Possible anti-recombinogenic role of Bloom's syndrome helicase in double-strand break processing

Nucleic Acids Research

Volumn 31, Issue 21, 2003, Pages 6272-6282

  Onclercq Delic, Rosine ^c   Calsou, Patrick ^a   Delteil, Christine ^a   Salles, Bernard ^a   Papadopoulo, Dora ^b   Amor Guéret, Mounira ^c  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b INSTITUT CURIE   (France)

^c INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; HELICASE; PROTEIN KINASE;

ARTICLE; BINDING AFFINITY; BLOOM SYNDROME; CONTROLLED STUDY; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVE SITE; GEL MOBILITY SHIFT ASSAY; GENE MUTATION; GENETIC CODE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANTIGENS, NUCLEAR; BLOOM SYNDROME; CELL LINE, TRANSFORMED; DNA; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PHOSPHORYLATION; PRECIPITIN TESTS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC;

MAMMALIA;

EID: 0344011101     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkg834     Document Type: Article

References (65)

1. German,J. (1993) Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine, 72, 393-406.
2. Ellis,N.A., Groden,J., Ye,T.Z., Straughen,J., Lennon,D.J., Ciocci,S., Proytcheva,M. and German,J. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell, 83, 8655-8666.
3. Karow,J.K., Chakraverty,R.K. and Hickson,I.D. (1997) The Bloom's syndrome gene product is a 3′-5′ DNA helicase. J. Biol. Chem., 272, 30611-30614.
4. Haber,J.E. (2000) Partners and pathways repairing a double-strand break. Trends Genet., 16, 259-264.
5. vanGent,D.C., Hoeijmakers,J.H. and Kanaar,R. (2001) Chromosomal stability and the DNA double-stranded break connection. Nature Rev. Genet., 2, 196-206.
6. Haber,J.E. (1999) DNA repair. Gatekeepers of recombination. Nature, 398, 665-667.
7. Takata,M., Sasaki,M.S., Sonoda,E., Morrison,C., Hashimoto,M., Utsumi,H., Yamaguchi-Iwai,Y., Shinohara,A. and Takeda,S. (1998) Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in verubrate cells. EMBO J., 17, 5497-5508.
8. VanDyck,E., Stasiak,A.Z., Stasiak,A. and West,S.C. (1999) Binding of double-strand breaks in DNA by human Rad52 protein. Nature, 398, 728-731.
9. Pierce,A.J., Hu,P., Han,M., Ellis,N. and Jasin,M. (2001) Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev., 15, 3237-3242.
10. Saintigny,Y., Delacôte,F., Vares,G., Petitot,F., Lambert,S., Averbeck,D. and Lopez,B.S. (2001) Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J., 20, 3861-3870.
11. Delacôte,F., Han,M., Stamato,T.D., Jasin,M. and Lopez,B.S. (2002) An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells. Nucleic Acids Res., 30, 3454-3463.
12. 2 phase DNA double-strand break repair. J. Biol. Chem., 276, 44413-44418.
13. Allen,C., Kurimasa,A., Brenneman,M.A., Chen,D.J. and Nickoloff,J.A. (2002) DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc. Natl Acad. Sci. USA, 99, 3758-3763.
14. Rünger,T.M. and Kraemer,K.H. (1989) Joining of linear plasmid DNA is reduced and error-prone in Bloom's syndrome cells. EMBO J., 8, 1419-1425.
15. Gaymes,T.J., North,P.S., Brady,N., Hickson,I.D., Mufti,G.J. and Rassool,F.V. (2002) Increased error-prone non homologous DNA end-joining - a proposed mechanism of chromosomal instability in Bloom's syndrome. Oncogene, 21, 2525-2533.
16. Langland,G., Elliott,J., Li,Y., Creaney,J., Dixon,K. and Groden,J. (2002) The BLM helicase is necessary for normal DNA double-strand break repair. Cancer Res., 62, 2766-2770.
17. Dutertre,S., Ababou,M., Onclercq,R., Delic,J., Chatton,B., Jaulin,C. and Amor-Gueret,M. (2000) Cell cycle regulation of the endogenous wild type Bloom's syndrome DNA helicase. Oncogene, 19, 2731-2738.
18. Kawabe,T., Tsuyama,N., Kitao,S., Nishikawa,K., Shimamoto,A., Shiratori,M., Matsumoto,T., Anno,K., Sato,T., Mitsui,Y., Seki,M., Enomoto,T., Goto,M., Ellis,N.A., Ide,T., Furuichi,Y. and Sugimoto,M. (2000) Differential regulation of human RecQ family helicases in cell transformation and cell cycle. Oncogene, 19, 4764-4772.
19. Thompson,L.H. and Schild,D. (2002) Recombinational DNA repair and human disease. Mutat. Res., 509, 49-78.
20. Sonoda,E., Sasaki,M.S., Morrison,C., Yamaguchi-Iwai,Y., Takata,M. and Takeda,S. (1999) Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol., 19, 5166-5169.
21. Wang,W., Seki,M., Narita,Y., Sonoda,E., Takeda,S., Yamada,K., Masuko,T., Katada,T. and Enomoto,T. (2000) Possible association of BLM in decreasing DNA double strand breaks during DNA replication. EMBO J., 19, 3428-3435.
22. Karow,J.K., Constantinou,A., Li,J.L., West,S.C. and Hickson,I.D. (2000) The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc. Natl Acad. Sci. USA, 97, 6504-6508.
23. Luo,G., Santoro,I.M., McDaniel,L.D., Nishijima,I., Mills,M., Youssoufian,H., Vogel,H., Schultz,R.A. and Bradley,A. (2000) Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nature Genet., 26, 424-429.
24. Ababou,M., Dutertre,S., Lecluse,Y., Onclercq,R., Chatton,B. and Amor-Gueret,M. (2000) ATM-dependent phosphorylation and accumulation of endogenous BLM protein in response to ionizing radiation. Oncogene, 19, 5955-5963.
25. Dutertre,S., Sekhri,R., Tintignac,L.A., Onclercq-Delic,R., Chatton,B., Jaulin,C. and Amor-Gueret,M. (2002) Dephosphorylation and subcellular compartment change of the mitotic Bloom's syndrome DNA helicase in response to ionizing radiation. J. Biol. Chem., 277, 6280-6286.
26. Dignam,J.D., Lebovitz,R.M. and Roeder,R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-89.
27. Hoppe,B.S., Jensen,R.B. and Kirchgessner,C.U. (2000) Complementation of the radiosensitive M059J cell line. Radiat. Res., 153, 125-130.
28. Jessberger,R. and Berg,P. (1991) Repair of deletions and double-strand gaps by homologous recombination in a mammalian in vitro system. Mol. Cell. Biol., 11, 445-457.
29. Smith,J., Andrau,J.C., Kallenbach,S., Laquerbe,A., Doyen,N. and Papadopoulo,D. (1998) Abnormal rearrangements associated with V(D)J recombination in Fanconi anemia. J. Mol. Biol., 281, 815-825.
30. Baldeyron,C., Jacquemin,E., Smith,J., Jacquemont,C., De Oliveira,I., Gad,S., Feunteun,J., Stoppa-Lyonnet,D. and Papadopoulo,D. (2002) A single mutated BRCA1 allele leads to impaired fidelity of double strand break end-joining. Oncogene, 21, 1401-1410.
31. Smith,J., Riballo,E., Kysela,B., Baldeyron,C., Manolis,K., Masson,C., Lieber,M.R., Papadopoulo,D. and Jeggo,P. (2003) Impact of DNA ligase IV on the fidelity of end-joining in human cells. Nucleic Acids Res., 31, 2157-2167.
32. Minc,E., de Coppet,P., Masson,P., Thiery,L., Dutertre,S., Amor-Gueret,M. and Jaulin,C. (1999) The human copper-zinc superoxide dismutase gene (SOD1) proximal promoter is regulated by Sp1, Egr-1 and WT1 via non-canonical binding sites. J. Biol. Chem., 274, 503-509.
33. Birnboim,H.C. and Doly,J. (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res., 7, 1513-1523.
34. Gottlieb,T.M. and Jackson,S.P. (1993) The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell, 72, 131-142.
35. Kusano,K., Johnson-Schlitz,D.M. and Engels,W.R. (2001) Sterility of Drosophila with mutations in the Bloom syndrome gene - complementation by Ku70. Science, 291, 2600-2602.
36. Suwa,A., Hirakata,M., Takeda,Y., Jesch,S.A., Mimori,T. and Hardin,J.A. (1994) DNA-dependent protein kinase (Ku protein-p350 complex) assembles on double-stranded DNA. Proc. Natl Acad Sci. USA, 91, 6904-6908.
37. Calsou,P., Delteil,C., Frit,P., Drouet,J. and Salles,B. (2003) Coordinated assembly of Ku and p460 subunits of the DNA-dependent protein kinase on DNA ends is necessary for XRCC4-ligase IV recruitment. J. Mol. Biol., 326, 93-103.
38. Chan,D.W. and Lees-Miller,S.P. (1996) The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. J. Biol. Chem., 271, 8936-8941.
39. Calsou,P., Frit,P., Humbert,O., Muller,C., Chen,D.J. and Salles,B. (1999) The DNA-dependent protein kinase catalytic activity regulates DNA end processing by means of Ku entry into DNA. J. Biol. Chem., 274, 7848-7856.
40. Frit,P., Li,R.Y., Arzel,D., Salles,B. and Calsou,P. (2000) Ku entry into DNA inhibits inward DNA transactions in vitro. J. Biol. Chem., 275, 35684-35691.
41. Chan,D.W., Chen,B.P., Prithivirajsingh,S., Kurimasa,A., Story,M.D., Qin,J. and Chen,D.J. (2002) Autophosphorylation of the DNA-dependent Protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev., 6, 2333-2338.
42. Merkle,D., Douglas,P., Moorhead,G.B., Leonenko,Z., Yu,Y., Cramb,D., Bazett-Jones,D.P. and Lees-Miller,S.P. (2002) The DNA-dependent protein kinase interacts with DNA to form a protein-DNA complex that is disrupted by phosphorylation. Biochemistry, 41, 12706-12714.
43. Escarceller,M., Buchwald,M., Singleton,B.K., Jeggo,P.A., Jackson,S.P., Moustacchi,E. and Papadopoulo D. (1998) Fanconi anemia C gene product plays a role in the fidelity of blunt DNA end-joining. J. Mol. Biol., 279, 375-385.
44. Mohaghegh,P., Karow,J.K., Brosh Jr,R.M., Bohr,V.A. and Hickson,I.D. (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res., 29, 2843-2849.
45. Wang,X.W., Tseng,A., Ellis,N.A., Spillare,E.A., Linke,S.P., Robles,A.I., Seker,H., Yang,Q., Hu,P., Beresten,S., Bemmels,N.A., Garfield,S. and Harris,C.C. (2001) Functional interaction of p53 and BLM DNA helicase in apoptosis. J. Biol. Chem., 276, 32948-32955.
46. Hsieh,C.L., Arlett,C.F. and Lieber,M.R. (1993) V(D)J recombination in ataxia telangiectasia, Bloom's syndrome and a DNA ligase I-associated immunodeficiency disorder. J. Biol. Chem., 268, 20105-20109.
47. Petrini,J.H., Donovan,J.W., Dimare,C. and Weaver,D.T. (1994) Normal V(D)J coding junction formation in DNA ligase I deficiency syndromes. J. Immunol., 152, 176-183.
48. Sack,S.Z., Liu,Y., German,J. and Green,N.S. (1998) Somatic hypermutation of immunoglobulin genes is independent of the Bloom's syndrome DNA helicase. Clin. Exp. Immunol., 112, 248-54.
49. Kaneko,H., Matsui,E., Fukao,T., Kasahara,K., Morimoto,W. and Kondo,N. (1999) Expression of the BLM gene in human haematopoietic cells. Clin. Exp. Immunol., 118, 285-289.
50. Chappell,C., Hanakahi,L.A., Karimi-Busheri,F., Weinfeld,M. and West,S.C. (2002) Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining. EMBO J., 21, 2827-2832.
51. Bertrand,P., Rouillard,D., Boulet,A., Levalois,C., Soussi,T. and Lopez,B.S. (1997) Increase of spontaneous intrachromosomal homologous recombination in mammalian cells expressing a mutant p53 protein. Oncogene, 14, 1117-1122.
52. Mekeel,K.L., Tang,W., Kachnic,L.A., Luo,C.M., DeFrank,J.S. and Powell,S.N. (1997) Inactivation of p53 results in high rates of homologous recombination. Oncogene, 14, 1847-1857.
53. Buchhop,S., Gibson,M.K., Wang,X.W., Wagner,P., Sturzbecher,H.W. and Harris,C.C. (1997) Interaction of p53 with the human Rad51 protein. Nucleic Acids Res., 25, 3868-3874.
54. Garkavtsev,I.V., Kley,N., Grigorian,I.A. and Gudkov A.V. (2001) The Bloom syndrome protein interacts and cooperates with p53 in regulation of transcription and cell growth control. Oncogene, 20, 8276-8280.
55. Yang,Q., Zhang,R., Wang,X.W., Spillare,E.A., Linke,S.P., Subramanian,D., Griffith,J.D., Li,J.L., Hickson,I.D., Shen,J.C., Loeb,L.A., Mazur,S.J., Appella,E., Brosh Jr.,R.M., Karmakar,P., Bohr,V.A. and Harris,C.C. (2002) The processing of Holliday junctions by BLM and WRN helicases is regulated by p53. J. Biol. Chem., 277, 31980-31987.
56. Sengupta,S., Linke,S.P., Pedeux,R., Yang,Q., Farnsworth,J., Garfield,S.H., Valerie,K., Shay,J.W., Ellis,N.A., Wasylyk,B. and Harris,C.C. (2003) BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J., 22, 1-13.
57. Lu,X. and Lane,D.P. (1993) Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell, 75, 765-778.
58. Michel,B. (2000) Replication fork arrest and DNA recombination. Trends Biochem. Sci., 4, 173-178.
59. Richardson,C. and Jasin,M. (2000) Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell. Biol., 20, 9068-9075.
60. Kraus,E., Leung,W.Y. and Haber,J.E. (2001) Break-induced replication: a review and an example in budding yeast. Proc. Natl Acad. Sci. USA, 98, 8255-8262.
61. Stavropoulos,D.J., Bradshaw,P.S., Li,X., Pasic,I., Truong,K., Ikura,M., Ungrin,M. and Meyn M.S. (2002) The Bloom syndrome helicase BLM interacts with TRF2 in ALT cells and promotes telomeric DNA synthesis. Hum. Mol. Genet., 11, 3135-44.
62. Nakayama,H. (2002) RecQ family helicases: roles as tumor suppressor proteins. Oncogene, 21, 9008-9021.
63. Stark,J.M. and Jasin M. (2003) Extensive loss of heterozygosity is suppressed during homologous repair of chromosomal breaks. Mol. Cell. Biol., 23, 733-743.
64. Hickson,I.D. (2003) RecQ helicases: caretakers of the genome. Nature Rev. Cancer, 3, 169-178.
65. Wu,L. and Hickson,I.D. (2002) The Bloom's syndrome helicase stimulates the activity of human topoisomerase IIIα. Nucleic Acids Res., 30, 4823-4829.