RecQ helicases: Conserved guardians of genomic integrity

Advances in Experimental Medicine and Biology

Volumn 767, Issue , 2013, Pages 161-184

  Larsen, Nicolai Balle ^a   Hickson, Ian D ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; APHIDICOLIN; BLOOM SYNDROME HELICASE; CARBOXY TERMINAL TELOPEPTIDE; DOUBLE STRANDED DNA; HELICASE; HYDROXYUREA; MITOMYCIN; RECQ HELICASE; RECQ1 HELICASE; RECQ4 HELICASE; RECQ5 HELICASE; SGS1 HELICASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; WERNER SYNDROME PROTEIN; ADENOSINE TRIPHOSPHATASE; DNA HELICASE;

BLOOM SYNDROME; CELL CYCLE S PHASE; DISSOLUTION; DNA END JOINING REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA STRUCTURE; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SUBSTRATE; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; HUMAN; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID EXCHANGE; SUMOYLATION; WERNER SYNDROME; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CROSSING OVER; DNA REPAIR; DNA STRAND; GENETIC CONSERVATION; GENETIC STABILITY; GENOME ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SPECIES COMPARISON; GENETICS; GENOMICS;

ADENOSINE TRIPHOSPHATASES; BLOOM SYNDROME; DNA HELICASES; GENOMICS; HUMANS; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; WERNER SYNDROME;

EID: 84873667075     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-5037-5_8     Document Type: Review

References (119)

1. Chu WK, Hickson ID. RecQ helicases: multifunctional genome caretakers. Nat Rev Cancer. 2009;9(9):644-54.
2. Bernstein KA, Gangloff S, Rothstein R. The RecQ DNA helicases in DNA repair. Annu Rev Genet. 2010;44:393-417.
3. Monnat Jr RJ. Human RECQ helicases: roles in DNA metabolism, mutagenesis and cancer biology. Semin Cancer Biol. 2010;20(5):329-39.
4. German J, Sanz MM, Ciocci S, Ye TZ, Ellis NA. Syndrome-causing mutations of the BLM gene in persons in the Bloom's Syndrome Registry. Hum Mutat. 2007;28(8):743-53.
5. German J, Archibald R, Bloom D. Chromosomal breakage in a rare and probably genetically determined syndrome of man. Science. 1965;148(3669):506-7.
6. Chaganti RS, Schonberg S, German J. A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc Natl Acad Sci USA. 1974;71(11):4508-12.
7. Fairman-Williams ME, Guenther UP, Jankowsky E. SF1 and SF2 helicases: family matters. Curr Opin Struct Biol. 2010;20(3):313-24.
8. Bernstein DA, Keck JL. Domain mapping of Escherichia coli RecQ de fi nes the roles of conserved N- and C-terminal regions in the RecQ family. Nucleic Acids Res. 2003;31(11):2778-85.
9. Bernstein DA, Zittel MC, Keck JL. High-resolution structure of the E.coli RecQ helicase catalytic core. EMBO J. 2003;22(19):4910-21.
10. Saf fi J, Pereira VR, Henriques JA. Importance of the Sgs1 helicase activity in DNA repair of Saccharomyces cerevisiae. Curr Genet. 2000;37(2):75-8.
11. Mullen JR, Kaliraman V, Brill SJ. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics. 2000;154(3):1101-14.
12. Bahr A, De Graeve F, Kedinger C, Chatton B. Point mutations causing Bloom's syndrome abolish ATPase and DNA helicase activities of the BLM protein. Oncogene. 1998;17(20):2565-71.
13. Rong SB, Valiaho J, Vihinen M. Structural basis of Bloom syndrome (BS) causing mutations in the BLM helicase domain. Mol Med. 2000;6(3):155-64.
14. Liu JL, Rigolet P, Dou SX, Wang PY, Xi XG. The zinc fi nger motif of Escherichia coli RecQ is implicated in both DNA binding and protein folding. J Biol Chem. 2004;279(41):42794-802.
15. Guo RB, Rigolet P, Zargarian L, Fermandjian S, Xi XG. Structural and functional characterizations reveal the importance of a zinc binding domain in Bloom's syndrome helicase. Nucleic Acids Res. 2005;33(10):3109-24.
16. Ren H, Dou SX, Zhang XD, et al. 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. 2008;412(3):425-33.
17. Pike AC, Shrestha B, Popuri V, et al. Structure of the human RECQ1 helicase reveals a putative strand-separation pin. Proc Natl Acad Sci USA. 2009;106(4):1039-44.
18. Lucic B, Zhang Y, King O, et al. A prominent beta-hairpin structure in the winged-helix domain of RECQ1 is required for DNA unwinding and oligomer formation. Nucleic Acids Res. 2011;39(5):1703-17.
19. Kitano K, Kim SY, Hakoshima T. Structural basis for DNA strand separation by the unconventional winged-helix domain of RecQ helicase WRN. Structure. 2010;18(2):177-87.
20. Huber MD, Duquette ML, Shiels JC, Maizels N. A conserved G4 DNA binding domain in RecQ family helicases. J Mol Biol. 2006;358(4):1071-80.
21. Liu Z, Macias MJ, Bottomley MJ, et al. The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Structure. 1999;7(12):1557-66.
22. Bernstein DA, Keck JL. Conferring substrate specificity to DNA helicases: role of the RecQ HRDC domain. Structure. 2005;13(8):1173-82.
23. Kitano K, Yoshihara N, Hakoshima T. Crystal structure of the HRDC domain of human Werner syndrome protein, WRN. J Biol Chem. 2007;282(4):2717-28.
24. Kim YM, Choi BS. Structure and function of the regulatory HRDC domain from human Bloom syndrome protein. Nucleic Acids Res. 2010;38(21):7764-77.
25. Sato A, Mishima M, Nagai A, et al. Solution structure of the HRDC domain of human Bloom syndrome protein BLM. J Biochem. 2010;148(4):517-25.
26. Karmakar P, Seki M, Kanamori M, et al. BLM is an early responder to DNA double-strand breaks. Biochem Biophys Res Commun. 2006;348(1):62-9.
27. von Kobbe C, Thoma NH, Czyzewski BK, Pavletich NP, Bohr VA. Werner syndrome protein contains three structure-speci fi c DNA binding domains. J Biol Chem. 2003;278(52):52997-3006.
28. Vindigni A, Hickson ID. RecQ helicases: multiple structures for multiple functions? HFSP J. 2009;3(3):153-64.
29. Perry JJ, Yannone SM, Holden LG, et al. WRN exonuclease structure and molecular mechanism imply an editing role in DNA end processing. Nat Struct Mol Biol. 2006;13(5):414-22.
30. Opresko PL, Laine JP, Brosh Jr RM, Seidman MM, Bohr VA. Coordinate action of the helicase and 3' to 5' exonuclease of Werner syndrome protein. J Biol Chem. 2001;276(48):44677-87.
31. Boubriak I, Mason PA, Clancy DJ, Dockray J, Saunders RD, Cox LS. DmWRNexo is a 3'-5' exonuclease: phenotypic and biochemical characterization of mutants of the Drosophila orthologue of human WRN exonuclease. Biogerontology. 2009;10(3):267-77.
32. Capp C, Wu JH, Hsieh TS. Drosophila RecQ4 has a 3 '-5 ' DNA helicase activity that is essential for viability. J Biol Chem. 2009;284(45):30845-52.
33. Abe T, Yoshimura A, Hosono Y, Tada S, Seki M, Enomoto T. The N-terminal region of RECQL4 lacking the helicase domain is both essential and suf fi cient for the viability of vertebrate cells. Role of the N-terminal region of RECQL4 in cells. Biochim Biophys Acta. 2011;1813(3):473-9.
34. Thangavel S, Mendoza-Maldonado R, Tissino E, et al. Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol Cell Biol. 2010;30(6):1382-96.
35. Chen CF, Brill SJ. An essential DNA strand-exchange activity is conserved in the divergent N-termini of BLM orthologs. EMBO J. 2010;29(10):1713-25.
36. Umezu K, Nakayama H. RecQ DNA helicase of Escherichia coli. Characterization of the helix-unwinding activity with emphasis on the effect of single-stranded DNA-binding protein. J Mol Biol. 1993;230(4):1145-50.
37. Harmon FG, Kowalczykowski SC. Biochemical characterization of the DNA helicase activity of the Escherichia coli RecQ helicase. J Biol Chem. 2001;276(1):232-43.
38. Shereda RD, Bernstein DA, Keck JL. A central role for SSB in Escherichia coli RecQ DNA helicase function. J Biol Chem. 2007;282(26):19247-58.
39. Shereda RD, Reiter NJ, Butcher SE, Keck JL. Identification of the SSB binding site on E. coli RecQ reveals a conserved surface for binding SSB's C terminus. J Mol Biol. 2009;386(3):612-25.
40. Harmon FG, DiGate RJ, Kowalczykowski SC. RecQ helicase and topoisomerase III comprise a novel DNA strand passage function: a conserved mechanism for control of DNA recombination. Mol Cell. 1999;3(5):611-20.
41. Harmon FG, Kowalczykowski SC. RecQ helicase, in concert with RecA and SSB proteins, initiates and disrupts DNA recombination. Genes Dev. 1998;12(8):1134-44.
42. Gangloff S, McDonald JP, 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. 1994;14(12):8391-8.
43. Ahmad F, Stewart E. 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. 2005;273(1):102-14.
44. Fricke WM, Kaliraman V, Brill SJ. Mapping the DNA topoisomerase III binding domain of the Sgs1 DNA helicase. J Biol Chem. 2001;276(12):8848-55.
45. Ui A, Satoh Y, Onoda F, Miyajima A, Seki M, Enomoto T. The N-terminal region of Sgs1, which interacts with Top3, is required for complementation of MMS sensitivity and suppression of hyper-recombination in sgs1 disruptants. Mol Genet Genomics. 2001;265(5):837-50.
46. Chang M, Bellaoui M, Zhang C, et al. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO J. 2005;24(11):2024-33.
47. Chen CF, Brill SJ. Binding and activation of DNA topoisomerase III by the Rmi1 subunit. J Biol Chem. 2007;282(39):28971-9.
48. Wu L, Davies SL, Levitt NC, Hickson ID. Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J Biol Chem. 2001;276(22):19375-81.
49. Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat Struct Mol Biol. 2010;17(11):1377-82.
50. Wu L, Davies SL, North PS, et al. The Bloom's syndrome gene product interacts with topoisomerase III. J Biol Chem. 2000;275(13):9636-44.
51. Yin J, Sobeck A, Xu C, et al. BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity. EMBO J. 2005;24(7):1465-76.
52. Raynard S, Zhao W, Bussen W, et al. Functional role of BLAP75 in BLM-topoisomerase IIIalpha-dependent holliday junction processing. J Biol Chem. 2008;283(23):15701-8.
53. Singh TR, Ali AM, Busygina V, et al. BLAP18/RMI2, a novel OB-fold-containing protein, is an essential component of the Bloom helicase-double Holliday junction dissolvasome. Genes Dev. 2008;22(20):2856-68.
54. Xu D, Guo R, Sobeck A, et al. RMI, a new OB-fold complex essential for Bloom syndrome protein to maintain genome stability. Genes Dev. 2008;22(20):2843-55.
55. Wang F, Yang Y, Singh TR, et al. Crystal structures of RMI1 and RMI2, two OB-fold regulatory subunits of the BLM complex. Structure. 2010;18(9):1159-70.
56. Brosh Jr RM, Li JL, Kenny MK, et al. Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J Biol Chem. 2000;275(31):23500-8.
57. Bergeron KL, Murphy EL, Brown LW, Almeida KH. Critical interaction domains between bloom syndrome protein and RAD51. Protein J. 2011;30(1):1-8.
58. Mohaghegh P, Karow JK, Brosh Jr RM, Bohr VA, Hickson ID. The Bloom's and Werner's syndrome proteins are DNA structure-speci fi c helicases. Nucleic Acids Res. 2001;29(13):2843-9.
59. Bennett RJ, Keck JL, Wang JC. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J Mol Biol. 1999;289(2):235-48.
60. Sun H, Karow JK, Hickson ID, Maizels N. The Bloom's syndrome helicase unwinds G4 DNA. J Biol Chem. 1998;273(42):27587-92.
61. Sun H, Bennett RJ, Maizels N. The Saccharomyces cerevisiae Sgs1 helicase ef fi ciently unwinds G-G paired DNAs. Nucleic Acids Res. 1999;27(9):1978-84.
62. Kamath-Loeb A, Loeb LA, Fry M. The werner syndrome protein is distinguished from the bloom syndrome protein by its capacity to tightly bind diverse DNA structures. PLoS One. 2012;7(1):e30189.
63. Karow JK, Constantinou A, Li JL, West SC, Hickson ID. The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc Natl Acad Sci USA. 2000;97(12):6504-8.
64. Bachrati CZ, Borts RH, Hickson ID. Mobile D-loops are a preferred substrate for the Bloom's syndrome helicase. Nucleic Acids Res. 2006;34(8):2269-79.
65. Bugreev DV, Yu X, Egelman EH, Mazin AV. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 2007;21(23):3085-94.
66. Bugreev DV, Mazina OM, Mazin AV. Bloom syndrome helicase stimulates RAD51 DNA strand exchange activity through a novel mechanism. J Biol Chem. 2009;284(39):26349-59.
67. Wu L, Hickson ID. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature. 2003;426(6968):870-4.
68. Wu L, Chan KL, Ralf C, et al. The HRDC domain of BLM is required for the dissolution of double Holliday junctions. EMBO J. 2005;24(14):2679-87.
69. Bussen W, Raynard S, Busygina V, Singh AK, Sung P. Holliday junction processing activity of the BLM-Topo IIIalpha-BLAP75 complex. J Biol Chem. 2007;282(43):31484-92.
70. Chen SH, Wu CH, Plank JL, Hsieh TS. Essential functions of the C-terminus of Drosophila topoisomerase IIIalpha in double Holliday junction dissolution. J Biol Chem. 2012;287(23): 19346-53.
71. Wu L, Bachrati CZ, Ou J, et al. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc Natl Acad Sci USA. 2006;103(11):4068-73.
72. Yang J, Bachrati CZ, Ou J, Hickson ID, Brown GW. Human topoisomerase IIIalpha is a single- stranded DNA decatenase that is stimulated by BLM and RMI1. J Biol Chem. 2010;285(28):21426-36.
73. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell. 2008;134(6):981-94.
74. Gravel S, Chapman JR, Magill C, Jackson SP. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 2008;22(20):2767-72.
75. Cejka P, Cannavo E, Polaczek P, et al. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature. 2010;467(7311):112-6.
76. Nimonkar AV, Genschel J, Kinoshita E, et al. BLM-DNA2-RPA-MRN and EXO1-BLMRPA- MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 2011;25(4):350-62.
77. Nimonkar AV, Ozsoy AZ, Genschel J, Modrich P, Kowalczykowski SC. Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc Natl Acad Sci USA. 2008;105(44):16906-11.
78. Li X, Heyer WD. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 2008;18(1):99-113.
79. Chu WK, Hanada K, Kanaar R, Hickson ID. BLM has early and late functions in homologous recombination repair in mouse embryonic stem cells. Oncogene. 2010;29(33):4705-14.
80. Myung K, Datta A, Chen C, Kolodner RD. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat Genet. 2001;27(1):113-6.
81. Sugawara N, Goldfarb T, Studamire B, Alani E, Haber JE. Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc Natl Acad Sci USA. 2004;101(25):9315-20.
82. Mankouri HW, Craig TJ, Morgan A. SGS1 is a multicopy suppressor of srs2: functional overlap between DNA helicases. Nucleic Acids Res. 2002;30(5):1103-13.
83. Putnam CD, Hayes TK, Kolodner RD. Speci fi c pathways prevent duplication-mediated genome rearrangements. Nature. 2009;460(7258):984-9.
84. Sebesta M, Burkovics P, Haracska L, Krejci L. Reconstitution of DNA repair synthesis in vitro and the role of polymerase and helicase activities. DNA Repair. 2011;10(6):567-76.
85. Ira G, Malkova A, Liberi G, Foiani M, Haber JE. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell. 2003;115(4):401-11.
86. Liberi G, Maf fi oletti G, Lucca C, et al. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 2005;19(3):339-50.
87. Mankouri HW, Ngo HP, Hickson ID. Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3. Mol Biol Cell. 2007;18(10):4062-73.
88. Ashton TM, Mankouri HW, Heidenblut A, McHugh PJ, Hickson ID. Pathways for Holliday junction processing during homologous recombination in Saccharomyces cerevisiae. Mol Cell Biol. 2011;31(9):1921-33.
89. Mankouri HW, Ashton TM, Hickson ID. Holliday junction-containing DNA structures persist in cells lacking Sgs1 or Top3 following exposure to DNA damage. Proc Natl Acad Sci USA. 2011;108(12):4944-9.
90. Hickson ID, Mankouri HW. Processing of homologous recombination repair intermediates by the Sgs1-Top3-Rmi1 and Mus81-Mms4 complexes. Cell Cycle. 2011;10(18):3078-85.
91. Wechsler T, Newman S, West SC. Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature. 2011;471(7340):642-6.
92. Sengupta S, Linke SP, Pedeux R, et al. BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J. 2003;22(5):1210-22.
93. Cobb JA, Bjergbaek L, Shimada K, Frei C, Gasser SM. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 2003;22(16):4325-36.
94. Bjergbaek L, Cobb JA, Tsai-P fl ugfelder M, Gasser SM. Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J. 2005;24(2):405-17.
95. Cobb JA, Schleker T, Rojas V, Bjergbaek L, Tercero JA, Gasser SM. Replisome instability, fork collapse, and gross chromosomal rearrangements arise synergistically from Mec1 kinase and RecQ helicase mutations. Genes Dev. 2005;19(24):3055-69.
96. Davies SL, North PS, Dart A, Lakin ND, Hickson ID. Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol Cell Biol. 2004;24(3):1279-91.
97. Davies SL, North PS, Hickson ID. Role for BLM in replication-fork restart and suppression of origin fi ring after replicative stress. Nat Struct Mol Biol. 2007;14(7):677-9.
98. Xu D, Muniandy P, Leo E, et al. Rif1 provides a new DNA-binding interface for the Bloom syndrome complex to maintain normal replication. EMBO J. 2010;29(18):3140-55.
99. Ralf C, Hickson ID, Wu L. The Bloom's syndrome helicase can promote the regression of a model replication fork. J Biol Chem. 2006;281(32):22839-46.
100. Chan KL, North PS, Hickson ID. BLM is required for faithful chromosome segregation and its localization de fi nes a class of ultra fi ne anaphase bridges. EMBO J. 2007;26(14):3397-409.
101. Baumann C, Korner R, Hofmann K, Nigg EA. PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell. 2007;128(1):101-14.
102. Spence JM, Phua HH, Mills W, Carpenter AJ, Porter AC, Farr CJ. Depletion of topoisomerase IIalpha leads to shortening of the metaphase interkinetochore distance and abnormal persistence of PICH-coated anaphase threads. J Cell Sci. 2007;120(pt 22):3952-64.
103. Chan KL, Hickson ID. New insights into the formation and resolution of ultra- fi ne anaphase bridges. Semin Cell Dev Biol. 2011;22(8):906-12.
104. Chan KL, Palmai-Pallag T, Ying SM, Hickson ID. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat Cell Biol. 2009;11(6):753-60.
105. Meetei AR, Sechi S, Wallisch M, et al. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol Cell Biol. 2003;23(10):3417-26.
106. Howlett NG, Taniguchi T, Durkin SG, D'Andrea AD, Glover TW. The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum Mol Genet. 2005;14(5):693-701.
107. Vinciguerra P, Godinho SA, Parmar K, Pellman D, D'Andrea AD. Cytokinesis failure occurs in Fanconi anemia pathway-de fi cient murine and human bone marrow hematopoietic cells. J Clin Invest. 2010;120(11):3834-42.
108. Lahkim Bennani-Belhaj K, Rouzeau S, Buhagiar-Labarchede G, et al. The Bloom syndrome protein limits the lethality associated with RAD51 de fi ciency. Mol Cancer Res. 2010;8(3):385-94.
109. Chan KL, Hickson ID. On the origins of ultra- fi ne anaphase bridges. Cell Cycle. 2009;8(19):3065-6.
110. Suski C, Marians KJ. Resolution of converging replication forks by RecQ and topoisomerase III. Mol Cell. 2008;30(6):779-89.
111. Lukas C, Savic V, Bekker-Jensen S, et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol. 2011;13(3):243-53.
112. Sofueva S, Osman F, Lorenz A, et al. Ultra fi ne anaphase bridges, broken DNA and illegitimate recombination induced by a replication fork barrier. Nucleic Acids Res. 2011;39(15):6568-84.
113. Cha RS, Kleckner N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science. 2002;297(5581):602-6.
114. Dou H, Huang C, Nguyen TV, Lu LS, Yeh ETH. SUMOylation and de-SUMOylation in response to DNA damage. FEBS Lett. 2011;585(18):2891-6.
115. Branzei D, Sollier J, Liberi G, et al. Ubc9-and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell. 2006;127(3):509-22.
116. Eladad S, Ye TZ, Hu P, et al. Intra-nuclear traf fi cking of the BLM helicase to DNA damageinduced foci is regulated by SUMO modification. Hum Mol Genet. 2005;14(10):1351-65.
117. Ouyang KJ, Woo LL, Zhu JM, Huo DZ, Matunis MJ, Ellis NA. SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLOS Biol. 2009;7(12):e1000252.
118. Weidtkamp-Peters S, Lenser T, Negorev D, et al. Dynamics of component exchange at PML nuclear bodies. J Cell Sci. 2008;121(pt 16):2731-43.
119. Lu CY, Tsai CH, Brill SJ, Teng SC. Sumoylation of the BLM ortholog, Sgs1, promotes telomere-telomere recombination in budding yeast. Nucleic Acids Res. 2010;38(2):488-98.