Activation of the DNA-binding ability of latent p53 protein by protein kinase C is abolished by protein kinase CK2

Biochemical Journal

Volumn 378, Issue 3, 2004, Pages 939-947

  Pospíšilová, Šárka ^a,b   Brázda, Václav ^c   Kuchaříková, Kateřina ^c,d   Luciani, M Gloria ^e   Hupp, Ted R ^f   Skládal, Petr ^d   Paleček, Emil ^c   Vojtěšek, Bořivoj ^a  

^a MASARYK MEMORIAL CANCER INSTITUTE   (Czech Republic)

^b UNIVERSITY HOSPITAL BRNO   (Czech Republic)

^c INSTITUTE OF BIOPHYSICS   (Czech Republic)

^d MASARYK UNIVERSITY   (Czech Republic)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

^f UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Activation; cdk2 cyclin A; DNA binding; Electrophoretic mobility shift assay (EMSA); p53; Phosphorylation

Indexed keywords

ANTIBODIES; BIOASSAY; BIOCHEMISTRY; DNA; ELECTROPHORESIS; PROTEINS;

OLIGOMERIZATION; PHOSPHORYLATION;

CYTOLOGY;

CASEIN KINASE II; CYCLIN A; CYCLIN DEPENDENT KINASE 2; PROTEIN KINASE C; PROTEIN P53; SERINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING; ENZYME ACTIVATION; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; HUMAN; INSECT CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; BINDING SITES; CASEIN KINASE II; CDC2-CDC28 KINASES; CELL LINE; CYCLIN-DEPENDENT KINASE 2; DNA; HUMANS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RESPONSE ELEMENTS; SPODOPTERA; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; ESCHERICHIA COLI; INSECTA;

EID: 12144288829     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20030662     Document Type: Article

References (54)

1. Lakin, N. D. and Jackson, S. P. (1999) Regulation of p53 in response to DNA damage. Oncogene 18, 7544-7655
2. Vogelstein, B., Lane, D. and Levine, A. J. (2000) Surfing the p53 network. Nature (London) 408, 307-310
3. Sionov, R. V. and Haupt, Y. (1999) The cellular response to p53: the decision between life and death. Oncogene 18, 6145-6157
4. Anderson, M. E., Woelker, B., Reed, M., Wang, P. and Tegtmeyer, P. (1997) Reciprocal interference between the sequence-specific core and nonspecific C-terminal DNA binding domains of p53: implications for regulation. Mol. Cell. Biol. 17, 6255-6264
5. Hupp, T. R. and Lane, D. P. (1995) Two distinct signaling pathways activate the latent DNA binding function of p53 in a casein kinase II-independent manner. J. Biol. Chem. 270, 18165-18174
6. Selivanova, G., Iotsova, V., Kiseleva, E., Strom, M., Bakalkin, G., Grafstrom, R. C. and Wiman, K. G. (1996) The single-stranded DNA end binding site of p53 coincides with the C-terminal regulatory region. Nucleic Acids Res. 24, 3560-3567
7. Jayaraman, L. and Prives, C. (1995) Activation of p53 sequence-specific DNA binding by short single strands of DNA. Cell 81, 1021-1029
8. 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
9. Pospisilova, S., Brazda, V., Amrichova, J., Kamermeierova, R., Palecek, E. and Vojtesek, B. (2000) Precise characterization of monoclonal antibodies to the C-terminal region of p53 protein using the PEPSCAN ELISA technique and a new non-radioactive gel shift assay. J. Immunol. Methods 237, 51-64
10. Brazda, V., Palecek, J., Pospisilova, S., Vojtesek, B. and Palecek, E. (2000) Specific modulation of p53 binding to consensus sequence within supercoiled DNA by monoclonal antibodies. Biochem. Biophys. Res. Commun. 267, 934-939
11. Bell, S., Klein, C., Muller, L., Hansen, S. and Buchner, J. (2002) p53 contains large unstructured regions in its native state. J. Mol. Biol. 322, 917-927
12. Nichols, N. M. and Matthews, K. S. (2002) Human p53 phosphorylation mimic, S392E, increases nonspecific DNA affinity and thermal stability. Biochemistry 41, 170-178
13. Dornan, D., Shimizu, H., Perkins, N. D. and Hupp, T. R. (2003) DNA-dependent acetylation of p53 by the transcription coactivator p300. J. Biol. Chem. 278, 13431-13441
14. Dornan, D., Shimizu, H., Burch, L., Smith, A. J. and Hupp, T. R. (2003) The proline repeat domain of p53 binds directly to the transcriptional coactivator p300 and allosterically controls DNA-dependent acetylation of p53. Mol. Cell. Biol. 23, 8846-8861
15. Shaw, P., Freeman, J., Bovey, R. and Iggo, R. (1996) Regulation of specific DNA binding by p53: evidence for a role for O-glycosylation and charged residues at the carboxy-terminus. Oncogene 12, 921-930
16. Rodriguez, M. S., Dargemont, C. and Hay, R. T. (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654-12659
17. Balint, E. E. and Vousden, K. H. (2001) Activation and activities of the p53 tumour suppressor protein. Br. J. Cancer 85, 1813-1823
18. Craig, A., Scott, M., Burch, L., Smith, G., Ball, K. and Hupp, T. (2003) Allosteric effects mediate CHK2 phosphorylation of the p53 transactivation domain. EMBO Rep. 4, 787-792
19. Dornan, D. and Hupp, T. R. (2001) Inhibition of p53-dependent transcription by BOX-I phospho-peptide mimetics that bind to p300. EMBO Rep. 2, 139-144
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. Lu, H., Fisher, R. P., Bailey, P. and Levine, A. J. (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
22. Appella, E. (2001) Modulation of p53 function in cellular regulation. Eur. J. Biochem. 268, 2763
23. Gu, W. and Roeder, R. G. (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90, 595-606
24. Baudier, J., Delphin, C., Grunwald, D., Khochbin, S. and Lawrence, J. J. (1992) Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc. Natl. Acad. Sci. U.S.A. 89, 11627-11631
25. Takenaka, I., Worin, 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
26. Waterman, M. J., 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. Nat. Genet. 19, 175-178
27. Youmell, M., Park, S. J., Basu, S. and Price, B. D. (1998) Regulation of the p53 protein by protein kinase C alpha and protein kinase C zeta. Biochem. Biophys. Res. Commun. 245, 514-518
28. Skouv, J., Jensen, P. O., Forchhammer, J., Larsen, J. K. and Lund, L. R. (1994) Tumor-promoting phorbol ester transiently down-modulates the p53 level and blocks the cell cycle. Cell Growth Differ. 5, 329-340
29. Delphin, C. and Baudier, J. (1994) The protein kinase C activator, phorbol ester, cooperates with the wild-type p53 species of Ras-transformed embryo fibroblasts growth arrest. J. Biol. Chem. 269, 29579-29587
30. Punnonen, K. and Yuspa, S. H. (1992) Ultraviolet light irradiation increases cellular diacylglycerol and induces translocation of diacylglycerol kinase in murine keratinocytes. J. Invest. Dermatol. 99, 221-226
31. Jinks, R. N., White, R. H. and Chamberlain, S. C. (1996) Dawn, diacylglycerol, calcium, and protein kinase C - the retinal wrecking crew. A signal transduction cascade for rhabdom shedding in the Limulus eye. J. Photochem. Photobiol. 35, 45-52
32. Blaydes, J. P. and Hupp, T. R. (1998) DNA damage triggers DRB-resistant phosphorylation of human p53 at the CK2 site. Oncogene 17, 1045-1052
33. Wallace, M., Coates, P. J., Wright, E. G. and Ball, K. L. (2001) Differential post-translational modification of the tumour suppressor proteins Rb and p53 modulate the rates of radiation-induced apoptosis in vivo. Oncogene 20, 3597-3608
34. Hao, M., Lowy, A. M., Kapoor, M., Deffie, A., Liu, G. and Lozano, G. (1996) Mutation of phosphoserine 389 affects p53 function in vivo. J. Biol. Chem. 271, 29380-29385
35. Schuster, N., Prowald, A., Schneider, E., Scheidtmann, K. H. and Montenarh, M. (1999) Regulation of p53 mediated transactivation by the beta-subunit of protein kinase CK2. FEBS Lett. 447, 160-166
36. Schuster, N., Gotz, C., Faust, M., Schneider, E., Prowald, A., Jungbluth, A. and Montenarh, M. (2001) Wild-type p53 inhibits protein kinase CK2 activity. J. Cell. Biochem. 81, 172-183
37. Delphin, C., Huang, K. P., Scotto, C., Chapel, A., Vincon, M., Chambaz, E., Garin, J. and Baudier, J. (1997) The in vitro phosphorylation of p53 by calcium-dependent protein kinase C - characterization of a protein-kinase-C- binding site on p53. Eur. J. Biochem. 245, 684-692
38. Luciani, M. G., Hutchins, J. R., Zheleva, D. and Hupp, T. R. (2000) The C-terminal regulatory domain of p53 contains a functional docking site for cyclin A. J. Mol. Biol. 300, 503-518
39. Hutchins, J. R., Hughes, M. and Clarke, P. R. (2000) Substrate specificity determinants of the checkpoint protein kinase Chk1. FEBS Lett. 466, 91-95
40. Vojtesek, B., Bartek, J., Midgley, C. A. and Lane, D. P. (1992)An immunochemical analysis of the human nuclear phosphoprotein p53. New monoclonal antibodies and epitope mapping using recombinant p53. J. Immunol. Methods 151, 237-244
41. Midgley, C. A., Fisher, C. J., Bartek, J., Vojtesek, B., Lane, D. and Barnes, D. M. (1992) Analysis of p53 expression in human tumours: an antibody raised against human p53 expressed in Escherichia coli. J. Cell Sci. 101, 183-189
42. Stephen, C. W., Helminen, P. and Lane, D. P. (1995) Characterization of epitopes on human p53 using phage-displayed peptide libraries: insights into antibody-peptide interactions. J. Mol. Biol. 248, 58-78
43. Blaydes, J. P., Luciani, M. G., Pospisilova, S., Ball, H. M., Vojtesek, B. and Hupp, T. R. (2001) Stoichiometric phosphorylation of human p53 at Ser315 stimulates p53-dependent transcription. J. Biol. Chem. 276, 4699-4708
44. Pospisilova, S., Kankova, K., Svitakova, M., Nenutil, R. and Vojtesek, B. (2001) New monoclonal antibodies recognizing p53 protein phosphorylated by casein kinase II at serine 392. Folia Biol. 47, 148-151
45. Hupp, T. R. and Lane, D. P. (1994) Allosteric activation of latent p53 tetramers. Curr. Biol. 4, 865-875
46. Palecek, E., Vlk, D., Stankova, V., Brazda, V., Vojtesek, B., Hupp, T. R., Schaper, A. and Jovin, T. M. (1997) Tumor suppresor protein p53 binds preferentially to supercoiled DNA. Oncogene 15, 2201-2209
47. Skladal, P. and Horacek, J. (1999) Kinetic studies of affinity interactions: comparison of piezoelectric and resonant mirror-based biosensors. Anal. Lett. 32, 1519-1529
48. Minamoto, T., Buschmann, T., Habelhah, H., Matusevich, E., Tahara, H., Boerresen-Dale, A. L., Harris, C., Sidransky, D. and Ronai, Z. (2001) Distinct pattern of p53 phosphorylation in human tumors. Oncogene 20, 3341-3347
49. Chiarugi, V., Cinelli, M. and Magnelli, L. (1998) Acetylation and phosphorylation of the carboxy-terminal domain of p53: regulative significance. Oncol. Res. 10, 55-57
50. Jagelska, E., Brazda, V., Pospisilova, S., Vojtesek, B. and Palecek, E. (2002) New ELISA technique for analysis of p53 protein/DNA binding properties. J. Immunol. Methods 267, 227-235
51. Sakaguchi, K., Sakamoto, H., Lewis, M. S., Anderson, C. W., Erickson, J. W., Appella, E. and Xie, D. (1997) Phosphorylation of serine 392 stabilizes the tetramer formation of tumor suppressor protein p53. Biochemistry 36, 10117-10124
52. Fiscella, M., Zambrano, N., Ullrich, S. J., Unger, T., Lin, D., Cho, B., Mercer, W. E., Anderson, C. W. and Appella, E. (1994) The carboxy-terminal serine 392 phosphorylation site of human p53 is not required for wild-type activities. Oncogene 9, 3249-3257
53. Gotz, C., Scholtes, P., Prowald, A., Schuster, N., Nastainczyk, W. and Montenarh, M. (1999) Protein kinase CK2 interacts with a multi-protein binding domain of p53. Mol. Cell. Biochem. 191, 111-120
54. Yakovleva, T., Pramanik, A., Kawasaki, T., Tan-No, K., Gileva, I., Lindegren, H., Langel, U., Ekstrom, T. J., Rigler, R., Terenius, L. and Bakalkin, G. (2001) p53 latency. C-terminal domain prevents binding of p53 core to target but not to nonspecific DNA sequences. J. Biol. Chem. 276, 15650-15658