Inhibition of Crm1-p53 interaction and nuclear export of p53 by poly(ADP-ribosyl)ation

Nature Cell Biology

Volumn 9, Issue 10, 2007, Pages 1175-1183

  Kanai, Masayuki ^a,b   Hanashiro, Kazuhiko ^a,b   Kim, Song Hee ^b   Hanai, Shuji ^c   Boulares, A Hamid ^d   Miwa, Masanao ^e   Fukasawa, Kenji ^a,b  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^d LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN P53;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; MOUSE; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; CELL NUCLEUS; DOGS; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; KARYOPHERINS; LUCIFERASES; MICE; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 34848853918     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1638     Document Type: Article

References (34)

1. Vousden, K. H. Activation of the p53 tumor suppressor protein. Biochim. Biophys. Acta 1602, 47-59 (2002).
2. Gottifredi, V. & Prives, C. The S phase checkpoint: When the crowd meets at the fork. Semin. Cell Dev. Biol. 16, 355-368 (2005).
3. Bode, A. M. & Dong, Z. Post-translational modification of p53 in tumorigenesis. Nature Rev. Cancer 4, 793-805 (2004).
4. Herceg, Z. & Wang, Z.-Q. Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res. 477, 97-110 (2001).
5. Bürkle, A. Poly(ADP-ribosyl)ation, a DNA damage-driven protein modification and regulator of genomic instability. Cancer Lett. 163, 1-5 (2001).
6. Wesierska-Gadek, J., Schmid, G. & Cerni, C. ADP-ribosylation of wild-type p53 in vitro: Binding of p53 protein to specific p53 consensus sequence prevents its modification. Biochem. Biophys. Res. Commun. 224, 96-102 (1996).
7. Mendoza-Alvarez, H. & Alvarez-Gonzalez, R. Regulation of p53 sequence-specific DNA-binding by covalent poly(ADP-ribosyl)ation. J. Biol. Chem. 276, 36425-36430 (2001).
8. Simbulan-Rosenthal, C. M., Rosenthal, D. S., Luo, R. & Smulson, M. E. Poly(ADP-ribosyl)ation of p53 during apoptosis in human osteosarcoma cells. Cancer Res. 59, 2190-2194 (1999).
9. Kanai, M., Tong, W.-M., Sugihara, E., Wang, Z.-Q., Fukasawa, K. & Miwa, M. Involvement of poly(ADP-ribose) polymerase 1 and poly(ADP-ribosyl)ation in regulation of centrosome function. Mol. Cell. Biol. 23, 2451-2462 (2003).
10. Vaziri, H. et al. ATM-dependent telomere loss in aging human diploid fibroblats and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J. 16, 6018-6033 (1997).
11. Valenzuela, M. T. et al. PARP-1 modifies the effectiveness of p53-mediated DNA damage response. Oncogene 21, 1108-1116 (2002).
12. Wieler, S., Gagné, J., Vaziri, H., Poirier, G. G. & Benchimol, S. Poly(ADP-ribose) polymerase-1 is a positive regulator of the p53-mediated G1 arrest response following ionizing radiation. J. Biol. Chem. 278, 18914-18921 (2003).
13. Agarwal, M. L., Agarwal, A., Taylor, W. R., Wang, Z.-Q., Wagner, E. F. & Stark, G. R. Defective induction but normal activation and function of p53 in mouse cells lacking poly-ADP-ribose polymerase. Oncogene 15, 1035-1041 (1997).
14. Michael, D. & Oren, M. The p53-Mdm2 module and the ubiquitin system. Semin. Cancer Biol. 13, 49-58 (2003).
15. Freedman, D. A. & Levine, A. J. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 18, 7288-7293 (1998).
16. Lain, S., Midgley, C., Sparks, A., Lane, E. B. & Lane, D. P. An inhibitor of nuclear export activates the p53 response and induces the localization of HDM2 and p53 to U1A-positive nuclear bodies associated with the PODs. Exp. Cell Res. 248, 457-472 (1999).
17. Lohrum, M. A., Woods, D. B., Ludwig, R. L., Balint, E. & Vousden, K. H. C-terminal ubiquitination of p53 contributes to nuclear export. Mol. Cell. Biol. 21, 8521-8532 (2001).
18. Zhang, Y. & Xiong, Y. A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation. Science 292 1910-1915 (2001).
19. Stommel, J. M., Marchenko, N. D., Jimenez, G. S., Moll, U. M., Hope, T. J. & Wahl, G. M. A leucine-rich nuclear export signal in the p53 tetramerization domain: Regulation of subcellular localization and p53 activity by NES masking. EMBO J. 18, 1660-1672 (1999).
20. Wesierska-Gadek, J., Wojciechowski, J. & Schmid, G. Central and carboxy-terminal regions of human p53 protein are essential for interaction and complex formation with PARP-1. J. Cell Biochem. 89, 220-232 (2003).
21. Lu, W., Pochampally, R., Chen, L., Traidej, M., Wang, Y. & Chen, J. Nuclear exclusion of p53 in a subset of tumors requires MDM2 function. Oncogene 19, 232-240 (2000).
22. Geyer, R. K., Yu, Z. K. & Maki, C. G. The MDM2 RING-finger domain is required to promote p53 nuclear export. Nature Cell Biol. 2, 569-573 (2000).
23. Boyd, S. D., Tsai, K. Y. & Jacks, T. An intact HDM2 RING-finger domain is required for nuclear exclusion of p53. Nature Cell Biol. 2 563-568 (2000).
24. Haupt, Y., Maya, R., Kazaz, A. & Oren, M. Mdm2 promotes the rapid degradation of p53. Nature 387, 296-299 (1997).
25. Kubbutat, M. H., Jones, S. N. & Vousden, K. Regulation of p53 stability by MDM2. Nature 387, 299-303 (1997).
26. Inoue, T., Wu, L., Stuart, J. & Maki, C. G. Control of p53 nuclear accumulation in stressed cells. FEBS Lett. 579, 4978-4984 (2005).
27. Wesierska-Gadek, J. & Schmid, G. Poly(ADP-ribose) polymerdse-1 regulates the stability of the wild-type p53 protein. Cell. Mol. Biol. Lett. 6, 117-140 (2001).
28. Lu, W., Chen, L., Peng, Y. & Chen, J. Activation of p53 by roscovitine-mediated suppression of MDM2 expression. Oncogene 20, 3206-3216 (2001).
29. Sherr, C. J. Divorcing ARF and p53: An unsettled case. Nature Rev. Cancer 6, 663-673 (2006).
30. Simbulan-Rosenthal, C. M., Rosenthal, D. S., Ding, R., Bhatia, K. & Smulson, M. E. Prolongation of the p53 response to DNA strand breaks in cells depleted of PARP by antisense RNA expression. Biochem. Biophys. Res. Commun. 253, 864-868 (1998).
31. Moll, U. M., Wolff, S., Speidel, D. & Deppert, W. Transcription-independent pro-apoptotic functions of p53. Curr. Opin. Cell Biol. 17, 631-636 (2005).
32. Tewari, M. et al. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81, 801-809 (1995).
33. Malanga, M., Pleschke, J. M., Kleczkowska, H. E. & Althaus, F. R. Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J. Biol. Chem. 273, 11839-11843 (1998).
34. Kraus, W.L. & Lis, J. T. PARP goes transcription. Cell 113, 677-688 (2003).