BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination

EMBO Journal

Volumn 22, Issue 5, 2003, Pages 1210-1222

  Sengupta, Sagar ^a   Linke, Steven P ^a   Pedeux, Remy ^a   Yang, Qin ^a   Farnsworth, Julie ^b   Garfield, Susan H ^a   Valerie, Kristoffer ^b   Shay, Jerry W ^c   Ellis, Nathan A ^d   Wasylyk, Bohdan ^e   Harris, Curtis C ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e INSERM   (France)

Author keywords

DNA repair; Nuclear trafficking; RAD51; Sister chromatid exchange

Indexed keywords

ALANINE; DNA; HELICASE; HYDROXYUREA; NUCLEAR PROTEIN; PROTEIN P53; SERINE;

ARTICLE; BLOOM SYNDROME; CONTROLLED STUDY; DNA REPLICATION; GENETIC COMPLEMENTATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SISTER CHROMATID EXCHANGE; WILD TYPE;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOSINE TRIPHOSPHATASES; BLOOM SYNDROME; BROMODEOXYURIDINE; CELL CYCLE; CELL LINE; DNA HELICASES; DNA REPLICATION; DNA-BINDING PROTEINS; FIBROBLASTS; HUMANS; HYDROXYUREA; MODELS, GENETIC; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SERINE; TUMOR SUPPRESSOR PROTEIN P53;

EUKARYOTA;

EID: 0037416149     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg114     Document Type: Article

References (43)

1. Ababou, M., Dumaire, V., Lecluse, Y. and Amor-Gueret, M. (2002) Bloom's syndrome protein response to ultraviolet-C radiation and hydroxyurea-mediated DNA synthesis inhibition. Oncogene, 21, 2079-2088.
2. Appella, E. and Anderson, C.W. (2001) Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem., 268, 2764-2772.
3. Balajee, A.S., May, A., Dianova, I. and Bohr, V.A. (1998) Efficient PCNA complex formation is dependent upon both transcription coupled repair and genome overall repair. Mutat. Res., 409, 135-146.
4. Bean, L.J. and Stark, G.R. (2001) Phosphorylation of serines 15 and 37 is necessary for efficient accumulation of p53 following irradiation with UV. Oncogene, 20, 1076-1084.
5. Bischof, O., Kim, S.H., Irving, J., Beresten, S., Ellis, N.A. and Campisi, J. (2001) Regulation and localization of the Bloom syndrome protein in response to DNA damage. J. Cell Biol., 153, 367-380.
6. Blander, G., Kipnis, J., Leal, J.F., Yu, C.E., Schellenberg, G.D. and Oren, M. (1999) Physical and functional interaction between p53 and the Werner's syndrome protein. J. Biol. Chem., 274, 29463-29469.
7. 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.
8. 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.
9. Chakraverty, R.K. and Hickson, I.D. (1999) Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. BioEssays, 21, 286-294.
10. waf?/cip? and hdm2 dependent on DNA damage in Bloom's syndrome fibroblasts. Carcinogenesis, 19, 2115-2120.
11. Franchitto, A. and Pichierri, P. (2002) Bloom's syndrome protein is required for correct relocalization of RAD50/MRE11/NBS1 complex after replication fork arrest. J. Cell Biol., 157, 19-30.
12. Gao, Y. et al. (2000) Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature, 404, 897-900.
13. Gatei, M., Zhou, B.B., Hobson, K., Scott, S., Young, D. and Khanna, K.K. (2001) Ataxia telangiectasia mutated (ATM) kinase and ATM and Rad3 related kinase mediate phosphorylation of Brcal at distinct and overlapping sites. In vivo assessment using phospho-specific antibodies. J. Biol. Chem., 276, 17276-17280.
14. Gottifredi, V., Shieh, S., Taya, Y. and Prives, C. (2001) From the cover: p53 accumulates but is functionally impaired when DNA synthesis is blocked. Proc. Natl Acad. Sci. USA, 98, 1036-1041.
15. Haber, J.E. (2000) Partners and pathways repairing a double-strand break. Trends Genet., 16, 259-264.
16. Hoeijmakers, J.H. (2001) Genome maintenance mechanisms for preventing cancer. Nature, 411, 366-374.
17. 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.
18. Kennedy, B.K., Barbie, D.A., Classon, M., Dyson, N. and Harlow, E. (2000) Nuclear organization of DNA replication in primary mammalian cells. Genes Dev., 14, 2855-2868.
19. Kuhn, E.M. and Therman, E. (1986) Cytogenetics of Bloom's syndrome. Cancer Genet. Cytogenet., 22, 1-18.
20. Lambert, S. and Lopez, B.S. (2001) Role of RAD51 in sister-chromatid exchanges in mammalian cells. Oncogene, 20, 6627-6631.
21. 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.
22. Lee, S., Cavallo, L. and Griffith, J. (1997) Human p53 binds Holliday junctions strongly and facilitates their cleavage. J. Biol. Chem., 272, 7532-7539.
23. Li, J., Ayyadevera, R. and Shmookler Reis, R.J. (1997) Carcinogens stimulate intrachromosomal homologous recombination at an endogenous locus in human diploid fibroblasts. Mutat. Res., 385, 173-193.
24. 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.
25. 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.
26. Oren, M. (1999) Regulation of the p53 tumor suppressor protein. J. Biol. Chem., 274, 36031-36034.
27. Ouellette, M.M., McDaniel, L.D., Wright, W.E., Shay, J.W. and Schultz, R.A. (2000) The establishment of telomerase-immortalized cell lines representing human chromosome instability syndromes. Hum. Mol. Genet., 9, 403-411.
28. Perry, P. and Wolff, S. (1974) New Giemsa method for the differential staining of sister chromatids. Nature, 251, 156-158.
29. Raderschall, E., Stout, K., Freier, S., Suckow, V., Schweiger, S. and Haaf, T. (2002) Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res., 62, 219-225.
30. Saintigny, Y. and Lopez, B.S. (2002) Homologous recombination induced by replication inhibition, is stimulated by expression of mutant p53. Oncogene, 21, 488-492.
31. Sengupta, S. and Wasylyk, B. (2001) Ligand-dependent interaction of the glucocorticoid receptor with p53 enhances their degradation by Hdm2. Genes Dev., 15, 2367-2380.
32. 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.
33. 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.
34. Spillare, E.A., Robles, A.I., Wang, X.W., Shen, J.C., Yu, C.E., Schellenberg, G.D. and Harris, C.C. (1999) p53-mediated apoptosis is attenuated Werner syndrome cells. Genes Dev., 13, 1355-1360.
35. 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.
36. Valerie, K. (1999) Viral vectors for gene therapy. In Wu-Pong, S. and Rojanasakul Y. (eds), Biopharmaceutical Drug Design and Development. Humana Press, Totowa, NJ, pp. 69-105.
37. van Brabant, A.J., Stan, R. and Ellis, N.A. (2000) DNA helicases, genomic instability and human genetic disease. Annu. Rev. Genomics Hum. Genet., 1, 409-459.
38. 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.
39. Wang, X.W. et al. (2001) Functional interaction of p53 and BLM DNA helicase in apoptosis. J. Biol. Chem., 276, 32948-32955.
40. Wang, Y., Cortez, D., Yazdi, P., Neff, N., Elledge, S.J. and Qin, J. (2000) BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev., 14, 927-939.
41. Willers, H., McCarthy, E.E., Wu, B., Wunsch, H., Tang, W., Taghian, D.G., Xia, F. and Powell, S.N. (2000) Dissociation of p53-mediated suppression of homologous recombination from G1/S cell cycle checkpoint control. Oncogene, 19, 632-639.
42. Wu, L., Davies, S.L., Levitt, N.C. and Hickson, I.D. (2001) Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J. Biol. Chem., 276, 19375-19381.
43. Yang, Q. et al. (2002) The processing of Holliday junctions by BLM and WRN helicases is regulated by p53. J. Biol. Chem., 277, 31980-31987.