Serine 15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2

EMBO Journal

Volumn 18, Issue 24, 1999, Pages 7002-7010

  Dumaz, Nicolas ^a   Meek, David W ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

HDM2; p300; p53; Phosphorylation; Transactivation

Indexed keywords

PROTEIN P53; REGULATOR PROTEIN; DNA BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; HYBRID PROTEIN; MDM2 PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOPROTEIN; PHOSPHOSERINE; PRKDC PROTEIN, HUMAN; PROTEIN MDM2; PROTEIN SERINE THREONINE KINASE; RECOMBINANT PROTEIN; SERINE;

ACETYLATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; AMINO ACID SUBSTITUTION; CELL LINE; CHEMISTRY; GENETIC TRANSFECTION; METABOLISM; REPORTER GENE; SITE DIRECTED MUTAGENESIS;

ANIMALIA;

AMINO ACID SUBSTITUTION; CELL LINE; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; GENES, REPORTER; HUMANS; MUTAGENESIS, SITE-DIRECTED; NUCLEAR PROTEINS; PHOSPHOSERINE; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; SERINE; TRANS-ACTIVATION (GENETICS); TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0033572746     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.24.7002     Document Type: Article

References (55)

1. Ashcroft, M., Kubbutat, M.H.G. and Vousden, K.H. (1999) Regulation of p53 function and stability by phosphorylation. Mol. Cell. Biol., 19, 1751-1758.
2. Avantaggiati, M.L., Ogryzko, V., Gardner, K., Giordano, A., Levine, A.S. and Kelly, K. (1997) Recruitment of p300/CBP in p53-dependent signal pathways. Cell, 89, 1175-1184.
3. Banin, S. et al. (1998) Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science, 281, 1674-1677.
4. Blattner, C., Tobiasch, E., Litfen, M., Rahmsdorf, H.J. and Herrlich, P. (1999) DNA damage-induced p53 stabilisation: no indication for an involvement of p53 phosphorylation. Oncogene, 18, 1723-1732.
5. Bottger, A., Bottger, V., Sparks, A., Liu, W.-L., Howard, S.F. and Lane, D.P. (1997) Design of a synthetic Mdm2-binding mini protein that activates the p53 response in vivo. Curr. Biol., 7, 860-869.
6. Canman, C.E., Lim, D.-S., Cimprich, K.A., Taya, Y., Tamai, K., Sakaguchi, K., Appella, E., Kastan, M.B. and Siliciano, J.D. (1998) Activation of the ATM kinase by ionising radiation and phosphorylation of p53. Science, 281, 1677-1679.
7. Chen, X., Farmer, G., Zhu, H., Prywes, R. and Prives, C. (1993) Cooperative DNA binding of p53 with TFIID (TBP): a possible mechanism for transcriptional activation [published erratum appears in Genes Dev., 1993, 7, 2652]. Genes Dev., 7, 1837-1849.
8. Deng, W.P. and Nickoloff, J.A. (1992) Site-directed mutagnesis of virtually any plasmid by eliminating a unique site. Anal. Biochem., 200, 81-88.
9. el Deiry, W., Kern, S.E., Pietenpol, J.A., Kinzler, K.W. and Vogelstein, B. (1992) Definition of a consensus binding site for p53. Nature Genet., 1, 45-49.
10. el Deiry, W. et al. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell, 75, 817-825.
11. Farmer, G., Colgan, J., Nakatani, Y, Manley, J.L. and Prives, C. (1996) Functional interaction between p53, the TATA-binding protein (TBP) and TBP-associated factors in vivo. Mol. Cell. Biol., 16, 4295-4303.
12. Fiscella, M., Ullrich, S.J., Zambrano, N., Shields, M.T., Lin, D., Lees-Miller, S., Anderson, C.W., Mercer, W.E. and Appella, E. (1993) Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression. Oncogene, 8. 1519-1528.
13. Giaccia, A.J. and Kastan, M.B. (1998) The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev., 12, 2973-2983.
14. Gu, W. and Roeder, R.G. (1997) Activation of p53 sequence-specific DNA binding by acetylation of the C-terminal domain. Cell, 90, 595-606.
15. Gu, W., Shi,X.-L. and Roeder, R.G. (1997) Synergistic activation of transcription by CBP and p53. Nature, 387, 819-823.
16. Hall, S.R., Campbell, L.E. and Meek, D.W. (1996) Phosphorylation of p53 at the casein kinase II site selectively regulates p53-dependent transcriptional repression but not transactivation. Nucleic Acids Res., 24, 1119-1126.
17. Haupt, Y. Maya, R., Kazaz, A. and Oren, M. (1997) Mdm2 protein promotes rapid degradation of p53. Nature. 387, 296-299.
18. 1 arrest. Proc. Natl Acad. Sci. USA. 93, 4827-4832.
19. Hupp, T.R., Meek, D.W., Midgley, C.A. and Lane, D.P. (1992) Regulation of the specific DNA binding function of p53. Cell, 71, 875-886.
20. Ko, L.J., Shieh, S.-Y., Chen, X., Jayaraman, L., Tamai, K., Taya, Y., Prives, C. and Pan, Z.-Q. (1997) p53 is phosphorylated by CDK7-cyclin h in a p36MAT1-dependent manner. Mol. Cell. Biol., 17, 7220-7229.
21. Kubbutat, M.H.G., Jones, S.N. and Vousden, K.H. (1997) Regulation of p53 stability by Mdm2. Nature, 387, 299-303.
22. Lambert, P.F., Kashanchi, F., Radonovich, M.F., Shiekhattar, R. and Brady, J.N. (1998) Phosphorylation of p53 serine 15 increases interaction with CBP. J. Biol. Chem., 273, 33048-33053.
23. Lees-Miller, S., Sakaguchi, K., Ullrich, S.J., Appella, E. and Anderson, C.W. (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.
24. Levine, A.J. (1997) p53, the cellular gatekeeper for growth and division. Cell. 88, 323-331.
25. Lill, N.L., Grossman, S.R., Ginsberg, D., DeCaprio, J. and Livingston, D.M. (1997) Binding and modulation of p53 by p300/CBP coactivators. Nature, 387, 823-826.
26. Liu, L., Scolnick, D.M., Trievel, R.C, Zhang, H.B., Marmorstein, R., Halazonetis, T.D. and Berger, S.L. (1999) p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol. Cell. Biol., 19, 1202-1209.
27. Liu, X., Miller, C.W., Koeffler, P.H. and Berk, A.J. (1993) The p53 activation domain binds the TATA box-binding polypeptide in holo-TFIID and a neighboring p53 domain inhibits transcription. Mol. Cell. Biol., 13, 3291-3300.
28. II31 protein is a transcriptional coactivator of the p53 protein. Proc. Natl Acad. Sci. USA, 92, 5154-5158.
29. Lu, H., Fisher, R.P, Bailey, P. and Levine, A.J. (1997) The CDK7-cyclin H-p36 complex of transcription factor TFIIH phosphorylates p53, enhancing its sequence-specific DNA binding activity in vitro. Mol. Cell. Biol., 17, 5923-5934.
30. Mack, D.H., Varlikar, J., Pipas, J.M. and Laimins, L.A. (1993) Specific-repression of TATA-mediated but not initiator-mediated transcription by wild-type p53. Nature, 363, 281-283.
31. Martin, D.W., Munoz, R.M., Subler, M.A. and Deb, S. (1993) p53 binds to the TATA-binding protein-TATA complex. J. Biol. Chem., 268, 13062-13067.
32. 2 terminus of p53 facilitates transactivation. Cancer Res., 55, 2410-2417.
33. Meek, D.W. (1999) Mechanisms of switching on p53: a role for covalent modification? Oncogene, in press.
34. Milne, D.M., Palmer, R.H., Campbell, D.G. and Meek, D.W. (1992) Phosphorylation of the p53 tumour-suppressor protein at three N-terminal sites by a novel casein kinase I-like enzyme. Oncogene, 7, 1361-1369.
35. Milne, D.M., Campbell, L., Campbell, D.G. and Meek, D.W. (1995) p53 is phosphorylated in vitro and in vivo by an ultra-violet radiation-induced protein kinase characteristic of the c-Jun kinase, JNK-1. J. Biol. Chem., 270, 5511-5518.
36. Oliner, J.D., Pietenpol, A., Thiagalingam, S., Gyuris, J., Kinzler, K.W. and Vogelstein, B. (1993) Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature, 362, 857-860.
37. Pise-Masison, C.A., Radonovich, M., Sakaguchi, K., Appella, E. and Brady, J.N. (1998) Phosphorylation of p53: a novel pathway for p53 inactivation in human T-cell lymphotropic virus type 1-transformed cells. J. Virol., 72, 6348-6355.
38. Prives, C. and Hall, P.A. (1999) The p53 pathway. J. Pathol., 187, 112-126.
39. Renzing, J. and Lane, D.P. (1995) p53-dependent growth arrest following calcium phosphate-mediated transfection of murine fibroblasts. Oncogene, 10, 1865-1868.
40. Sakaguchi, K., Herrera, J.E., Saito, S., Miki, T., Bustin, M., Vassilev, A., Anderson, C.W. and Appella, E. (1998) DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev., 12, 2831-2841.
41. Scolnick, D.M., Chehab, N.H., Stavridi, E.S., Lien, M.C. Caruso, L., Moran, E., Berger, S.L. and Halazonetis, T.D. (1997) CREB-binding protein and p300/CBP-associated factor are transcriptional coactivators of the p53 tumor suppressor protein. Cancer Res., 57, 3693-3696.
42. Seto, E., Usheva, A., Zambetti, G.P, Momand, J., Horikoshi, N., Weinmann, R., Levine, A.J. and Shenk, T. (1992) Wild-type p53 binds to the TATA-binding protein and represses transcription. Proc. Natl Acad. Sci. USA, 89, 12028-12032.
43. Shieh, S.-Y., Ikeda, M., Taya, Y. and Prives, C. (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell, 91, 325-334.
44. Shieh, S.-Y., Taya, Y. and Prives, C. (1999) DNA damage-inducible phosphorylation of p53 at N-terminal sites including a novel site. Ser20, requires tetramerisation. EMBO J., 18, 1815-1823.
45. Siliciano, J.D., Canman, C.E., Taya, Y., Sakaguchi, K., Appella, E. and Kastan, M.B. (1997) DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev., 11, 3471-3481.
46. Takenaka, I., Morin, F., Seizinger, B.R. and Kley, N. (1995) Regulation of the sequence-specific DNA binding function of p53 by protein kinase C and protein phosphatases. J. Biol. Chem., 270, 5405-5411.
47. II60. Science, 267, 100-104.
48. Tibbetts, R.S., Brumbaugh, K.M., Williams, J.M., Sarkaria, J.N., Cliby, W.A., Shieh, S.-Y., Taya, Y., Prives, C. and Abraham, R.T. (1999) A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev., 13, 152-157.
49. Truant, R., Xiao, H., Ingles, C.J. and Greenblatt, J. (1993) Direct interaction between the transcriptional activation domain of human p53 and the TATA box-binding protein. J. Biol. Chem., 268, 2284-2287.
50. Unger, T., Nau, M.M., Segal, S. and Minna, J.D. (1992) p53: a transdominant regulator of transcription whose function is ablated by mutations occurring in human cancer. EMBO J., 11, 1383-1390.
51. Unger, T., Juven-Gershon, T., Moallem, E., Berger, M., Vogt Sionov, R., Lozano, G., Oren, M. and Haupl, Y. (1999a) Critical role for Ser20 of human p53 in the negative regulation of p53 by MDM2. EMBO J., 18, 1805-1814.
52. Unger,T., Vogt Sionov, R., Moallem, E., Yee, C.Y., Howley, P.M., Oren, M. and Haupt, Y. (1999b) Mutations in serines 15 and 20 of human p53 impair its apoptotic function. Oncogene, 18, 3205-3212.
53. 1 cyclin-dependent kinases. Nature, 376, 88-91.
54. Waterman, M.J.F., Stavridi, E.S., Waterman, J.L. and Halazonetis, T.D. (1998) ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nature Genet., 19, 175-178.
55. Yuan, Z.-M. et al. (1999) Role for p300 in stabilisation of p53 in response to DNA damage. J. Biol. Chem., 274, 1883-1886.