The Werner syndrome helicase/exonuclease processes mobile D-loops through branch migration and degradation

PLoS ONE

Volumn 4, Issue 3, 2009, Pages

  Opresko, Patricia L ^a   Sowd, Gregory ^a   Wang, Hong ^b,c  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ENDONUCLEASE; HELICASE; WERNER SYNDROME PROTEIN; EXODEOXYRIBONUCLEASE; EXONUCLEASE; RECQ HELICASE; WRN PROTEIN, HUMAN;

ARTICLE; BASE MISPAIRING; CONTROLLED STUDY; D LOOP; DNA DEGRADATION; DNA STRAND; DNA STRUCTURE; ENZYME ACTIVITY; ENZYME CHEMISTRY; ENZYME SUBSTRATE; HOMOLOGOUS RECOMBINATION; SINGLE STRANDED DNA BREAK; TELOMERE; TERMINAL SEQUENCE; DNA REPAIR; DNA REPLICATION; GENETIC RECOMBINATION; GENETICS; HUMAN; PLASMID; WERNER SYNDROME;

DNA REPAIR; DNA REPLICATION; EXODEOXYRIBONUCLEASES; EXONUCLEASES; HUMANS; PLASMIDS; RECOMBINATION, GENETIC; RECQ HELICASES; TELOMERE; WERNER SYNDROME;

EID: 62849091779     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004825     Document Type: Article

References (62)

1. Kudlow BA, Kennedy BK, Monnat RJ Jr (2007) Werner and Hutchinson-Gilford progeria syndromes: mechanistic basis of human progeroid diseases. Nat Rev Mol Cell Biol 8: 394-404.
2. Yu CE, Oshima J, Fu YH, Wijsman EM, Hisama F, et al. (1996) Positional cloning of the Werner's syndrome gene. Science 272: 258-262.
3. Hickson ID (2003) RecQ helicases: caretakers of the genome. Nat Rev Cancer 3: 169-178.
4. Opresko PL, Cheng WH, Bohr VA (2004) Junction of RecQ helicase biochemistry and human disease. J Biol Chem 279: 18099-18102.
5. Brosh RM Jr, Bohr VA (2007) Human premature aging, DNA repair and RecQ helicases. Nucleic Acids Res 35: 7527-7544.
6. Sung P, Klein H (2006) Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol 7: 739-750.
7. Wu L, Hickson ID (2006) DNA helicases required for homologous recombination and repair of damaged replication forks. Annu Rev Genet 40: 279-306.
8. Heller RC, Marians KJ (2006) Replisome assembly and the direct restart of stalled replication forks. Nat Rev Mol Cell Biol 7: 932-943.
9. Tarsounas M, West SC (2005) Recombination at mammalian telomeres: an alternative mechanism for telomere protection and elongation. Cell Cycle 4: 672-674.
10. Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265: 1241-1243.
11. McIlwraith MJ, Vaisman A, Liu Y, Fanning E, Woodgate R, et al. (2005) Human DNA polymerase eta promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol Cell 20: 783-792.
12. Adams MD, McVey M, Sekelsky JJ (2003) Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science 299: 265-267.
13. Schwacha A, Kleckner N (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
14. Bugreev DV, Yu X, Egelman EH, Mazin AV (2007) Novel pro- and antirecombination activities of the Bloom's syndrome helicase. Genes Dev 21: 3085-3094.
15. 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: 3073-3084.
16. Bugreev DV, Brosh RM Jr, Mazin AV (2008) RECQ1 Possesses DNA Branch Migration Activity. J Biol Chem 283: 20231-20242.
17. Bachrati CZ, Hickson ID (2003) RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem J 374: 577-606.
18. Ozsoy AZ, Ragonese HM, Matson SW (2003) Analysis of helicase activity and substrate specificity of Drosophila RECQ5. Nucleic Acids Res 31: 1554-1564.
19. Popuri V, Bachrati CZ, 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: 17766-17776.
20. Wu L, Hickson ID (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874.
21. Huang S, Li B, Gray MD, Oshima J, Mian IS, et al. (1998) The premature ageing syndrome protein, WRN, is a 3′←.5′ exonuclease. Nat Genet 20: 114-116.
22. Saintigny Y, Makienko K, Swanson C, Emond MJ, Monnat JR Jr (2002) Homologous recombination resolution defect in werner syndrome. Mol Cell Biol 22: 6971-6978.
23. Dhillon KK, Sidorova J, Saintigny Y, Poot M, Gollahon K, et al. (2007) Functional role of the Werner syndrome RecQ helicase in human fibroblasts. Aging Cell 6: 53-61.
24. Prince PR, Emond MJ, Monnat RJ Jr (2001) Loss of Werner syndrome protein function promotes aberrant mitotic recombination. Genes Dev 15: 933-938.
25. Swanson C, Saintigny Y, Emond MJ, Monnat RJ Jr (2004) The Werner syndrome protein has separable recombination and survival functions. DNA Repair 3: 475-482.
26. Crabbe L, Verdun RE, Haggblom CI, Karlseder J (2004) Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306: 1951-1953.
27. Bai Y, Murnane JP (2003) Telomere instability in a human tumor cell line expressing a dominant-negative WRN protein. Hum Genet 113: 337-347.
28. Laud PR, Multani AS, Bailey SM, Wu L, Ma J, et al. (2005) Elevated telomere-telomere recombination in WRN-deficient, telomere dysfunctional cells promotes escape from senescence and engagement of the ALT pathway. Genes Dev 19: 2560-2570.
29. Li B, Jog SP, Reddy S, Comai L (2008) WRN controls formation of extrachromosomal telomeric circles and is required for TRF2DeltaB-mediated telomere shortening. Mol Cell Biol 28: 1892-1904.
30. Chai W, Du Q, Shay JW, Wright WE (2006) Human telomeres have different overhang sizes at leading versus lagging strands. Mol Cell 21: 427-435.
31. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, et al. (1999) Mammalian telomeres end in a large duplex loop. Cell 97: 503-514.
32. Wang RC, Smogorzewska A, De Lange T (2004) Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119: 355-368.
33. de LT (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110.
34. Johnson FB, Marciniak RA, McVey M, Stewart SA, Hahn WC, et al. (2001) The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J 20: 905-913.
35. Cohen H, Sinclair DA (2001) Recombination-mediated lengthening of terminal telomeric repeats requires the Sgs1 DNA helicase. Proc Natl Acad Sci 98: 3174-3179.
36. Orren DK, Theodore S, Machwe A (2002) The Werner Syndrome Helicase/ Exonuclease (WRN) Disrupts and Degrades D- Loops in Vitro. Biochemistry 41: 13483-13488.
37. Opresko PL, Otterlei M, Graakjaer J, Bruheim P, Dawut L, 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: 763-774.
38. Opresko PL, Mason PA, Podell ER, Lei M, Hickson ID, et al. (2005) POT1 stimulates RecQ helicases WRN and BLM to unwind telomeric DNA substrates. J Biol Chem 280: 32069-32080.
39. Opresko PL (2007) Telomere ResQue and preservation-Roles for the Werner syndrome protein and other RecQ helicases. Mech Ageing Dev 129: 79-90.
40. Opresko PL, von Kobbe C, Laine JP, Harrigan J, Hickson ID, et al. (2002) Telomere-binding Protein TRF2 Binds to and Stimulates the Werner and Bloom Syndrome Helicases. J Biol Chem 277: 41110-41119.
41. Brosh RM Jr, Orren DK, Nehlin JO, Ravn PH, Kenny MK, et al. (1999) Functional and physical interaction between WRN helicase and human replication protein A. J Biol Chem 274: 18341-18350.
42. Opresko PL, Laine JP, Brosh RM Jr, Seidman MM, Bohr VA (2001) Coordinate Action of the Helicase and 39 to 59 Exonuclease of Werner Syndrome Protein. J Biol Chem 276: 44677-44687.
43. Choudhary S, Sommers JA, Brosh RM Jr (2004) Biochemical and kinetic characterization of the DNA helicase and exonuclease activities of werner syndrome protein. J Biol Chem 279: 34603-34613.
44. Perry JJ, Yannone SM, Holden LG, Hitomi C, Asaithamby A, et al. (2006) WRN exonuclease structure and molecular mechanism imply an editing role in DNA end processing. Nat Struct Mol Biol 13: 414-422.
45. Choi JM, Kang SY, Bae WJ, Jin KS, Ree M, et al. (2007) Probing the roles of active site residues in the 39-59 exonuclease of the Werner syndrome protein. J Biol Chem 282: 9941-9951.
46. Machwe A, Xiao L, Orren DK (2006) Length-dependent degradation of single-stranded 3′ ends by the Werner syndrome protein (WRN): implications for spatial orientation and coordinated 3′ to 5′ movement of its ATPase/helicase and exonuclease domains. BMC Mol Biol 7: 6.
47. Kamath-Loeb AS, Shen JC, Loeb LA, Fry M (1998) Werner Syndrome Protein. Ii. characterization of the integral 3′←5′ dna exonuclease. J Biol Chem 273: 34145-34150.
48. 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.
49. Brosh RM Jr, Waheed J, Sommers JA (2002) Biochemical characterization of the DNA substrate specificity of werner syndrome helicase. J Biol Chem 277: 23236-23245.
50. 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.
51. Machwe A, Xiao L, Theodore S, Orren DK (2002) DNase I footprinting and enhanced exonuclease function of the bipartite Werner syndrome protein (WRN) bound to partially melted duplex DNA. J Biol Chem 277: 4492-4504.
52. Compton SA, Tolun G, Kamath-Loeb AS, Loeb LA, Griffith JD (2008) The Werner syndrome protein binds replication fork and holliday junction DNAs as an oligomer. J Biol Chem 283: 24478-24483.
53. Driscoll HC, Matson SW, Sayer JM, Kroth H, Jerina DM, et al. (2003) Inhibition of Werner syndrome helicase activity by benzo [c]phenanthrene diol epoxide dA adducts in DNA is both strand-and stereoisomer-dependent. J Biol Chem 278: 41126-41135.
54. Baumann P, Benson FE, West SC (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87: 757-766.
55. McIlwraith MJ, Van DE, Masson JY, Stasiak AZ, Stasiak A, et al. (2000) Reconstitution of the strand invasion step of double-strand break repair using human Rad51 Rad52 and RPA proteins. J Mol Biol 304: 151-164.
56. Donmez I, Rajagopal V, Jeong YJ, Patel SS (2007) Nucleic acid unwinding by hepatitis C virus and bacteriophage t7 helicases is sensitive to base pair stability. J Biol Chem 282: 21116-21123.
57. SantaLucia J, Jr. (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc Natl Acad Sci U S A 95: 1460-1465.
58. Mohaghegh P, Karow JK, Brosh JR Jr, Bohr VA, Hickson ID (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res 29: 2843-2849.
59. Verdun RE, Crabbe L, Haggblom C, Karlseder J (2005) Functional human telomeres are recognized as DNA damage in g2 of the cell cycle. Mol Cell 20: 551-561.
60. Sowd G, Lei M, Opresko PL (2008) Mechanism and substrate specificity of telomeric protein POT1 stimulation of the Werner syndrome helicase. Nucleic Acids Res 36: 4242-4256.
61. Hile SE, Yan G, Eckert KA (2000) Somatic mutation rates and specificities at TC/AG and GT/CA microsatellite sequences in nontumorigenic human lymphoblastoid cells. Cancer Res 60: 1698-1703.
62. Bachrati CZ, Hickson ID (2006) Analysis of the DNA unwinding activity of RecQ family helicases. Methods Enzymol 409: 86-100.