Mapping the interactions of the p53 transactivation domain with the KIX domain of CBP

Biochemistry

Volumn 48, Issue 10, 2009, Pages 2115-2124

  Lee, Chul Won ^a   Arai, Munehito ^a,b   Martinez Yamout, Maria A ^a   Dyson, H Jane ^a   Wright, Peter E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION DOMAINS; BINDING AFFINITIES; BINDING SURFACES; CHEMICAL SHIFT PERTURBATIONS; ISOTHERMAL TITRATION CALORIMETRIES; NMR SPECTROSCOPIES; STRUCTURAL DOMAINS; SUB-DOMAINS; TRANSACTIVATION; TRANSACTIVATION DOMAINS; TRANSCRIPTIONAL CO-ACTIVATORS; TUMOR SUPPRESSORS;

AMINES; BINDING ENERGY; CHEMICAL REACTIONS; CHLORINATION; CONTEXT SENSITIVE GRAMMARS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; PHOSPHORYLATION; TRANSCRIPTION FACTORS;

BINDING SITES;

CARRIER PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LIGAND; NUCLEAR RECEPTOR COACTIVATOR; PEPTIDE; PHOSPHOTRANSFERASE; PROTEIN P53; SERINE; THREONINE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; ENZYME ACTIVATION; EXPERIMENT; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REGULATORY MECHANISM; SPIN LABELING; TRANSCRIPTION INITIATION;

ANIMALS; BINDING SITES; BINDING, COMPETITIVE; CALORIMETRY; CREB-BINDING PROTEIN; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HUMANS; MICE; MODELS, CHEMICAL; MODELS, MOLECULAR; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTO-ONCOGENE PROTEINS C-MYB; RECOMBINANT PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 64349086059     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi802055v     Document Type: Article

References (65)

1. Goodman, R. H., and Smolik, S. (2000) CBP/p300 in cell growth, transformation, and development. Genes Dev. 14, 1553-1577.
2. Chrivia, J. C., Kwok, R. P., Lamb, N., Hagiwara, M., Montminy, M., and Goodman, R. H. (1993) Phosphorylated CREB binds specifically to nuclear protein CBP. Nature 365, 855-859.
3. Giordano, A., and Avantaggiati, M. L. (1999) p300 and CBP: Partners for life and death. J. Cell. Phys. 181, 218-230.
4. Ernst, P., Wang, J., Huang, M., Goodman, R. H., and Korsmeyer, S. J. (2001) MLL and CREB bind cooperatively to the nuclear coactivator CREB-binding protein. Mol. Cell. Biol. 21, 2249-2258.
5. Bannister, A. J., Oehler, T., Wilhelm, D., Angel, P., and Kouzarides, T. (1995) Stimulation of c-Jun activity by CBP: c-Jun residues Ser63/73 are required for CBP induced stimulation in vivo and CBP binding in vitro. Oncogene 11, 2509-2514.
6. Dai, P., Akimaru, H., Tanaka, Y., Hou, D. X., Yasukawa, T., Kanei-Ishii, C., Takahashi, T., and Ishii, S. (1996) CBP as a transcriptional coactivator of c-Myb. Genes Dev. 10, 528-540.
7. Kwok, R. P. S., Laurance, M. E., Lundblad, J. R., Goldman, P. S., Shih, H., Connor, L. M., Marriott, S. J., and Goodman, R. H. (1996) Control of cAMP-regulated enhancers by the viral transactivator Tax through CREB and the co-activator CBP. Nature 380, 642-646.
8. Vendel, A. C., and Lumb, K. J. (2003) Molecular recognition of the human coactivator CBP by the HIV-1 transcriptional activator Tat. Biochemistry 42, 910-916.
9. Radhakrishnan, I., Pérez-Alvarado, G. C., Parker, D., Dyson, H. J., Montminy, M. R., and Wright, P. E. (1997) Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: A model for activator:coactivator interactions. Cell 91, 741-752.
10. Zor, T., De Guzman, R. N., Dyson, H. J., and Wright, P. E. (2004) Solution structure of the KIX domain of CBP bound to the transactivation domain of c-Myb. J. Mol. Biol. 337, 521-534.
11. Campbell, K. M., and Lumb, K J. (2002) Structurally distinct modes of recognition of the KIX domain of CBP by Jun and CREB. Biochemistry 41, 13956-13964.
12. Goto, N. K., Zor, T., Martinez-Yamout, M., Dyson, H. J., and Wright, P. E. (2002) Cooperativity in transcription factor binding to the coactivator CREB-binding protein (CBP). The mixed lineage leukemia protein (MLL) activation domain binds to an allosteric site on the Kix domain. J. Biol. Chem. 277, 43168-43174.
13. Vendel, A. C., McBryant, S. J., and Lumb, K. J. (2003) KIX-mediated assembly of the CBP-CREB-HTLV-1 tax coactivator-activator complex. Biochemistry 42, 12481-12487.
14. Ramirez, J. A., and Nyborg, J. K (2007) Molecular characterization of HTLV-1 Tax interaction with the KIX domain of CBP/p300. J. Mol. Biol. 372, 958-969.
15. Bode, A. M., and Dong, Z. (2004) Post-translational modification of p53 in tumorigenesis. Nat. Rev. Cancer 4, 793-805.
16. Vousden, K H., and Lane, D. P. (2007) p53 in health and disease. Nat. Rev. Mol. Cell. Biol. 8, 275-283.
17. Grossman, S. R. (2001) p300/CBP/p53 interaction and regulation of the p53 response. Eur. J. Biochem. 268, 2773-2778.
18. Moll, U. M., and Petrenko, O. (2003) The MDM2-p53 interaction. Mol. Cancer Res. 1, 1001-1008.
19. Chang, J., Kim, D. H., Lee, S. W., Choi, K. Y., and Sung, Y. C. (1995) Transactivation ability of p53 transcriptional activation domain is directly related to the binding affinity to TATA-binding protein. J. Biol. Chem. 270, 25014-25019.
20. Ayed, A., Mulder, F. A., Yi, G. S., Lu, Y., Kay, L. E., and Arrowsmith, C. H. (2001) Latent and active p53 are identical in conformation. Nat. Struct. Biol. 8, 756-760.
21. Dawson, R., Muller, L., Dehner, A., Klein, C., Kessler, H., and Buchner, J. (2003) The N-terminal domain of p53 is natively unfolded. J. Mol. Biol. 332, 1131-1141.
22. Unger, T., Mietz, J. A., Scheffner, M., Yee, C. L., and Howley, P. M. (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.
23. Candau, R., Scolnick, D. M., Darpino, P., Ying, C. Y., Halazonetis, T. D., and Berger, S. L. (1997) Two tandem and independent sub-activation domains in the amino terminus of p53 require the adaptor complex for activity. Oncogene 15, 807-816.
24. Venot, C., Maratrat, M., Sierra, V., Conseiller, E., and Debussche, L. (1999) Definition of a p53 transactivation function-deficient mutant and characterization of two independent p53 transactivation subdomains. Oncogene 18, 2405-2410.
25. Zhu, J., Zhang, S., Jiang, J., and Chen, X. (2000) Definition of the p53 functional domains necessary for inducing apoptosis. J. Biol. Chem. 275, 39927-39934.
26. Avantaggiati, M. L., Ogryzko, V., Gardner, K., Giordano, A., Levine, A., and Kelly, K (1997) Recruitment of p300/CBP in p53-dependent signal pathways. Cell 89, 1175-1184.
27. 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, 823-827.
28. Gu, W., Shi, X. L., and Roeder, R. G. (1997) Synergistic activation of transcription by CBP and p53. Nature 387, 819-823.
29. 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.
30. Livengood, J. A., Scoggin, K. E. S., van Orden, K., McBryant, S. J., Edayathumangalam, R. S., Laybourn, P. J., and Nyborg, J. K (2002) p53 transcriptional activity Is mediated through the SRC1-interacting domain of CBP/p300. J. Biol. Chem. 277, 9054-9061.
31. van Orden, K., Giebler, H. A., Lemasson, I., Gonzales, M., and Nyborg, J. K. (1999) Binding of p53 to the KIX domain of CREB binding proteinsA potential link to human T-cell leukemia virus, type I-associated leukemogenesis. J. Biol. Chem. 274, 26321-26328.
32. Grossman, S. R., Perez, M., Kung, A. L., Joseph, M., Mansur, C., Xiao, Z. X., Kumar, S., Howley, P. M., and Livingston, D. M. (1998) p300/MDM2 complexes participate in MDM2-mediated p53 degradation. Mol. Cell 2, 405-415.
33. Wadgaonkar, R., and Collins, T. (1999) Murine double minute (MDM2) blocks p53-coactivator interaction, a new mechanism for inhibition of p53-dependent gene expression. J. Biol. Chem. 274, 13760-13767.
34. Teufel, D. P., Freund, S. M., Bycroft, M., and Fersht, A. R. (2007) Four domains of p300 each bind tightly to a sequence spanning both transactivation subdomains of p53. Proc. Natl. Acad. Sci. U.S.A. 104, 7009-7014.
35. Giebler, H. A., Loring, J. E., van Orden, K., Colgin, M. A., Garrus, J. E., Escudero, K. W., Brauweiler, A., and Nyborg, J. K. (1997) Anchoring of CREB binding protein to the human T-cell leukemia virus type 1 promoter: a molecular mechanism of Tax transactivation. Mol. Cell. Biol. 17, 5156-5164.
36. Harrod, R., Tang, Y., Nicot, C., Lu, H. S., Vassilev, A., Nakatani, Y., and Giam, C. Z. (1998) An exposed KID-like domain in human T-cell lymphotropic virus type 1 Tax is responsible for the recruitment of coactivators CBP/p300. Mol. Cell. Biol. 18, 5052-5061.
37. Ariumi, Y., Kaida, A., Lin, J. Y., Hirota, M., Masui, O., Yamaoka, S., Taya, Y., and Shimotohno, K (2000) HTLV-1 Tax oncoprotein represses the p53-mediated trans-activation function through coactivator CBP sequestration. Oncogene 19, 1491-1499.
38. Chaudhry, S., Freebern, W. J., Smith, J. L., Butscher, W. G., Haggerty, C. M., and Gardner, K. (2002) Cross-tegulation of T cell growth factor expression by p53 and the Tax oncogene. J. Immunol. 169, 6767-6778.
39. Sugase, K., Landes, M. A., Wright, P. E., and Martinez-Yamout, M. (2008) Overexpression of post-translationally modified peptides in Escherichia coli by co-expression with modifying enzymes. Protein Expression Purif. 57, 108-115.
40. Delaglio, F., Grzesiek, S., Vuister, G. W., Guang, Z., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
41. Johnson, B. A., and Blevins, R. A. (1994) NMRView: A computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 604-613.
42. Grzesiek, S., and Bax, A. (1992) Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein. J. Magn. Reson. 96, 432-440.
43. Wittekind, M., and Mueller, L. (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J. Magn. Reson. 101, 201-205.
44. Wang, Z. X., and Jiang, R. F. (1996) A novel two-site binding equation presented in terms of the total ligand concentration. FEBS Lett. 392, 245-249.
45. Press,W. H., Teukolsky, S. A., Vetterling, W. T., and Flannery, B. P. (1992) Numerical Recipes in C., Cambridge University Press, Cambridge, U.K.
46. Lee, H., Mok, K. H., Muhandiram, R., Park, K. H., Suk, J. E., Kim, D. H., Chang, J., Sung, Y. C., Choi, K. Y., and Han, K. H. (2000) Local structural elements in the mostly unstructured transcriptional activation domain of human p53. J. Biol. Chem. 275, 29426-29432.
47. Zor, T, Mayr, B. M., Dyson, H. J., Montminy, M. R., and Wright, P. E. (2002) Roles of phosphorylation and helix propensity in the binding of the KIX domain of CREB-binding protein by constitutive (c-Myb) and inducible (CREB) activators. J. Biol. Chem. 277, 42241-42248.
48. Jabbur, J. R., and Zhang, W. (2002) p53 antiproliferative function is enhanced by aspartate substitution at threonine 18 and serine 20. Cancer Biol. Ther. 1, 277-283.
49. Chao, C., Herr, D., Chun, J., and Xu, Y. (2006) Ser18 and 23 phosphorylation is required for p53-dependent apoptosis and tumor suppression. EMBO J. 25, 2615-2622.
50. Nakamizo, A., Amano, T, Zhang, W., Zhang, X. Q., Ramdas, L., Liu, T. J., Bekele, B. N., Shono, T, Sasaki, T, Benedict, W. F., Sawaya, R., and Lang, F. F. (2008) Phosphorylation of Thr18 and Ser20 of p53 in Ad-p53-induced apoptosis. Neuro-oncol. 10, 275-291.
51. Sugase, K., Dyson, H. J., and Wright, P. E. (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447, 1021-1025.
52. Kussie, P. H., Gorina, S., Marechal, V., Elenbaas, B., Moreau, J., Levine, A. J., and Pavletich, N. P. (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274, 948-953.
53. Bochkareva, E., Kaustov, L., Ayed, A., Yi, G. S., Lu, Y., Pineda-Lucena, A., Liao, J. C. C., Okorokov, A. L., Milner, J., Arrowsmith, C. H., and Bochkarev, A. (2005) Single-stranded DNA mimicry in the p53 transactivation domain interaction with replication protein A. Proc. Natl. Acad. Sci. U.S.A. 102, 15412-15417.
54. Di Lello, P., Jenkins, L. M. M., Jones, T. N., Nguyen, B. D., Hara, T., Yamaguchi, H., Dikeakos, J. D., Appella, E., Legault, P., and Omichinski, J. G. (2006) Structure of the Tfb1/p53 complex: insights into the interaction between the p62/Tfb1 subunit of TFIIH and the activation domain of p53. Mol. Cell 22, 731-740.
55. Appella, E., and Anderson, C. W. (2001) Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268, 2764-2772.
56. Xu, Y. (2003) Regulation of p53 responses by post-translational modifications. Cell Death Differ. 10, 400-403.
57. Sakaguchi, K., Saito, S., Higashimoto, Y., Roy, S., Anderson, C. W., and Appella, E. (2000) Damage-mediated phosphorylation of human p53 threonine 18 through a cascade mediated by a casein 1-like kinase. Effect on Mdm2 binding. J . Biol. Chem. 275, 9278-9283.
58. Schon, O., Friedler, A., Bycroft, M., Freund, S. M., and Fersht, A. R. (2002) Molecular mechanism of the interaction between MDM2 and p53. J. Mol. Biol. 323, 491-501.
59. Dumaz, N., and Meek, D. W. (1999) Serine15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2. EMBO J. 18, 7002-7010.
60. 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.
61. 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.
62. Parker, D., Ferreri, K., Nakajima, T., LaMorte, V. J., Evans, R., Koerber, S. C., Hoeger, C., and Montminy, M. (1996) Phosphorylation of CREB at Ser133 induces complex formation with CPB via a direct mechanism. Mol. Cell. Biol. 16, 694-703.
63. Tanikawa, J., Nomura, T., Macmillan, E. M., Shinagawa, T., Jin, W., Kokura, K., Baba, D., Shirakawa, M., Gonda, T. J., and Ishii, S. (2004) p53 suppresses c-Myb-induced trans-activation and transformation by recruiting the corepressor mSin3A. J. Biol. Chem. 279, 55393-55400.
64. De Guzman, R. N., Goto, N. K., Dyson, H. J., and Wright, P. E. (2006) Structural basis for cooperative transcription factor binding to the CBP coactivator. J. Mol. Biol. 355, 1005-1013.
65. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55.