p53 modulates homologous recombination by transcriptional regulation of the RAD51 gene

EMBO Reports

Volumn 7, Issue 2, 2006, Pages 219-224

  Arias Lopez, Carmen ^a   Lazaro Trueba, Iciar ^a   Kerr, Peter ^b   Lord, Christopher J ^b   Dexter, Tim ^b   Iravani, Marjan ^b   Ashworth, Alan ^b   Silva, Augusto ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Genome stability; Homologous recombination; p53; Rad51; Transcriptional repression

Indexed keywords

DOUBLE STRANDED DNA; MESSENGER RNA; PROTEIN P53; RAD51 PROTEIN; FLUORESCENT DYE; LUCIFERASE;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA RESPONSIVE ELEMENT; DNA STRAND BREAKAGE; DOWN REGULATION; GENETIC TRANSCRIPTION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANSCRIPTION REGULATION; WILD TYPE; CHROMATIN IMMUNOPRECIPITATION; FLUORESCENCE MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC RECOMBINATION; GENETICS; METABOLISM; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FLUORESCENT DYES; GENES, REPORTER; HUMANS; LUCIFERASES; MICROSCOPY, FLUORESCENCE; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33645814188     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/sj.embor.7400587     Document Type: Article

References (37)

1. Baptiste N, Friedlander P, Chen X, Prives C (2002) The proline-rich domain of p53 is required for cooperation with anti-neoplastic agents to promote apoptosis of tumor cells. Oncogene 21: 9-21
2. Baumann P, West SC (1998) Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem Sci 23: 247-251
3. Bernstein C, Bernstein H, Payne CM, Garewal H (2002) DNA repair/ pro-apoptotic dual-role proteins in five major DNA repair pathways: fail-safe protection against carcinogenesis. Mutat Res 511: 145-178
4. Bertrand P, Saintigny Y, Lopez BS (2004) p53's double life: transactivation-independent repression of homologous recombination. Trends Genet 20: 235-243
5. Boehden GS, Akyuz N, Roemer K, Wiesmuller L (2003) p53 mutated in the transactivation domain retains regulatory functions in homology-directed double-strand break repair. Oncogene 22: 4111-4117
6. Collis SJ, Tighe A, Scott SD, Roberts SA, Hendry JH, Margison GP (2001) Ribozyme minigene-mediated RAD51 down-regulation increases radiosensitivity of human prostate cancer cells. Nucleic Acids Res 29: 1534-1538
7. Dudenhoffer C, Kurth M, Janus F, Deppert W, Wiesmuller L (1999) Dissociation of the recombination control and the sequence-specific transactivation function of P53. Oncogene 18: 5773-5784
8. Espinosa JM, Emerson BM (2001) Transcriptional regulation by p53 through intrinsic DNA/chromatin binding and site-directed cofactor recruitment. Mol Cell 8: 57-69
9. Greenblatt MS, Bennett WP, Hollstein M, Harris CC (1994) Mutations in the p53 tumor suppressor gene: Clues to cancer etiology and molecular pathogenesis. Cancer Res 54: 4855-4878
10. Haaf T, Golub EI, Reddy G, Radding CM, Ward DC (1995) Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 92: 2298-2302
11. Ho J, Benchimol S (2003) Transcriptional repression mediated by the p53 tumour suppressor. Cell Death Differ 10: 404-408
12. Ivanov A, Cragg MS, Erenpreisa J, Emzinsh D, Lukman H, Illidge TM (2003) Endopolyploid cells produced after severe genotoxic damage have the potential to repair DNA double strand breaks. J Cell Sci 116: 4095-4106
13. Jimenez GS, Nister M, Stommel JM, Beeche M, Barcarse EA, Zhang XQ, O'Gorman S, Wahl GM (2000) A transactivation-deficient mouse model provides insights into Trp53 regulation and function. Nat Genet 26: 37-43
14. Kho PS, Wang Z, Zhuang L, Li Y, Chew JL, Ng HH, Liu ET, Yu Q (2004) p53-regulated transcriptional program associated with genotoxic stress-induced apoptosis. J Biol Chem 279: 21183-21192
15. Linke SP et al (2003) p53 interacts with hRAD51 and hRAD54, and directly modulates homologous recombination. Cancer Res 63: 2596-2605
16. Liu G, Parant JM, Lang G, Chau P, Chavez-Reyes A, El-Naggar AK, Multani A, Chang S, Lozano G (2004) Chromosome stability, in the absence of apoptosis, is critical for suppression of tumorigenesis in Trp53 mutant mice. Nat Genet 36: 63-68
17. Lu H, Levine AJ (1995) Human TAFII31 protein is a transcriptional coactivator of the p53 protein. Proc Natl Acad Sci USA 92: 5148-5154
18. Lu X, Bocangel D, Nannenga B, Yamaguchi H, Appella E, Donehower LA (2004) The p53-induced oncogenic phosphatase PPM1D interacts with uracil DNA glycosylase and suppresses base excision repair. Mol Cell 15: 621-634
19. Lundin C, Schultz N, Arnaudeau C, Mohindra A, Hansen LT, Helleday T (2003) RAD51 is involved in repair of damage associated with DNA replication in mammalian cells. J Mol Biol 328: 521-535
20. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM (2003) p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11: 577-590
21. Niculescu AB, Chen X, Smeets M, Hengst L, Prives C, Reed SI (1998) Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: PRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol Cell Biol 18: 629-643
22. Raderschall E, Golub EI, Haaf T (1999) Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc Natl Acad Sci USA 96: 1921-1926
23. Richardson C, Stark JM, Ommundsen M, Jasin M (2004) Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability. Oncogene 23: 546-553
24. Romanova LY, Willers H, Blagosklonny MV, Powell SN (2004) The interaction of p53 with replication protein A mediates suppression of homologous recombination. Oncogene 23: 9025-9033
25. Russell JS, Brady K, Burgan WE, Cerra MA, Oswald KA, Camphausen K, Tofilon PJ (2003) Gleevec-mediated inhibition of Rad51 expression and enhancement of tumor cell radiosensitivity. Cancer Res 63: 7377-7383
26. Saintigny Y, Lopez BS (2002) Homologous recombination induced by replication inhibition, is stimulated by expression of mutant p53. Oncogene 21: 488-492
27. Sengupta S, Harris CC (2005) p53: Traffic cop at the crossroads of DNA repair and recombination. Nat Rev Mol Cell Biol 6: 44-55
28. Shu Z, Smith S, Wang L, Rice MC, Kmiec EB (1999) Disruption of muREC2/ RAD51L1 in mice results in early embryonic lethality which can be partially rescued in a p53(-/-) background. Mol Cell Biol 19: 8686-8693
29. St Clair S, Giono L, Varmeh-Ziaie S, Resnick-Silverman L, Liu WJ, Padi A, Dastidar J, DaCosta A, Mattia M, Manfredi JJ (2004) DNA damage-induced downregulation of Cdc25C is mediated by p53 via two independent mechanisms: One involves direct binding to the cdc25C promoter. Mol Cell 16: 725-736
30. Tutt A, Bertwistle D, Valentine J, Gabriel A, Swift S, Ross G, Griffin C, Thacker J, Ashworth A (2001) Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J 20: 4704-4716
31. Van Gent DC, Hoeijmakers JH, Kanaar R (2001) Chromosomal stability and the DNA double-stranded break connection. Nat Rev Genet 2: 196-206
32. Vispe S, Cazaux C, Lesca C, Defais M (1998) Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res 26: 2859-2864
33. Wang L, Wu Q, Qiu P, Mirza A, McGuirk M, Kirschmeier P, Greene JR, Wang Y, Pickett CB, Liu S (2001) Analyses of p53 target genes in the human genome by bioinformatic and microarray approaches. J Biol Chem 276: 43604-43610
34. Willers H, McCarthy EE, Wu B, Wunsch H, Tang W, Taghian DG, Xia F, Powell SN (2000) Dissociation of p53-mediated suppression of homologous recombination from G1/S cell cycle checkpoint control. Oncogene 19: 632-639
35. Yoon D, Wang Y, Stapleford K, Wiesmuller L, Chen J (2004) P53 inhibits strand exchange and replication fork regression promoted by human Rad51. J Mol Biol 336: 639-654
36. Yu J, Zhang L, Hwang PM, Rago C, Kinzler KW, Vogelstein B (1999) Identification and classification of p53-regulated genes. Proc Natl Acad Sci USA 96: 14517-14522
37. Zhivotovsky B, Kroemer G (2004) Apoptosis and genomic instability. Nat Rev Mol Cell Biol 5: 752-762