RecQ helicases: caretakers of the genome (original) (raw)
Soultanas, P. & Wigley, D. B. Unwinding the 'Gordian knot' of helicase action. Trends Biochem. Sci.26, 47–54 (2001). ArticleCASPubMed Google Scholar
Chakraverty, R. K. & Hickson, I. D. Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. BioEssays21, 286–294 (1999). ArticleCASPubMed Google Scholar
Karow, J. K., Wu, L. & Hickson, I. D. RecQ family helicases: roles in cancer and aging. Curr. Opin. Genet. Dev.10, 32–38 (2000). ArticleCASPubMed Google Scholar
van Brabant, A. J., Stan, R. & Ellis, N. A. DNA helicases, genomic instability, and human genetic disease. Annu. Rev. Genomics Hum. Genet.1, 409–459 (2000). ArticleCASPubMed Google Scholar
Mohaghegh, P. & Hickson, I. D. DNA helicase deficiencies associated with cancer predisposition and premature ageing disorders. Hum. Mol. Genet.10, 741–746 (2001). ArticleCASPubMed Google Scholar
Nakayama, H. et al. Isolation and genetic characterization of a thymineless death-resistant mutant of Escherichia coli K12: identification of a new mutation (recQ1) that blocks the RecF recombination pathway. Mol. Gen. Genet.195, 474–480 (1984). ArticleCASPubMed Google Scholar
Morozov, V., Mushegian, A. R., Koonin, E. V. & Bork, P. A putative nucleic acid-binding domain in Bloom's and Werner's syndrome helicases. Trends Biochem. Sci.22, 417–418 (1997). ArticleCASPubMed Google Scholar
Liu, Z. et al. The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Structure Fold. Des.7, 1557–1566 (1999). ArticleCASPubMed Google Scholar
Kaneko, H. et al. BLM (the causative gene of Bloom syndrome) protein translocation into the nucleus by a nuclear localization signal. Biochem. Biophys. Res. Commun.240, 348–353 (1997). ArticleCASPubMed Google Scholar
Matsumoto, T., Shimamoto, A., Goto, M. & Furuichi, Y. Impaired nuclear localization of defective DNA helicases in Werner's syndrome. Nature Genet.16, 335–336 (1997). ArticleCASPubMed Google Scholar
Huang, S. et al. The premature ageing syndrome protein, WRN, is a 3′–5′ exonuclease. Nature Genet.20, 114–116 (1998). ArticleCASPubMed Google Scholar
Kamath-Loeb, A. S., Shen, J. C., Loeb, L. A. & Fry, M. Werner syndrome protein. II. Characterization of the integral 3′–5′ DNA exonuclease. J. Biol. Chem.273, 34145–34150 (1998). ArticleCASPubMed Google Scholar
Shen, J. C. et al. Werner syndrome protein. I. DNA helicase and DNA exonuclease reside on the same polypeptide. J. Biol. Chem.273, 34139–34144 (1998). ArticleCASPubMed Google Scholar
Opresko, P. L., Laine, J. P., Brosh, R. M. Jr, Seidman, M. M. & Bohr, V. A. Coordinate action of the helicase and 3′ to 5′ exonuclease of Werner syndrome protein. J. Biol. Chem.276, 44677–44687 (2001). References 11–14 show that the WRN protein is a combined helicase/nuclease, unlike other RecQ-family helicases. ArticleCASPubMed Google Scholar
Shimamoto, A., Nishikawa, K., Kitao, S. & Furuichi, Y. Human RecQ5β, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with topoisomerases 3α and 3β. Nucleic Acids Res.28, 1647–1655 (2000). ArticleCASPubMedPubMed Central Google Scholar
Ellis, N. A. et al. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell83, 655–666 (1995). Reports the identification of the gene that is defective in Bloom's syndrome as encoding a RecQ helicase. ArticleCASPubMed Google Scholar
Yu, C. et al. Positional cloning of the Werner's syndrome gene. Science272, 258–262 (1996). Reports the identification of the gene that is defective in Werner's syndrome as encoding a RecQ helicase. ArticleCASPubMed Google Scholar
Kitao, S. et al. Mutations in RECQL4 cause a subset of cases of Rothmund–Thomson syndrome. Nature Genet.22, 82–84 (1999). Reports the identification of the gene that is defective in Rothmund–Thomson syndrome as encoding a RecQ helicase. ArticleCASPubMed Google Scholar
Wang, L. L. et al. Clinical manifestations in a cohort of 41 Rothmund–Thomson syndrome patients. Am. J. Med. Genet.102, 11–17 (2001). ArticleCASPubMed Google Scholar
Moser, M. J., Oshima, J. & Monnat, R. J., Jr . WRN mutations in Werner syndrome. Hum. Mutat.13, 271–279 (1999). ArticleCASPubMed Google Scholar
Straughen, J. E. et al. A rapid method for detecting the predominant Ashkenazi Jewish mutation in the Bloom's syndrome gene. Hum. Mutat.11, 175–178 (1998). ArticleCASPubMed Google Scholar
Lengauer, C., Kinzler, K. W. & Vogelstein, B. Genetic instabilities in human cancers. Nature396, 643–649 (1998). ArticleCASPubMed Google Scholar
Levitt, N. C. & Hickson, I. D. Caretaker tumour suppressor genes that defend genome integrity. Trends Mol. Med.8, 179–186 (2002). ArticleCASPubMed Google Scholar
Calin, G. et al. Somatic frameshift mutations in the Bloom syndrome BLM gene are frequent in sporadic gastric carcinomas with microsatellite mutator phenotype. BMC Genet.2, 14 (2001). ArticleCASPubMedPubMed Central Google Scholar
Gruber, S. B. et al. BLM heterozygosity and the risk of colorectal cancer. Science297, 2013 (2002). ArticleCASPubMed Google Scholar
Goss, K. H. et al. Enhanced tumor formation in mice heterozygous for Blm mutation. Science297, 2051–2053 (2002). This paper, as well as reference 30, indicates thatBLMheterozygosity predisposes humans and mice to cancer. ArticlePubMedCAS Google Scholar
Oakley, T. J. & Hickson, I. D. Defending genome integrity during S-phase: putative roles for RecQ helicases and topoisomerase III. DNA Repair1, 1–33 (2002). Article Google Scholar
Lonn, U., Lonn, S., Nylen, U., Winblad, G. & German, J. An abnormal profile of DNA replication intermediates in Bloom's syndrome. Cancer Res.50, 3141–3145 (1990). CASPubMed Google Scholar
Chaganti, R. S., Schonberg, S. & German, J. A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc. Natl Acad. Sci. USA71, 4508–4512 (1974). ArticleCASPubMedPubMed Central Google Scholar
Sonoda, E. et al. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol.19, 5166–5169 (1999). ArticleCASPubMedPubMed Central Google Scholar
Prince, P. R., Emond, M. J. & Monnat, R. J., Jr . Loss of Werner syndrome protein function promotes aberrant mitotic recombination. Genes Dev.15, 933–938 (2001). ArticleCASPubMedPubMed Central Google Scholar
Saintigny, Y., Makienko, K., Swanson, C., Emond, M. J. & Monnat, R. J. Jr . Homologous recombination resolution defect in Werner syndrome. Mol. Cell. Biol.22, 6971–6978 (2002). Indicates that the WRN protein is involved in the resolution of recombinase structures. ArticleCASPubMedPubMed Central Google Scholar
Fukuchi, K., Martin, G. M. & Monnat, R. J. Mutator phenotype of Werner syndrome is characterized by extensive deletions. Proc. Natl Acad. Sci. USA86, 5893–5897 (1989). ArticleCASPubMedPubMed Central Google Scholar
Chester, N., Kuo, F., Kozak, C., O'Hara, C. D. & Leder, P. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev.12, 3382–3393 (1998). ArticleCASPubMedPubMed Central Google Scholar
Luo, G. et al. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nature Genet.26, 424–429 (2000). Identified a viable, cancer-prone mouse for Bloom's syndrome. ArticleCASPubMed Google Scholar
Lebel, M. & Leder, P. A deletion within the murine Werner syndrome helicase induces sensitivity to inhibitors of topoisomerase and loss of cellular proliferative capacity. Proc. Natl Acad. Sci. USA95, 13097–13102 (1998). ArticleCASPubMedPubMed Central Google Scholar
Lebel, M., Cardiff, R. D. & Leder, P. Tumorigenic effect of nonfunctional p53 or p21 in mice mutant in the Werner syndrome helicase. Cancer Res.61, 1816–1819 (2001). CASPubMed Google Scholar
Mohaghegh, P., Karow, J. K., Brosh, R. M. Jr, Bohr, V. A. Jr & Hickson, I. D. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res.29, 2843–2849 (2001). ArticleCASPubMedPubMed Central Google Scholar
Sun, H., Karow, J. K., Hickson, I. D. & Maizels, N. The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem.273, 27587–27592 (1998). ArticleCASPubMed Google Scholar
Fry, M. & Loeb, L. A. Human werner syndrome DNA helicase unwinds tetrahelical structures of the fragile X syndrome repeat sequence d(CGG)n. J. Biol. Chem.274, 12797–12802 (1999). ArticleCASPubMed Google Scholar
Sun, H., Bennett, R. J. & Maizels, N. The Saccharomyces cerevisiae Sgs1 helicase efficiently unwinds G-G paired DNAs. Nucleic Acids Res.27, 1978–1984 (1999). ArticleCASPubMedPubMed Central Google Scholar
Wu, X. & Maizels, N. Substrate-specific inhibition of RecQ helicase. Nucleic Acids Res.29, 1765–1771 (2001). References 43–47 revealed that G-quadruplex DNA is a preferred substrate for RecQ helicases. ArticleCASPubMedPubMed Central Google Scholar
Han, H. & Hurley, L. H. G-quadruplex DNA: a potential target for anti-cancer drug design. Trends Pharmacol. Sci.21, 136–142 (2000). ArticleCASPubMed Google Scholar
Karow, J. K., Constantinou, A., Li, J. L., West, S. C. & Hickson, I. D. The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc. Natl Acad. Sci. USA97, 6504–6508 (2000). ArticleCASPubMedPubMed Central Google Scholar
Constantinou, A. et al. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep.1, 80–84 (2000). References 49 and 50 identified BLM and WRN as Holliday junction branch-migration proteins. ArticleCASPubMedPubMed Central Google Scholar
West, S. C. Processing of recombination intermediates by the RuvABC proteins. Annu. Rev. Genet.31, 213–244 (1997). ArticleCASPubMed Google Scholar
Yankiwski, V., Marciniak, R. A., Guarente, L. & Neff, N. F. Nuclear structure in normal and Bloom syndrome cells. Proc. Natl Acad. Sci. USA97, 5214–5219 (2000). ArticleCASPubMedPubMed Central Google Scholar
Sanz, M. M., Proytcheva, M., Ellis, N. A., Holloman, W. K. & German, J. BLM, the Bloom's syndrome protein, varies during the cell cycle in its amount, distribution, and co-localization with other nuclear proteins. Cytogenet. Cell Genet.91, 217–223 (2000). ArticleCASPubMed Google Scholar
Zhong, S. et al. A role for PML and the nuclear body in genomic stability. Oncogene18, 7941–7947 (1999). ArticleCASPubMed Google Scholar
Hodges, M., Tissot, C., Howe, K., Grimwade, D. & Freemont, P. S. Structure, organization, and dynamics of promyelocytic leukemia protein nuclear bodies. Am. J. Hum. Genet.63, 297–304 (1998). ArticleCASPubMedPubMed Central Google Scholar
Ruggero, D., Wang, Z. G. & Pandolfi, P. P. The puzzling multiple lives of PML and its role in the genesis of cancer. Bioessays22, 827–835 (2000). ArticleCASPubMed Google Scholar
Wu, L., Davies, S. L., Levitt, N. C. & Hickson, I. D. Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J. Biol. Chem.276, 19375–19381 (2001). ArticleCASPubMed Google Scholar
Bischof, O. et al. Regulation and localization of the Bloom syndrome protein in response to DNA damage. J. Cell Biol.153, 367–380 (2001). ArticleCASPubMedPubMed Central Google Scholar
Pedrazzi, G. et al. Direct association of Bloom's syndrome gene product with the human mismatch repair protein MLH1. Nucleic Acids Res.29, 4378–4386 (2001). ArticleCASPubMedPubMed Central Google Scholar
Wang, Y. et al. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev.14, 927–939 (2000). CASPubMedPubMed Central Google Scholar
Gray, M. D., Wang, L., Youssoufian, H., Martin, G. M. & Oshima, J. Werner helicase is localized to transcriptionally active nucleoli of cycling cells. Exp. Cell Res.242, 487–494 (1998). ArticleCASPubMed Google Scholar
Marciniak, R. A., Lombard, D. B., Johnson, F. B. & Guarente, L. Nucleolar localization of the Werner syndrome protein in human cells. Proc. Natl Acad. Sci. USA95, 6887–6892 (1998). ArticleCASPubMedPubMed Central Google Scholar
Sakamoto, S. et al. Werner helicase relocates into nuclear foci in response to DNA damaging agents and co-localizes with RPA and Rad51. Genes Cells6, 421–430 (2001). ArticleCASPubMed Google Scholar
Blander, G. et al. Physical and functional interaction between p53 and the Werner's syndrome protein. J. Biol. Chem.274, 29463–29469 (1999). ArticleCASPubMed Google Scholar
Wang, X. W. et al. Functional interaction of p53 and BLM DNA helicase in apoptosis. J. Biol. Chem.276, 32948–32955 (2001). ArticleCASPubMed Google Scholar
Brosh, R. M. Jr . et al. p53 Modulates the exonuclease activity of Werner syndrome protein. J. Biol. Chem.276, 35093–35102 (2001). ArticleCASPubMed Google Scholar
Yang, Q. et al. The processing of Holliday junctions by BLM and WRN helicases is regulated by p53. J. Biol. Chem.277, 31980–31987 (2002). ArticleCASPubMed Google Scholar
Brosh, R. M. Jr . et al. Functional and physical interaction between WRN helicase and human replication protein A. J. Biol. Chem.274, 18341–18350 (1999). ArticleCASPubMed Google Scholar
Shen, J. C., Gray, M. D., Oshima, J. & Loeb, L. A. Characterization of Werner syndrome protein DNA helicase activity: directionality, substrate dependence and stimulation by replication protein A. Nucleic Acids Res.26, 2879–2885 (1998). ArticleCASPubMedPubMed Central Google Scholar
Brosh, R. M. Jr et al. Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem.275, 23500–23508 (2000). ArticleCASPubMed Google Scholar
von Kobbe, C. et al. Colocalization, physical, and functional interaction between Werner and Bloom syndrome proteins. J. Biol. Chem.277, 22035–22044 (2002). ArticleCASPubMed Google Scholar
Gangloff, S., McDonald, J. P., Bendixen, C., Arthur, L. & Rothstein, R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol.14, 8391–8398 (1994). ArticleCASPubMedPubMed Central Google Scholar
Bennett, R. J., Noirot-Gros, M. F. & Wang, J. C. Interaction between yeast sgs1 helicase and DNA topoisomerase III. J. Biol. Chem.275, 26898–26905 (2000). CASPubMed Google Scholar
Harmon, F. G., DiGate, R. J. & Kowalczykowski, S. C. RecQ helicase and topoisomerase III comprise a novel DNA strand passage function: a conserved mechanism for control of DNA recombination. Mol. Cell3, 1–20 (1999). Article Google Scholar
Wu, L. et al. The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem.275, 9636–9644 (2000). ArticleCASPubMed Google Scholar
Johnson, F. B. et al. Association of the Bloom syndrome protein with topoisomerase IIIalpha in somatic and meiotic cells. Cancer Res.60, 1162–1167 (2000). CASPubMed Google Scholar
Wu, L. & Hickson, I. D. The Bloom's syndrome helicase stimulates the activity of human topoisomerase III alpha. Nucleic Acids Res.30, 4823–4829 (2002). ArticleCASPubMedPubMed Central Google Scholar
Stewart, G. S. et al. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell99, 577–587 (1999). ArticleCASPubMed Google Scholar
Rotman, G. & Shiloh, Y. ATM: a mediator of multiple responses to genotoxic stress. Oncogene18, 6135–6144 (1999). ArticleCASPubMed Google Scholar
Featherstone, C. & Jackson, S. P. DNA repair: the Nijmegen breakage syndrome protein. Curr. Biol.8, R622–R625 (1998). ArticleCASPubMed Google Scholar
Beamish, H. et al. Functional link between BLM defective in Bloom's syndrome and the ataxia-telangiectasia-mutated protein, ATM. J. Biol. Chem.277, 30515–30523 (2002). ArticleCASPubMed Google Scholar
Langland, G. et al. The Bloom's syndrome protein (BLM) interacts with MLH1 but is not required for DNA mismatch repair. J. Biol. Chem.276, 30031–30035 (2001). ArticleCASPubMed Google Scholar
Buermeyer, A. B., Deschenes, S. M., Baker, S. M. & Liskay, R. M. Mammalian DNA mismatch repair. Annu. Rev. Genet.33, 533–564 (1999). ArticleCASPubMed Google Scholar
Myung, K., Datta, A., Chen, C. & Kolodner, R. D. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nature Genet.27, 113–116 (2001). ArticleCASPubMed Google Scholar
Lebel, M., Spillare, E. A., Harris, C. C. & Leder, P. The Werner syndrome gene product co-purifies with the DNA replication complex and interacts with PCNA and topoisomerase I. J. Biol. Chem.274, 37795–37799 (1999). ArticleCASPubMed Google Scholar
Brosh, R. M. Jr, Driscoll, H. C., Dianov, G. L. & Sommers, J. A. Biochemical characterization of the WRN–FEN-1 functional interaction. Biochemistry41, 12204–12216 (2002). ArticleCASPubMed Google Scholar
Brosh, R. M. Jr et al. Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. EMBO J.20, 5791–5801 (2001). ArticleCASPubMedPubMed Central Google Scholar
Kamath-Loeb, A. S., Loeb, L. A., Johansson, E., Burgers, P. M. & Fry, M. Interactions between the Werner syndrome helicase and DNA polymerase delta specifically facilitate copying of tetraplex and hairpin structures of the d(CGG)n trinucleotide repeat sequence. J. Biol. Chem.276, 16439–16446 (2001). ArticleCASPubMed Google Scholar
Mol, C. D., Parikh, S. S., Putnam, C. D., Lo, T. P. & Tainer, J. A. DNA repair mechanisms for the recognition and removal of damaged DNA bases. Annu. Rev. Biophys. Biomol. Struct.28, 101–128 (1999). ArticleCASPubMed Google Scholar
Li, B. & Comai, L. Functional interaction between Ku and the Werner syndrome protein in DNA end processing. J. Biol. Chem.275, 28349–28352 (2000). ArticleCASPubMed Google Scholar
Orren, D. K. et al. A functional interaction of Ku with Werner exonuclease facilitates digestion of damaged DNA. Nucleic Acids Res.29, 1926–1934 (2001). ArticleCASPubMedPubMed Central Google Scholar
Karmakar, P. et al. Werner protein is a target of DNA-dependent protein kinase in vivo and in vitro, and its catalytic activities are regulated by phosphorylation. J. Biol. Chem.277, 18291–18302 (2002). ArticleCASPubMed Google Scholar
Li, B. & Comai, L. Displacement of DNA-PKcs from DNA ends by the Werner syndrome protein. Nucleic Acids Res.30, 3653–3661 (2002). References 91–95 show that WRN is complexed with the DNA-dependent protein kinase in human cells. ArticleCASPubMedPubMed Central Google Scholar
Cox, M. M. Recombinational DNA repair of damaged replication forks in Escherichia coli: questions. Annu. Rev. Genet.35, 53–82 (2001). ArticleCASPubMed Google Scholar
Cox, M. M. et al. The importance of repairing stalled replication forks. Nature404, 37–41 (2000). ArticleCASPubMed Google Scholar
Kowalczykowski, S. C. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci.25, 156–165 (2000). ArticleCASPubMed Google Scholar
Postow, L. et al. Positive torsional strain causes the formation of a four-way junction at replication forks. J. Biol. Chem.276, 2790–2796 (2001). ArticleCASPubMed Google Scholar
McGlynn, P. & Lloyd, R. G. 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. USA98, 8227–8234 (2001). ArticleCASPubMedPubMed Central Google Scholar
Wu, L. & Hickson, I. D. RecQ helicases and topoisomerases: components of a conserved complex for the regulation of genetic recombination. Cell Mol. Life Sci.58, 894–901 (2001). ArticleCASPubMed Google Scholar
Harley, C. B., Futcher, A. B. & Greider, C. W. Telomeres shorten during ageing of human fibroblasts. Nature345, 458–460 (1990). ArticleCASPubMed Google Scholar
Olovnikov, A. M. Principles of marginotomy in template synthesis of polynucleotides. Doklady. Biochem.210, 394–397 (1971). Google Scholar
Nugent, C. I. & Lundblad, V. The telomerase reverse transcriptase: components and regulation. Genes Dev.12, 1073–1085 (1998). ArticleCASPubMed Google Scholar
McEachern, M. J., Krauskopf, A. & Blackburn, E. H. Telomeres and their control. Annu. Rev. Genet.34, 331–358 (2000). ArticleCASPubMed Google Scholar
Huang, P. et al. SGS1 is required for telomere elongation in the absence of telomerase. Curr. Biol.11, 125–129 (2001). ArticleCASPubMed Google Scholar
Cohen, H. & Sinclair, D. A. Recombination-mediated lengthening of terminal telomeric repeats requires the Sgs1 DNA helicase. Proc. Natl Acad. Sci. USA98, 3174–3179 (2001). ArticleCASPubMedPubMed Central Google Scholar
Johnson, F. B. et al. The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J.20, 905–913 (2001). References 107–109 identified a role for RecQ helicases in telomere maintenance. ArticleCASPubMedPubMed Central Google Scholar
Yeager, T. R. et al. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res.59, 4175–4179 (1999). CASPubMed Google Scholar
Opresko, P. L. et al. Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem.277, 41110–41119 (2002). ArticleCASPubMed Google Scholar
Gao, W., Khang, C. H., Park, S. Y., Lee, Y. H. & Kang, S. Evolution and organization of a highly dynamic, subtelomeric helicase gene family in the rice blast fungus Magnaporthe grisea. Genetics162, 103–112 (2002). CASPubMedPubMed Central Google Scholar
Ohsugi, I. et al. Telomere repeat DNA forms a large non-covalent complex with unique cohesive properties which is dissociated by Werner syndrome DNA helicase in the presence of replication protein A. Nucleic Acids Res.28, 3642–3648 (2000). ArticleCASPubMedPubMed Central Google Scholar