The N terminus of the murine p53 tumour suppressor is an independent regulatory domain affecting activation and thermostability

Journal of Molecular Biology

Volumn 275, Issue 4, 1998, Pages 575-588

  Hansen, Silke ^a,b   Lane, David P ^a   Midgley, Carol A ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Activation; Conformation; P53 tumour suppressor; Sequence specific DNA binding; Thermostability

Indexed keywords

AMINO ACID; ANTIBODY; PROTEIN P53;

AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTALLOGRAPHY; DNA BINDING; GENE ACTIVATION; MIGRATION; MOUSE; NONHUMAN; OLIGOMERIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; THERMOSTABILITY; TRANSCRIPTION INITIATION;

ANIMALIA; MURINAE; UNIDENTIFIED BACULOVIRUS;

EID: 0032579321     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1507     Document Type: Article

References (46)

1. Baker, S. J., Markowitz, S., Fearon, E. R., Willson, J. K. & Vogelstein, B. (1990). Suppression of human color-ectal-carcinoma cell-growth by wild type p53. Science, 249, 912-915.
2. Ball, R. K., Siegl, B., Quellhorst, S., Brandner, G. & Braun, D. G. (1984). Monoclonal antibodies against simian virus 40 nuclear large T tumour antigen: epitope mapping, papova virus cross-reaction and cell surface staining. EMBO J. 3, 1488-1491.
3. Bargonetti, J., Manfredi, J. J., Chen, X., Marshak, D. R. & Prives, C. (1993). A proteolytic fragment from the central region of p53 has marked sequence-specific DNA-binding activity when generated from wild-type but not from oncogenic mutant p53 protein. Genes Dev. 7, 2565-2574.
4. Cho, Y., Gorina, S., Jeffrey, P. D. & Pavletich, N. P. (1994). Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science, 265, 346-355.
5. Dippold, W. G., Jay, G., DeLeo, A. B., Khoury, G. & Old, L. J. (1981). p53 transformation-related protein: detection by monoclonal antibody in mouse and human cells. Proc. Natl Acad. Sci. USA, 78, 1695-1699.
6. El-Deiry, W., Kern, S. E., Pietenpol, J. A., Kinzler, K. W. & Vogelstein, B. (1992). Definition of a consensus binding site for p53. Nature Genet. 1, 45-49.
7. Gannon, J. V., Greaves, R., Iggo, R. & Lane, D. P. (1990). Activating mutations in p53 produce a common conformational effect. A monoclonal antibody specific for the mutant form. EMBO J. 9, 1595-1602.
8. Greaves, R. (1988). The expression of murine p53 in E. coli. PhD thesis, Imperial College of Science and Technology, London.
9. Hainaut, P., Butcher, S. & Milner, J. (1995). Temperature sensitivity for conformation is an intrinsic property of wild-type p53. Br. J. Cancer, 71, 227-231.
10. Halazonetis, T. D. & Kandil, A. N. (1993). Conformational shifts propagate from the oligomerization domain of p53 to its tetrameric DNA binding domain and restore DNA binding to select p53 mutants. EMBO J. 12, 5057-5064.
11. Halazonetis, T. D., Davis, L. J. & Kandil, A. N. (1993). Wild-type p53 adopts a 'mutant'-like conformation when bound to DNA. EMBO J. 12, 1021-1028.
12. Hansen, S., Hupp, T. R. & Lane, D. P. (1996a). Allosteric regulation of the thermostability and DNA binding activity of human p53 by specific interacting proteins. J. Biol. Chem. 271, 3917-3924.
13. Hansen, S., Midgley, C. A., Lane, D. P., Freeman, B. C., Morimoto, R. I. & Hupp, T. R. (1996b). Modification of two distinct COOH-terminal domains is required for murine p53 activation by bacterial Hsp70. J. Biol. Chem. 271, 30922-30928.
14. Harlow, E. & Lane, D. P. (1988). Antibodies: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
15. Harlow, E., Crawford, L. V., Pim, D. C. & Williamson, N. M. (1981). Monoclonal antibodies specific for simian virus 40 tumour antigens. J. Virol. 39, 861-869.
16. Haupt, Y., Maya, R., Kazaz, A. & Oren, M. (1997). Mdm2 promotes the rapid degradation of p53. Nature, 387, 296-299.
17. Hupp, T. R. & Lane, D. P. (1994). Regulation of the cryptic sequence-specific DNA binding function of p53 by protein kinases. Cold Spring Harbor Symp. Quant. Biol. 59, 195-206.
18. Hupp, T. R., Meek, D. W., Midgley, C. A. & Lane, D. P. (1992). Regulation of the specific DNA binding function of p53. Cell, 71, 875-886.
19. Hupp, T. R., Meek, D. W., Midgley, C. A. & Lane, D. P. (1993). Activation of the cryptic DNA binding function of mutant forms of p53. Nucl. Acids Res. 21, 3167-3174.
20. Hupp, T. R., Sparks, A. & Lane, D. P. (1995). Small peptides activate the latent DNA binding function of p53. Cell, 83, 237-245.
21. Johnson, C. R., Morin, P. E., Arrowsmith, C. H. & Freire, E. (1995). Thermodynamic analysis of the structural stability of the tetrameric oligomerization domain of p53 tumor suppressor. Biochemistry, 34, 5309-5316.
22. Kubbutat, M. H. & Vousden, K. H (1997). Proteolytic cleavage of human p53 by calpain: a potential regulator of protein stability. Mol. Cell. Biol. 17, 460-468.
23. Kubbutat, M. H., Jones, S. N. & Vousden, K. H. (1997). Regulation of p53 stability by Mdm2. Nature, 387, 299-303.
24. Lane, D. P., Stephen, C. W., Midgley, C. A., Sparks, A., Hupp, T. R., Daniels, D. A., Greaves, R., Reid, A., Vojtesek, B. & Picksley, S. M. (1996). Epitope analysis of the murine p53 tumour suppressor protein. Oncogene, 12, 2461-2466.
25. Lu, H. & Levine, A. J. (1995). Human Taf-31 is a transcriptional coactivator of the p53 protein. Proc. Natl Acad. Sci. USA, 92, 5154-5158.
26. Midgley, C. A. & Lane, D. P. (1997). p53 protein stability in tumour cells is not determined by mutation but is dependent on mdm2 binding. Oncogene, 15, 1179-1189.
27. Midgley, C. A., Owens, B., Briscoe, C. V., Brynmor, T. & Lane, D. P. (1995). Coupling between gamma irradiation, p53 induction and the apoptotic response depends upon cell type in vivo. J. Cell Sci. 1843-1848.
28. Midgley, C. A., Craig, A. L., Hite, J. P. & Hupp, T. R. (1997). Baculovirus expression and the study of the regulation of the tumour suppressor protein p53. In DNA Transfer to Cultured Cells (Freshney, R. I., ed.), Wiley-Liss, NY.
29. Milner, J. & Watson, J. V. (1990). Addition of fresh medium induces cell cycle and conformation changes in p53, a tumour suppressor protein. Oncogene, 5, 1683-1690.
30. Milner, J., Metcalf, E. A. & Cook, A. C. (1991). Tumour suppressor p53: analysis of wild-type and mutant p53 complexes. Mol. Cell. Biol. 11, 12-19.
31. Molinari, M., Okorokov, A. L. & Milner, J. (1996). Interaction with damaged DNA induces selective proteolytic cleavage of p53 to yield 40 kDa and 35 kDa fragments competent for sequence-specific DNA binding. Oncogene, 13, 2077-2086.
32. Pavletich, N. P., Chambers, K. A. & Pabo, C. O. (1993). The DNA-binding domain of p53 contains the four conserved regions and the major mutation hot spots. Genes Dev. 7, 2556-2564.
33. Pietenpol, J. A., Tokino, T., Thiagalingam, S., El-Deiry, W. S., Kinzler, K. W. & Vogelstein, B. (1994). Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc. Natl Acad. Sci. USA, 91, 1990-2002.
34. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Shaulian, E., Zauberman, A., Milner, J., Davies, E. A. & Oren, M. (1993). Tight DNA binding and oligomerization are dispensable for the ability of p53 to transactivate target genes and suppress transformation. EMBO J. 12, 2789-2797.
36. Soussi, T. & May, P. (1996). Structural aspects of the p53 protein in relation to gene evolution: a second look. J. Mol. Biol. 260, 623-637.
37. Srinvivasan, R. & Maxwell, S. A. (1996). A cellular protein activates the sequence-specific DNA binding of p53 by interacting with the conserved region. Oncogene, 12, 193-200.
38. Thut, C. J., Chen, J. L., Klemin, R. & Tijan, R. (1995). p53 transcriptional activation mediated by coactivators TAFII40 and TAFFII60. Science, 267, 100-104.
39. Unger, T., Mietz, J. A., Scheffner, M., Yee, C. L. & 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.
40. Wade-Evans, A. & Jenkins, J. R. (1985). Precise epitope mapping of the murine transformation-associated protein, p53. EMBO J. 4, 699-706.
41. Wang, P., Reed, M., Wang, Y., Mayr, G., Stenger, J. E., Anderson, M. E., Schwedes, J. F. & Tegtmeyer, P. (1994). p53 domains: structure, oligomerization, and transformation. Mol. Cell. Biol. 14, 5182-5191.
42. Wang, Y. & Prives, C. (1995). Increased and altered DNA binding of human p53 by S and G2/M but not G1 cyclin-dependent kinases. Nature, 376, 88-91.
43. Wang, Y., Reed, M., Wang, P., Stenger, J. E., Mayr, G., Anderson, M. E., Schwedes, J. F. & Tegtmeyer, P. (1993). p53 domains: identification and characterisation of two autonomous DNA-binding regions. Genes Dev. 7, 2575-2586.
44. Wang, Y., Schwedes, J. F., Parks, D., Mann, K. & Tegtmeyer, P. (1995). Interaction of p53 with its consensus DNA-binding site. Mol. Cell. Biol. 15, 2157-2165.
45. Yewdell, J. W., Gannon, J. V. & Lane, D. P. (1986). Monoclonal antibody analysis of p53 expression in normal and transformed cells. J. Virol. 59, 444-452.
46. Zhang, W., Guo, X.-Y. D. & Deisseroth, A. B. (1994). The requirement of the carboxyl terminus of p53 for DNA binding and transcriptional activation depends on the specific p53 binding DNA element. Oncogene, 9, 2513-2521.