Nucleic Acids Research, 2001, Vol. 29, No. 13 2843-2849
© 2001 Oxford University Press
The Bloom’s and Werner’s syndrome proteins are DNA structure-specific helicases
Imperial Cancer Research Fund Laboratories, University of Oxford, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford OX3 9DS, UK and 1Laboratory of Molecular Genetics, National Institutes on Aging, NIH, 5600 Nathan Shock Drive, Baltimore, MD 21224, USA
BLM and WRN, the products of the Bloom’s and Werner’s syndrome genes, are members of the RecQ family of DNA helicases. Although both have been shown previously to unwind simple, partial duplex DNA substrates with 3'
5' polarity, little is known about the structural features of DNA that determine the substrate specificities of these enzymes. We have compared the substrate specificities of the BLM and WRN proteins using a variety of partial duplex DNA molecules, which are based upon a common core nucleotide sequence. We show that neither BLM nor WRN is capable of unwinding duplex DNA from a blunt-ended terminus or from an internal nick. However, both enzymes efficiently unwind the same blunt-ended duplex containing a centrally located 12 nt single-stranded ‘bubble’, as well as a synthetic X-structure (a model for the Holliday junction recombination intermediate) in which each ‘arm’ of the 4-way junction is blunt-ended. Surprisingly, a 3'-tailed duplex, a standard substrate for 3'5' helicases, is unwound much less efficiently by BLM and WRN than are the bubble and X-structure substrates. These data show conclusively that a single-stranded 3'-tail is not a structural requirement for unwinding of standard B-form DNA by these helicases. BLM and WRN also both unwind a variety of different forms of G-quadruplex DNA, a structure that can form at guanine-rich sequences present at several genomic loci. Our data indicate that BLM and WRN are atypical helicases that are highly DNA structure specific and have similar substrate specificities. We interpret these data in the light of the genomic instability and hyper-recombination characteristics of cells from individuals with Bloom’s or Werner’s syndrome.
* To whom correspondence should be addressed. Tel: +44 1865 222417; Fax: +44 1865 222431; Email: i.hickson{at}icrf.icnet.uk
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S. Cui, D. Arosio, K. M. Doherty, R. M. Brosh Jr, A. Falaschi, and A. Vindigni Analysis of the unwinding activity of the dimeric RECQ1 helicase in the presence of human replication protein A Nucleic Acids Res., April 19, 2004; 32(7): 2158 - 2170. [Abstract] [Full Text] [PDF]
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 S. Sharma, M. Otterlei, J. A. Sommers, H. C. Driscoll, G. L. Dianov, H.-I Kao, R. A. Bambara, and R. M. Brosh Jr. WRN Helicase and FEN-1 Form a Complex upon Replication Arrest and Together Process Branchmigrating DNA Structures Associated with the Replication Fork Mol. Biol. Cell, February 1, 2004; 15(2): 734 - 750. [Abstract] [Full Text] [PDF]
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C. von Kobbe, N. H. Thoma, B. K. Czyzewski, N. P. Pavletich, and V. A. Bohr Werner Syndrome Protein Contains Three Structure-specific DNA Binding Domains J. Biol. Chem., December 26, 2003; 278(52): 52997 - 53006. [Abstract] [Full Text] [PDF]
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J. P. Braybrooke, J.-L. Li, L. Wu, F. Caple, F. E. Benson, and I. D. Hickson Functional Interaction between the Bloom's Syndrome Helicase and the RAD51 Paralog, RAD51L3 (RAD51D) J. Biol. Chem., November 28, 2003; 278(48): 48357 - 48366. [Abstract] [Full Text] [PDF]
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H. Plchova, F. Hartung, and H. Puchta Biochemical Characterization of an Exonuclease from Arabidopsis thaliana Reveals Similarities to the DNA Exonuclease of the Human Werner Syndrome Protein J. Biol. Chem., November 7, 2003; 278(45): 44128 - 44138. [Abstract] [Full Text] [PDF]
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R. Onclercq-Delic, P. Calsou, C. Delteil, B. Salles, D. Papadopoulo, and M. Amor-Gueret Possible anti-recombinogenic role of Bloom's syndrome helicase in double-strand break processing Nucleic Acids Res., November 1, 2003; 31(21): 6272 - 6282. [Abstract] [Full Text] [PDF]
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H. C. Driscoll, S. W. Matson, J. M. Sayer, H. Kroth, D. M. Jerina, and R. M. Brosh Jr. Inhibition of Werner Syndrome Helicase Activity by Benzo[c]phenanthrene Diol Epoxide dA Adducts in DNA Is Both Strand-and Stereoisomer-dependent J. Biol. Chem., October 17, 2003; 278(42): 41126 - 41135. [Abstract] [Full Text] [PDF]
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K. Baynton, M. Otterlei, M. Bjoras, C. von Kobbe, V. A. Bohr, and E. Seeberg WRN Interacts Physically and Functionally with the Recombination Mediator Protein RAD52 J. Biol. Chem., September 19, 2003; 278(38): 36476 - 36486. [Abstract] [Full Text] [PDF]
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J. A. Harrigan, P. L. Opresko, C. von Kobbe, P. S. Kedar, R. Prasad, S. H. Wilson, and V. A. Bohr The Werner Syndrome Protein Stimulates DNA Polymerase {beta} Strand Displacement Synthesis via Its Helicase Activity J. Biol. Chem., June 13, 2003; 278(25): 22686 - 22695. [Abstract] [Full Text] [PDF]
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M. J. Cocco, L. A. Hanakahi, M. D. Huber, and N. Maizels Specific interactions of distamycin with G-quadruplex DNA Nucleic Acids Res., June 1, 2003; 31(11): 2944 - 2951. [Abstract] [Full Text] [PDF]
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A. R. Meetei, S. Sechi, M. Wallisch, D. Yang, M. K. Young, H. Joenje, M. E. Hoatlin, and W. Wang A Multiprotein Nuclear Complex Connects Fanconi Anemia and Bloom Syndrome Mol. Cell. Biol., May 15, 2003; 23(10): 3417 - 3426. [Abstract] [Full Text] [PDF]
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 P. L. Opresko, W.-H. Cheng, C. von Kobbe, J. A. Harrigan, and V. A. Bohr Werner syndrome and the function of the Werner protein; what they can teach us about the molecular aging process. Carcinogenesis, May 1, 2003; 24(5): 791 - 802. [Abstract] [Full Text] [PDF]
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A. Z. Ozsoy, H. M. Ragonese, and S. W. Matson Analysis of helicase activity and substrate specificity of Drosophila RECQ5 Nucleic Acids Res., March 1, 2003; 31(5): 1554 - 1564. [Abstract] [Full Text] [PDF]
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S. Cui, R. Klima, A. Ochem, D. Arosio, A. Falaschi, and A. Vindigni Characterization of the DNA-unwinding Activity of Human RECQ1, a Helicase Specifically Stimulated by Human Replication Protein A J. Biol. Chem., January 10, 2003; 278(3): 1424 - 1432. [Abstract] [Full Text] [PDF]
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G. Blander, N. Zalle, Y. Daniely, J. Taplick, M. D. Gray, and M. Oren DNA Damage-induced Translocation of the Werner Helicase Is Regulated by Acetylation J. Biol. Chem., December 20, 2002; 277(52): 50934 - 50940. [Abstract] [Full Text] [PDF]
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