DIDS, a chemical compound that inhibits RAD51-mediated homologous pairing and strand exchange

Nucleic Acids Research

Volumn 37, Issue 10, 2009, Pages 3367-3376

  Ishida, Takako ^a   Takizawa, Yoshimasa ^a   Kainuma, Takashi ^a   Inoue, Jin ^b   Mikawa, Tsutomu ^b,c   Shibata, Takehiko ^b   Suzuki, Hidekazu ^d   Tashiro, Satoshi ^d   Kurumizaka, Hitoshi ^a  

^a WASEDA UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c RIKEN SPring 8 center ^*  (Japan)

^d HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; RAD51 PROTEIN;

ARTICLE; BASE PAIRING; BINDING SITE; CONTROLLED STUDY; DNA BINDING; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; HUMAN; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DNA BINDING; SURFACE PLASMON RESONANCE; UPREGULATION;

4,4'-DIISOTHIOCYANOSTILBENE-2,2'-DISULFONIC ACID; ADENOSINE TRIPHOSPHATE; DNA; ENZYME INHIBITORS; HUMANS; RAD51 RECOMBINASE;

EUKARYOTA;

EID: 67249134799     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp200     Document Type: Article

References (44)

1. Whitaker,S.J. (1992) DNA damage by drugs and radiation: What is important and how is it measured? Eur. J. Cancer, 28, 273-276.
2. Cox,M.M., Goodman,M.F., Kreuzer,K.N., Sherratt,D.J., Sandler,S.J. and Marians,K.J. (2000) The importance of repairing stalled replication forks. Nature, 404, 37-41.
3. Symington,L.S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev., 66, 630-670.
4. West,S.C. (2003) Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol., 4, 435-445.
5. San Filippo,J., Sung,P. and Klein,H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem., 77, 229-257.
6. Sung,P., Krejci,L., Van Komen,S. and Sehorn,M.G. (2003) Rad51 recombinase and recombination mediators. J. Biol. Chem., 278 42729-42732.
7. Lim,D.-S. and Hasty,P. (1996) A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell Biol., 16, 7133-7143.
8. Tsuzuki,T., Fujii,Y., Sakumi,K., Tominaga,Y., Nakao,K., Sekiguchi,M., Matsushiro,A., Yoshimura,Y. and Morita,T. (1996) Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl Acad. Sci. USA, 93, 6236-6240.
9. Sonoda,E., Sasaki,M.S., Buerstedde,J.-M., Bezzubova,O., Shinohara,A., Ogawa,H., Takata,M., Yamaguchi-Iwai,Y. and Takeda,S. (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J., 17, 598-608.
10. Kato,M., Yano,K., Matsuo,F., Saito,H., Katagiri,T., Kurumizaka,H., Yoshimoto,M., Kasumi,F., Akiyama,F., Sakamoto,G. et al. (2000) Identification of Rad51 alteration in patients with bilateral breast cancer. J. Hum. Genet., 45, 133-137.
11. Levy-Lahad,E., Lahad,A., Eisenberg,S., Dagan,E., Paperna,T., Kasinetz,L., Catane,R., Kaufman,B., Beller,U., Renbaum,P. et al. (2001) A single nucleotide polymorphism in the RAD51 gene modifies cancer risk in BRCA2 but not BRCA1 carriers. Proc. Natl Acad. Sci. USA, 98, 3232-3236.
12. Wang,W.W., Spurdle,A.B., Kolachana,P., Bove,B., Modan,B., Ebbers,S.M., Suthers,G., Tucker,M.A., Kaufman,D.J., Doody,M.M. et al. (2001) A single nucleotide polymorphism in the 5′ untranslated region of RAD51 and risk of cancer among BRCA1/2 mutation carriers. Cancer Epidemiol. Biomarkers Prev., 10, 955-960.
13. Blasiak,J., Przybylowska,K., Czechowska,A., Zadrozny,M., Pertynński,T., Rykała,J., Kolacińska,A., Morawiec,Z. and Drzewoski,J. (2003) Analysis of the G/C polymorphism in the 5′-untranslated region of the RAD51 gene in breast cancer. Acta Biochim Pol., 50, 249-253.
14. Jakubowska,A., Narod,S.A., Goldgar,D.E., Mierzejewski,M., Masoj,B., Nej,K., Huzarska,J., Byrski,T., Górski,B. and Lubiński,J. (2003) Breast cancer risk reduction associated with the RAD51 polymorphism among carriers of the BRCA1 5382insC mutation in Poland. Cancer Epidemiol. Biomarkers Prev., 12, 457-459.
15. Ishida,T., Takizawa,Y., Sakane,I. and Kurumizaka,H. (2007) Altered DNA binding by the human Rad51-R150Q mutant found in breast cancer patients. Biol. Pharm. Bull., 30, 1374-1378.
16. Slupianek,A., Schmutte,C., Tombline,G., Nieborowska-Skorska,M., Hoser,G., Nowicki,M.O., Pierce,A.J., Fishel,R. and Skorski,T. (2001) BCR/ ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol. Cell, 8, 795-806.
17. Sung,P. (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science, 265, 1241-1243.
18. Sung,P. and Robberson,D.L. (1995) DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell, 82, 453-461.
19. Baumann,P., Benson,F.E. and West,S.C. (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell, 87, 757-766.
20. Maeshima,K., Morimatsu,K. and Horii,T. (1996) Purification and characterization of XRad51.1 protein, Xenopus RAD51 homologue: recombinant XRad51.1 promotes strand exchange reaction. Genes Cells 1, 1057-1068.
21. Gupta,R.C., Bazemore,L.R., Golub,E.I. and Radding,C.M. (1997) Activities of human recombination protein Rad51. Proc. Natl Acad. Sci. USA, 94, 463-468.
22. Matsuo,Y., Sakane,I., Takizawa,Y., Takahashi,M. and Kurumizaka,H. (2006) Roles of the human Rad51 L1 and L2 loops in DNA binding. FEBS J., 273, 3148-3159.
23. Henricksen,L.A., Umbricht,C.B. and Wold,M.S. (1994) Recombinant replication protein A: Expression, complex formation, and functional characterization. J. Biol. Chem., 269, 11121-11132.
24. Bradford,M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
25. Kagawa,W., Kurumizaka,H., Ikawa,S., Yokoyama,S. and Shibata,T. (2001) Homologous pairing promoted by the human Rad52 protein. J. Biol. Chem., 276, 35201-35208.
26. Kagawa,W., Kagawa,A., Saito,K., Ikawa,S., Shibata,T., Kurumizaka,H. and Yokoyama,S. (2008) Identification of a second DNA binding site in the human Rad52 protein. J. Biol. Chem., 283, 24264-24273.
27. Nomme,J., Takizawa,Y., Martinez,S.F., Renodon-Corniè re,A., Fleury,F., Weigel,P., Yamamoto,K., Kurumizaka,H. and Takahashi,M. (2008) Inhibition of filament formation of human Rad51 protein by a small peptide derived from the BRC-motif of the BRCA2 protein. Genes Cells 13, 471-481.
28. Davies,A.A., Masson,J.Y., McIlwraith,M.J., Stasiak,A.Z., Stasiak,A., Venkitaraman,A.R. and West,S.C. (2001) Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol. Cell, 7, 273-282.
29. Pellegrini,L., Yu,D.S., Lo,T., Anand,S., Lee,M., Blundell,T.L. and Venkitaraman,A.R. (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature, 420, 287-293.
30. Galkin,V.E., Esashi,F., Yu,X., Yang,S., West,S.C. and Egelman,E.H. (2005) BRCA2 BRC motifs bind RAD51-DNA filaments. Proc. Natl Acad. Sci. USA, 102, 8537-8542.
31. Ishida,T., Takizawa,Y., Sakane,I. and Kurumizaka,H. (2008) The Lys313 residue of the human Rad51 protein negatively regulates the strand-exchange activity. Genes Cells, 13, 91-103.
32. Klein,H.L. (2008) The consequences of Rad51 overexpression for normal and tumor cells. DNA Repair, 7, 686-693.
33. Rukść,A., Birmingham,E.C. and Baker,M.D. (2007) Altered DNA repair and recombination responses in mouse cells expressing wildtype or mutant forms of RAD51. DNA Repair, 6, 1876-1889.
34. Richardson,C., Stark,J.M., Ommundsen,M. and Jasin,M. (2004) Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability. Oncogene, 23, 546-553.
35. Hannay,J.A., Liu,J., Zhu,Q.S., Bolshakov,S.V., Li,L., Pisters,P.W., Lazar,A.J., Yu,D., Pollock,R.E. and Lev,D. (2007) Rad51 overexpression contributes to chemoresistance in human soft tissue sarcoma cells: A role for p53/activator protein 2 transcriptional regulation. Mol. Cancer Ther., 6, 1650-1660.
36. Martin,R.W., Orelli,B.J., Yamazoe,M., Minn,A.J., Takeda,S. and Bishop,D.K. (2007) RAD51 up-regulation bypasses BRCA1 function and is a common feature of BRCA1-deficient breast tumors. Cancer Res., 67, 9658-9665.
37. Aihara,H., Ito,Y., Kurumizaka,H., Yokoyama,S. and Shibata,T. (1999) The N-terminal domain of the human Rad51 protein binds DNA: Structure and a DNA binding surface as revealed by NMR. J. Mol. Biol., 290, 495-504.
38. Zhang,X.P., Lee,K.I., Solinger,J.A., Kiianitsa,K. and Heyer,W.D. (2005) Gly-103 in the N-terminal domain of Saccharomyces cerevisiae Rad51 protein is critical for DNA binding. J. Biol. Chem., 280, 26303-26311.
39. Shin,D.S., Pellegrini,L., Daniels,D.S., Yelent,B., Craig,L., Bates,D., Yu,D.S., Shivji,M.K., Hitomi,C., Arvai,A.S. et al. (2003) Fulllength archaeal Rad51 structure and mutants: Mechanisms for RAD51 assembly and control by BRCA2. EMBO J., 22, 4566-4576.
40. Chen,L-.T., Ko,T-.P., Chang,Y-.W., Lin,K-.A., Wang,A.H-.J. and Wang,T-.F. (2007) Structural and functional analyses of five conserved positively charged residues in the L1 and N-terminal DNA binding motifs of archaeal RadA protein. PLoS One, 9, 1-11.
41. Hikiba,J., Hirota,K., Kagawa,W., Ikawa,S., Kinebuchi,T., Sakane,I., Takizawa,Y., Yokoyama,S., Mandon-Pépin,B., Nicolas,A. et al. (2008) Structural and functional analyses of the DMC1-M200V polymorphism found in the human population. Nucleic Acids Res., 36, 4181-4190.
42. Hikiba,J., Takizawa,Y., Ikawa,S., Shibata,T. and Kurumizaka,H. (2009) Biochemical analysis of the human DMC1-I37N polymorphism. FEBS J., 276, 457-465.
43. Macara,I.G. and Cantley,L.C. (1981) Interactions between transport inhibitors at the anion binding sites of the band 3 dimer. Biochemistry, 20, 5095-5105.
44. Jayathilaka,K., Sheridan,S.D., Bold,T.D., Bochenska,K., Logan,H.L., Weichselbaum,R.R., Bishop,D.K. and Connell,P.P. (2008) A chemical compound that stimulates the human homologous recombination protein RAD51. Proc. Natl Acad. Sci. USA, 105, 15848-15853.