A model for dsDNA translocation revealed by a structural motif common to RecG and Mfd proteins

EMBO Journal

Volumn 22, Issue 3, 2003, Pages 724-734

  Mahdi, Akeel A ^a   Briggs, Geoffrey S ^a   Sharples, Gary J ^a,b   Wen, Qin ^a   Lloyd, Robert G ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

DNA replication; Holliday junctions; RecB; Recombination; Repair; RuvABC

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARGININE; DOUBLE STRANDED DNA; GLUTAMIC ACID; HELICASE; PROTEIN MFD; RECG HELICASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; DNA BINDING; DNA DENATURATION; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVITY; GENE TRANSLOCATION; HOLLIDAY JUNCTION; HYDROGEN BOND; HYDROLYSIS; MOTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ARGININE; BACTERIAL PROTEINS; DNA; DNA HELICASES; DNA REPLICATION; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS;

NEGIBACTERIA;

EID: 0037415719     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg043     Document Type: Article

References (54)

1. Al-Deib, A.A., Mahdi, A.A. and Lloyd, R.G. (1996) Modulation of recombination and DNA repair by the RecG and PriA helicases of Escherichia coli K-12. J. Bacteriol., 178, 6782-6789.
2. Bolt, E.L. and Lloyd, R.G. (2002) Substrate specificity of RusA resolvase reveals the DNA structures targeted by RuvAB and RecG in vivo. Mol. Cell, 10, 187-198.
3. Caruthers, J.M. and McKay, D.B. (2002) Helicase structure and mechanism. Curr. Opin. Struct. Biol., 12, 123-133.
4. Chakraverty, R.K. and Hickson, I.D. (1999) Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. BioEssays, 21, 286-294.
5. Chan, S.N., Harris, L., Bolt, E.L., Whitby, M.C. and Lloyd, R.G. (1997) Sequence-specificity and biochemical characterization of the RusA Holliday junction resolvase of Escherichia coli. J. Biol. Chem., 272, 14873-14882.
6. Cote, J., Quinn, J., Workman, J.L. and Peterson, C.L. (1994) Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science, 265, 53-60.
7. Cox, M.M., Goodman, M.F., Kreuzer, K.N., Sherratt, D.J., Sandler, S.J. and Marians, K.J. (2000) The importance of repairing stalled replication forks. Nature, 404, 37-41.
8. Cuff, J.A., Clamp, M.E., Siddiqui, A.S., Finlay, M. and Barton, G.J. (1998) JPred: a consensus secondary structure prediction server. Bioinformatics, 14, 892-893.
9. Davies, G.P., Kemp, P., Molineux, I.J. and Murray, N.E. (1999a) The DNA translocation and ATPase activities of restriction-deficient mutants of EcoKI. J. Mol. Biol., 292, 787-796.
10. Davies, G.P., Martin, I., Sturrock, S.S., Cronshaw, A., Murray, N.E. and Dryden, D.T. (1999b) On the structure and operation of type I DNA restriction enzymes. J. Mol. Biol., 290, 565-579.
11. Dillingham, M.S., Wigley, D.B. and Webb, M.R. (2002) Direct measurement of single-stranded DNA translocation by PcrA helicase using the fluorescent base analogue 2-aminopurine. Biochemistry, 41, 643-651.
12. Ellis, D.J., Dryden, D.T., Berge, T., Edwardson, J.M. and Henderson, R.M. (1999) Direct observation of DNA translocation and cleavage by the EcoKI endonuclease using atomic force microscopy. Nat. Struct. Biol., 6, 15-17.
13. Firman, K. and Szczelkun, M.D. (2000) Measuring motion on DNA by the type I restriction endonuclease EcoR124I using triplex displacement. EMBO J., 19, 2094-2102.
14. Flaus, A. and Owen-Hughes, T. (2001) Mechanisms for ATP-dependent chromatin remodelling. Curr. Opin. Genet. Dev., 11, 148-154.
15. Fukuoh, A., Iwasaki, H., Ishioka, K. and Shinagawa, H. (1997) ATP-dependent resolution of R-loops at the ColE1 replication origin by Escherichia coli RecG protein, a Holliday junction-specific helicase. EMBO J., 16, 203-209.
16. Gorbalenya, A.E. and Koonin, E.V. (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol., 3, 419-429.
17. Gregg, A.V., McGlynn, P., Jaktaji, R.P. and Lloyd, R.G. (2002) Direct rescue of stalled DNA replication forks via the combined action of PriA and RecG helicase activities. Mol. Cell, 9, 241-251.
18. Guex, N. and Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis, 18, 2714-2723.
19. Hall, M.C. and Matson, S.W. (1999) Helicase motifs: the engine that powers DNA unwinding. Mol. Microbiol., 34, 867-877.
20. Hamiche, A., Sandaltzopoulos, R., Gdula, D.A. and Wu, C. (1999) ATP-dependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell, 97, 833-842.
21. Janscak, P., Sandmeier, U. and Bickle, T.A. (1999) Single amino acid substitutions in the HsdR subunit of the type IB restriction enzyme EcoAI uncouple the DNA translocation and DNA cleavage activities of the enzyme. Nucleic Acids Res., 27, 2638-2643.
22. Kaplan, D.L. and O'Donnell, M. (2002) DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands. Mol. Cell, 10, 647-657.
23. Kuzminov, A. (2001) DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc. Natl Acad. Sci. USA, 98, 8461-8468.
24. Lloyd, R.G. and Sharples, G.J. (1993) Dissociation of synthetic Holliday junctions by E. coli RecG protein. EMBO J., 12, 17-22.
25. Mahdi, A.A., McGlynn, P., Lovett, S.D. and Lloyd, R.G. (1997) DNA binding and helicase domains of the Escherichia coli recombination protein RecG. Nucleic Acids Res., 25, 3875-3880.
26. Marians, K.J. (2000) Replication and recombination intersect. Curr. Opin. Genet. Dev., 10, 151-156.
27. McGlynn, P. and Lloyd, R.G. (1999) RecG helicase activity at three- and four-strand DNA structures. Nucleic Acids Res., 27, 3049-3056.
28. McGlynn, P. and Lloyd, R.G. (2000) Modulation of RNA polymerase by (p)ppGpp reveals a RecG-dependent mechanism for replication fork progression. Cell, 101, 35-45.
29. McGlynn, P. and Lloyd, R.G. (2001) Rescue of stalled replication forks by RecG: simultaneous translocation on the leading and lagging strand templates supports an active DNA unwinding model of fork reversal and Holliday junction formation. Proc. Natl Acad. Sci. USA, 98, 8227-8234.
30. McGlynn, P. and Lloyd, R.G. (2002) Genome stability and the processing of damaged replication forks by RecG. Trends Genet., 18, 413-419.
31. McGlynn, P., Al-Deib, A.A., Liu, J., Marians, K.J. and Lloyd, R.G. (1997) The DNA replication protein PriA and the recombination protein RecG bind D-loops. J. Mol. Biol., 270, 212-221.
32. McGlynn, P., Mahdi, A.A. and Lloyd, R.G. (2000) Characterisation of the catalytically active form of RecG helicase. Nucleic Acids Res., 28, 2324-2332.
33. McGlynn, P., Lloyd, R.G. and Marians, K.J. (2001) Formation of Holliday junctions by regression of stalled replication forks: RecG stimulates fork regression even when the DNA is negatively supercoiled. Proc. Natl Acad. Sci. USA, 98, 8235-8240.
34. Park, J.S., Marr, M.T. and Roberts, J.W. (2002) E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell, 109, 757-767.
35. Richmond, E. and Peterson, C.L. (1996) Functional analysis of the DNA-stimulated ATPase domain of yeast SW12/SNF2. Nucleic Acids Res., 24, 3685-3692.
36. Rost, B. (1996) PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol., 266, 525-539.
37. Rouleau, N., Domans'kyi, A., Reeben, M., Moilanen, A.M., Havas, K., Kang, Z., Owen-Hughes, T., Palvimo, J.J. and Janne, O.A. (2002) Novel ATPase of SNF2-like protein family interacts with androgen receptor and modulates androgen-dependent transcription. Mol. Biol. Cell, 13, 2106-2119.
38. Saha, A., Wittmeyer, J. and Caims, B.R. (2002) Chromatin remodeling by RSC involves ATP-dependent DNA translocation. Genes Dev., 16, 2120-2134.
39. Selby, C.P. and Sancar, A. (1994) Mechanisms of transcription-repair coupling and mutation frequency decline. Microbiol. Rev., 58, 317-329.
40. Sharples, G.J., Ingleston, S.M. and Lloyd, R.G. (1999) Holliday junction processing in bacteria: insights from the evolutionary conservation of RuvABC, RecG and RusA. J. Bacteriol., 181, 5543-5550.
41. Shen, X., Mizuguchi, G., Hamiche, A. and Wu, C. (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature, 406, 541-544.
42. Singleton, M.R. and Wigley,D.B. (2002) Modularity and specialization in superfamily 1 and 2 helicases. J. Bacteriol., 184, 1819-1826.
43. Singleton, M.R., Scaife, S. and Wigley, D.B. (2001) Structural analysis of DNA replication fork reversal by RecG. Cell, 107, 79-89.
44. Sogo, J.M., Lopes, M. and Foiani, M. (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science, 297, 599-602.
45. Soultanas, P., Dillingham, M.S., Wiley, P., Webb, M.R. and Wigley, D.B. (2000) Uncoupling DNA translocation and helicase activity in PcrA: direct evidence for an active mechanism. EMBO J., 19, 3799-3810.
46. Szczelkun, M.D. (2002) Kinetic models of translocation, head-on collision and DNA cleavage by type I restriction endonucleases. Biochemistry, 41, 2067-2074.
47. Tercero, J.A. and Diffley, J.F. (2001) Regulation of DNA replication fork progression through damaged DNA by the Mecl/Rad53 checkpoint. Nature, 412, 553-557.
48. Travers, A. (1999) An engine for nucleosome remodeling. Cell, 96, 311-314.
49. Vale, R.D. and Milligan, R.A. (2000) The way things move: looking under the hood of molecular motor proteins. Science, 288, 88-95.
50. Velankar, S.S., Soultanas, P., Dillingham, M.S., Subramanya, H.S. and Wigley, D.B. (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell, 97, 75-84.
51. Vincent, S.D., Mahdi, A.A. and Lloyd, R.G. (1996) The RecG branch migration protein of Escherichia coli dissociates R-loops. J. Mol. Biol., 264, 713-721.
52. Whitby, M.C. and Lloyd, R.G. (1998) Targeting Holliday junctions by the RecG branch migration protein of Escherichia coli. J. Biol. Chem., 273, 19729-19739.
53. Whitby, M.C., Vincent, S. and Lloyd, R.G. (1994) Branch migration of Holliday junctions: identification of RecG protein as a junction specific DNA helicase. EMBO J., 13, 5220-5228.
54. Whitehouse, I., Flaus, A., Caims, B.R., White, M.F., Workman, J.L. and Owen-Hughes, T. (1999) Nucleosome mobilization catalysed by the yeast SWI/SNF complex. Nature, 400, 784-787.