Single-molecule imaging of the oligomer formation of the nonhexameric escherichia coliUvrD helicase

Biophysical Journal

Volumn 104, Issue 4, 2013, Pages 924-933

  Yokota, Hiroaki ^a,b   Chujo, Yuko Ayabe ^c   Harada, Yoshie ^a  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL DNA; ESCHERICHIA COLI PROTEIN; HELICASE; SINGLE STRANDED DNA; UVRD PROTEIN, E COLI;

ARTICLE; BLEACHING; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; KINETICS; METABOLISM; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE;

ADENOSINE TRIPHOSPHATE; DNA HELICASES; DNA, BACTERIAL; DNA, SINGLE-STRANDED; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MICROSCOPY, FLUORESCENCE; PHOTOBLEACHING; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

EID: 84874126667     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.01.014     Document Type: Article

References (58)

1. 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
2. M.R. Singleton, and M.R. Sawaya D.B. Wigley Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides Cell 101 2000 589 600
3. E.J. Enemark, and L. Joshua-Tor On helicases and other motor proteins Curr. Opin. Struct. Biol. 18 2008 243 257
4. J.Y. Lee, and W. Yang UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke Cell 127 2006 1349 1360
5. H. Jia, and S. Korolev T.M. Lohman Rotations of the 2B sub-domain of E. coli UvrD helicase/translocase coupled to nucleotide and DNA binding J. Mol. Biol. 411 2011 633 648
6. S. Korolev, and J. Hsieh G. Waksman Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP Cell 90 1997 635 647
7. S.S. Velankar, and P. Soultanas D.B. Wigley Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism Cell 97 1999 75 84
8. T. Ha, and I. Rasnik S. Chu Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase Nature 419 2002 638 641
9. I. Rasnik, and S. Myong T. Ha DNA-binding orientation and domain conformation of the E. coli rep helicase monomer bound to a partial duplex junction: single-molecule studies of fluorescently labeled enzymes J. Mol. Biol. 336 2004 395 408
10. M.N. Dessinges, and T. Lionnet V. Croquette Single-molecule assay reveals strand switching and enhanced processivity of UvrD Proc. Natl. Acad. Sci. USA 101 2004 6439 6444
11. S. Dumont, and W. Cheng C. Bustamante RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP Nature 439 2006 105 108
12. S. Myong, and M.M. Bruno T. Ha Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase Science 317 2007 513 516
13. B. Sun, and K.J. Wei X.G. Xi Impediment of E. coli UvrD by DNA-destabilizing force reveals a strained-inchworm mechanism of DNA unwinding EMBO J. 27 2008 3279 3287
14. N. Fili, and G.I. Mashanov J.E. Molloy Visualizing helicases unwinding DNA at the single molecule level Nucleic Acids Res. 38 2010 4448 4457
15. H. Balci, and S. Arslan T. Ha Single-molecule nanopositioning: structural transitions of a helicase-DNA complex during ATP hydrolysis Biophys. J. 101 2011 976 984
16. A.K. Byrd, and D.L. Matlock K.D. Raney Dda helicase tightly couples translocation on single-stranded DNA to unwinding of duplex DNA: Dda is an optimally active helicase J. Mol. Biol. 420 2012 141 154
17. L.E. Mechanic, M.E. Latta, and S.W. Matson A region near the C-terminal end of Escherichia coli DNA helicase II is required for single-stranded DNA binding J. Bacteriol. 181 1999 2519 2526
18. J.L. Kim, and K.A. Morgenstern 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
19. I. Wong, and T.M. Lohman Allosteric effects of nucleotide cofactors on Escherichia coli Rep helicase-DNA binding Science 256 1992 350 355
20. W. Cheng, and J. Hsieh T.M. Lohman E. coli Rep oligomers are required to initiate DNA unwinding in vitro J. Mol. Biol. 310 2001 327 350
21. Y. Yang, and S.X. Dou X.G. Xi Evidence for a functional dimeric form of the PcrA helicase in DNA unwinding Nucleic Acids Res. 36 2008 1976 1989
22. N.K. Maluf, C.J. Fischer, and T.M. Lohman A dimer of Escherichia coli UvrD is the active form of the helicase in vitro J. Mol. Biol. 325 2003 913 935
23. B. Sikora, and Y. Chen K.D. Raney Hepatitis C virus NS3 helicase forms oligomeric structures that exhibit optimal DNA unwinding activity in vitro J. Biol. Chem. 283 2008 11516 11525
24. T.M. Lohman, and K.P. Bjornson Mechanisms of helicase-catalyzed DNA unwinding Annu. Rev. Biochem. 65 1996 169 214
25. D. Shu, and H. Zhang P. Guo Counting of six pRNAs of φ29 DNA-packaging motor with customized single-molecule dual-view system EMBO J. 26 2007 527 537
26. F. Xiao, H. Zhang, and P. Guo Novel mechanism of hexamer ring assembly in protein/RNA interactions revealed by single molecule imaging Nucleic Acids Res. 36 2008 6620 6632
27. M.H. Ulbrich, and E.Y. Isacoff Subunit counting in membrane-bound proteins Nat. Methods 4 2007 319 321
28. A. Jain, and R. Liu T. Ha Probing cellular protein complexes using single-molecule pull-down Nature 473 2011 484 488
29. Y. Harada, and T. Funatsu T. Yanagida Single-molecule imaging of RNA polymerase-DNA interactions in real time Biophys. J. 76 1999 709 715
30. S. Myong, and I. Rasnik T. Ha Repetitive shuttling of a motor protein on DNA Nature 437 2005 1321 1325
31. P.C. Blainey, and A.M. van Oijen X.S. Xie A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA Proc. Natl. Acad. Sci. USA 103 2006 5752 5757
32. A. Granéli, and C.C. Yeykal E.C. Greene Long-distance lateral diffusion of human Rad51 on double-stranded DNA Proc. Natl. Acad. Sci. USA 103 2006 1221 1226
33. J. Gorman, and A. Chowdhury E.C. Greene Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6 Mol. Cell 28 2007 359 370
34. J.H. Kim, and R.G. Larson Single-molecule analysis of 1D diffusion and transcription elongation of T7 RNA polymerase along individual stretched DNA molecules Nucleic Acids Res. 35 2007 3848 3858
35. H. Yokota, and Y.W. Han Y. Harada Single-molecule visualization of binding modes of helicase to DNA on PEGylated surfaces Chem. Lett. 38 2009 308 309
36. J. van Mameren, and M. Modesti G.J. Wuite Counting RAD51 proteins disassembling from nucleoprotein filaments under tension Nature 457 2009 745 748
37. J.A. Ali, N.K. Maluf, and T.M. Lohman An oligomeric form of E. coli UvrD is required for optimal helicase activity J. Mol. Biol. 293 1999 815 834
38. N.K. Maluf, and T.M. Lohman Self-association equilibria of Escherichia coli UvrD helicase studied by analytical ultracentrifugation J. Mol. Biol. 325 2003 889 912
39. N.K. Maluf, J.A. Ali, and T.M. Lohman Kinetic mechanism for formation of the active, dimeric UvrD helicase-DNA complex J. Biol. Chem. 278 2003 31930 31940
40. G.T. Runyon, I. Wong, and T.M. Lohman Overexpression, purification, DNA binding, and dimerization of the Escherichia coli uvrD gene product (helicase II) Biochemistry 32 1993 602 612
41. K. Chao, and T.M. Lohman DNA and nucleotide-induced conformational changes in the Escherichia coli Rep and helicase II (UvrD) proteins J. Biol. Chem. 265 1990 1067 1076
42. J.A. Ali, and T.M. Lohman Kinetic measurement of the step size of DNA unwinding by Escherichia coli UvrD helicase Science 275 1997 377 380
43. M. Manosas, and X.G. Xi V. Croquette Active and passive mechanisms of helicases Nucleic Acids Res. 38 2010 5518 5526
44. L.E. Mechanic, M.C. Hall, and S.W. Matson Escherichia coli DNA helicase II is active as a monomer J. Biol. Chem. 274 1999 12488 12498
45. G.T. Hermanson Bioconjugate Techniques 2nd ed. 2008 Academic Press New York
46. G.R. Drapeau Substrate specificity of a proteolytic enzyme isolated from a mutant of Pseudomonas fragi J. Biol. Chem. 255 1980 839 840
47. Y. Harada, and K. Sakurada T. Yanagida Mechanochemical coupling in actomyosin energy transduction studied by in vitro movement assay J. Mol. Biol. 216 1990 49 68
48. C.E. Aitken, R.A. Marshall, and J.D. Puglisi An oxygen scavenging system for improvement of dye stability in single-molecule fluorescence experiments Biophys. J. 94 2008 1826 1835
49. T.M. Lohman, and K. Chao G.T. Runyon Large-scale purification and characterization of the Escherichia coli rep gene product J. Biol. Chem. 264 1989 10139 10147
50. C.J. Fischer, N.K. Maluf, and T.M. Lohman Mechanism of ATP-dependent translocation of E. coli UvrD monomers along single-stranded DNA J. Mol. Biol. 344 2004 1287 1309
51. E.J. Tomko, and C.J. Fischer T.M. Lohman A nonuniform stepping mechanism for E. coli UvrD monomer translocation along single-stranded DNA Mol. Cell 26 2007 335 347
52. E.J. Tomko, C.J. Fischer, and T.M. Lohman Single-stranded DNA translocation of E. coli UvrD monomer is tightly coupled to ATP hydrolysis J. Mol. Biol. 418 2012 32 46
53. T.M. Lohman, E.J. Tomko, and C.G. Wu Non-hexameric DNA helicases and translocases: mechanisms and regulation Nat. Rev. Mol. Cell Biol. 9 2008 391 401
54. B. Nanduri, and A.K. Byrd K.D. Raney Pre-steady-state DNA unwinding by bacteriophage T4 Dda helicase reveals a monomeric molecular motor Proc. Natl. Acad. Sci. USA 99 2002 14722 14727
55. K.P. Bjornson, and M. Amaratunga T.M. Lohman Single-turnover kinetics of helicase-catalyzed DNA unwinding monitored continuously by fluorescence energy transfer Biochemistry 33 1994 14306 14316
56. M.S. Dillingham, D.B. Wigley, and M.R. Webb Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed Biochemistry 39 2000 205 212
57. M.S. Dillingham, D.B. Wigley, and M.R. Webb Direct measurement of single-stranded DNA translocation by PcrA helicase using the fluorescent base analogue 2-aminopurine Biochemistry 41 2002 643 651
58. A. Niedziela-Majka, and M.A. Chesnik T.M. Lohman Bacillus stearothermophilus PcrA monomer is a single-stranded DNA translocase but not a processive helicase in vitro J. Biol. Chem. 282 2007 27076 27085