An ATP/ADP-dependent molecular switch regulates the stability of p53-DNA complexes

Molecular and Cellular Biology

Volumn 19, Issue 11, 1999, Pages 7501-7510

  Okorokov, Andrei L ^a   Milner, Jo ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DNA; MUTANT PROTEIN; PROTEIN P53;

ARTICLE; DNA DAMAGE; DNA PROTEIN COMPLEX; ENZYME ACTIVITY; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN STABILITY; TUMOR SUPPRESSOR GENE;

EID: 0032694244     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.11.7501     Document Type: Article

References (51)

1. Bakalkin, G., G. Selivanova, T. Yakovleva, E. Kiseleva, E. Kashuba, K. Magnusson, L. Szekely, G. Klein, L. Terenius, and K. Wiman. 1995. p53 binds single-stranded DNA ends through the C-terminal domain and internal DNA segments via the middle domain. Nucleic Acids Res. 23:362-369.
2. Balagurumoorthy, P., H. Sakamoto, M. S. Lewis, N. Zambrano, G. M. Clore, A. M. Gronenborn, E. Appella, and R. E. Harrington. 1995. Four p53 DNA-binding domain peptides bind natural p53-response elements and bend the DNA. Proc. Natl. Acad. Sci. USA 92:8591-8595.
3. Bargonetti, J., J. J. Manfredi, X. Chen, D. R. Marshak, and C. Prives. 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. Brain, R., and J. R. Jenkins. 1994. Human p53 directs DNA strand reassociation and is photolabelled by 8-azido ATP. Oncogene 9:1775-1780.
5. Cho, Y., S. Gorina, P. D. Jeffrey, and N. P. Pavletich. 1994. Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenicmutations. Science 265:346-355.
6. Clore, G. M., J. Ernst, R. Clubb, J. G. Omichinski, W. M. Kennedy, K. Sakaguchi, E. Appella, and A. M. Gronenborn. 1995. Refined solution structure of the oligomerization domain of the tumour suppressor p53. Nat. Struct. Biol. 2:321-333.
7. Clore, G. M., J. G. Omichinski, K. Sakaguchi, N. Zambrano, H. Sakamoto, E. Appella, and A. M. Gronenborn. 1994. High-resolution structure of the oligomerization domain of p53 by multidimensional NMR. Science 265: 386-391.
8. Davison, T. S., P. Yin, E. Nie, and C. H. Arrowsmith. 1998. Oligomerisation and p53 function, p. 40. In Abstracts of the 9th p53 Workshop 1998.
9. Davison, T. S., P. Yin, E. Nie, C. Kay, and C. H. Arrowsmith. 1998. Characterisation of the oligomerisation defects of two p53 mutants found in families with Li-Fraumeni and Li-Fraumeni-like syndrome. Oncogene 17: 651-656.
10. Fishel, R. 1998. Mismatch repair, molecular switches, and signal transduction. Genes Dev. 12:2096-2101.
11. Ford, J. M., and P. C. Hanawalt. 1995. Li-Fraumeni syndrome fibroblasts homozygous for p53 mutations are deficient in global DNA-repair but exhibit normal transcription-coupled repair and enhanced UV resistance. Proc. Natl. Acad. Sci. USA 92:8876-8880.
12. Funk, W. D., D. J. Pak, R. H. Karas, W. E. Wright, and J. W. Shay. 1992. A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol. 12:2866-2871.
13. Gottlieb, T., and M. Oren. 1996. p53 in growth-control and neoplasia. Biochim. Biophys. Acta Rev. Cancer 1287:77-102.
14. Gradia, S., S. Acharya, and R. Fishel. 1997. The human mismatch recognition complex hMSH2-hMSH6 functions as a novel molecular switch. Cell 91: 995-1005.
15. Hall, A. R., and J. Milner. 1997. Specific p53-DNA complexes contain an mdm2-related protein. Oncogene 14:1371-1376.
16. Jayaraman, L., and C. Prives. 1995. Activation of p53 sequence-specific DNA binding by short single strands of DNA requires the C-terminus. Cell 81:1021-1029.
17. Jeffry, P. D., S. Gorina, and N. P. Pavletich. 1995. Crystal structure of the tetramerization domain of the p53 tumor suppressor at 1.7 angstroms. Science 267:1498-1502.
18. Kalbitzer, H. R., R. S. Goody, and A. Wittinghofer. 1984. Electron-paramagnetic-resonance studies of manganese(II) complexes with elongation factor Tu from Bacillus stearothermophilus. Observation of a GTP hydrolysis intermediate state complex. Eur. J. Biochem. 141:591-597.
19. Kastan, M. 1996. Signalling to p53 - where does it all start. Bioessays 18: 617-619.
20. Ko, L. J., and C. Prives. 1996. p53 - puzzle and paradigm. Genes Dev. 10: 1054-1072.
21. Kondratov, R. V., E. N. Pugacheva, N. V. Kuznetsov, V. S. Prasolov, B. P. Kopnin, and P. M. Chumakov. 1996. Human adenosine-deaminase gene contains p53-responsive element. Proc. Russian Acad. Sci. 346:260-262.
22. Lee, S., B. Elenbaas, A. Levine, and J. Griffith. 1995. p53 and its 14 kDa C-terminal domain recognize primary DNA-damage in the form of insertion/ deletion mismatches. Cell 81:1013-1020.
23. Lee, S. M., L. Cavallo, and J. Griffith. 1997. Human p53 binds Holliday junctions strongly and facilitates their cleavage. J. Biol. Chem. 272:7532-7539.
24. Lee, W., T. S. Harvey, Y. Yin, P. Yau, D. Litchfield, and C. H. Arrowsmith. 1994. Solution structure of the tetrameric minimum transforming domain of p53. Nat. Struct. Biol. 1:877-890.
25. Leveillard, T., L. Andera, N. Bissonnette, L. Schaeffer, L. Bracco, J. M. Egly, and B. Wasylyk. 1996. Functional interactions between p53 and the TFIIH complex are affected by tumor-associated mutations. EMBO J. 15:1615-1624.
26. Levine, A. J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323-331.
27. Linke, S., K. Clarkin, A. Dileonardo, A. Tsou, and G. Wahl. 1996. A reversible, p53-dependent G(0)/G(1) cell-cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10:934-947.
28. Lomax, M. E., D. M. Barnes, T. R. Hupp, S. M. Picksley, and R. S. Camplejohn. 1998. Characterisation of p53 oligomerisation domain mutations isolated from Li-Fraumeni and Li-Fraumeni like family members. Oncogene 17:643-649.
29. McKay, B. C., M. A. Francis, and A. J. Rainbow. 1997. Wildtype p53 is required for heat shock and ultraviolet light enhanced repair of a UV-damaged reporter gene. Carcinogenesis 18:245-249.
30. McLure, K. G., and P. W. K. Lee. 1998. How p53 binds DNA as a tetramer. EMBO J. 17:3342-3350.
31. Mee, T., and J. Milner. 1998. Unpublished data.
32. Miller, M., J. Lubkowski, J. K. M. Rao, A. T. Danishefsky, J. G. Omichinski, K. Sakaguchi, H. Sakamoto, E. Appella, A. M. Gronenborn, and G. M. Clore. 1996. The oligomerization domain of p53: crystal structure of the trigonal form. FEBS Lett. 99:166-170.
33. Milner, J., E. A. Medcalf, and A. Cook. 1991. The tumor suppressor p53: analysis of wild-type and mutant complexes. Mol. Cell. Biol. 11:12-19.
34. Molinari, M., A. L. Okorokov, and J. Milner. 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.
35. Nagaich, A. K., V. B. Zhurkin, H. Sakamoto, A. A. Gorin, G. M. Clore, A. M. Gronenborn, E. Appella, and R. E. Harrington. 1997. Architectural accommodation in the complex of four p53 DNA binding domain peptides with the p21/waf1/cip1 DNA response element. J. Biol. Chem. 272:14830-14841.
36. Nelson, W. G., and M. B. Kastan. 1994. DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol. 14:1815-1823.
37. Oberosler, P., P. Hloch, U. Ramsperger, and H. Stahl. 1993. p53-catalyzed annealing of complementary single-stranded nucleic acids. EMBO J. 12: 2389-2396.
38. Okorokov, A. L., F. Ponchel, and J. Milner. 1997. Induced N-and C-terminal cleavage of p53: a core fragment of p53, generated by interaction with damaged DNA, promotes cleavage of the N-terminus of full-length p53, whereas ssDNA induces C-terminal cleavage of p53 EMBO J. 16:6008-6017.
39. Pavletich, N. P., K. A. Chambers, and C. O. Pabo. 1993. The DNA-binding domain of p53 contains the four conserved regions and the major mutation hot spots. Genes Dev. 7:2556-2564.
40. Reed, M., B. Woelker, P. Wang, Y. Wang, M. Anderson, and P. Tegtmeyer. 1995. The C-terminal domain of p53 recognizes DNA damaged by ionizing radiation. Proc. Natl. Acad. Sci. USA 92:9455-9459.
41. Sancar, A., and J. E. Hearst. 1993. Molecular matchmakers. Science 259: 1415-1420.
42. Sherley, J. L. 1991. Guanine nucleotide biosynthesis is regulated by the cellular p53 concentration. J. Biol. Chem. 264:24815-24828.
43. Sprang, S. R. 1997. G protein mechanisms: insights from structural analysis. Annu. Rev. Biochem. 66:639-678.
44. Temeles, G. L., J. B. Gibs, J. S. D'Alonzo, I. S. Sigal, and E. M. Scolnick. 1985. Yeast and mammalian ras proteins have conserved biochemical properties. Nature 313:700-703.
45. Venkatachalam, S., S. Yu-Ping, S. N. Jones, H. Vogel, A. Bradley, D. Pinkel, and L. A. Donehower. 1998. Retention of wild-type p53 in tumors from p53 heterozygous mice: reduction of p53 dosage can promote cancer formation. EMBO J. 17:4657-4667.
46. Walker, J. E., M. Saraste, M. J. Runswick, and N. G. Gay. 1982. Distantly related sequences in the alpha-and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945-951.
47. Wang, X., W. Vermeulen, J. D. Coursen, M. Gibson, S. E. Lupold, K. Forrester, G. W. Xu, L. Elmore, H. Yeh, J. H. J. Hoeijmakers, and C. C. Harris. 1996. The XPB and XPD DNA helicases are components of the p53-mediated apoptosis pathway. Genes Dev. 10:1219-1232.
48. Wang, X. W., H. Yeh, L. Schaeffer, R. Roy, V. Moncollin, J. M. Egly, Z. Wang, E. C. Friedberg, M. K. Evans, B. G. Taffe, V. A. Bohr, G. Weeda, J. H. J. Hoeijmakers, K. Forrester, and C. C. Harris. 1995. p53 modulation of TFIIH-associated nucleotide excision-repair activity. Nat. Genet. 10:188-195.
49. Wang, Y., M. Reed, P. Wang, J. E. Stenger, G. Mayr, M. E. Anderson, J. F. Schwedes, and P. Tegtmeyer. 1993. p53 domains: identification and characterization of two autonomous DNA-binding regions. Genes Dev. 7:2575-2586.
50. Waterman, J., J. Shenk, and T. Halazonetis. 1995. The dihedral symmetry of the p53 tetramerization domain mandates a conformational switch upon DNA-binding. EMBO J. 14:512-519.
51. Yamauchi, M., and T. A. Baker. 1998. An ATP-ADP switch in MuB controls progression of the Mu transposition pathway. EMBO J. 15:5509-5518.