M. Sheldrick Experimental phasing with SHELXC/D/E: combining chain tracing with density modification Acta Crystallogr. D Biol. Crystallogr. 66 2010 479 485
40. M.R. Singleton, M.R. Sawaya, T. Ellenberger, and D.B. Wigley Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides Cell 101 2000 589 600
41. M.R. Singleton, M.S. Dillingham, and D.B. Wigley Structure and mechanism of helicases and nucleic acid translocases Annu. Rev. Biochem. 76 2007 23 50
42. P. Soultanas, and D.B. Wigley Site-directed mutagenesis reveals roles for conserved amino acid residues in the hexameric DNA helicase DnaB from Bacillus stearothermophilus Nucleic Acids Res. 30 2002 4051 4060
43. R.M. Story, and T.A. Steitz Structure of the recA protein-ADP complex Nature 355 1992 374 376
44. N.A. Tanner, S.M. Hamdan, S. Jergic, K.V. Loscha, P.M. Schaeffer, N.E. Dixon, and A.M. van Oijen Single-molecule studies of fork dynamics in Escherichia coli DNA replication Nat. Struct. Mol. Biol. 15 2008 998
45. N.D. Thomsen, and J.M. Berger Running in reverse: the structural basis for translocation polarity in hexameric helicases Cell 139 2009 523 534
46. 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 97 1999 75 84
47. P.H. von Hippel, and E. Delagoutte A general model for nucleic acid helicases and their "coupling" within macromolecular machines Cell 104 2001 177 190
48. G. Wang, M.G. Klein, E. Tokonzaba, Y. Zhang, L.G. Holden, and X.S. Chen The structure of a DnaB-family replicative helicase and its interactions with primase Nat. Struct. Mol. Biol. 15 2008 94 100
49. J.G. Yodh, M. Schlierf, and T. Ha Insight into helicase mechanism and function revealed through single-molecule approaches Q. Rev. Biophys. 43 2010 185 217
50. A. Yuzhakov, Z. Kelman, and M. O'Donnell Trading places on DNA - a three-point switch underlies primer handoff from primase to the replicative DNA polymerase Cell 96 1999 153 163
51. 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.
52. Eisenberg, D., and McLachlan, A.D. (1986). Solvation energy in protein folding and binding. Nature 319, 199-203.