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Review Article

The role of RecQ helicases in non-homologous end-joining

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Pages 463-472 | Received 17 May 2014, Accepted 03 Jul 2014, Published online: 22 Jul 2014

References

  • Ahnesorg P, Smith P, Jackson SP. (2006). XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 124:301–13
  • Aygün O, Svejstrup J, Liu Y. (2008). A RECQ5-RNA polymerase II association identified by targeted proteomic analysis of human chromatin. Proc Natl Acad Sci USA 105:8580–4
  • Aygün O, Xu X, Liu Y, et al. (2009). Direct inhibition of RNA polymerase II transcription by RECQL5. J Biol Chem 284:23197–203
  • Babbe H, McMenamin J, Hobeika E, et al. (2009). Genomic instability resulting from Blm deficiency compromises development, maintenance, and function of the B cell lineage. J Immunol 182:347–60
  • Baynton K, Otterlei M, Bjørås M, et al. (2003). WRN interacts physically and functionally with the recombination mediator protein RAD52. J Biol Chem 278:36476–86
  • Bechter OE, Zou Y, Walker W, et al. (2004). Telomeric recombination in mismatch repair deficient human colon cancer cells after telomerase inhibition. Cancer Res 64:3444–51
  • Bernstein DA, Keck JL. (2003). Domain mapping of Escherichia coli RecQ defines the roles of conserved N- and C-terminal regions in the RecQ family. Nucleic Acids Res 31:2778–85
  • Berti M, Ray Chaudhuri A, Thangavel S, et al. (2013). Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nat Struct Mol Biol 20:347–54
  • Bione S, Maestrini E, Rivella S, et al. (1994). Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet 8:323–27
  • Blander G, Kipnis J, Leal JF, et al. (1999). Physical and functional interaction between p53 and the Werner’s syndrome protein. J Biol Chem 274:29463–9
  • Blasco MA. (2005). Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 6:611–22
  • Boboila C, Yan C, Wesemann DR, et al. (2010). Alternative end-joining catalyzes class switch recombination in the absence of both Ku70 and DNA ligase 4. J Exp Med 207:417–27
  • Bohr VA. (2008). Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem Sci 33:609–20
  • Bothmer A, Rommel PC, Gazumyan A, et al. (2013). Mechanism of DNA resection during intrachromosomal recombination and immunoglobulin class switching. J Exp Med 210:115–23
  • Branzei D, Foiani M. (2007). RecQ helicases queuing with Srs2 to disrupt Rad51 filaments and suppress recombination. Genes Dev 21:3019–26
  • Brosh RM. (2013). DNA helicases involved in DNA repair and their roles in cancer. Nat Rev Cancer 13:542–58
  • Brosh RM, Li JL, Kenny MK, et al. (2000). Replication protein A physically interacts with the Bloom’s syndrome protein and stimulates its helicase activity. J Biol Chem 275:23500–8
  • Brosh RM, Majumdar A, Desai S, et al. (2001). Unwinding of a DNA triple helix by the Werner and Bloom syndrome helicases. J Biol Chem 276:3024–30
  • Brosh RM, Orren DK, Nehlin JO, et al. (1999). Functional and physical interaction between WRN helicase and human replication protein A. J Biol Chem 274:18341–50
  • Capp C, Wu J, Hsieh T-S. (2009). Drosophila RecQ4 has a 3″–5″ DNA helicase activity that is essential for viability. J Biol Chem 284:30845–52
  • Chan SH, Yu AM, McVey M. (2010). Dual roles for DNA polymerase theta in alternative end-joining repair of double-strand breaks in Drosophila. PLoS Genet 6:e1001005
  • Chen L, Huang S, Lee L, et al. (2003a). WRN, the protein deficient in Werner syndrome, plays a critical structural role in optimizing DNA repair. Aging Cell 2:191–9
  • Chen L, Lee L, Kudlow BA, et al. (2003b). LMNA mutations in atypical Werner’s syndrome. Lancet 362:440–5
  • Cheng W-H, von Kobbe C, Opresko PL, et al. (2004). Linkage between Werner syndrome protein and the Mre11 complex via Nbs1. J Biol Chem 279:21169–76
  • Collart C, Allen GE, Bradshaw CR, et al. (2013). Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 341:893–6
  • Cooper MP, Machwe A, Orren DK, et al. (2000). Ku complex interacts with and stimulates the Werner protein. Genes Dev 14:907–12
  • Crespan E, Czabany T, Maga G, Hübscher U. (2012). Microhomology-mediated DNA strand annealing and elongation by human DNA polymerases λ and β on normal and repetitive DNA sequences. Nucleic Acids Res 40:5577–90
  • Croteau DL, Popuri V, Opresko PL, Bohr VA. (2014). Human RecQ helicases in DNA repair, recombination, and replication. Annu Rev Biochem 83:519–52
  • Croteau DL, Singh DK, Hoh Ferrarelli L, et al. (2012). RECQL4 in genomic instability and aging. Trends Genet 28:624–31
  • Cui S, Arosio D, Doherty KM, et al. (2004). Analysis of the unwinding activity of the dimeric RECQ1 helicase in the presence of human replication protein A. Nucleic Acids Res 32:2158–70
  • Cui S, Klima R, Ochem A, et al. (2003). Characterization of the DNA-unwinding activity of human RECQ1, a helicase specifically stimulated by human replication protein A. J Biol Chem 278:1424–32
  • Davalos AR, Campisi J. (2003). Bloom syndrome cells undergo p53-dependent apoptosis and delayed assembly of BRCA1 and NBS1 repair complexes at stalled replication forks. J Biol Chem 162:1197–209
  • De Sandre-Giovannoli A, Bernard R, Cau P, et al. (2003). Lamin a truncation in Hutchinson-Gilford progeria. Science 300:2055
  • Difilippantonio MJ, Zhu J, Chen HT, et al. (2000). DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 404:510–14
  • Ding Q, Reddy YVR, Wang W, et al. (2003). Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol Cell Biol 23:5836–48
  • Ding S-L, Yu J-C, Chen S-T, et al. (2009). Genetic variants of BLM interact with RAD51 to increase breast cancer susceptibility. Carcinogenesis 30:43–9
  • Durante M, Bedford JS, Chen DJ, et al. (2013). From DNA damage to chromosome aberrations: joining the break. Mut Res 756:5–13
  • Enokido Y, Tamura T, Ito H, et al. (2010). Mutant huntingtin impairs Ku70-mediated DNA repair. J Cell Biol 189:425–43
  • Espejel S, Franco S, Rodríguez-Perales S, et al. (2002). Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. EMBO J 21:2207–19
  • Fan W, Luo J. (2008). RecQ4 facilitates UV light-induced DNA damage repair through interaction with nucleotide excision repair factor xeroderma pigmentosum group A (XPA). J Biol Chem 283:29037–44
  • Fattah F, Lee EH, Weisensel N, et al. (2010). Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet 6:e1000855
  • Ferguson DO, Sekiguchi JM, Chang S, et al. (2000). The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc Natl Acad Sci USA 97:6630–3
  • Franchitto A, 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
  • Freire R, d’Adda Di Fagagna F, Wu L, et al. (2001). Cleavage of the Bloom’s syndrome gene product during apoptosis by caspase-3 results in an impaired interaction with topoisomerase III alpha. Nucleic Acids Res 29:3172–80
  • Garcia PL, Liu Y, Jiricny J, et al. (2004). Human RECQ5beta, a protein with DNA helicase and strand-annealing activities in a single polypeptide. EMBO J 23:2882–91
  • Gellert M. (2002). V(D)J recombination: RAG proteins, repair factors, and regulation. Annu Rev Biochem 71:101–32
  • Ghosh A, Rossi ML, Aulds J, et al. (2009). Telomeric D-loops containing 8-oxo-2′-deoxyguanosine are preferred substrates for Werner and Bloom syndrome helicases and are bound by POT1. J Biol Chem 284:31074–84
  • Ghosh AK, Rossi ML, Singh DK, et al. (2012). RECQL4, the protein mutated in Rothmund-Thomson syndrome, functions in telomere maintenance. J Biol Chem 287:196–209
  • Gomez M, Wu J, Schreiber V, et al. (2006). PARP1 Is a TRF2-associated poly(ADP-ribose)polymerase and protects eroded telomeres. Mol Biol Cell 17:1686–96
  • Grabarz A, Guirouilh-Barbat J, Barascu A, et al. (2013). A role for BLM in double-strand break repair pathway choice: prevention of CtIP/Mre11-mediated alternative nonhomologous end-joining. Cell Rep 5:21–8
  • Gu Y, Seidl KJ, Rathbun GA, et al. (1997). Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity 7:653–65
  • Guo R-B, Rigolet P, Ren H, et al. (2007). Structural and functional analyses of disease-causing missense mutations in Bloom syndrome protein. Nucleic Acids Res 35:6297–310
  • Helleday T, Lo J, van Gent DC, Engelward BP. (2007). DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst.) 6:923–35
  • Hogg M, Sauer-Eriksson AE, Johansson E. (2012). Promiscuous DNA synthesis by human DNA polymerase θ. Nucleic Acids Res 40:2611–22
  • Hu Y, Lu X, Barnes E, et al. (2005). Recql5 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers. Mol Cell Biol 25:3431–42
  • Hu Y, Lu X, Zhou G, et al. (2009). Recql5 plays an important role in DNA replication and cell survival after camptothecin treatment. Mol Biol Cell 20:114–23
  • Indig FE, Rybanska I, Karmakar P, et al. (2012). Nucleolin inhibits G4 oligonucleotide unwinding by Werner helicase. PLoS One 7:e35229
  • Indiviglio SM, Bertuch AA. (2009). Ku’s essential role in keeping telomeres intact. Proc Natl Acad Sci USA 106:12217–18
  • Izumikawa K, Yanagida M, Hayano T, et al. (2008). Association of human DNA helicase RecQ5beta with RNA polymerase II and its possible role in transcription. Biochem J 413:505–16
  • Jeppesen DK, Bohr VA, Stevnsner T. (2011). DNA repair deficiency in neurodegeneration. Prog Neurobiol 94:166–200
  • Kamranvar SA, Chen X, Masucci MG. (2013). Telomere dysfunction and activation of alternative lengthening of telomeres in B-lymphocytes infected by Epstein-Barr virus. Oncogene 32:5522–30
  • Karmakar P, Piotrowski J, Brosh RM, et al. (2002a). 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 277:18291–302
  • Karmakar P, Snowden CM, Ramsden DA, Bohr VA. (2002b). Ku heterodimer binds to both ends of the Werner protein and functional interaction occurs at the Werner N-terminus. Nucleic Acids Res 30:3583–91
  • Kassube SA, Jinek M, Fang J, et al. (2013). Structural mimicry in transcription regulation of human RNA polymerase II by the DNA helicase RECQL5. Nat Struct Mol Biol 20:892–9
  • Kawabe T, Tsuyama N, Kitao S, et al. (2000). Differential regulation of human RecQ family helicases in cell transformation and cell cycle. Oncogene 19:4764–72
  • Kitao S, Lindor NM, Shiratori M, et al. (1999). Rothmund-Thomson syndrome responsible gene, RECQL4: genomic structure and products. Genomics 61:268–76
  • Kitao S, Ohsugi I, Ichikawa K, et al. (1998). Cloning of two new human helicase genes of the RecQ family: biological significance of multiple species in higher eukaryotes. Genomics 54:443–52
  • Kotnis A, Du L, Liu C, et al. (2009). Non-homologous end joining in class switch recombination: the beginning of the end. Philos Trans R Soc Lond B Biol Sci 364:653–65
  • Kumata Y, Tada S, Yamanada Y, et al. (2007). Possible involvement of RecQL4 in the repair of double-strand DNA breaks in Xenopus egg extracts. Biochim Biophys Acta 1773:556–64
  • Kusumoto R, Dawut L, Marchetti C, et al. (2008). Werner protein cooperates with the XRCC4-DNA ligase IV complex in end-processing. Biochemistry 47:7548–56
  • Kusumoto-Matsuo R, Ghosh D, Karmakar P, et al. (2014). Serines 440 and 467 in the Werner syndrome protein are phosphorylated by DNA-PK and affects its dynamics in response to DNA double strand breaks. Aging (Albany NY) 6:70–81
  • Kusumoto-Matsuo R, Opresko PL, Ramsden D, et al. (2010). Cooperation of DNA-PKcs and WRN helicase in the maintenance of telomeric D-loops. Aging (Albany NY) 2:274–84
  • Larizza L, Roversi G, Volpi L. (2010). Rothmund-Thomson syndrome. Orphanet J Rare Dis 5:2
  • Lee-Theilen M, Matthews AJ, Kelly D, et al. (2011). CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nat Struct Mol Biol 18:75–9
  • Li B, Comai L. (2001). Requirements for the nucleolytic processing of DNA ends by the Werner syndrome protein-Ku70/80 complex. J Biol Chem 276:9896–902
  • Ma J-L, Kim EM, Haber JE, Lee SE. (2003). Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol Cell Biol 23:8820–8
  • Ma Y, Pannicke U, Schwarz K, Lieber MR. (2002). Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108:781–94
  • Macris MA, Krejci L, Bussen W, et al. (2006). Biochemical characterization of the RECQ4 protein, mutated in Rothmund-Thomson syndrome. DNA Repair (Amst.) 5:172–80
  • Malu S, De Ioannes P, Kozlov M, et al. (2012). Artemis C-terminal region facilitates V(D)J recombination through its interactions with DNA Ligase IV and DNA-PKcs. J Exp Med 209:955–63
  • Mansour WY, Rhein T, Dahm-Daphi J. (2010). The alternative end-joining pathway for repair of DNA double-strand breaks requires PARP1 but is not dependent upon microhomologies. Nucleic Acids Res 38:6065–77
  • Marciniak RA, Lombard DB, Johnson FB, Guarente L. (1998). Nucleolar localization of the Werner syndrome protein in human cells. Proc Natl Acad Sci USA 95:6887–92
  • Mari P-O, Florea BI, Persengiev SP, et al. (2006). Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc Natl Acad Sci USA 103:18597–602
  • Maynard S, Keijzers G, Hansen A-M, et al. (2014). Associations of subjective vitality with DNA damage, cardiovascular risk factors and physical performance. Acta Physiol (Oxf). [Epub ahead of print]. doi:10.1111/apha.12296
  • Maynard S, Schurman SH, Harboe C, et al. (2009). Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 30:2–10
  • McVey M, Lee SE. (2008). MMEJ repair of double-strand breaks (director’s cut): deleted sequences and alternative endings. Trends Genet 24:529–38
  • Mendez-Bermudez A, Hidalgo-Bravo A, Cotton VE, et al. (2012). The roles of WRN and BLM RecQ helicases in the alternative lengthening of telomeres. Nucleic Acids Res 40:10809–20
  • Mohaghegh P, Karow JK, Brosh RM, et al. (2001). The Bloom’s and Werner’s syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res 29:2843–9
  • Møllersen L, Rowe AD, Larsen E, et al. (2010). Continuous and periodic expansion of CAG repeats in Huntington’s disease R6/1 mice. PLoS Genet 6:e1001242
  • Navarro CL, De Sandre-Giovannoli A, Bernard R, et al. (2004). Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum Mol Genet 13:2493–503
  • Nick McElhinny SA, Havener JM, Garcia-Diaz M, et al. (2005). A gradient of template dependence defines distinct biological roles for family X polymerases in nonhomologous end joining. Mol Cell 19:357–66
  • Nimonkar AV, Genschel J, Kinoshita E, et al. (2011). BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev 25:350–62
  • Nimonkar AV, Ozsoy AZ, Genschel J, et al. (2008). Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc Natl Acad Sci USA 105:16906–11
  • Nussenzweig A, Chen C, da Costa Soares V, et al. (1996). Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382:551–5
  • Nussenzweig A, Nussenzweig MC. (2007). A backup DNA repair pathway moves to the forefront. Cell 131:223–5
  • Nussenzweig A, Sokol K, Burgman P, et al. (1997). Hypersensitivity of Ku80-deficient cell lines and mice to DNA damage: the effects of ionizing radiation on growth, survival, and development. Proc Natl Acad Sci USA 94:13588–93
  • O’Sullivan RJ, Arnoult N, Lackner DH, et al. (2014). Rapid induction of alternative lengthening of telomeres by depletion of the histone chaperone ASF1. Nat Struct Mol Biol 21:167–74
  • Opresko PL, Otterlei M, Graakjaer J, et al. (2004). The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mol Cell 14:763–74
  • Opresko PL, von Kobbe C, Laine J-P, et al. (2002). Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J Biol Chem 277:41110–19
  • Ouyang H, Nussenzweig A, Kurimasa A, et al. (1997). Ku70 is required for DNA repair but not for T cell antigen receptor gene recombination in vivo. J Exp Med 186:921–9
  • Owen BAL, Yang Z, Lai M, et al. (2005). (CAG)(n)-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition. Nat Struct Mol Biol 12:663–70
  • Paeschke K, McDonald KR, Zakian VA. (2010). Telomeres: structures in need of unwinding. FEBS Lett 584:3760–72
  • Pagon RA, Adam MP, Bird TD, et al. (1993). Bloom’s syndrome. Seattle, WA: University of Washington
  • Parsons JL, Dianova II, Allinson SL, Dianov GL. (2005). Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. FEBS J 272:2012–21
  • Parvathaneni S, Stortchevoi A, Sommers JA, et al. (2013). Human RECQ1 interacts with Ku70/80 and modulates DNA end-joining of double-strand breaks. PLoS One 8:e62481
  • Paul K, Wang M, Mladenov E, et al. (2013). DNA ligases I and III cooperate in alternative non-homologous end-joining in vertebrates. PLoS One 8:e59505
  • Paull TT, Gellert M. (1998). The 3″ to 5″ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol Cell 1:969–79
  • Petkovic M, Dietschy T, Freire R, et al. (2005). The human Rothmund-Thomson syndrome gene product, RECQL4, localizes to distinct nuclear foci that coincide with proteins involved in the maintenance of genome stability. J Cell Sci 118:4261–9
  • Popuri V, Bachrati CZ, Muzzolini L, et al. (2008). The human RecQ helicases, BLM and RECQ1, display distinct DNA substrate specificities. J Biol Chem 283:17766–76
  • Popuri V, Croteau DL, Brosh RM, Bohr VA. (2012a). RECQ1 is required for cellular resistance to replication stress and catalyzes strand exchange on stalled replication fork structures. Cell Cycle 11:4252–65
  • Popuri V, Ramamoorthy M, Tadokoro T, et al. (2012b). Recruitment and retention dynamics of RECQL5 at DNA double strand break sites. DNA Repair (Amst.) 11:624–35
  • Popuri V, Tadokoro T, Croteau DL, Bohr VA. (2013). Human RECQL5: guarding the crossroads of DNA replication and transcription and providing backup capability. Crit Rev Biochem Mol Biol 48:289–99
  • Rai R, Zheng H, He H, et al. (2010). The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J 29:2598–610
  • Ramamoorthy M, May A, Tadokoro T, et al. (2013). The RecQ helicase RECQL5 participates in psoralen-induced interstrand cross-link repair. Carcinogenesis 34:2218–30
  • Reddy YVR, Ding Q, Lees-Miller SP, et al. (2004). Non-homologous end joining requires that the DNA-PK complex undergo an autophosphorylation-dependent rearrangement at DNA ends. J Biol Chem 279:39408–13
  • Ren H, Dou S-X, Zhang X-D, et al. (2008). The zinc-binding motif of human RECQ5beta suppresses the intrinsic strand-annealing activity of its DExH helicase domain and is essential for the helicase activity of the enzyme. Biochem J 412:425–33
  • Reynolds P, Anderson JA, Harper JV, et al. (2012). The dynamics of Ku70/80 and DNA-PKcs at DSBs induced by ionizing radiation is dependent on the complexity of damage. Nucleic Acids Res 40:10821–31
  • Riballo E, Woodbine L, Stiff T, et al. (2009). XLF-Cernunnos promotes DNA ligase IV-XRCC4 re-adenylation following ligation. Nucleic Acids Res 37:482–92
  • Rong SB, Väliaho J, Vihinen M. (2000). Structural basis of Bloom syndrome (BS) causing mutations in the BLM helicase domain. Mol Med 6:155–64
  • Rossi ML, Ghosh AK, Kulikowicz T, et al. (2010). Conserved helicase domain of human RecQ4 is required for strand annealing-independent DNA unwinding. DNA Repair (Amst.) 9:796–804
  • Rothkamm K, Löbrich M. (2003). Evidence for a lack of DNA double-strand break repair in human cells exposed to very low X-ray doses. Proc Natl Acad Sci USA 100:5057–62
  • Sallmyr A, Tomkinson AE, Rassool FV. (2008). Up-regulation of WRN and DNA ligase IIIalpha in chronic myeloid leukemia: consequences for the repair of DNA double-strand breaks. Blood 112:1413–23
  • Sanz MM, Proytcheva M, Ellis NA, et al. (2000). 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 91:217–23
  • Saponaro M, Kantidakis T, Mitter R, et al. (2014). RECQL5 controls transcript elongation and suppresses genome instability associated with transcription stress. Cell 157:1037–49
  • Sattler M, Verma S, Shrikhande G, et al. (2000). The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J Biol Chem 275:24273–8
  • Schurman SH, Hedayati M, Wang Z, et al. (2009). Direct and indirect roles of RECQL4 in modulating base excision repair capacity. Hum Mol Genet 18:3470–83
  • Schwendener S, Raynard S, Paliwal S, et al. (2010). Physical interaction of RECQ5 helicase with RAD51 facilitates its anti-recombinase activity. J Biol Chem 285:15739–45
  • Sengupta S, Linke SP, Pedeux R, et al. (2003). BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J 22:1210–22
  • Sengupta S, Robles AI, Linke SP, et al. (2004). Functional interaction between BLM helicase and 53BP1 in a Chk1-mediated pathway during S-phase arrest. J Cell Biol 166:801–13
  • Sfeir A, de Lange T. (2012). Removal of shelterin reveals the telomere end-protection problem. Science 336:593–7
  • Sharma S, Brosh RM. (2007). Human RECQ1 is a DNA damage responsive protein required for genotoxic stress resistance and suppression of sister chromatid exchanges. PLoS One 2:e1297
  • Sharma S, Phatak P, Stortchevoi A, et al. (2012). RECQ1 plays a distinct role in cellular response to oxidative DNA damage. DNA Repair (Amst.) 11:537–49
  • Shen JC, Gray MD, Oshima J, Loeb LA. (1998). Characterization of Werner syndrome protein DNA helicase activity: directionality, substrate dependence and stimulation by replication protein A. Nucleic Acids Res 26:2879–85
  • Siitonen HA, Sotkasiira J, Biervliet M, et al. (2009). The mutation spectrum in RECQL4 diseases. Eur J Hum Genet 17:151–8
  • Simsek D, Brunet E, Wong SY-W, et al. (2011). DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet 7:e1002080
  • Simsek D, Jasin M. (2010). Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat Struct Mol Biol 17:410–16
  • Singh DK, Ahn B, Bohr VA. (2009). Roles of RECQ helicases in recombination based DNA repair, genomic stability and aging. Biogerontology 10:235–52
  • Singh DK, Karmakar P, Aamann M, et al. (2010). The involvement of human RECQL4 in DNA double-strand break repair. Aging Cell 9:358–71
  • Singh DK, Popuri V, Kulikowicz T, et al. (2012). The human RecQ helicases BLM and RECQL4 cooperate to preserve genome stability. Nucleic Acids Res 40:6632–48
  • Slupianek A, Poplawski T, Jozwiakowski SK, et al. (2011). BCR/ABL stimulates WRN to promote survival and genomic instability. Cancer Res 71:842–51
  • So S, Adachi N, Lieber MR, Koyama H. (2004). Genetic interactions between BLM and DNA ligase IV in human cells. J Biol Chem 279:55433–42
  • Stavnezer J, Guikema JEJ, Schrader CE. (2008). Mechanism and regulation of class switch recombination. Annu Rev Immunol 26:261–92
  • Sykora P, Yang J-L, Ferrarelli LK, et al. (2013). Modulation of DNA base excision repair during neuronal differentiation. Neurobiol Aging 34:1717–27
  • Szekely AM, Bleichert F, Nümann A, et al. (2005). Werner protein protects nonproliferating cells from oxidative DNA damage. Mol Cell Biol 25:10492–506
  • Tadokoro T, Ramamoorthy M, Popuri V, et al. (2012). Human RECQL5 participates in the removal of endogenous DNA damage. Mol Biol Cell 23:4273–85
  • Tamura T, Sone M, Iwatsubo T, et al. (2011). Ku70 alleviates neurodegeneration in Drosophila models of Huntington’s disease. PLoS One 6:e27408
  • Thangavel S, Mendoza-Maldonado R, Tissino E, et al. (2010). Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol Cell Biol 30:1382–96
  • Tripathi V, Kaur S, Sengupta S. (2008). Phosphorylation-dependent interactions of BLM and 53BP1 are required for their anti-recombinogenic roles during homologous recombination. Carcinogenesis 29:52–61
  • Truong LN, Li Y, Shi LZ, et al. (2013). Microhomology-mediated end joining and homologous recombination share the initial end resection step to repair DNA double-strand breaks in mammalian cells. Proc Natl Acad Sci USA 110:7720–5
  • van der Burg M, Ijspeert H, Verkaik NS, et al. (2009). A DNA-PKcs mutation in a radiosensitive T-B- SCID patient inhibits Artemis activation and nonhomologous end-joining. J Clin Invest 119:91–8
  • von Kobbe C, Harrigan JA, May A, et al. (2003). Central role for the Werner syndrome protein/poly(ADP-ribose) polymerase 1 complex in the poly(ADP-ribosyl)ation pathway after DNA damage. Mol Cell Biol 23:8601–13
  • von Kobbe C, Harrigan JA, Schreiber V, et al. (2004a). Poly(ADP-ribose) polymerase 1 regulates both the exonuclease and helicase activities of the Werner syndrome protein. Nucleic Acids Res 32:4003–14
  • von Kobbe C, Karmakar P, Dawut L, et al. (2002). Colocalization, physical, and functional interaction between Werner and Bloom syndrome proteins. J Biol Chem 277:22035–44
  • von Kobbe C, May A, Grandori C, Bohr VA. (2004b). Werner syndrome cells escape hydrogen peroxide-induced cell proliferation arrest. FASEB J 18:1970–2
  • Walker JR, Corpina RA, Goldberg J. (2001). Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 412:607–14
  • Wang H, Perrault AR, Takeda Y, et al. (2003a). Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res 31:5377–88
  • Wang LL, Gannavarapu A, Kozinetz CA, et al. (2003b). Association between osteosarcoma and deleterious mutations in the RECQL4 gene in Rothmund-Thomson syndrome. J Natl Cancer Inst 95:669–74
  • Wang W, Bambara RA. (2005). Human Bloom protein stimulates flap endonuclease 1 activity by resolving DNA secondary structure. J Biol Chem 280:5391–9
  • Wang XW, Tseng A, Ellis NA, et al. (2001). Functional interaction of p53 and BLM DNA helicase in apoptosis. J Biol Chem 276:32948–55
  • Wang Y, Cortez D, Yazdi P, et al. (2000). BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev 14:927–39
  • Weeda G, Eveno E, Donker I, et al. (1997). A mutation in the XPB/ERCC3 DNA repair transcription gene, associated with trichothiodystrophy. Am J Hum Genet 60:320–9
  • Weissman L, Jo D-G, Sørensen MM, et al. (2007). Defective DNA base excision repair in brain from individuals with Alzheimer’s disease and amnestic mild cognitive impairment. Nucleic Acids Res 35:5545–55
  • Werner SR, Prahalad AK, Yang J, Hock JM. (2006). RECQL4-deficient cells are hypersensitive to oxidative stress/damage: Insights for osteosarcoma prevalence and heterogeneity in Rothmund-Thomson syndrome. Biochem Biophys Res Commun 345:403–9
  • Weterings E, Chen DJ. (2007). DNA-dependent protein kinase in nonhomologous end joining: a lock with multiple keys? J Cell Biol 179:183–6
  • Weterings E, Verkaik NS, Brüggenwirth HT, et al. (2003). The role of DNA dependent protein kinase in synapsis of DNA ends. Nucleic Acids Res 31:7238–46
  • Weterings E, Verkaik NS, Keijzers G, et al. (2009). The Ku80 carboxy terminus stimulates joining and artemis-mediated processing of DNA ends. Mol Cell Biol 29:1134–42
  • Wheeler VC, Lebel L-A, Vrbanac V, et al. (2003). Mismatch repair gene Msh2 modifies the timing of early disease in Hdh(Q111) striatum. Hum Mol Genet 12:273–81
  • Wilson DM, Bohr VA, McKinnon PJ. (2008). DNA damage, DNA repair, ageing and age-related disease. Mech Ageing Dev 129:349–52
  • Woo LL, Futami K, Shimamoto A, et al. (2006). The Rothmund-Thomson gene product RECQL4 localizes to the nucleolus in response to oxidative stress. Exp Cell Res 312:3443–57
  • Wu J, Capp C, Feng L, Hsieh T-S. (2008a). Drosophila homologue of the Rothmund-Thomson syndrome gene: essential function in DNA replication during development. Dev Biol 323:130–42
  • Wu W, Wang M, Wu W, et al. (2008b). Repair of radiation induced DNA double strand breaks by backup NHEJ is enhanced in G2. DNA Repair (Amst.) 7:329–38
  • Xu X, Rochette PJ, Feyissa EA, et al. (2009a). MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J 28:3005–14
  • Xu Y, Lei Z, Huang H, et al. (2009b). dRecQ4 is required for DNA synthesis and essential for cell proliferation in Drosophila. PLoS One 4:e6107
  • Yano K-I, Morotomi-Yano K, Wang S-Y, et al. (2008). Ku recruits XLF to DNA double-strand breaks. EMBO Rep 9:91–6
  • Yu AM, McVey M. (2010). Synthesis-dependent microhomology-mediated end joining accounts for multiple types of repair junctions. Nucleic Acids Res 38:5706–17
  • Yu CE, Oshima J, Fu YH, et al. (1996). Positional cloning of the Werner’s syndrome gene. Science 272:258–62
  • Yu CE, Oshima J, Goddard KA, et al. (1994). Linkage disequilibrium and haplotype studies of chromosome 8p 11.1–21.1 markers and Werner syndrome. Am J Hum Genet 55:356–64
  • Yu X, Gabriel A. (2003). Ku-dependent and Ku-independent end-joining pathways lead to chromosomal rearrangements during double-strand break repair in Saccharomyces cerevisiae. Genetics 163:843–56
  • Zheng L, Kanagaraj R, Mihaljevic B, et al. (2009). MRE11 complex links RECQ5 helicase to sites of DNA damage. Nucleic Acids Res 37:2645–57
  • Zhu Z, Chung W-H, Shim EY, et al. (2008). Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981–94

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