Phosphorylation and nuclear accumulation are distinct events contributing to the activation of p53

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 546, Issue 1-2, 2004, Pages 7-15

  O'Hagan, Heather M ^a   Ljungman, Mats ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

ATM; DRB; Inhibition of transcription; Ionizing radiation; Leptomycin B

Indexed keywords

5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; BENZIMIDAZOLE DERIVATIVE; LEPTOMYCIN B; PROTEIN KINASE; PROTEIN P21; PROTEIN P53; SERINE;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IONIZING RADIATION; NUCLEAR IMPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

EID: 1642481261     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2003.10.003     Document Type: Article

References (35)

1. Blaydes J.P., Craig A.L., Wallace M., Ball H.M.L., Traynor N.J., Gibbs N.K., Hupp T.R. Synergistic activation of p53-dependent transcription by two cooperating damage recognition pathways. Oncogene. 19:2000;3829-3839.
2. Offer H., Milyavsky M., Erez N., Matas D., Zurer I., Harris C.C., Rotter V. Structural and functional involvement of p53 in BER in vitro and in vivo. Oncogene. 20:2001;581-589.
3. McKay B.C., Ljungman M., Rainbow A.J. Potential roles for p53 in nucleotide excision repair. Carcinogenesis. 20:1999;1389-1396.
4. Dulic V., Kaufmann W.K., Wilson S.J., Tlsty T.D., Lees E., Harper J.W., Elledge S.J., Reed S.I. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell. 76:1994;1013-1023.
5. Symonds H., Krall L., Remington L., Saenzrobles M., Lowe S., Jacks T., Vandyke T. p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell. 78:1994;703-711.
6. Graeber T., Osmanian C., Jacks T., Housman D., Koch C., Lowe S., Giaccia A. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumors. Nature. 379:1996;88-91.
7. Webley K., Bond J.A., Jones C.J., Blaydes J.P., Craig A., Hupp T., Wynford-Thomas D. Posttranslational modifications of p53 in replicative senescence overlapping but distinct from those induced by DNA damage. Mol. Cell. Biol. 20:2000;2803-2808.
8. Ljungman M., Zhang F. Blockage of RNA polymerase as a possible trigger for UV light-induced apoptosis. Oncogene. 13:1996;823-831.
9. Ljungman M., Zhang F.F., Chen F., Rainbow A.J., McKay B.C. Inhibition of RNA polymerase II as a trigger for the p53 response. Oncogene. 18:1999;583-592.
10. Ljungman M., O'Hagan H.M., Paulsen M.T. Induction of ser15 and lys382 modifications of p53 by blockage of transcription elongation. Oncogene. 20:2001;5964-5971.
11. Yamaizumi M., Sugano T. UV-induced nuclear accumulation of p53 is evoked through DNA damage of actively transcribed genes independent of the cell cycle. Oncogene. 9:1994;2775-2784.
12. Maki C.G., Huibregtse J.M., Howley P.M. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res. 56:1996;2649-2654.
13. Chen F., Chang D., Goh M., Klibanov S.A., Ljungman M. Role of p53 in cell cycle regulation and apoptosis following exposure to proteasome inhibitors. Cell Growth Differ. 11:2000;239-246.
14. Ljungman M. Dial 9-1-1 for p53: mechanisms of p53 activation by cellular stress. Neoplasia. 2:2000;208-225.
15. *) promote dephosphorylation of the carboxyl-terminal domain of RNA polymerase II largest subunit. J. Biol. Chem. 269:1994;13331-13336.
16. Klibanov S.A., O'Hagan H.M., Ljungman M. Accumulation of soluble and nucleolar-associated p53 proteins following cellular stress. J. Cell Sci. 114:2001;1867-1873.
17. Bakkenist C.J., Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 421:2003;499-506.
18. el-Deiry W.S., Harper J.W., O'Connor P.M., Velculescu V.E., Canman C.E., Jackman J., Pietenpol J.A., Burrell M., Hill D.E., Wang Y.et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54:1994;1169-1174.
19. Maeda T., Chong M.T., Espino R.A., Chua P.P., Cao J.Q., Chomey E.G., Luong L., Tron V.A. Role of p21(Waf-1) in regulating the G1 and G2/M checkpoints in ultraviolet-irradiated keratinocytes. J. Invest. Derm. 119:2002;513-521.
20. Kastan M.B., Lim D.S. The many substrates and functions of ATM. Nature Rev. Mol. Cell Biol. 1:2000;179-186.
21. Khanna K.K., Lavin M.F., Jackson S.P., Mulhern T.D. ATM, a central controller of cellular responses to DNA damage. Cell Death Diff. 8:2001;1052-1065.
22. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2001;2177-2196.
23. Canman C.E., Lim D.S., Cimprich K.A., Taya Y., Tamai K., Sakaguchi K., Appella E., Kastan M.B., Siliciano J.D. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science. 281:1998;1677-1679.
24. Banin S., Moyal L., Shieh S.Y., Taya Y., Anderson C.W., Chessa L., Smorodinsky N.I., Prives C., Reiss Y., Shiloh Y., Ziv Y. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science. 281:1998;1674-1677.
25. Siliciano J.D., Canman C.E., Taya Y., Sakaguchi K., Appella E., Kastan M.B. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 11:1997;3471-3481.
26. Kudo N., Matsumori N., Taoka H., Fujiwara D., Schreiner E.P., Wolff B., Yoshida M., Horinouchi S. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. U.S.A. 96:1999;9112-9117.
27. Kudo N., Wolff B., Sekimoto T., Schreiner E.P., Yoneda Y., Yanagida M., Horinouchi S., Yoshida M. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:1998;540-547.
28. Fornerod M., Ohno M., Yoshida M., Mattaj I.W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 90:1997;1051-1060.
29. Smart P., Lane E.B., Lane D.P., Midgley C., Vojtesek B., Lain S. Effects on normal fibroblasts and neuroblastoma cells of the activation of the p53 response by the nuclear export inhibitor leptomycin B. Oncogene. 18:1999;7378-7386.
30. Laín 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. 248:1999;457-472.
31. Freedman D.A., Levine A.J. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 18:1998;7288-7293.
32. Hietanen S., Lain S., Krausz E., Blattner C., Lane D.P. Activation of p53 in cervical carcinoma cells by small molecules. Proc. Natl. Acad. Sci. USA. 97:2000;8501-8506.
33. Dumaz N., Meek D.W. Serine15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2. EMBO J. 18:1999;7002-7010.
34. Blattner C., Sparks A., Lane D. Transcription factor E2F-1 is upregulated in response to DNA damage in a manner analogous to that of p53. Mol. Cell. Biol. 19:1999;3704-3713.
35. Chang D., Chen F., Zhang F.F., McKay B.C., Ljungman M. Dose-dependent effects of DNA-damaging agents on p53-mediated cell cycle arrest. Cell Growth Differ. 10:1999;155-162.