Jun NH₂-Terminal Kinase Phosphorylation of p53 on Thr-81 Is Important for p53 Stabilization and Transcriptional Activities in Response to Stress

REFERENCES

• Adler, V., A. Schaffer, J. Kim, L. Dolan, and Z. Ronai. 1995. UV-irradiation and heat shock mediate JNK activation via alternate pathways. J. Biol. Chem. 270:26071–26077.
   PubMed Web of Science ®Google Scholar
• Adler, V., M. R. Pincus, T. Minamoto, S. Y. Fuchs, M. J. Bluth, P. W. Brandt-Rauf, F. K. Friedman, R. C. Robinson, J. M. Chen, X. W. Wang, C. C. Harris, and Z. Ronai. 1997. Conformation-dependent phosphorylation of p53. Proc. Natl. Acad. Sci. USA 94:1686–1691.
   PubMed Web of Science ®Google Scholar
• Ashcroft, M., Y. Taya, and K. H. Vousden. 2000. Stress signals utilize multiple pathways to stabilize p53. Mol. Cell. Biol. 20:3224–3233.
   PubMed Web of Science ®Google Scholar
• Banin, S., L. Moyal, S. Shieh, Y. Taya, C. W. Anderson, L. Chessa, N. Smorodinsky, C. Prives, Y. Reiss, Y. Shiloh, and Y. Ziv. 1998. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281:1674–1677.
   PubMed Web of Science ®Google Scholar
• Beroud, C., and T. Soussi. 1998. p53 gene mutation: software and database. Nucleic Acids Res. 26:200–204.
   PubMedGoogle Scholar
• Buckbinder, L., R. Talbott, S. Velasco-Miguel, I. Takenaka, B. Faha, B. Seizinger, and N. Kley. 1995. Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature 377:646–649.
   PubMed Web of Science ®Google Scholar
• Bulavin, D. V., S. Saito, M. C. Hollander, K. Sakaguchi, C. W. Anderson, E. Appella, and A. J. Fornace Jr.. 1999. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J. 18:6845–6854.
   PubMed Web of Science ®Google Scholar
• Buschmann, T., V. Adler, E. Matusevich, S. Y. Fuchs, and Z. Ronai. 2000. p53 phosphorylation and association with murine double minute 2, c-Jun NH2-terminal kinase, p14ARF, and p300/CBP during the cell cycle and after exposure to ultraviolet irradiation. Cancer Res. 60:896–900.
   PubMed Web of Science ®Google Scholar
• Chao, C., S. Saito, J. Kang, C. W. Anderson, E. Appella, and Y. Xu. 2000. p53 transcriptional activity is essential for p53-dependent apoptosis following DNA damage. EMBO 19:4967–4975.
   PubMed Web of Science ®Google Scholar
• Chehab, N. H., A. Malikzay, E. S. Stavridi, and T. Halazonetis. 1999. Phosphorylation of Ser-20 mediates stabilization of human p53 in response to DNA damage. Proc. Natl. Acad. Sci. USA 96:13777–13782.
   PubMed Web of Science ®Google Scholar
• Dumaz, N., and D. W. Meek. 1999. Serine 15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2. EMBO J. 18:7002–7010.
   PubMed Web of Science ®Google Scholar
• El Diery, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. N. Trent, D. Lin, W. E. Mercer, K. W. Kinzier, and B. Vogelstien. 1993. Waf1, a potential mediator of p53 tumor suppression. Cell 75:817–825.
   PubMedGoogle Scholar
• Friedlander, P., Y. Legros, T. Soussl, and C. Prives. 1996. Regulation of mutant p53 temperature-sensitive DNA binding. J. Biol. Chem. 271:25468–25478.
   PubMed Web of Science ®Google Scholar
• Fuchs, S. Y., B. Xie, V. A. Adler, V. A. Fried, R. J. Davis, and Z. Ronai. 1997. c-Jun NH2-terminal kinases target the ubiquitination of their associated transcription factors. J. Biol. Chem. 272:32163–32168.
   PubMed Web of Science ®Google Scholar
• Fuchs, S. Y., L. R. Dolan, R. Davis, and Z. Ronai. 1996. Phosphorylation dependent targeting of c-jun ubiquitination by JNK. Oncogene 13:1529–1533.
   Google Scholar
• Fuchs, S. Y., V. A. Fried, and Z. Ronai. 1998. Stress-activated kinases regulate protein stability. Oncogene 17:1483–1490.
   PubMedGoogle Scholar
• Fuchs, S. Y., V. Adler, T. Buschmann, Z. Yin, X. Wu, S. N. Jones, and Z. Ronai. 1998. JNK targets p53 ubiquitination and degradation in nonstressed cells. Genes Dev. 12:2658–2663.
   PubMed Web of Science ®Google Scholar
• Fuchs, S. Y., V. Adler, M. R. Pincus, and Z. Ronai. 1998. MEKK1/JNK signaling stabilizes and activates p53. Proc. Natl. Acad. Sci. USA 95:10541–10546.
   PubMed Web of Science ®Google Scholar
• Fuchs, S. Y., and Z. Ronai. 1999. Ubiquitination and degradation of ATF2 are dimerization dependent. Mol. Cell. Biol. 19:3289–3298.
   PubMedGoogle Scholar
• Gatti, A., H. H. Li, J. A. Traugh, and X. Liu. 2000. Phosphorylation of human p53 on Thr-55. Biochemistry 39:9837–9842.
   PubMedGoogle Scholar
• Giaccia, A., and M. B. Kastan. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12:2973–2983.
   PubMed Web of Science ®Google Scholar
• Glickman, M. H., D. M. Rubin, V. A. Fried, and D. Finley. 1998. The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol. Cell. Biol. 18:3149–3162.
   PubMed Web of Science ®Google Scholar
• Gostissa, M., A. Hengstermann, V. Fogal, P. Sandy, S. E. Schwarz, M. Scheffner, and G. Del Sal. 1999. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J. 18:6462–6471.
   PubMed Web of Science ®Google Scholar
• Gu, W., and R. G. Roeder. 1997. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 95:595–606.
   Google Scholar
• Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1999. MDM2 promotes the rapid degradation of p53. Nature 387:296–299.
   Google Scholar
• Haupt, Y., S. Rowan, E. Shaullan, A. Kazaz, K. Vousden, and M. Oren. 1997. p53 mediated apoptosis in HeLa cells: transcription dependent and independent mechanisms. Leukemia 3:339
   Google Scholar
• Hengstermann, A, N. J. Whitaker, D. Zimmer, H. Zentgraf, and M. Scheffner. 1998. Characterization of sequence elements involved in p53 stability regulation reveals cell type dependence for p53 degradation. Oncogene 17:2933–2941.
   PubMedGoogle Scholar
• Hermeking, H., C. Lengauer, K. Polyak, T. He, L. Zhang, S. Thiagalingan, K. W. Kinzier, and B. Vogelstein. 1997. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1:3–11.
   PubMed Web of Science ®Google Scholar
• Hirao, A., Y. Y. Kong, S. Matsuoka, A. Wakeham, J. Ruland, H. Yoshida, D. Liu, S. J. Elledge, and T. W. Mak. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287:1824–1827.
   PubMed Web of Science ®Google Scholar
• Huang, C., W. Ma, A. Maxiner, Y. Sun, and Z. Dong. 1999. p38 kinase mediates UV-induced phosphorylation of p53 protein at serine 389. J. Biol. Chem. 274:12229–12235.
   PubMedGoogle Scholar
• Hupp, T. R., D. W. Meek, C. A. Midgley, and D. P. Lane. 1992. Regulation of the specific DNA binding function of p53. Cell 71:875–886.
   PubMed Web of Science ®Google Scholar
• Khanna, K., K. Keating, S. Kozlov, S. Scott, M. Gatei, K. Hobson, Y. Taya, B. Gabrielli, D. Chan, S. P. Lees-Miller, and M. F. Lavin. 1998. ATM associates with and phosphorylates p53: mapping the region of interaction. Nat. Genet. 20:398–400.
   PubMed Web of Science ®Google Scholar
• Kim, A. L., A. J. Raffo, P. W. Brandt-Rauf, M. R. Pincus, R. Monaco, P. Abarzua, and R. L. Fine. 1999. Conformation and molecular basis for induction of apoptosis by a p53 c-terminal peptide in human cancer cells. J. Biol. Chem. 274:34924–34931.
   PubMed Web of Science ®Google Scholar
• Kubbutat, M. H., S. N. Jones, and K. H. Vousden. 1997. Regulation of p53 stability by Mdm2. Nature 387:299–303.
   PubMed Web of Science ®Google Scholar
• Lees-Miller, S. P., K. Sakaguchi, S. J. Ullrich, E. Appella, and C. W. Anderson. 1992. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12:5041–5049.
   PubMed Web of Science ®Google Scholar
• Lu, H., R. P. Fisher, P. Bailey, and A. J. Levine. 1997. The CDK7-cycH-p36 complex of transcription factor IIH phosphorylates p53 enhancing its sequence-specific DNA binding activity in vitro. Mol. Cell. Biol. 17:5923–5934.
   PubMedGoogle Scholar
• Meek, D. W.. 1998. Multiple phosphorylation and the integration of stress signals at p53. Cell Signal. 10:159–166.
   PubMed Web of Science ®Google Scholar
• Milne, D. M., L. E. Campbell, D. G. Campbell, and D. W. Meek. 1995. p53 is phosphorylated in vitro and in vivo by an ultraviolet radiation-induced protein kinase characteristic of the c-Jun kinase, JNK1. J. Biol. Chem. 270:5511–5518.
   PubMed Web of Science ®Google Scholar
• Miyashita, T., and J. C. Reed. 1995. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293–299.
   PubMed Web of Science ®Google Scholar
• Nakagawa, A., Y. Taya, K. Tamal, and M. Yamaizumi. 1999. Requirement of ATM in phosphorylation of the human p53 protein at serine 15 following DNA double-strand breaks. Mol. Cell. Biol. 19:2828–2834.
   PubMed Web of Science ®Google Scholar
• Naica, A., and V. M. Rangnekar. 1998. The G1-phase growth-arresting action of interleukin-1 is independent of p53 and p21/WAF1 function. J. Biol. Chem. 273:30517–30523.
   PubMedGoogle Scholar
• Ndubuisi, M. I., G. G. Guo, V. A. Fried, J. D. Etllnger, and P. B. Sehgal. 1999. Cellular physiology of STAT3; where's the cytoplasmic monomer?. J. Biol. Chem. 274:25499–25509.
   PubMedGoogle Scholar
• Oren, M.. 1999. Regulation of the p53 tumor suppressor protein. J. Biol. Chem. 274:36031–36034.
   PubMed Web of Science ®Google Scholar
• Owen-Schaub, L. B., W. Zhang, J. C. Cusack, L. Angelo, S. Santee, T. Fujiwara, J. Roth, A. B. Deisseroth, W.-W. Zhang, E. Kruzel, and R. Radinsky. 1995. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol. Cell. Biol. 15:3032–3040.
   PubMed Web of Science ®Google Scholar
• Polyak, K., Y. Xia, J. Zweler, K. Kinzler, and B. Vogelstein. 1997. A model for p53-induced apoptosis. Nature 389:300–305.
   PubMed Web of Science ®Google Scholar
• Potapova, O., M. Gorospe, R. H. Dougherty, N. M. Dean, W. A. Gaarde, and N. J. Holbrook. 2000. Inhibition of c-Jun N-terminal kinase 2 expression suppresses growth and induces apoptosis of human tumor cells in a p53-dependent manner. Mol. Cell. Biol. 20:1713–1722.
   PubMed Web of Science ®Google Scholar
• Prives, C., and P. A. Hall. 1999. The p53 pathway. J. Pathol. 187:112–126.
   PubMed Web of Science ®Google Scholar
• Rosenfeld, J., J. Capdeville, J. C. Guillernot, and P. Ferrara. 1992. In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 203:173–179.
   PubMed Web of Science ®Google Scholar
• Sakaguchi, K., J. E. Herrera, S. Saito, T. Miki, M. Bustin, A. Vassilev, C. W. Anderson, and E. Appella. 1998. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev. 12:2831–2841.
   PubMed Web of Science ®Google Scholar
• Sanchez-Prieto, R., J. M. Rojas, Y. Taya, and J. S. Gutkind. 2000. A role for the p38 mitogen-activated protein kinase pathway in the transcriptional activation of p53 on genotoxic stress by chemotherapeutic agents. Cancer Res. 60:2464–2472.
   PubMed Web of Science ®Google Scholar
• Shieh, S.-Y., J. Ahn, K. Tamai, Y. Taya, and C. Prives. 2000. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphoryiate p53 at multiple DNA damage inducible sites. Genes Dev. 14:289–300.
   PubMed Web of Science ®Google Scholar
• Shieh, S.-Y., Y. Taya, and C. Prives. 1999. DNA damage-inducible phosphorylation of p53 at N-terminal sites including a novel site, Ser20, requires tetramerization. EMBO J. 18:1815–1823.
   PubMed Web of Science ®Google Scholar
• Siliciano, J., C. Canman, Y. Taya, K. Sakaguchi, E. Apella, and M. B. Kastan. 1997. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 11:3471–3481.
   PubMed Web of Science ®Google Scholar
• Takenaka, I., F. Morin, B. Seizinger, and N. Kley. 1995. Regulation of the sequence-specific DNA binding function of p53 by protein kinase C and protein phosphatases. J. Biol. Chem. 270:5405–5411.
   PubMed Web of Science ®Google Scholar
• Theodosiou, A., A. Smith, C. Gillieron, S. Arkinstall, and A. Ashworth. 1999. MKP5, a new member of the MAP kinase phosphatase family, which selectively dephosphorylates stress-activated kinases. Oncogene 18:6981–6988.
   PubMed Web of Science ®Google Scholar
• Tishler, R. B., D. M. Lamppu, S. Park, and B. D. Price. 1995. Microtubule-active drugs taxol, vinblastine, and nocodazole increase the levels of transcriptionally active p53. Cancer Res. 55:6021–6025.
   PubMed Web of Science ®Google Scholar
• Unger, T., T. Juven-Gershon, E. Moallem, M. Berger, R. Vogt Sionov, G. Lozano, M. Oren, and Y. Haupt. 1999. Critical role for Ser20 of human p53 in the negative regulation of p53 by Mdm2. EMBO J. 18:1805–1814.
   PubMed Web of Science ®Google Scholar
• Unger, T., J. A. Mietz, M. Scheffner, C. Yee, and P. M. Howley. 1993. Functional domains of wild-type and mutant p53 proteins involved in transcriptional regulation, transdominant inhibition, and transformation suppression. Mol. Cell. Biol. 13:5186–5194.
   PubMedGoogle Scholar
• Unger, T., R. Sionov, E. Moallem, C. Yee, P. M. Howley, M. Oren, and Y. Haupt. 1999. Mutations in serines 15 and 20 of human p53 impair its apoptotic activity. Oncogene 18:3205–3212.
   PubMed Web of Science ®Google Scholar
• Velculescu, V. E., and W. S. El-Deiry. 1996. Biological and clinical importance of the p53 tumor suppressor gene. Clin. Chem. 42:858–868.
   PubMed Web of Science ®Google Scholar
• Walker, K., and A. J. Levine. 1996. Identification of a novel p53 functional domain that is necessary for efficient growth suppression. Proc. Natl. Acad. Sci. USA 93:15335–15340.
   PubMed Web of Science ®Google Scholar