Skip to main content
Log in

RecQ helicases and topoisomerase III in cancer and aging

  • Published:
Biogerontology Aims and scope Submit manuscript

Abstract

RecQ helicases have in recent years attracted increasing attention due to the important roles they play in maintaining genomic integrity, which is essential for the life of a cell and the survival of a species. Humans with mutations in RecQ homologues are cancer prone and suffer from premature aging. A great effort has therefore been made to understand the molecular mechanisms and the biological pathways, in which RecQ helicases are involved. It has become clear that these enzymes work in close concert with DNA topoisomerase III, and studies in both yeast and mammalian systems point to a role of the proteins in processes involving homologous recombination. In this review we discuss the genetic and biochemical evidence for possible functions of RecQ helicases and DNA topoisomerase III in multiple cellular processes such as DNA recombination, DNA replication, and cell cycle checkpoint control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ababou M, Dumaire V, Lecluse Y, and Amor-Gueret M (2002) Bloom's syndrome protein response to ultraviolet-C radiation and hydroxyurea-mediated DNA synthesis inhibition. Oncogene 21: 2079-2088

    PubMed  CAS  Google Scholar 

  • Beamish H, Kedar P, Kaneko H, Chen P, Fukao T, Peng C, Beresten S, Gueven N, Purdie D, Lees-Miller S, Ellis N, Kondo N and Lavin MF (2002) Functional link between BLM defective in Bloom's syndrome and the ataxia-telangiectasiamutated protein, ATM. J Biol Chem 277: 30515-30523

    PubMed  CAS  Google Scholar 

  • Bennett RJ, Sharp JA and Wang JC (1998) Purification and characterization of the Sgs1 DNA helicase activity of Saccharomyces cerevisiae. J Biol Chem 273: 9644-9650

    PubMed  CAS  Google Scholar 

  • Bennett RJ, Keck JL and Wang JC (1999) Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J Mol Biol 289: 235-248

    PubMed  CAS  Google Scholar 

  • Bennett RJ, Noirot-Gros MF and Wang JC (2000) Interaction between yeast sgs1 helicase and DNA topoisomerase III. J Biol Chem 275: 26898-26905

    PubMed  CAS  Google Scholar 

  • Blander G, Kipnis J, Leal JF, Yu CE, Schellenberg GD and Oren M (1999) Physical and functional interaction between p53 and the Werner's syndrome protein. J Biol Chem 274: 29463-29469

    PubMed  CAS  Google Scholar 

  • Boddy MN, Lopez-Girona A, Shanahan P, Interthal H, Heyer WD and Russell P (2000) Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol Cell Biol 20: 8758-8766

    PubMed  CAS  Google Scholar 

  • Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR, III and Russell P (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107: 537-548

    PubMed  CAS  Google Scholar 

  • Brosh Jr. RM, Li JL, Kenny MK, Karow JK, Cooper MP, Kureekattil RP, Hickson ID and Bohr VA (2000) Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J Biol Chem 275: 23500-23508

    PubMed  CAS  Google Scholar 

  • Brosh Jr. RM, Majumdar A, Desai S, Hickson ID, Bohr VA and Seidman MM (2001a) Unwinding of a DNA triple helix by the Werner and Bloom syndrome helicases. J Biol Chem 276: 3024-3030

    PubMed  CAS  Google Scholar 

  • Brosh Jr. RM, Orren DK, Nehlin JO, Ravn PH, Kenny MK, Machwe A and Bohr VA (1999) Functional and physical interaction between WRN helicase and human replication protein A. J Biol Chem 274: 18341-18350

    PubMed  CAS  Google Scholar 

  • Brosh Jr. RM, von Kobbe C, Sommers JA, Karmakar P, Opresko PL, Piotrowski J, Dianova I, Dianov GL and Bohr VA (2001b) Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. EMBO J 20: 5791-5801

    PubMed  CAS  Google Scholar 

  • Caspari T, Murray JM and Carr AM (2002) Cdc2-cyclin B kinase activity links Crb2 and Rqh1-topoisomerase III. Genes Dev 16: 1195-1208

    PubMed  CAS  Google Scholar 

  • Chakraverty RK and Hickson ID (1999) Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. Bioessays 21: 286-294

    PubMed  CAS  Google Scholar 

  • Chakraverty RK, Kearsey JM, Oakley TJ, Grenon M, de La Torre Ruiz MA, Lowndes NF and Hickson ID (2001) Topoisomerase III acts upstream of Rad53p in the S-phase DNA damage checkpoint. Mol Cell Biol 21: 7150-7162

    PubMed  CAS  Google Scholar 

  • Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70: 369-413

    PubMed  CAS  Google Scholar 

  • Chen CY, Graham J and Yan H (2001) Evidence for a replication function of FFA-1, the Xenopus orthologue of Werner syndrome protein. J Cell Biol 152: 985-996

    PubMed  CAS  Google Scholar 

  • Cho RJ, Campbell MJ, Winzeler EA, Steinmetz L, Conway A, Wodicka L, Wolfsberg TG, Gabrielian AE, Landsman D, Lockhart DJ and Davis RW (1998) A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 2: 65-73

    PubMed  CAS  Google Scholar 

  • Cohen H and Sinclair DA (2001) Recombination-mediated lengthening of terminal telomeric repeats requires the Sgs1 DNA helicase. Proc Natl Acad Sci USA 98: 3174-3179

    PubMed  CAS  Google Scholar 

  • Constantinou A, Tarsounas M, Karow JK, Brosh RM, Bohr VA, Hickson ID and West SC (2000) Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep 1: 80-84

    PubMed  CAS  Google Scholar 

  • Doe CL, Dixon J, Osman F and Whitby MC (2000) Partial suppression of the fission yeast rqh1(-) phenotype by expression of a bacterial Holliday junction resolvase. EMBO J 19: 2751-2762

    PubMed  CAS  Google Scholar 

  • Doe CL, Ahn JS, Dixon J and Whitby MC (2002) Mus81-eme1 and rqh1 involvement in processing stalled and collapsed replication forks. J Biol Chem 277: 32753-32759

    PubMed  CAS  Google Scholar 

  • Dutertre S, Ababou M, Onclercq R, Delic J, Chatton B, Jaulin C and Amor-Gueret M (2000) Cell cycle regulation of the endogenous wild type Bloom's syndrome DNA helicase. Oncogene 19: 2731-2738

    PubMed  CAS  Google Scholar 

  • Duvic M and Lemak NA (1995) Werner's syndrome. Dermatol Clin 13: 163-168

    PubMed  CAS  Google Scholar 

  • Ellis NA, Groden J, Ye TZ, Straughen J, Lennon DJ, Ciocci S, Proytcheva M and German J (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83: 655-666

    PubMed  CAS  Google Scholar 

  • Foiani M, Pellicioli A, Lopes M, Lucca C, Ferrari M, Liberi G, Muzi FM and Plevanil P (2000) DNA damage checkpoints and DNA replication controls in Saccharomyces cerevisiae. Mutat Res 451: 187-196

    PubMed  CAS  Google Scholar 

  • Franchitto A and Pichierri P (2002) Bloom's syndrome protein is required for correct relocalization of RAD50/MRE11/NBS1 complex after replication fork arrest. J Cell Biol 157: 19-30

    PubMed  CAS  Google Scholar 

  • Frei C and Gasser SM (2000) The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev 14: 81-96

    PubMed  CAS  Google Scholar 

  • Gangloff S, McDonald JP, Bendixen C, Arthur L and Rothstein R (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol 14: 8391-8398

    PubMed  CAS  Google Scholar 

  • Gangloff S, Soustelle C and Fabre F (2000) Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat Genet 25: 192-194

    PubMed  CAS  Google Scholar 

  • German J (1993) Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine (Baltimore) 72: 393-406

    CAS  Google Scholar 

  • German J (1995) Bloom's syndrome. Dermatol Clin 13: 7-18

    PubMed  CAS  Google Scholar 

  • Goodwin A, Wang SW, Toda T, Norbury C and Hickson ID (1999) Topoisomerase III is essential for accurate nuclear division in Schizosaccharomyces pombe. Nucleic Acids Res 27: 4050-4058

    PubMed  CAS  Google Scholar 

  • Goulaouic H, Roulon T, Flamand O, Grondard L, Lavelle F and Riou JF (1999) Purification and characterization of human DNA topoisomerase IIIalpha. Nucleic Acids Res 27: 2443-2450

    PubMed  CAS  Google Scholar 

  • Gray MD, Shen JC, Kamath-Loeb AS, Blank A, Sopher BL, Martin GM, Oshima J and Loeb LA (1997) The Werner syndrome protein is a DNA helicase. Nat Genet 17: 100-103

    PubMed  CAS  Google Scholar 

  • Haber JE (2000) Lucky breaks: analysis of recombination in Saccharomyces. Mutat Res 451: 53-69

    PubMed  CAS  Google Scholar 

  • Hand R and German J (1975) A retarded rate of DNA chain growth in Bloom's syndrome. Proc Natl Acad Sci USA 72: 758-762

    PubMed  CAS  Google Scholar 

  • Heo SJ, Tatebayashi K, Ohsugi I, Shimamoto A, Furuichi Y and Ikeda H (1999) Bloom's syndrome gene suppresses premature ageing caused by Sgs1 deficiency in yeast. Genes Cells 4: 619-625

    PubMed  CAS  Google Scholar 

  • Huang P, Pryde FE, Lester D, Maddison RL, Borts RH, Hickson ID and Louis EJ (2001) SGS1 is required for telomere elongation in the absence of telomerase. Curr Biol 11: 125-129

    PubMed  CAS  Google Scholar 

  • Johnson FB, Marciniak RA, McVey M, Stewart SA, Hahn WC and Guarente L (2001) The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J 20: 905-913

    PubMed  CAS  Google Scholar 

  • Kamath-Loeb AS, Shen JC, Loeb LA and Fry M (1998) Werner syndrome protein. II. Characterization of the integral 3′→5′ DNA exonuclease. J Biol Chem 273: 34145-34150

    PubMed  CAS  Google Scholar 

  • Kamath-Loeb AS, Johansson E, Burgers PM and Loeb LA (2000) Functional interaction between the Werner Syndrome protein and DNA polymerase delta. Proc Natl Acad Sci USA 97: 4603-4608

    PubMed  CAS  Google Scholar 

  • Karow JK, Chakraverty RK and Hickson ID (1997) The Bloom's syndrome gene product is a 3′-5′ DNA helicase. J Biol Chem 272: 30611-30614

    PubMed  CAS  Google Scholar 

  • Karow JK, Constantinou A, Li JL, West SC and Hickson ID (2000) The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc Natl Acad Sci USA 97: 6504-6508

    PubMed  CAS  Google Scholar 

  • Kim RA and Wang JC (1992) Identification of the yeast TOP3 gene product as a single strand-specific DNA topoisomerase. J Biol Chem 267: 17178-17185

    PubMed  CAS  Google Scholar 

  • Kitao S, Lindor NM, Shiratori M, Furuichi Y and Shimamoto A (1999a) Rothmund-thomson syndrome responsible gene, RECQL4: genomic structure and products. Genomics 61: 268-276

    PubMed  CAS  Google Scholar 

  • Kitao S, Shimamoto A, Goto M, Miller RW, Smithson WA, Lindor NM and Furuichi Y (1999b) Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat Genet 22: 82-84

    PubMed  CAS  Google Scholar 

  • Langland G, Elliott J, Li Y, Creaney J, Dixon K and Groden J (2002) The BLM helicase is necessary for normal DNA double-strand break repair. Cancer Res 62: 2766-2770

    PubMed  CAS  Google Scholar 

  • Laursen LV, Ampatzidou E, Andersen AH and Murray JM (2003) Role for the fission yeast RecQ helicase in DNA repair in G2. Mol Cell Biol 23: 3692-3705

    PubMed  CAS  Google Scholar 

  • Lebel M, Spillare EA, Harris CC and Leder P (1999) 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

    PubMed  CAS  Google Scholar 

  • Lee SK, Johnson RE, Yu SL, Prakash L and Prakash S (1999) Requirement of yeast SGS1 and SRS2 genes for replication and transcription. Science 286: 2339-2342

    PubMed  CAS  Google Scholar 

  • Li W and Wang JC (1998) Mammalian DNA topoisomerase IIIalpha is essential in early embryogenesis. Proc Natl Acad Sci USA 95: 1010-1013

    PubMed  CAS  Google Scholar 

  • Liao S, Graham J and Yan H (2000) The function of Xenopus Bloom's syndrome protein homolog (xBLM) in DNA replication. Genes Dev 14: 2570-2575

    PubMed  CAS  Google Scholar 

  • Lindsay HD, Griffiths DJ, Edwards RJ, Christensen PU, Murray JM, Osman F, Walworth N and Carr AM (1998) S-phase-specific activation of Cds1 kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe. Genes Dev 12: 382-395

    PubMed  CAS  Google Scholar 

  • Liu Z, Macias MJ, Bottomley MJ, Stier G, Linge JP, Nilges M, Bork P and Sattler M (1999) The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Structure Fold Des 7: 1557-1566

    PubMed  CAS  Google Scholar 

  • Lonn U, Lonn S, Nylen U, Winblad G and German J (1990) An abnormal profile of DNA replication intermediates in Bloom's syndrome. Cancer Res 50: 3141-3145

    PubMed  CAS  Google Scholar 

  • Maftahi M, Han CS, Langston LD, Hope JC, Zigouras N and Freyer GA (1999) The top3(+) gene is essential in Schizosaccharomyces pombe and the lethality associated with its loss is caused by Rad12 helicase activity. Nucleic Acids Res 27: 4715-4724

    PubMed  CAS  Google Scholar 

  • McGlynn P, Lloyd RG and Marians KJ (2001) Formation of Holliday junctions by regression of nascent DNA in intermediates containing stalled replication forks: RecG stimulates regression even when the DNA is negatively supercoiled. Proc Natl Acad Sci USA 98: 8235-8240

    PubMed  CAS  Google Scholar 

  • Michel B (2000) Replication fork arrest and DNA recombination. Trends Biochem Sci 25: 173-178

    PubMed  CAS  Google Scholar 

  • Milne GT, Ho T and Weaver DT (1995) Modulation of Saccharomyces cerevisiae DNA double-strand break repair by SRS2 and RAD51. Genetics 139: 1189-1199

    PubMed  CAS  Google Scholar 

  • Mohaghegh P, Karow JK, Brosh JR, Jr., Bohr VA and Hickson ID (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res 29: 2843-2849

    PubMed  CAS  Google Scholar 

  • Morozov V, Mushegian AR, Koonin EV and Bork P (1997) A putative nucleic acid-binding domain in Bloom's and Werner's syndrome helicases. Trends Biochem Sci 22: 417-418

    PubMed  CAS  Google Scholar 

  • Murray JM, Lindsay HD, Munday CA and Carr AM (1997) Role of Schizosaccharomyces pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance. Mol Cell Biol 17: 6868-6875

    PubMed  CAS  Google Scholar 

  • Nakayama H, Nakayama K, Nakayama R, Irino N, Nakayama Y and Hanawalt PC (1984) 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

    PubMed  CAS  Google Scholar 

  • Ng SW, Liu Y, Hasselblatt KT, Mok SC and Berkowitz RS (1999) A new human topoisomerase III that interacts with SGS1 protein. Nucleic Acids Res 27: 993-1000

    PubMed  CAS  Google Scholar 

  • Ogburn CE, Oshima J, Poot M, Chen R, Hunt KE, Gollahon KA, Rabinovitch PS and Martin GM (1997) An apoptosisinducing genotoxin differentiates heterozygotic carriers for Werner helicase mutations from wild-type and homozygous mutants. Hum Genet 101: 121-125

    PubMed  CAS  Google Scholar 

  • Okada M, Goto M, Furuichi Y and Sugimoto M (1998) Differential effects of cytotoxic drugs on mortal and immortalized B-lymphoblastoid cell lines from normal andWerner's syndrome patients. Biol Pharm Bull 21: 235-239

    PubMed  CAS  Google Scholar 

  • Opresko PL, von Kobbe C, Laine JP, Harrigan J, Hickson ID and Bohr VA (2002) Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J Biol Chem 277: 41110-41119

    PubMed  CAS  Google Scholar 

  • Paques F and Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404

    PubMed  CAS  Google Scholar 

  • Pichierri P, Franchitto A, Mosesso P and Palitti F (2001) Werner's syndrome protein is required for correct recovery after replication arrest and DNA damage induced in S-phase of cell cycle. Mol Biol Cell 12: 2412-2421

    PubMed  CAS  Google Scholar 

  • Poot M, Hoehn H, Runger TM and Martin GM (1992) Impaired S-phase transit of Werner syndrome cells expressed in lymphoblastoid cell lines. Exp Cell Res 202: 267-273

    PubMed  CAS  Google Scholar 

  • Poot M, Gollahon KA and Rabinovitch PS (1999) Werner syndrome lymphoblastoid cells are sensitive to camptothecin-induced apoptosis in S-phase. Hum Genet 104: 10-14

    PubMed  CAS  Google Scholar 

  • Poot M, Yom JS, Whang SH, Kato JT, Gollahon KA and Rabinovitch PS (2001) Werner syndrome cells are sensitive to DNA cross-linking drugs. FASEB J 15: 1224-1226

    PubMed  CAS  Google Scholar 

  • Postow L, Ullsperger C, Keller RW, Bustamante C, Vologodskii AV and Cozzarelli NR (2001) Positive torsional strain causes the formation of a four-way junction at replication forks. J Biol Chem 276: 2790-2796

    PubMed  CAS  Google Scholar 

  • Prince PR, Emond MJ and Monnat RJ, Jr. (2001) Loss of Werner syndrome protein function promotes aberrant mitotic recombination. Genes Dev 15: 933-938

    PubMed  CAS  Google Scholar 

  • Robu ME, Inman RB and Cox MM (2001) RecA protein promotes the regression of stalled replication forks in vitro. Proc Natl Acad Sci USA 98: 8211-8218

    PubMed  CAS  Google Scholar 

  • Rong L and Klein HL (1993) Purification and characterization of the SRS2 DNA helicase of the yeast Saccharomyces cerevisiae. J Biol Chem 268: 1252-1259

    PubMed  CAS  Google Scholar 

  • Saffi J, Pereira VR and Henriques JA (2000) Importance of the Sgs1 helicase activity in DNA repair of Saccharomyces cerevisiae. Curr Genet 37: 75-78

    PubMed  CAS  Google Scholar 

  • Saintigny Y, Makienko K, Swanson C, Emond MJ and Monnat JR, Jr. (2002) Homologous recombination resolution defect in werner syndrome. Mol Cell Biol 22: 6971-6978

    PubMed  CAS  Google Scholar 

  • Sakamoto S, Nishikawa K, Heo SJ, Goto M, Furuichi Y and Shimamoto A (2001) Werner helicase relocates into nuclear foci in response to DNA damaging agents and co-localizes with RPA and Rad51. Genes Cells 6: 421-430

    PubMed  CAS  Google Scholar 

  • Shen JC, Gray MD, Oshima J, Kamath-Loeb AS, Fry M and Loeb LA (1998) Werner syndrome protein. I. DNA helicase and dna exonuclease reside on the same polypeptide. J Biol Chem 273: 34139-34144

    PubMed  CAS  Google Scholar 

  • Shimamoto A, Nishikawa K, Kitao S and Furuichi Y (2000) Human RecQ5beta, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with topoisomerases 3alpha and 3beta. Nucleic Acids Res 28: 1647-1655

    PubMed  CAS  Google Scholar 

  • Sinclair DA and Guarente L (1997) Extrachromosomal rDNA circles - a cause of aging in yeast. Cell 91: 1033-1042

    PubMed  CAS  Google Scholar 

  • Sinclair DA, Mills K and Guarente L (1997) Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science 277: 1313-1316

    PubMed  CAS  Google Scholar 

  • Spillare EA, Robles AI, Wang XW, Shen JC, Yu CE, Schellenberg GD and Harris CC (1999) p53-mediated apoptosis is attenuated in Werner syndrome cells. Genes Dev 13: 1355-1360

    PubMed  CAS  Google Scholar 

  • Stewart E, Chapman CR, Al Khodairy F, Carr AM and Enoch T (1997) rqh1+, a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J 16: 2682-2692

    PubMed  CAS  Google Scholar 

  • Sun H, Karow JK, Hickson ID and Maizels N (1998) The Bloom's syndrome helicase unwinds G4 DNA. J Biol Chem 273: 27587-27592

    PubMed  CAS  Google Scholar 

  • Sun H, Bennett RJ and Maizels N (1999) The Saccharomyces cerevisiae Sgs1 helicase efficiently unwinds G-G paired DNAs. Nucleic Acids Res 27: 1978-1984

    PubMed  CAS  Google Scholar 

  • Suzuki N, Shimamoto A, Imamura O, Kuromitsu J, Kitao S, Goto M and Furuichi Y (1997) DNA helicase activity in Werner's syndrome gene product synthesized in a baculovirus system. Nucleic Acids Res 25: 2973-2978

    PubMed  CAS  Google Scholar 

  • Tahara H, Tokutake Y, Maeda S, Kataoka H, Watanabe T, Satoh M, Matsumoto T, Sugawara M, Ide T, Goto M, Furuichi Y and Sugimoto M (1997) Abnormal telomere dynamics of Blymphoblastoid cell strains from Werner's syndrome patients transformed by Epstein-Barr virus. Oncogene 15: 1911-1920

    PubMed  CAS  Google Scholar 

  • Takeuchi F, Hanaoka F, Goto M, Akaoka I, Hori T, Yamada M and Miyamoto T (1982) Altered frequency of initiation sites of DNA replication in Werner's syndrome cells. Hum Genet 60: 365-368

    PubMed  CAS  Google Scholar 

  • Vennos EM and James WD (1995) Rothmund-Thomson syndrome. Dermatol Clin 13: 143-150

    PubMed  CAS  Google Scholar 

  • Wallis JW, Chrebet G, Brodsky G, Rolfe M and Rothstein R (1989) A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58: 409-419

    PubMed  CAS  Google Scholar 

  • Wang JC (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3: 430-440

    PubMed  CAS  Google Scholar 

  • Wang XW, Tseng A, Ellis NA, Spillare EA, Linke SP, Robles AI, Seker H, Yang Q, Hu P, Beresten S, Bemmels NA, Garfield S and Harris CC (2001) Functional interaction of p53 and BLM DNA helicase in apoptosis. J Biol Chem 276: 32948-32955

    PubMed  CAS  Google Scholar 

  • Wang Y, Cortez D, Yazdi P, Neff N, Elledge SJ and Qin J (2000) BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev 14: 927-939

    PubMed  CAS  Google Scholar 

  • Watt PM, Hickson ID, Borts RH and Louis EJ (1996) SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144: 935-945

    PubMed  CAS  Google Scholar 

  • Wu L, Davies SL, North PS, Goulaouic H, Riou JF, Turley H, Gatter KC and Hickson ID (2000) The Bloom's syndrome gene product interacts with topoisomerase III. J Biol Chem 275: 9636-9644

    PubMed  CAS  Google Scholar 

  • Wu L, Davies SL, Levitt NC and Hickson ID (2001) Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J Biol Chem 276: 19375-19381

    PubMed  CAS  Google Scholar 

  • Yamagata K, Kato J, Shimamoto A, Goto M, Furuichi Y and Ikeda H (1998) Bloom's andWerner's syndrome genes suppress hyperrecombination in yeast sgs1 mutant: implication for genomic instability in human diseases. Proc Natl Acad Sci USA 95: 8733-8738

    PubMed  CAS  Google Scholar 

  • Yan H, Chen CY, Kobayashi R and Newport J (1998) Replication focus-forming activity 1 and theWerner syndrome gene product. Nat Genet 19: 375-378

    PubMed  CAS  Google Scholar 

  • Yu CE, Oshima J, Fu YH, Wijsman EM, Hisama F, Alisch R, Matthews S, Nakura J, Miki T, Ouais S, Martin GM, Mulligan J and Schellenberg GD (1996) Positional cloning of the Werner's syndrome gene. Science 272: 258-262

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anni H. Andersen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laursen, L.V., Bjergbaek, L., Murray, J.M. et al. RecQ helicases and topoisomerase III in cancer and aging. Biogerontology 4, 275–287 (2003). https://doi.org/10.1023/A:1026218513772

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026218513772

Navigation