The RecQ DNA helicases in DNA repair

Annual Review of Genetics

Volumn 44, Issue , 2010, Pages 393-417

  Bernstein, Kara A ^a   Gangloff, Serge ^b,c   Rothstein, Rodney ^a  

^a NewYork Presbyterian Hospital   (United States)

^b INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^c CNRS   (France)

Author keywords

Bloom syndrome; DNA repair; homologous recombination; RecQ,Werner syndrome; Rothmund Thomson syndrome

Indexed keywords

BLOOM SYNDROME HELICASE; CHECKPOINT KINASE 2; PROTEIN MLH1; RAD51 PROTEIN; RECQ HELICASE; SINGLE STRANDED DNA; WERNER SYNDROME PROTEIN;

BLOOM SYNDROME; CAENORHABDITIS ELEGANS; CANCER SUSCEPTIBILITY; CELL DIVISION; CLINICAL FEATURE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; DNA SYNTHESIS; DOUBLE STRANDED DNA BREAK; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; GENE ACTIVITY; GENE DELETION; GENE FREQUENCY; GENE FUNCTION; GENE LOCUS; GENE MUTATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; HUMAN; MEIOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; ROTHMUND THOMSON SYNDROME; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; TELOMERE; WERNER SYNDROME; XENOPUS LAEVIS;

BACTERIA; DISEASE; DNA REPAIR; GENOMIC INSTABILITY; HUMANS; RECQ HELICASES;

EID: 78149434190     PISSN: 00664197     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-genet-102209-163602     Document Type: Review

References (172)

1. Ahmad F, Stewart E. 2005. The N-terminal region of the Schizosaccharomyces pombe recQ helicase, Rqh1p, physically interacts with topoisomerase III and is required for Rqh1p function. Mol. Genet. Genomics 273:102-14
2. Argueso J, Kijas A, Sarin S, Heck J, Waase M, Alani E. 2003. Systematic mutagenesis of the Saccharomyces cerevisiae MLH1 gene reveals distinct roles for Mlh1p in meiotic crossing over and in vegetative and meiotic mismatch repair. Mol. Cell. Biol. 23:873-86
3. Bachrati C, Borts R, Hickson I. 2006. Mobile D-loops are a preferred substrate for the Bloom's syndrome helicase. Nucleic Acids Res. 34:2269-79
4. Bachrati C, Hickson I. 2003. RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem. J. 374:577-606
5. Bae SH, Bae KH, Kim JA, Seo YS. 2001. RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes. Nature 412:456-61
6. Baumann C, Korner R, Hofmann K, Nigg EA. 2007. PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 128:101-14
7. Bennett RJ, Keck J, Wang J. 1999. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J. Mol. Biol. 289:235-48
8. Bennett RJ, Noirot-Gros M, Wang J. 2000. Interaction between yeast Sgs1 helicase and DNA topoiso-merase III. J. Biol. Chem. 275:26898-905
9. Bennett RJ, Sharp JA, Wang JC. 1998. Purification and characterization of the Sgs1 DNA helicase activity of Saccharomyces cerevisiae. J. Biol. Chem. 273:9644-50
10. Bernstein KA, Shor E, Sunjevaric I, Fumasoni M, Burgess RC, et al. 2009. Sgs1 function in the repair of DNA replication intermediates is separable from its role in homologous recombinational repair. EMBO J. 28:915-25
11. Bhattacharyya S, Sandy A, Groden J. 2010. Unwinding protein complexes in ALTernative telomere maintenance. J. CellBiochem. 109:7-15
12. Bjergbaek L, Cobb JA, Tsai-Pflugfelder M, Gasser SM. 2005. Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J. 24:405-17
13. Blander G, Kipnis J, Leal JFM, Yu CE, Schellenberg GD, Oren M. 1999. Physical and functional interaction between p53 and the Werner's syndrome protein. J. Biol. Chem. 274:29463-69
14. Bloom D. 1954. Congenital telangiectatic erythema resembling lupus erythematosus in dwarfs; probably a syndrome entity. AMAAm.J. Dis. Child. 88:754-58
15. Bonetti D, Martina M, Clerici M, Lucchini G, Longhese MP. 2009. Multiple pathways regulate 3' overhang generation at S. cerevisiae telomeres. Mol. Cell 35:70-81
16. Branzei D, SollierJ, Liberi G, Zhao X, Maeda D, et al. 2006. Ubc9-and Mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127:509-22
17. Branzei D, Vanoli F, Foiani M. 2008. SUMOylation regulates Rad18-mediated template switch. Nature 456:915-20
18. Brosh RM Jr, Orren DK, NehlinJO, Ravn PH, Kenny MK, et al. 1999. Functional and physical interaction between WRN helicase and human replication protein A. J. Biol. Chem. 274:18341-50
19. Brosh RM, Li JL, Kenny MK, Karow JK, Cooper MP, 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
20. Bugreev D, Brosh RJ, Mazin A. 2008. RECQ1 possesses DNA branch migration activity. J. Biol. Chem. 283:20231-42
21. Bugreev D, Yu X, Egelman E, Mazin A. 2007. Novel pro-and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 21:3085-94
22. Bussen W, Raynard S, Busygina V, Singh A, Sung P. 2007. Holliday junction processing activity of the BLM-Topo IIIalpha-BLAP75 complex.J. Biol. Chem. 282:31484-92
23. Caspari T, Murray JM, Carr AM. 2002. Cdc2-cyclin B kinase activity links Crb2 and Rqh1-topoisomerase III. Genes Dev. 16:1195-208
24. Cejka P, Cannavo E, Polaczek P, Masuda-Sasa T, Pokharel S, et al. 2010. DNA end resection by the Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature In press
25. Cejka P, Kowalczykowski SC. 2010. The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds Holliday junctions. J. Biol. Chem. 285:8290-301
26. Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC. 2010. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat. Struct. Mol. Biol. In press
27. Chan KL, North PS, Hickson ID. 2007. BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 26:3397-409
28. Chan KL, Palmai-Pallag T, Ying S, Hickson ID. 2009. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 11:753-60
29. Chang M, Bellaoui M, Zhang C, Desai R, Morozov P, et al. 2005. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO J. 24:2024-33
30. Chang S,Multani AS, Cabrera NG, Naylor ML, LaudP, etal. 2004. Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nat. Genet. 36:877-82
31. Chen C, Brill S. 2007. Binding and activation of DNA topoisomerase III by the Rmi1 subunit. J. Biol. Chem. 282:28971-79
32. Chen CF, Brill SJ. 2010. An essential DNA strand-exchange activity is conserved in the divergent N-termini of BLM orthologs. EMBO J. 29:1713-25
33. Chester N, KuoF, KozakC, O'Hara CD, LederP. 1998. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev. 12:3382-93
34. Chiolo I, Carotenuto W, Maffioletti G, Petrini J, Foiani M, Liberi G. 2005. Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation. Mol. Cell. Biol. 25:5738-51
35. Chung WH, Zhu Z, Papusha A, Malkova A, Ira G. 2010. Defective resection at DNA doubled-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet. 6(5):e1000948
36. Cobb JA, Bjergbaek L, Shimada K, Frei C, Gasser SM. 2003. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22:4325-36
37. Constantinou A, Tarsounas M, Karow JK, Brosh RM, Bohr VA, et al. 2000. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep. 1:80-84
38. Crabbe L, Verdun RE, Haggblom CI, Karlseder J. 2004. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306:1951-53
39. Cromie G, Hyppa R, Smith G. 2008. The fission yeast BLM homolog Rqh1 promotes meiotic recombination. Genetics 179:1157-67
40. Davies SL, North PS, Dart A, Lakin ND, Hickson ID. 2004. Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell. Biol. 24:1279-91
41. Dherin C, Gueneau E,Francin M, Nunez M, Miron S, et al. 2008. Characterization of a highly conserved binding site of Mlh1 required for exonuclease I-dependent mismatch repair. Mol. Cell. Biol. 29:907-18
42. - phenotype by expression of a bacterial Holliday junction resolvase. EMBO J. 19:2751-62
43. Dutertre S, Ababou M, Onclercq R, Delic J, Chatton B, et al. 2000. Cell cycle regulation of the endogenous wild type Bloom's syndrome DNA helicase. Oncogene 19:2731-38
44. Ellis NA, Groden J, Ye TZ, Straughen J, Lennon DJ, et al. 1995. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83:655-66
45. Frei C, 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
46. Fricke W, Kaliraman V, Brill S. 2001. Mapping the DNA topoisomerase III binding domain of the Sgs1 DNA helicase. J. Biol. Chem. 276:8848-55
47. Fukuchi K, Martin GM, Monnat RJ Jr. 1989. Mutator phenotype of Werner syndrome is characterized by extensive deletions. Proc. Natl. Acad. Sci. USA 86:5893-97
48. Fukuchi K, Tanaka K, Nakura J, Kumahara Y, Uchida T, Okada Y. 1985. Elevated spontaneous mutation rate in SV40-transformed Werner syndrome fibroblast cell lines. Somat. Cell Mol. Genet. 11:303-8
49. Gangloff S, de Massy B, Arthur L, Rothstein R, Fabre F. 1999. The essential role of yeast topoisomerase III in meiosis depends on recombination. EMBO J. 18:1701-11
50. Gangloff S, McDonald J, Bendixen C, Arthur L, Rothstein R. 1994. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14:8391-98
51. German J. 1993. Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine 72:393-406
52. German J, Archibald R, Bloom D. 1965. Chromosomal breakage in a rare and probably genetically determined syndrome of man. Science 148:506-7
53. German J, Sanz MM, Ciocci S, Ye TZ, Ellis NA. 2007. Syndrome-causing mutations of the BLM gene in persons in the Bloom's syndrome registry. Hum. Mutat. 28:743-53
54. Gharibyan V, Youssoufian H. 1999. Localization of the Bloom syndrome helicase to punctate nuclear structures and the nuclear matrix and regulation during the cell cycle: comparison with the Werner's syndrome helicase. Mol. Carcinog. 26:261-73
55. Gilbertson L, Stahl F. 1996. A test of the double-strand break repair model for meiotic recombination in Saccharomyces cerevisiae. Genetics 144:27-41
56. Gorbalenya AE, Koonin EV. 1993. Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3:419-29
57. Goss KH, Risinger MA, Kordich JJ, Sanz MM, Straughen JE, et al. 2002. Enhanced tumor formation in mice heterozygous for Blm mutation. Science 297:2051-53
58. Goto M. 1997. Hierarchical deterioration of body systems in Werner's syndrome: implications for normal ageing. Mech. Ageing Dev. 98:239-54
59. Grabowski MM, Svrzikapa N, Tissenbaum HA. 2005. Bloom syndrome ortholog HIM-6 maintains genomic stability in C. elegans. Mech. Ageing Dev. 126:1314-21
60. Gravel S, Chapman JR, Magill C, Jackson SP. 2009. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22:2767-72
61. Harmon F, Kowalczykowski S. 1998. RecQ helicase, in concert with RecA and SSB proteins, initiates and disrupts DNA recombination. Genes Dev. 12:1134-44
62. Hartung F, Puchta H. 2006. The RecQ gene family in plants. J. Plant Physiol. 163:287-96
63. Hodgkin J, Horvitz H, Brenner S. 1979. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91:67-94
64. Hoki Y, Araki R, Fujimori A, Ohhata T, Koseki H, et al. 2003. Growth retardation and skin abnormalities of the Recql4-deficient mouse. Hum. Mol. Genet. 12:2293-99
65. Hu Y, Raynard S, Sehorn MG, Lu X, Bussen W, et al. 2007. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev. 21:3073-84
66. Huang S, Lee L, Hanson NB, Lenaerts C, Hoehn H, et al. 2006. The spectrum of WRN mutations in Werner syndrome patients. Hum. Mutat. 27:558-67
67. Huber MD, Lee DC, Maizels N. 2002. G4 DNA unwinding by BLM and Sgs1p: substrate specificity and substrate-specific inhibition. Nucleic Acids Res. 30:3954-61
68. Hyun M,Bohr V, Ahn B. 2008. Biochemical characterization of the WRN-1 RecQ helicase of Caenorhab-ditis elegans. Biochemistry 47:7583-93
69. Ira G, Malkova A, Liberi G, Foiani M, Haber J. 2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401-11
70. Jessop L, Lichten M. 2008. Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol. Cell 31:313-23
71. Jessop L, Rockmill B, Roeder G, Lichten M. 2006. Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genet. 2(9):e155
72. Jiao R, Bachrati C, Pedrazzi G, Kuster P, Petkovic M, et al. 2004. Physical and functional interaction between the Bloom's syndrome gene product and the largest subunit of chromatin assembly factor 1. Mol. Cell. Biol. 24:4710-19
73. Johnson F, Lombard D, Neff N, Mastrangelo M, Dewolf W, et al. 2000. Association of the Bloom syndrome protein with topoisomerase IIIalpha in somatic and meiotic cells. Cancer Res. 60:1162-67
74. Kamath-Loeb A, Johansson E, Burgers P, Loeb L. 2000. Functional interaction between the Werner syndrome protein and DNA polymerase delta. Proc. Natl. Acad. Sci. USA 97:4603-8
75. Karow J, Constantinou A, Li J, West S, Hickson I. 2000. The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc. Natl. Acad. Sci. USA 97:6504-8
76. Karow JK, Newman RH, Freemont PS, Hickson ID. 1999. Oligomeric ring structure of the Bloom's syndrome helicase. Curr. Biol. 9:597-600
77. Kerrest A, Anand RP, Sundararajan R, Bermejo R, Liberi G, et al. 2009. SRS2 and SGS1 prevent chromosomal breaks and stabilize triplet repeats by restraining recombination. Nat. Struct. Mol. Biol. 16:159-67
78. Khakhar RR, Cobb JA, Bjergbaek L, Hickson ID, Gasser SM. 2003. RecQ helicases: multiple roles in genome maintenance. Trends Cell Biol. 13:493-501
79. Kitao S, Ohsugi I, Ichikawa K, Goto M, Furuichi Y, Shimamoto A. 1998. Cloning of two new human helicase genes of the RecQ family: biological significance of multiple species in higher eukaryotes. Genomics 54:443-52
80. Kitao S, Shimamoto A, Goto M, Miller RW, Smithson WA, et al. 1999. Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet. 22:82-84
81. Kobbe D, Blanck S, Demand K, Focke M, Puchta H. 2008. AtRECQ2, a RecQ helicase homologue from Arabidopsis thaliana, is able to disrupt various recombinogenic DNA structures in vitro. Plant J. 55:397-405
82. Krejci L, Van Komen S, Li Y, Villemain J, ReddyMS, etal. 2003. DNAhelicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305-9
83. Kusano K, Johnson-Schlitz DM, Engels WR. 2001. Sterility ofDrosophila with mutations in the Bloom syndrome gene: complementation by Ku70. Science 291:2600-2
84. Liao S, Toczylowski T, Yan H. 2008. Identification of the Xenopus DNA2 protein as a major nuclease for the 5'-3' strand-specific processing of DNAends. Nucleic Acids Res. 36(19):6091-100
85. Langland G, Kordich J, Creaney J, Goss K, Lillard-Wetherell K, et al. 2001. The Bloom's syndrome protein (BLM) interacts with MLH1 but is not required for DNA mismatch repair. J. Biol. Chem. 276:30031-35
86. Larrivee M, LeBel C, Wellinger RJ. 2004. The generation of proper constitutive G-tails on yeast telomeres is dependent on the MRX complex. Genes Dev. 18:1391-96
87. Lebel M, Leder P. 1998. A deletion within the murine Werner syndrome helicase induces sensitivity to inhibitors of topoisomerase and loss of cellular proliferative capacity. Proc. Natl. Acad. Sci. USA 95:13097-102
88. Lebel M, Spillare EA, Harris CC, 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. 274:37795-99
89. Lengsfeld BM, Rattray AJ, Bhaskara V, Ghirlando R, Paull TT. 2007. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28:638-51
90. LeRoy G, Carroll R, Kyin S, Seki M, Cole M. 2005. Identification of RecQL1 as a Holliday junction processing enzyme in human cell lines. Nucleic Acids Res. 33:6251-57
91. Li D, Frazier M, Evans DB, Hess KR, Crane CH, et al. 2006. Single nucleotide polymorphisms of RecQ1, RAD54L, and ATM genes are associated with reduced survival of pancreatic cancer. J. Clin. Oncol. 24:1720-28
92. Li JL, Harrison RJ, Reszka AP, Brosh RM Jr, Bohr VA, et al. 2001. Inhibition of the Bloom's and Werner's syndrome helicases by G-quadruplex interacting ligands. Biochemistry 40:15194-202
93. Liberi G, Maffioletti G, Lucca C, Chiolo I, Baryshnikova A, et al. 2005. Rad51-dependent DNA structures accumulate at damaged replication forks in Sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19:339-50
94. Lisby M, Rothstein R. 2009. Choreography of recombination proteins during the DNA damage response. DNA Repair (Amst) 8:1068-76
95. Liu Z, Macias M, Bottomley M, Stier G, Linge J, et al. 1999. The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Structure 7:1557-66
96. Lonn U, Lonn S, Nylen U, Winblad G, German J. 1990. An abnormal profile of DNA replication intermediates in Bloom's syndrome. Cancer Res. 50:3141-45
97. Louis E, Borts R. 2003. Meiotic recombination: too much of a good thing? Curr. Biol. 13:R953-55
98. Lu CY, Tsai CH, Brill SJ, Teng SC. 2009. Sumoylation of the BLM ortholog, Sgs1, promotes telomere-telomere recombination in budding yeast. Nucleic Acids Res. 38(2):488-98
99. Luo G, Santoro IM, McDaniel LD, Nishijima I, Mills M, et al. 2000. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet. 26:424-29
100. Lydeard JR, Lipkin-Moore Z, Jain S, Eapen VV, HaberJE. 2010. Sgs1 and Exo1 redundantly inhibit break-induced replication and de novo telomere addition at broken chromosome ends. PLoS Genet. 6(5):e100097
101. Mann MB, Hodges CA, Barnes E, Vogel H, HassoldTJ, Luo G 2005. Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund-Thomson syndrome. Hum. Mol. Genet. 14:813-25
102. Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455(7214):770-75
103. Miozzo M, Castorina P, Riva P, Dalpra L, Fuhrman Conti AM, et al. 1998. Chromosomal instability in fibroblasts and mesenchymal tumors from 2 sibs with Rothmund-Thomson syndrome. Int. J. Cancer 77:504-10
104. Miyajima A, Seki M, Onoda F, Shiratori M, Odagiri N, et al. 2000. Sgs1 helicase activity is required for mitotic but apparently not for meiotic functions. Mol. Cell. Biol. 20:6399-409
105. Moens PB, Freire R, Tarsounas M, Spyropoulos B, Jackson SP. 2000. Expression and nuclear localization of BLM, a chromosome stability protein mutated in Bloom's syndrome, suggest a role in recombination during meiotic prophase. J. Cell Sci. 113(4):663-72
106. Mohaghegh P, Karow JK, Brosh RM Jr, Bohr VA, Hickson ID. 2001. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res. 29:2843-49
107. Mullen J, Kaliraman V, Brill S. 2000. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154:1101-14
108. Mullen J, Nallaseth F, Lan Y, Slagle C, Brill S. 2005. Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex. Mol. Cell. Biol. 25:4476-87
109. Muzzolini L, Beuron F, Patwardhan A, Popuri V, Cui S, et al. 2007. Different quaternary structures of human RECQ1 are associated with its dual enzymatic activity. PLoS Biol. 5:e20
110. Nasmyth KA. 1982. Molecular genetics of yeast mating type. Annu. Rev. Genet. 16:439-500
111. Nimonkar AV, Ozsoy AZ, Genschel J, Modrich P, Kowalczykowski SC. 2008. Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc. Natl. Acad. Sci. USA 105:16906-11
112. Niu H, Chung W-H, Zhu Z, Kwon Y, Zhao W, et al. 2010. Mechanism of the ATP-dependent DNA end resection machinery from S. cerevisiae. Nature. In press
113. Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, Hunter N. 2007. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130:259-72
114. Oh S, Lao J, Taylor A, Smith G, Hunter N. 2008. RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol. Cell 31:324-36
115. Opresko P, Sowd G, Wang H. 2009. The Werner syndrome helicase/exonuclease processes mobile D-loops through branch migration and degradation. PLoS ONE 4:e4825
116. Pedruzzi I, Burckert N, Egger P, De Virgilio C. 2000. Saccharomyces cerevisiae Ras/cAMP pathway controls post-diauxic shift element-dependent transcription through the zinc finger protein Gis1. EMBO J. 19:2569-79
117. Pike A, Shrestha B, Popuri V, Burgess-Brown N, Muzzolini L, et al. 2009. Structure of the human RECQ1 helicase reveals a putative strand-separation pin. Proc. Natl. Acad. Sci. USA 106:1039-44
118. Plank J, Wu J, Hsieh T. 2006. Topoisomerase IIIalpha and Bloom's helicase can resolve a mobile double Holliday junction substrate through convergent branch migration. Proc. Natl. Acad. Sci. USA 103:11118-23
119. Poot M, Hoehn H, Runger TM, Martin GM. 1992. Impaired S-phase transit of Werner syndrome cells expressed in lymphoblastoid cell lines. Exp. Cell Res. 202:267-73
120. Popuri V, Bachrati C, Muzzolini L, Mosedale G, Costantini S, et al. 2008. The human Recq helicases, Blm and Recq1, display distinct DNA substrate specificities. J. Biol. Chem. 283:17766-76
121. Puranam KL, Blackshear PJ. 1994. Cloning and characterization of RECQL, a potential human homo-logue of the Escherichia coli DNA helicase RecQ. J. Biol. Chem. 269:29838-45
122. Raynard S, Bussen W, Sung P. 2006. A double Holliday junction dissolvasome comprising BLM, topoi-somerase IIIalpha, and BLAP75. J. Biol. Chem. 281:13861-64
123. Raynard S, Zhao W, Bussen W, Lu L, Ding Y, et al. 2008. Functional Role of BLAP75 in BLM-topoisomerase III{alpha}-dependent Holliday junction processing. J. Biol. Chem. 283:15701-8
124. Robert T, Dervins D, Fabre F, Gangloff S. 2006. Mrc1 and Srs2 are major actors in the regulation of spontaneous crossover. EMBO J. 25:2837-46
125. Rockmill B, Fung JC, Branda SS, Roeder GS. 2003. The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr. Biol. 13:1954-62
126. Rockmill B, Voelkel-Meiman K, Roeder GS. 2006. Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae.Genetics 174:1745-54
127. Rog O, Miller KM, Ferreira MG, Cooper JP. 2009. Sumoylation of RecQ helicase controls the fate of dysfunctional telomeres. Mol. Cell 33:559-69
128. Saffi J, Feldmann H, Winnacker E, Henriques J. 2001. Interaction of the yeast Pso5/Rad16 and Sgs1 proteins: influences on DNA repair and aging. Mutat. Res. 486:195-206
129. Salk D, Bryant E, Au K, Hoehn H, Martin GM. 1981. Systematic growth studies, cocultivation, and cell hybridization studies of Werner syndrome cultured skin fibroblasts. Hum. Genet. 58:310-16
130. Seki M, Otsuki M, Ishii Y, Tada S, Enomoto T. 2008. RecQ family helicases in genome stability. Cell Cycle 7:2472-78
131. Seki M, Yanagisawa J, Kohda T, Sonoyama T, Ui M, Enomoto T. 1994. Purification of two DNA-dependent adenosinetriphosphatases having DNA helicase activity from HeLa cells and comparison of the properties of the two enzymes. J. Biochem. 115:523-31
132. Sengupta S, Linke SP, Pedeux R, Yang Q, Farnsworth J, et al. 2003. BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J. 22:1210-22
133. Sengupta S, Robles AI, Linke SP, Sinogeeva NI, Zhang R, 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
134. 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
135. Shimamoto A, Nishikawa K, Kitao S, 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. 28:1647-55
136. Siitonen HA, Kopra O, Kaariainen H, Haravuori H, Winter RM, et al. 2003. Molecular defect of RAPADILINO syndrome expands the phenotype spectrum of RECQL diseases. Hum. Mol. Genet. 12:2837-44
137. Siitonen HA, Sotkasiira J, Biervliet M, Benmansour A, Capri Y, et al. 2009. The mutation spectrum in RECQL4 diseases. Eur. J. Hum. Genet. 17:151-58
138. Singh T, Ali A, Busygina V, Raynard S, Fan Q, et al. 2008. BLAP18/RMI2, a novel OB-fold-containing protein, is an essential component of the Bloom helicase-double Holliday junction dissolvasome. Genes Dev. 22:2856-68
139. Spillare EA, Robles AI, Wang XW, Shen JC, Yu CE, et al. 1999. p53-mediated apoptosis is attenuated in Werner syndrome cells. Genes Dev. 13:1355-60
140. Sun H, Bennett RJ, Maizels N. 1999. The Saccharomyces cerevisiae Sgs1 helicase efficiently unwinds G-G paired DNAs. Nucleic Acids Res. 27:1978-84
141. Tahara H, Kusunoki M, Yamanaka Y, Matsumura S, Ide T. 2005. G-tail telomere HPA: simple measurement of human single-stranded telomeric overhangs. Nat. Methods 2:829-31
142. Theobald D, Mitton-Fry R, Wuttke D. 2003. Nucleic acid recognition by OB-fold proteins. Annu. Rev. Biophys. Biomol. Struct. 32:115-33
143. Tronnersjo S, Hanefalk C, Balciunas D, Hu G, Nordberg N, et al. 2007. The jmjN and jmjC domains of the yeast zinc finger protein Gis1 interact with 19 proteins involved in transcription, sumoylation and DNA repair. Mol. Genet. Genomics 277:57-70
144. Tsukada Y, Fang J, Erdjument-Bromage H, Warren M, Borchers C, et al. 2006. Histone demethylation by a family of JmjC domain-containing proteins. Nature 439:811-16
145. Van Brabant AJ, Ye T, Sanz M, German IJ, Ellis NA, Holloman WK. 2000. Binding and melting of D-loops by the Bloom syndrome helicase. Biochemistry 39:14617-25
146. Van Maldergem L, Siitonen HA, Jalkh N, Chouery E, De Roy M, et al. 2006. Revisiting the craniosynostosis-radial ray hypoplasia association: Baller-Gerold syndrome caused by mutations in the RECQL4 gene. J. Med. Genet. 43:148-52
147. Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, Fabre F. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309-12
148. Versini G, Comet I, Wu M, Hoopes L, Schwob E, Pasero P. 2003. The yeast Sgs1 helicase is differentially required for genomic and ribosomal DNA replication. EMBO J. 22:1939-49
149. Vindigni A, Hickson I. 2009. RecQ helicases: multiple structures for multiple functions? HFSP J. 3:153-64
150. von Kobbe C, Karmakar P, Dawut L, Opresko P, Zeng X, et al. 2002. Colocalization, physical, and functional interaction between Werner and Bloom syndrome proteins. J. Biol. Chem. 277:22035-44
151. Wallis JW, Chrebet G, Brodsky G, Rolfe M, Rothstein R. 1989. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58:409-19
152. Wang T, Kung W. 2002. Supercomplex formation between Mlh1-Mlh3 and Sgs1-Top3 heterocom-plexes in meiotic yeast cells. Biochem. Biophys. Res. Commun. 296:949-53
153. Wang XW, Tseng A, Ellis NA, Spillare EA, Linke SP, et al. 2001. Functional interaction of p53 and BLM DNA helicase in apoptosis. J. Biol. Chem. 276:32948-55
154. Wang Y, Cortez D, Yazdi P, Neff N, Elledge SJ, Qin J. 2000. BASC, a super complex of BRCA1-associated proteins involvedinthe recognition and repairofaberrant DNA structures.Genes Dev. 14:927-39
155. Watt P, Hickson I, Borts R, Louis E. 1996. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144:935-45
156. Watt P, Louis E, Borts R, Hickson I. 1995. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81:253-60
157. White CI, Haber JE. 1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9:663-73
158. Wu L, Bachrati CZ, Ou J, Xu C, Yin J, et al. 2006. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. USA 103:4068-73
159. Wu L, Chan K, Ralf C, Bernstein D, Garcia P, et al. 2005. The HRDC domain of BLM is required for the dissolution of double Holliday junctions. EMBO J. 24:2679-87
160. Wu L, Davies S, Levitt N, Hickson I. 2001. Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J. Biol. Chem. 276:19375-81
161. Wu L, Davies SL, North PS, Goulaouic H, Riou JF, et al. 2000. The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem. 275:9636-44
162. Wu L, Hickson I. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870-74
163. Xu D, Guo R, Sobeck A, Bachrati C, Yang J, et al. 2008. RMI, a new OB-fold complex essential for Bloom syndrome protein to maintain genome stability. Genes Dev. 22:2843-55
164. Xu H, Deprez E, Zhang A, Tauc P, Ladjimi M, et al. 2003. The Escherichia coli RecQ helicase functions as a monomer. J. Biol. Chem. 278:34925-33
165. Xu X, Rochette PJ, Feyissa EA, Su TV, Liu Y. 2009. MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J. 28:3005-14
166. Yamane K, Toumazou C, Tsukada Y, Erdjument-Bromage H, Tempst P, et al. 2006. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125:483-95
167. Yang Q, Zhang R, Wang X, Spillare E, Linke S, et al. 2002. The processing of Holliday junctions by BLM and WRN helicases is regulated by p53. J. Biol. Chem. 277:31980-87
168. Yin J, Sobeck A, Xu C, Meetei AR, Hoatlin M, et al. 2005. BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity. EMBO J. 24:1465-76
169. Yu CE, Oshima J, Fu YH, Wijsman EM, Hisama F, et al. 1996. Positional cloning of the Werner's syndrome gene. Science 272:258-62
170. Zhang X, Dou S, Xie P, Hu J, Wang P, Xi X. 2006. E. coli RecQ is a rapid, efficient and monomeric helicase. J. Biol. Chem. 281:12655-63
171. Zhong S, Hu P, Ye T, Stan R, Ellis N, Pandolfi P. 1999. A role for PML and the nuclear body in genomic stability. Oncogene 18:7941-47
172. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981-94