p53 protein exhibits 3'-to-5' exonuclease activity

Cell

Volumn 85, Issue 7, 1996, Pages 1089-1099

  Mummenbrauer, Torsten ^a   Janus, Friedemann ^a   Müller, Beate ^a   Wiesmüller, Lisa ^a   Deppert, Wolfgang ^a   Grosse, Frank ^b  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; EXONUCLEASE; GUANOSINE PHOSPHATE; PHOSPHATE; PROTEIN P53;

ANIMAL CELL; CROSS LINKING; ENZYME ACTIVITY; IMMUNOAFFINITY CHROMATOGRAPHY; INSECT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVIEW;

ANIMALIA; INSECTA;

EID: 0030604728     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81309-4     Document Type: Article

References (83)

1. Bakalkin, G., Yakovleva, T., Selivanova, G., Magnusson, K.P., Skekely, L., Kiseleva, E., Klein, G., Teresenius, L., and Wiman, K.G. (1994). p53 binds single-stranded DNA ends and catalyzes DNA renaturation and strand transfer. Proc. Natl. Acad. Sci. USA 91, 413-417.
2. Bargonetti, J., Friedman, P.N., Kern, S.E., Vogelstein, B., and Prives, C. (1991). Wild-type but not mutant p53 immunopurified proteins bind to sequences adjacent to the SV40 origin of replication. Cell 65, 1083-1091.
3. Bargonetti, J., Manfredi, J.J., Chen, X., Marshak, D.R., and 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. Bhattacharyya, N.P., Skandalis, A., Ganesh, A., Groden, J. and Meuth, M. (1994). Mutator phenotypes in human colorectal carcinoma cell lines. Proc. Natl. Acad. Sci. USA 91, 6319-6323.
5. Bialek, G., and Grosse, F. (1993). An error-correcting proofreading exonuclease-polymerase that copurifies with DNA-polymerase-α-primase. J. Biol. Chem. 268, 6024-6033.
6. Bodmer, W., Bishop, T., and Karran, P. (1994). Genetic steps in colorectal cancer. Nature Genet. 6, 217-219.
7. Brain, R., and Jenkins, J.R. (1994). Human p53 directs DNA strand reassociation and is photolabelled by 8-Azido ATP. Oncogene 9, 1775-1780.
8. Cho, Y., Gorina, S., Jeffrey, P.D., and Pavletich, N.P. (1994). Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science 265, 346-355.
9. Cox, L.S., and Lane, D.P. (1995). Tumor suppressors, kinases and clamps: how p53 regulates the cell cycle in response to DNA damage. Bioassays 17, 501-508.
10. Cox, L.S., Hupp, T., Midgley, C.A., and Lane, D.P. (1995). A direct effect of activated human p53 on nuclear DNA replication. EMBO J. 14, 2099-2105.
11. Deppert, W. (1994). The yin and yang of p53 in cellular proliferation. Cancer Biol. 5, 187-202.
12. Donehower, L.A., Harvey, M., Slagle, B.L., McArthur, M.J., Montgomery, C.A., Butel, J.S., and Bradley, A. (1992). Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature 356, 215-221.
13. Dutta, A., Ruppert, J.M., Aster, J.C., and Winchester, E. (1993). Inhibition of DNA replication factor RPA by p53. Nature 365, 79-82.
14. El-Deiry, W.S., 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.
15. El-Deiry, W.S., Tokino, T., Velculescu, V.E., Levy, D.B., Parsons, R., Trent, J.M., Lin, D., Mercer, W.E., Kinzler, K.W., and Vogelstein, B. (1993). WAF1, a potential mediator of p53 tumor suppression. Cell 75, 817-825.
16. Fishel, R., and Kolodner, R.D. (1995). Identification of mismatch repair genes and their role in the development of cancer. Curr. Opin. Genet. Dev. 5, 382-395.
17. Flores-Rozas, H., Kelman, Z., Dean, F.B., Pan, Z.-Q., Harper, J.W., Elledge, S.J., O'Donnell, M., and Hurwitz, J. (1994). Cdk-interacting protein 1 directly binds with proliferating cell nuclear antigen and inhibits DNA replication catalyzed by the DNA polymerase delta holoenzyme. Proc. Natl. Acad. Sci. USA 91, 8655-8659.
18. Foord, O.S., Bhattacharya, P., Reich, Z., and Rotter, V. (1991). A DNA binding domain is contained in the C-terminus of wild type p53 protein. Nucleic Acids Res. 19, 5191-5198.
19. Foord, O., Navot, N., and Rotter, V. (1993). Isolation and characterization of DNA sequences that are specifically bound by wild type p53 protein. Mol. Cell. Biol. 13, 1378-1384.
20. Friend, S. (1994). p53: a glimpse at the puppet behind the shadow play. Science 265, 334-335.
21. Fritsche, M., Haessler, C., and Brandner, G. (1993). Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene 8, 307-318.
22. Funk, W.D., Pak, D.T., Karas, R.H., Wright, W.E., and Shay, J.W. (1992). A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol. 12, 2866-2871.
23. Grosse, F., and Manns, A. (1993). Terminal deoxyribonucleotidyl transferase. In Methods in Molecular Biology: Enzymes of Molecular Biology, M.M. Burrell, ed. (Totowa, New Jersey: Humana Press), pp. 95-105.
24. Harper, J.W., Adami, G.R., Wei, M., Keyomarsi, K., and Elledge, S.J. (1993). The p21 CDK-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75, 805-816.
25. Harris, C.C., and Hollstein, M. (1993). Clinical implications of the tumor-suppressor gene. New Engl. J. Med. 329, 1318-1327.
26. Hartwell, L.H., and Kastan, M.B. (1994). Cell cycle control and cancer. Science 266, 1821-1828.
27. Harvey, M., McArthur, M.J., Montgomery, C.A.J., Butel, J.S., Bradley, A., and Donehower, L.A. (1993). Spontaneous and carcinogen-induced tumorigenesis in p53-deficient mice. Nature Genet. 5, 225-229.
28. Hohn, K.T., and Grosse, F. (1987). Processivity of the DNA polymerase α-primase complex from calf thymus. Biochemistry 26, 2870-2878.
29. Hollstein, M., Sidransky, D., Vogelstein, B., and Harris, C.C. (1991). p53 mutations in human cancers. Science 253, 49-53.
30. Hupp, T.R., and Lane, D.P. (1994). Allosteric activation of latent p53 tetramers. Curr. Biol. 4, 865-875.
31. Hupp, T.R., Meek, D.W., Midgley, C.A., and Lane, D.P. (1992). Regulation of specific DNA binding function of p53. Cell 71, 875-886.
32. Kastan, M.B., Zhan, Q., El-Deiry, W.S., Carrier, F., Jacks, T., Walsh, W.V., Plunkett, B.S., Vogelstein, B., and Fornace, A.J. (1992). A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in Ataxia-Telangiectasia. Cell 71, 587-597.
33. Kern, S.E., Kinzler, K.W., Baker, S.J., Nigro, J.M., Rotter, V., Levine, A.J., Friedman, P., Prives, C., and Vogelstein, B. (1991a). Mutant p53 binds DNA abnormally in vitro. Oncogene 6, 131-136.
34. Kern, S.E., Kinzler, K.W., Bruskin, A., Jarosz, D., Friedman, P., Prives, C., and Vogelstein, B. (1991b). Identification of p53 as a sequence-specific DNA-binding protein. Science 252, 1708-1711.
35. Kern, S.E., Pietenpol, J.A., Thiagalingam, S., Seymour, A., Kinzler, K.W., and Vogelstein, B. (1992). Oncogenic forms of p53 inhibit p53-regulated gene expression. Science 256, 827-830.
36. Kornberg, A., and Baker, T. (1991). DNA Replication, Second Edition (San Francisco, California: W. H. Freeman).
37. Kuerbitz, S.J., Plunkett, B.S., Walsh, W.V., and Kastan, M.B. (1992). Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl. Acad. Sci. USA 89, 7491-7495.
38. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
39. Lane, D.P. (1992). p53, guardian of the genome. Nature 358, 15-16.
40. Leach, F.S., Nicolaides, N.C., Papadopoulos, N., Liu, B., Jen, J., Parsons, R., Peltomäki, P., Sistonen, P., Aaltonen, L.A., Nyström-Lahti, M., et al. (1993). Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 75, 1215-1225.
41. Lee, S., Elenbaas, B., Levine, A., and Griffith, J. (1995). p53 and its 14 kDa C-terminal domain recognize primary DNA damage in the form of insertion/deletion mismatches. Cell 81, 1013-1020.
42. Li, R., and Botchan, M.R. (1993). The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell 73, 1207-1221.
43. Li, R., Waga, S., Hannon, G.J., Beach, D., and Stillman, B. (1994). Differential effects by the p21 CDK inhibitor on PCNA-dependent DNA replication and repair. Nature 371, 534-537.
44. Lin, D., Shieds, M.T., Ullrich, S.J., Appella, E., and Mercer, W.E. (1992). Growth arrest induced by wild-type p53 protein blocks cells prior to or near the restriction point in late G1 phase. Proc. Natl. Acad. Sci. USA 89, 9210-9214.
45. Lin, J., Chen, J., Elenbaas, B., and Levine, A.J. (1994). Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to mdm-2 and the adenovirus 5 E1B 55-kD protein. Genes Dev. 8, 1235-1246.
46. Linn, S.M., Lloyd, R.S., and Roberts, R.J. (1993). Nucleases, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Laboratories).
47. Marx, J. (1993). How p53 suppresses cell growth. Science 262, 1644-1645.
48. Meek, D.W. (1994). Post-translational modification of p53. Semin. Cancer Biol. 5, 203-210.
49. Mercer, W.E., Shields, M.T., Amin, M., Sauve, G.J., Appella, E., Romano, J.W., and Ullrich, S.J. (1990). Negative growth regulation in a glioblastoma tumor cell line that conditionally expresses human wild-type p53. Proc. Natl. Acad. Sci. USA 87, 6166-6170.
50. Michalovitz, D., Halevy, O., and Oren, M. (1990). Conditional inhibition of transformation and of cell proliferation by a temperature-sensitive mutant of p53. Cell 62, 671-680.
51. Miyashita, T., and Reed, J.C. (1995). Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293-299.
52. Modrich, P. (1987). DNA mismatch correction. Annu. Rev. Biochem. 56, 435-466.
53. Modrich, P. (1989). Methyl-directed DNA mismatch correction. J. Biol. Chem. 264, 6597-6600.
54. Modrich, P. (1994). Mismatch repair, genetic stability, and cancer. Science 266, 1959-1960.
55. Mol, C.D., Kuo, C.-F., Thayer, M.M., Cunningham, R.P., and Tainer, J.A. (1995). Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature 374, 381-386.
56. Mosner, J., and Deppert, W. (1994). p53 and mdm2 are expressed independently during cellular proliferation. Oncogene 9, 3321-3328.
57. Mosner, J., Mummenbrauer, T., Bauer, C., Sczakiel, G., Grosse, F., and Deppert, W. (1995). Negative feedback regulation of wild-type p53 biosynthesis. EMBO J. 14, 4442-4449.
58. Müller, B., Paulsen, D., and Deppert, W. (1996). Specific binding of MAR/SAR DNA-elements by mutant p53. Oncogene, in press.
59. Nasheuer, H.-P., and Grosse, F. (1987). Immunoaffinity-purified DNA polymerase α displays novel properties. Biochemistry 26, 8458-8466.
60. Nasheuer, H.-P., and Grosse, F. (1988). DNA polymerase α-primase from calf thymus: determination of the polypeptide responsible for primase activity. J. Biol. Chem. 263, 8981-8988.
61. Nelson, W.G., and Kastan, M.B. (1994). DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol. 14, 1815-1823.
62. Oberosler, P., Hloch, P., Ramsperger, U., and Stahl, H. (1993). p53-catalyzed annealing of complementary single-stranded nucleic acids. EMBO J. 12, 2389-2396.
63. Ory, K., Legros, Y., Auguin, C., and Soussi, T. (1994). Analysis of the most representative tumour-derived p53 mutants reveals that changes in protein conformation are not correlated with loss of transactivation or inhibition of cell proliferation. EMBO J. 13, 3496-3504.
64. + tumor cells. Cell 75, 1227-1236.
65. Pavletich, N.P., Chambers, K.A., and 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.
66. Radman, M., and Wagner, R. (1993). Missing mismatch repair. Nature 366, 722.
67. Rolley, N., Butcher, S., and Milner, J. (1995). Specific DNA binding by different classes of human p53 mutants. Oncogene 11, 763-770.
68. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular cloning: A Laboratory Manual (Cold Spring Harbor, New York: Cold Spring Harbor Laboratories).
69. Schärer, E., and Iggo, R. (1992). Mammalian p53 can function as a transcription factor in yeast. Nucleic Acids Res. 20, 1539-1545.
70. Shaulsky, G., Goldfinger, N., Ben-Ze'ev, A., and Rotter, V. (1990). Nuclear accumulation of p53 protein is mediated by several nuclear localization signals and plays a role in tumorigenesis. Mol. Cell Biol. 10, 6565-6577.
71. Steinmeyer, K., and Deppert, W. (1988). DNA binding properties of murine p53. Oncogene 3, 501-507.
72. Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorf, J.W. (1990). Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzym. 185, 60-89.
73. Stürzbecher, H.W., Brain, R., Addison, C., Rudge, K., Remm, M., Grimaldi, M., Keenan, E., and Jenkins, J.R. (1992). A C-terminal alpha-helix plus basic region motif is the major structural determinant of p53 tetramerization. Oncogene 7, 1513-1523.
74. Suwa, A., Hirakata, M., Takeda, Y., Jesch, S.A., Mimori, T., and Hardin, J.A. (1994). DNA-dependent protein kinase (Ku protein-p350 complex) assembles on double-stranded DNA. Proc. Natl. Acad. Sci. USA 91, 6904-6908.
75. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J., and Stahl, F.W. (1983). The double-strand break repair model. Cell 33, 25-35.
76. Tuteja, N., Tuteja, R., Ochem, A., Taneja, P., Huang, N.-W., Simoncsits, A., Susic, S., Rahman, K., Marusic, L., Chen, J., et al. (1994). Human DNA helicase II: a novel DNA unwinding enzyme identified as the Ku autoantigen. EMBO J. 13, 4991-5001.
77. Vogelstein, B., and Kinzler, K.W. (1992). p53 function and dysfunction. Cell 70, 523-526.
78. Waga, S., Hannon, G.J., Beach, D., and Stillman, B. (1994). The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369, 574-578.
79. Wang, T.S.-F. (1991). Eukaryotic DNA polymerases. Annu. Rev. Biochem. 60, 513-552.
80. Wang, Y., Reed, M., Wang, P., Stenger, J.E., Mayr, G., Anderson, M.E., Schwedes, J.F., and Tegtmeyer, P. (1993). p53 domains: identification and characterization of two autonomous DNA-binding regions. Genes Dev. 7, 2575-2586.
81. Wiesmüller, L., Cammenga, J., and Deppert, W. (1996). In vivo assay of p53 function in homologous recombination. J. Virol. 70, 737-744.
82. Wilcock, D., and Lane, D.P. (1991). Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells. Nature 349, 429-431.
83. Zambetti, G.P., Bargonetti, J., Walker, K., Prives, C., and Levine, A.J. (1992). Wild-type p53 mediates positive regulation of gene expression through a specific DNA sequence element. Genes Dev. 6, 1143-1152.