Transcription inhibition by 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole (DRB) causes DNA damage and triggers homologous recombination repair in mammalian cells

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 706, Issue 1-2, 2011, Pages 1-6

  Stoimenov, Ivaylo ^a   Gottipati, Ponnari ^b   Schultz, Niklas ^a   Helleday, Thomas ^a,b  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

DNA damage repair; DRB; Homologous recombination; Mammalian cells; Transcription

Indexed keywords

5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; HISTONE H2AX; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; RAD51 PROTEIN; RNA POLYMERASE II; XRCC3 PROTEIN;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; ENZYME PHOSPHORYLATION; GENE TRANSCRIPTION INHIBITION; GENETIC TRANSCRIPTION; HOMOLOGOUS RECOMBINATION; MAMMAL CELL; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; STRESS; TRANSCRIPTIONAL STRESS;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; ENZYME INHIBITORS; HISTONES; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; MICROSCOPY, CONFOCAL; MUTATION; PHOSPHORYLATION; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 78650420121     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.10.012     Document Type: Article

References (25)

1. Aguilera A. The connection between transcription and genomic instability. EMBO J. 2002, 21:195-201.
2. Prado F., Aguilera A. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 2005, 24:1267-1276.
3. Takeuchi Y., Horiuchi T., Kobayashi T. Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev. 2003, 17:1497-1506.
4. Gottipati P., Cassel T.N., Savolainen L., Helleday T. Transcription-associated recombination is dependent on replication in mammalian cells. Mol. Cell Biol. 2008, 28:154-164.
5. Garcia-Rubio M., Huertas P., Gonzalez-Barrera S., Aguilera A. Recombinogenic effects of DNA-damaging agents are synergistically increased by transcription in Saccharomyces cerevisiae. New insights into transcription-associated recombination. Genetics 2003, 165:457-466.
6. Gonzalez-Aguilera C., Tous C., Gomez-Gonzalez B., Huertas P., Luna R., Aguilera A. The THP1-SAC3-SUS1-CDC31 complex works in transcription elongation-mRNA export preventing RNA-mediated genome instability. Mol. Biol. Cell 2008, 19:4310-4318.
7. Huertas P., Aguilera A. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 2003, 12:711-721.
8. Yamaguchi-Iwai Y., Sonoda E., Sasaki M.S., Morrison C., Haraguchi T., Hiraoka Y., Yamashita Y.M., Yagi T., Takata M., Price C., Kakazu N., Takeda S. Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J. 1999, 18:6619-6629. 10: C. Morrison, et al., The essential functions of hu...[PMID:10490626]Related Articles, Links.
9. Zandomeni R., Mittleman B., Bunick D., Ackerman S., Weinmann R. Mechanism of action of dichloro-beta-D-ribofuranosylbenzimidazole: effect on in vitro transcription. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:3167-3170.
10. Klibanov S.A., O'Hagan H.M., Ljungman M. Accumulation of soluble and nucleolar-associated p53 proteins following cellular stress. J. Cell Sci. 2001, 114:1867-1873.
11. Ljungman M., Zhang F., Chen F., Rainbow A.J., McKay B.C. Inhibition of RNA polymerase II as a trigger for the p53 response. Oncogene 1999, 18:583-592.
12. Nickoloff J.A., Reynolds R.J. Transcription stimulates homologous recombination in mammalian cells. Mol. Cell Biol. 1990, 10:4837-4845.
13. Chavez S., Aguilera A. The yeast HPR1 gene has a functional role in transcriptional elongation that uncovers a novel source of genome instability. Genes Dev. 1997, 11:3459-3470.
14. Helleday T., Arnaudeau C., Jenssen D. A partial hprt gene duplication generated by non-homologous recombination in V79 Chinese hamster cells is eliminated by homologous recombination. J. Mol. Biol. 1998, 279:687-694.
15. Haaf T., Golub E.I., Reddy G., Radding C.M., Ward D.C. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:2298-2302.
16. Lundin C., Erixon K., Arnaudeau C., Schultz N., Jenssen D., Meuth M., Helleday T. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell Biol. 2002, 22:5869-5878.
17. Petermann E., Orta M.L., Issaeva N., Schultz N., Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 2010, 37:492-502.
18. Kinner A., Wu W., Staudt C., Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 2008, 36:5678-5694.
19. Marti T.M., Hefner E., Feeney L., Natale V., Cleaver J.E. H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:9891-9896.
20. Tebbs R.S., Zhao Y., Tucker J.D., Scheerer J.B., Siciliano M.J., Hwang M., Liu N., Legerski R.J., Thompson L.H. Correction of chromosomal instability and sensitivity to diverse mutagens by a cloned cDNA of the XRCC3 DNA repair gene. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:6354-6358.
21. Chodosh L.A., Fire A., Samuels M., Sharp P.A. 5,6-Dichloro-1-beta-D-ribofuranosylbenzimidazole inhibits transcription elongation by RNA polymerase II in vitro. J. Biol. Chem. 1989, 264:2250-2257.
22. Bartkova J., Rezaei N., Liontos M., Karakaidos P., Kletsas D., Issaeva N., Vassiliou L.V., Kolettas E., Niforou K., Zoumpourlis V.C., Takaoka M., Nakagawa H., Tort F., Fugger K., Johansson F., Sehested M., Andersen C.L., Dyrskjot L., Orntoft T., Lukas J., Kittas C., Helleday T., Halazonetis T.D., Bartek J., Gorgoulis V.G. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006, 444:633-637.
23. Arnaudeau C., Lundin C., Helleday T. DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol. 2001, 307:1235-1245.
24. Prado F., Aguilera A. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 2005, 3.
25. Derheimer F.A., O'Hagan H.M., Krueger H.M., Hanasoge S., Paulsen M.T., Ljungman M. RPA and ATR link transcriptional stress to p53. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12778-12783.