An essential DNA strand-exchange activity is conserved in the divergent N-termini of BLM orthologs

EMBO Journal

Volumn 29, Issue 10, 2010, Pages 1713-1725

  Chen, Chi Fu ^a   Brill, Steven J ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

BLM; Bloom's syndrome; DNA helicase; Sgs1; Synthetic lethality

Indexed keywords

BINDING PROTEIN; DOUBLE STRANDED DNA; FUNGAL PROTEIN; HETERODUPLEX; PROTEIN SGS1; PROTEIN TOP3 RMI1; RECQ HELICASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BLM GENE; BLOOM SYNDROME; CANCER SUSCEPTIBILITY; CONTROLLED STUDY; DNA BINDING; DNA STRAND; DROSOPHILA; GENE; GENE MUTATION; GENE REPRESSION; GENETIC CONSERVATION; GENETIC RECOMBINATION; GENOMIC INSTABILITY; HUMAN; IN VIVO STUDY; LETHALITY; MISMATCH REPAIR; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

ALLELES; ANIMALS; BLOOM SYNDROME; CONSERVED SEQUENCE; DNA; DNA HELICASES; DNA, SINGLE-STRANDED; DROSOPHILA MELANOGASTER; HUMANS; KINETICS; MUTATION; PROTEIN STRUCTURE, TERTIARY; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 77952583242     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.61     Document Type: Article

References (55)

1. Adams MD, McVey M, Sekelsky JJ (2003) Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science 299: 265-267
2. Bachrati CZ, Borts RH, Hickson ID (2006) Mobile D-loops are a preferred substrate for the Bloom's syndrome helicase. Nucleic Acids Res 34: 2269-2279
3. Bennett RJ, Keck JL (2004) Structure and function of RecQ DNA helicases. Crit Rev Biochem Mol Biol 39: 79-97
4. Bennett RJ, Noirot-Gros MF, Wang JC (2000) Interaction between yeast Sgs1 helicase and DNA topoisomerase III. J Biol Chem 275: 26898-26905
5. Bennett RJ, Wang JC (2001) Association of yeast DNA topoisome-rase III and Sgs1 DNA helicase: studies of fusion proteins. Proc Natl Acad Sci USA 98: 11108-11113
6. Bernstein DA, Keck JL (2005) Conferring substrate specificity to DNA helicases: role of the RecQ HRDC domain. Structure 13: 1173-1182
7. Bernstein DA, Zittel MC, Keck JL (2003) High-resolution structure of the E. coli RecQ helicase catalytic core. EMBO J 22: 4910-4921
8. Bernstein KA, Shor E, Sunjevaric I, Fumasoni M, Burgess RC, Foiani M, Branzei D, Rothstein R (2009) Sgs1 function in the repair of DNA replication intermediates is separable from its role in homologous recombinational repair. EMBO J 28: 915-925
9. Bugreev DV, Mazina OM, Mazin AV (2009) Bloom syndrome heli-case stimulates RAD51 DNA strand exchange activity through a novel mechanism. J Biol Chem 284: 26349-26359
10. Capp C, Wu J, Hsieh TS (2009) Drosophila RecQ4 has a 3-5DNA helicase activity that is essential for viability. J Biol Chem 284: 30845-30852
11. Chaganti RS, Schonberg S, German J (1974) A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc Natl Acad Sci USA 71: 4508-4512
12. Chen CF, Brill SJ (2007) Binding and activation of DNA topoisomerase III by the Rmi1 subunit. J Biol Chem 282: 28971-28979
13. Cheok CF, Wu L, Garcia PL, Janscak P, Hickson ID (2005) The Bloom's syndrome helicase promotes the annealing of complementary single-stranded DNA. Nucleic Acids Res 33: 3932-3941
14. Chu WK, Hickson ID (2009) RecQ helicases: multifunctional genome caretakers. Nat Rev Cancer 9: 644-654
15. Cromie GA, Hyppa RW, Smith GR (2008) The fission yeast BLM homolog Rqh1 promotes meiotic recombination. Genetics 179: 1157-1167
16. Fricke WM, Kaliraman V, Brill SJ (2001) Mapping the DNA topoi-somerase III binding domain of the Sgs1 DNA helicase. J Biol Chem 276: 8848-8855
17. Gangloff S, McDonald JP, 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: 8391-8398
18. Garcia PL, Liu Y, Jiricny J, West SC, Janscak P (2004) Human RECQ5beta, a protein with DNA helicase and strand-annealing activities in a single polypeptide. EMBO J 23: 2882-2891
19. 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: 743-753
20. Goldfarb T, Alani E (2005) Distinct roles for the Saccharomyces cerevisiae mismatch repair proteins in heteroduplex rejection, mismatch repair and nonhomologous tail removal. Genetics 169: 563-574
21. Hu Y, Lu X, Barnes E, Yan M, Lou H, Luo G (2005) Recql5 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers. Mol Cell Biol 25: 3431-3442
22. Karow JK, Constantinou A, Li JL, West SC, Hickson ID (2000) The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc Natl Acad Sci USA 97: 6504-6508
23. LeRoy G, Carroll R, Kyin S, Seki M, Cole MD (2005) Identification of RecQL1 as a Holliday junction processing enzyme in human cell lines. Nucleic Acids Res 33: 6251-6257
24. Lo YC, Paffett KS, Amit O, Clikeman JA, Sterk R, Brenneman MA, Nickoloff JA (2006) Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol Cell Biol 26: 4086-4094
25. Lu J, Mullen JR, Brill SJ, Kleff S, Romeo A, Sternglanz R (1996) Human homologs of yeast DNA helicase. Nature 383: 678-679
26. Machwe A, Lozada EM, Xiao L, Orren DK (2006) Competition between the DNA unwinding and strand pairing activities of the Werner and Bloom syndrome proteins. BMC Mol Biol 7: 1
27. Machwe A, Xiao L, Groden J, Matson SW, Orren DK (2005) RecQ family members combine strand pairing and unwinding activities to catalyze strand exchange. J Biol Chem 280: 23397-23407
28. Macris MA, Krejci L, Bussen W, Shimamoto A, Sung P (2006) Biochemical characterization of the RECQ4 protein, mutated in Rothmund-Thomson syndrome. DNA Repair (Amst) 5: 172-180
29. McIlwraith MJ, Vaisman A, Liu Y, Fanning E, Woodgate R, West SC (2005) Human DNA polymerase eta promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol Cell 20: 783-792
30. Mimitou EP, Symington LS (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455: 770-774
31. Miyajima A, Seki M, Onoda F, Ui A, Satoh Y, Ohno Y, Enomoto T (2000) Different domains of Sgs1 are required for mitotic and meiotic functions. Genes Genet Syst 75: 319-326 (Pubitemid 32175846)
32. Muftuoglu M, Kulikowicz T, Beck G, Lee JW, Piotrowski J, Bohr VA (2008) Intrinsic ssDNA annealing activity in the C-terminal region of WRN. Biochemistry 47: 10247-10254
33. Mullen JR, Kaliraman V, Brill SJ (2000) Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154: 1101-1114
34. Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ (2001) Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157: 103-118
35. Mullen JR, Nallaseth FS, Lan YQ, Slagle CE, Brill SJ (2005) Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex. Mol Cell Biol 25: 4476-4487
36. Muzzolini L, Beuron F, Patwardhan A, Popuri V, Cui S, Niccolini B, Rappas M, Freemont PS, Vindigni A (2007) Different quaternary structures of human RECQ1 are associated with its dual enzymatic activity. PLoS Biol 5: e20
37. 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: 16906-16911
38. Plank J, Hsieh TS (2009) Helicase-appended topoisomerases: new insight into the mechanism of directional strand exchange. J Biol Chem 284: 30737-30741
39. Plank JL, Wu J, Hsieh TS (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: 11118-11123
40. Ralf C, Hickson ID, Wu L (2006) The Bloom's syndrome helicase can promote the regression of a model replication fork. J Biol Chem 281: 22839-22846
41. Rockmill B, Fung JC, Branda SS, Roeder GS (2003) The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol 13: 1954-1962
42. Sharma S, Sommers JA, Choudhary S, Faulkner JK, Cui S, Andreoli L, Muzzolini L, Vindigni A, Brosh Jr RM (2005) Biochemical analysis of the DNA unwinding and strand annealing activities catalyzed by human RECQ1. J Biol Chem 280: 28072-28084
43. Sugawara N, Goldfarb T, Studamire B, Alani E, Haber JE (2004) Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc Natl Acad Sci USA 101: 9315-9320
44. Sun H, Karow JK, Hickson ID, Maizels N (1998) The Bloom's syndrome helicase unwinds G4 DNA. J Biol Chem 273: 27587-27592
45. Ui A, Satoh Y, Onoda F, Miyajima A, Seki M, Enomoto T (2001) 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 265: 837-850
46. 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: 409-419
47. Wang W, Seki M, Narita Y, Nakagawa T, Yoshimura A, Otsuki M, Kawabe Y, Tada S, Yagi H, Ishii Y, Enomoto T (2003) Functional relation among RecQ family helicases RecQL1, RecQL5, and BLM in cell growth and sister chromatid exchange formation. Mol Cell Biol 23: 3527-3535
48. Weinert BT, Rio DC (2007) DNA strand displacement, strand annealing and strand swapping by the Drosophila Bloom's syndrome helicase. Nucleic Acids Res 35: 1367-1376
49. Weinstein J, Rothstein R (2008) The genetic consequences of ablating helicase activity and the Top3 interaction domain of Sgs1. DNA Repair (Amst) 7: 558-571
50. Wu L, Chan KL, Ralf C, Bernstein DA, Garcia PL, Bohr VA, Vindigni A, Janscak P, Keck JL, Hickson ID (2005) The HRDC domain of BLM is required for the dissolution of double Holliday junctions. EMBO J 24: 2679-2687
51. Wu L, Davies SL, Levitt NC, Hickson ID (2001) Potential role for the BLM Helicase in recombinational repair via a conserved interaction with RAD51. J Biol Chem 276: 19375-19381
52. Wu L, Davies SL, North PS, Goulaouic H, Riou JF, Turley H, Gatter KC, Hickson ID (2000) The Bloom's syndrome gene product interacts with topoisomerase III. J Biol Chem 275: 9636-9644
53. Wu L, Hickson ID (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874
54. Xu X, Liu Y (2009) Dual DNA unwinding activities of the Rothmund-Thomson syndrome protein, RECQ4. EMBO J 28: 568-577
55. 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: 981-994