Discriminatory suppression of homologous recombination by p53

Nucleic Acids Research

Volumn 32, Issue 22, 2004, Pages 6479-6489

  Yun, Sheng ^a   Lie A Cheong, Chadwick ^a   Porter, Andrew C G ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; PROTEIN P53; RAD51 PROTEIN;

ARTICLE; CHROMOSOME; COMPARATIVE STUDY; CONTROLLED STUDY; DNA INTEGRATION; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME REPRESSION; GENE DISRUPTION; GENE TARGETING; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC SUSCEPTIBILITY; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MISMATCH REPAIR; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SOMATIC CELL; TRANSACTIVATION; TRANSCRIPTION REGULATION; VERTEBRATE;

BASE PAIR MISMATCH; CELL LINE; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; GENE TARGETING; HUMANS; RECOMBINATION, GENETIC; RNA INTERFERENCE; TUMOR SUPPRESSOR PROTEIN P53;

VERTEBRATA;

EID: 13544267789     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh986     Document Type: Article

References (63)

1. van Gent,D.C., Hoeijmakers,J.H. and Kanaar,R. (2001) Chromosomal stability and the DNA double-stranded break connection. Nature Rev. Genet., 2, 196-206.
2. Sonoda,E., Sasaki,M.S., Buerstedde,J.M., Bezzubova,O., Shinohara,A., Ogawa,H., Takata,M., Yamaguchi-Iwai,Y. andTakeda,S. (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J., 17, 598-608.
3. 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.
4. Porter,A.C.G. (2002) Homologous recombination. In Sons,J.W. (ed.), Wiley Encyclopedia of Molecular Medicine. John Wiley & Sons, Inc., NY, Vol. 3, pp. 1662-1666.
5. Inoue,K. and Lupski,J.R. (2002) Molecular mechanisms for genomic disorders. Annu. Rev. Genomics Hum. Genet., 3, 199-242.
6. Saintigny,Y., Dumay,A., Lambert,S. and Lopez,B.S. (2001) A novel role for the Bcl-2 protein family: specific suppression of the RAD51 recombination pathway. EMBO J., 20, 2596-2607.
7. Slupianek,A., Schmutte,C., Tombline,G., Nieborowska-Skorska,M., Hoser,G., Nowicki,M.O., Pierce,A.J., Fisbel,R. and Skorski,T. (2001) BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol. Cell, 8, 795-806.
8. Wiese,C., Pierce,A.J., Gauny,S.S., Jasin,M. and Kronenberg,A. (2002) Gene conversion is strongly induced in human cells by double-strand breaks and is modulated by the expression of BCL-x(L). Cancer Res., 62, 1279-1283.
9. Elliott,B. and Jasin,M. (2001) Repair of double-strand breaks by homologous recombination in mismatch repair-defective mammalian cells. Mol. Cell. Biol., 21, 2671-2682.
10. Evans,E. and Alani,E. (2000) Roles for mismatch repair factors in regulating genetic recombination. Mol. Cell. Biol., 20, 7839-7844.
11. de Wind,N., Dekker,M., Berns,A., Radman,M. and te Riele,H. (1995) Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell, 82, 321-330.
12. Powell,S.N., Willers,H. and Xia,F. (2002) BRCA2 keeps Rad51 in line. High-fidelity homologous recombination prevents breast and ovarian cancer? Mol. Cell, 10, 1262-1263.
13. Jasin,M. (2002) Homologous repair of DNA damage and tumorigenesis: the BRCA connection. Oncogene, 21, 8981-8993.
14. Tutt,A. and Ashworth,A. (2002) The relationship between the roles of BRCA genes in DNA repair and cancer predisposition. Trends Mol. Med., 8, 571-576.
15. 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. et al. (2002) The processing of Holliday junctions by BLM and WRN helicases is regulated by p53. J. Biol. Chem., 277, 31980-31987.
16. Traverso,G., Bettegowda,C., Kraus,J., Speicher,M.R., Kinzler,K.W., Vogelstein,B. and Lengauer,C. (2003) Hyper-recombination and genetic instability in BLM-deficient epithelial cells. Cancer Res. 63, 8578-8581.
17. Bertrand,P., Saintigny,Y. and Lopez,B.S. (2004) p53's double life: transactivation-independent repression of homologous recombination. Trends Genet., 20, 235-243.
18. Wiesmuller,L., Cammenga,J. and Deppert,W.W. (1996) In vivo assay of p53 function in homologous recombination between simian virus 40 chromosomes. J. Virol., 70, 737-744.
19. Slebos,R.J. and Taylor,J.A. (2001) A novel host cell reactivation assay to assess homologous recombination capacity in human cancer cell lines. Biochem. Biophys. Res. Commun., 281, 212-219.
20. Linke,S.P., Sengupta,S., Khabie,N., Jeffries,B.A., Buchhop,S., Miska,S., Henning,W., Pedeux,R., Wang,X.W., Hofseth,L.J. et al. (2003) p53 interacts with hRAD51 and bRAD54, and directly modulates homologous recombination. Cancer Res., 63, 2596-2605.
21. 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.
22. 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.
23. 1 checkpoint. Oncogene, 18, 3553-3563.
24. Dudenhoffer,C., Kurth,M., Janus,F., Deppert,W. and Wiesmuller,L. (1999) Dissociation of the recombination control and the sequence-specific transactivation function of P53. Oncogene, 18 5773-5784.
25. 1/S cell cycle checkpoint control. Oncogene, 19, 632-639.
26. Lu,X., Lozano,G. and Donehower,L.A. (2003) Activities of wildtype and mutant p53 in suppression of homologous recombination as measured by a retroviral vector system. Mutat. Res., 522, 69-83.
27. Saintigny,Y. and Lopez,B.S. (2002) Homologous recombination induced by replication inhibition, is stimulated by expression of mutant p53. Oncogene, 21, 488-492.
28. Zink,D., Mayr,C., Janz,C. and Wiesmuller,L. (2002) Association of p53 and MSH2 with recombinative repair complexes during S phase. Oncogene, 21, 4788-4800.
29. Kumari,A., Schultz,N. and Helleday,T. (2004) p53 protects from replication-associated DNA double-strand breaks in mammalian cells. Oncogene, 23, 2324-2329.
30. Xia,S.J., Shammas,M.A. and Shmookler Reis,R.J. (1997) Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase. Mol. Cell. Biol., 17, 7151-7158.
31. Vasquez,K.M., Marburger,K., Intody,Z. and Wilson,J.H. (2001) Manipulating the mammalian genome by homologous recombination. Proc. Natl Acad. Sci. USA, 98, 8403-8410.
32. Dudenhoffer,C., Rohaly,G., Will,K., Deppert,W. and Wiesmuller,L. (1998) Specific mismatch recognition in heteroduplex intermediates by p53 suggests a role in fidelity control of homologous recombination. Mol. Cell. Biol., 18, 5332-5342.
33. Susse,S., Janz,C., Janus,F.,Deppert,W. and Wiesmuller,L. (2000) Role of heteroduplex joints in the functional interactions between human Rad51 and wild-type p53. Oncogene, 19, 4500-4512.
34. Bunz,F., Fauth,C., Speicher,M.R., Dutriaux,A., Sedivy,J.M., Kinzler,K.W., Vogelstein,B. and Lengauer,C. (2002) Targeted inactivation of p53 in human cells does not result in aneuploidy. Cancer Res., 62, 1129-1133.
35. Dominguez-Bendala,J., Priddle,H., Clarke,A. and McWhir,J. (2003) Elevated expression of exogenous Rad51 leads to identical increases in gene-targeting frequency in murine embryonic stem (ES) cells with both functional and dysfunctional p53 genes. Exp. Cell Res., 286, 298-307.
36. Willers,H., McCarthy,E.E., Hubbe,P., Dahm-Daphi,J. and Powell,S.N. (2001) Homologous recombination in extrachromosomal plasmid substrates is not suppressed by p53. Carcinogenesis, 22, 1757-1763.
37. Yáñez,R.J. and Porter,A.C.G. (1999) Gene targeting is enhanced in human cells overexpressing hRAD51. Gene Ther., 6, 1282-1290.
38. Johnson,R.D., Liu,N. and Jasin,M. (1999) Mammalian XRCC2promotes the repair of DNA double-strand breaks by homologous recombination. Nature, 401, 397-399.
39. Yáñez,R.J. and Porter,A.C.G. (2002) Differential effects of Rad52p overexpression on gene targeting and extrachromosomal homologous recombination in a human cell line. Nucleic Acids Res., 30, 740-748.
40. Liang,F., Romanienko,P.J., Weaver,D.T., Jeggo,P.A. and Jasin,M. (1996) Chromosomal double-strand break repair in Ku80-deficient cells. Proc. Natl Acad. Sci. USA, 93, 8929-8933.
41. Brummelkamp,T.R., Bernards,R. and Agami,R. (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science, 296, 550-553.
42. Yáñez,R.J. and Porter,A.C.G. (1999) Influence of DNA delivery method on gene targeting frequencies in human cells. Somat. Cell Mol. Genet., 25, 27-31.
43. Fei,P. and El-Deiry,W.S. (2003) P53 and radiation responses. Oncogene, 22, 5774-5783.
44. Nevins,J.R. (1982) Induction of the synthesis of a 70,000 dalton mammalian heat shock protein by the adenovirus E1A gene product. Cell, 29, 913-919.
45. Steegenga,W.T., Van Laar,T., Shvarts,A., Terleth,C., Van der Eb,A.J. and Jochemsen,A.G. (1995) Distinct modulation of p53 activity in transcription and cell-cycle regulation by the large (54 kDa) and small (21 kDa) adenovirus E1B proteins. Virology, 212, 543-554.
46. Steegenga,W.T., van Laar,T., Riteco,N., Mandarino,A., Shvarts,A., van der Eb,A.J. and Jochemsen,A.G. (1996) Adenovirus E1A proteins inhibit activation of transcription by p53. Mol. Cell. Biol. 16, 2101-2109.
47. Lin,J., Chen,J., Elenbaas,B. and Levine,A.J. (1994) Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to mdm-2 and the adenovirus 5 E1B 55-kD protein. Genes Dev., 8, 1235-1246.
48. Yew,P.R. and Berk,A.J. (1992) Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature, 357, 82-85.
49. Jasin,M. (1996) Genetic manipulation of genomes with rare-cutting endonucleases. Trends Genet., 12, 224-228.
50. Miller,D.G., Petek,L.M. and Russell,D.W. (2003) Human gene targeting by adeno-associated virus vectors is enhanced by DNA double-strand breaks. Mol. Cell. Biol., 23, 3550-3557.
51. te Riele,H., Maandag,E.R. and Berns,A. (1992) Highly efficient gene targeting in embryonic stem cells through homologous recombination with isogenic DNA constructs. Proc. Natl Acad. Sci. USA 89, 5128-5132.
52. Deng,C. and Capecchi,M.R. (1992) Reexamination of gene targeting frequency as a function of the extent of homology between the targeting vector and the target locus. Mol. Cell. Biol., 12, 3365-3371.
53. Boyer,J.C., Umar,A., Risinger,J.I., Lipford,J.R., Kane,M., Yin,S., Barrett,J.C., Kolodner,R.D. and Kunkel,T.A. (1995) Microsatellite instability, mismatch repair deficiency, and genetic defects in human cancer cell lines. Cancer Res., 55, 6063-6070.
54. Karran,P. (2000) DNA double strand break repair in mammalian cells. Curr. Opin. Genet. Dev., 10, 144-150.
55. Tutt,A., Bertwistle,D., Valentine,J., Gabriel,A., Swift,S., Ross,G., Griffin,C., Thacker,J. and 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.
56. Essers,J., Hendriks,R.W., Swagemakers,S.M., Troelstra,C., de Wit,J., Bootsma,D., Hoeijmakers,J.H. and Kanaar,R. (1997) Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell, 89, 195-204.
57. Seidman,M.M. (1987) Intermolecular homologous recombination between transfected sequences in mammalian cells is primarily nonconservative. Mol. Cell. Biol., 7, 3561-3565.
58. Lin,F.L., Sperle,K. and Sternberg,N. (1984) Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol. Cell. Biol., 4 1020-1034.
59. Bill,C.A., Yu,Y., Miselis,N.R., Little,J.B. and Nickoloff,J.A. (1997) A role for p53 in DNA end rejoining by human cell extracts. Mutat. Res., 385, 21-29.
60. Okorokov,A.L., Warnock,L. and Milner,J. (2002) Effect of wild-type, S15D and R175H p53 proteins on DNA end joining in vitro: potential mechanism of DNA double-strand break repair modulation. Carcinogenesis, 23, 549-557.
61. Hirata,R., Chamberlain,J., Dong,R. and Russell,D.W. (2002) Targeted transgene insertion into human chromosomes by adeno-associated virus vectors. Nat. Biotechnol., 20, 735-738.
62. Wurtele,H., Little,K.C. and Chartrand,P. (2003) Illegitimate DNA integration in mammalian cells. Gene Ther., 10, 1791-1799.
63. Bergsmedh,A., Szeles,A., Henriksson,M., Bratt,A., Folkman,M.J., SpeLz,A.L. and Holmgren,L. (2001) Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc. Natl Acad. Sci. USA, 98, 6407-6411.