UV irradiation leads to transient changes in phosphorylation and stability of tumor suppressor protein p53

International Journal of Oncology

Volumn 9, Issue 6, 1996, Pages 1277-1285

  Scheidtmann, Karl Heinz ^a   Landsberg, Gerd ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

apoptosis; growth arrest; p53; phosphorylation; stabilization; UV irradiation

Indexed keywords

PROTEIN P53;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FIBROBLAST; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RAT; TUMOR SUPPRESSOR GENE; ULTRAVIOLET RADIATION;

EID: 0029843545     PISSN: 10196439     EISSN: None     Source Type: Journal    
DOI: 10.3892/ijo.9.6.1277     Document Type: Article

References (76)

1. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B and Craig RW: Participation of p53 protein in the cellular response to DNA damage. Cancer Res 51: 6304-6311, 1991.
2. Lin D, Shields MT, Ullrich SJ, Appella E and Mercer WE: Growth arrest induced by wild-type p53 protein blocks cells prior to or near the restriction point. Proc Natl Acad Sci USA 89: 9210-9214, 1992.
3. Deppert W: The yin and yang of p53 in cellular proliferation. Semin Cancer Biol 5: 187-202, 1994.
4. Ko LJ and Prives C: p53: puzzle and paradigm. Gene Develop 10: 1054-1072, 1996.
5. Liebermann DA, Hoffman B and Steinman RA: Molecular controls of growth arrest and apoptosis: p53-dependent and independent pathways. Oncogene 11: 199-210, 1995.
6. White E: Life, death, and the persuit of apoptosis. Gene Develop 10: 1-15, 1996.
7. Agoff SN, Hou J, Linzer DIH and Wu B: Regulation of the human hsp70 promoter by p53. Science 259: 84-87, 1993.
8. Lu H and Levine AJ: Human TAF31 protein is a transcriptional coactivator of the p53 protein. Proc Natl Acad Sci USA 92: 5154-5158, 1995.
9. Ragimov N, Krauskopf A, Navot N, Rotter V and Oren M: Wild-type but not mutant p53 can repress transcription initiation in vitro by interfering with the binding of basal transcription factors to the TATA motif. Oncogene 8: 1183-1193, 1993.
10. Seto E, Usheva A, Zambetti GP, Momand J, Horikoshi N, Weinmann R, Levine AJ and Shenk T: Wild-type p53 binds to the TATA-binding protein and represses transcription. Proc Natl Acad Sci USA 89: 12028-12032, 1992.
11. Thut CJ, Chen J-L, Klemm R and Tjian R: Transcriptional activation mediated by coactivators TAFII40 and TAFII60. Science 267: 100-104, 1995.
12. Borellini F and Glazer RI: Induction of SP1-p53 DNA binding heterocomplexes during granulocyte/macrophage colony stimulating factor-dependent proliferation in human erythroleukemia cell lineTF-1. J Biol Chem 268: 7923-7928, 1993.
13. Gualberto A and Baldwin AS Jr: p53 and SP1 interact and cooperate in the tumor necrosis factor-induced transcriptional activation of the HIV-1 long terminal repeat. J Biol Chem 270: 19680-19683, 1995.
14. Perrem K, Rayner J, Voss T, Stürzbecher H, Jackson P and Braithwaite A: p53 represses SV40 transcription by preventing formation of transcription complexes. Oncogene 11: 1299-1307, 1995.
15. O'Connor DJ, Lam EWF, Griffin S, Zhong F, Leighton LC, Burbidge SA and Lu X: Physical and functional interactions between p53 and cell cycle co-operating factors, E2F1 and DP1. EMBO J 14: 6184-6192, 1995.
16. El-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer E, Kinzler KW and Vogelstein B: Waf1 a potential mediator of p53 tumor suppression. Cell 75: 817-825, 1993.
17. 1 cyclin-dependent kinases. Cell 75: 805-816, 1993.
18. Morris GF, Bischoff JR and Mathews MB: Transcriptional activation of the human proliferating-cell nuclear antigen promoter by p53. Proc Natl Acad Sci USA 93: 895-899, 1996.
19. Shivakumar CV, Brown DR, Deb S and Deb SP: Wild-type human p53 transactivates the human proliferating cell nuclear antigen promoter. Mol Cell Biol 15: 6785-6793, 1995.
20. Kastan MB, Zhan Q, El-Deiry WS, Carrier F, Jacks T, Walsh WV, Plunkett BS, Vogelstein B and Fornace AJ Jr: A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71: 587-597, 1992.
21. Miyashita T and Reed JC: Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80: 293-299, 1995.
22. Oltvai ZN, Millman CL and Korsmeyer SJ: Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74: 609-619, 1993.
23. Barak Y, Juven T, Haffner R and Oren M: mdm2 expression is induced by wild-type p53 activity. EMBO J 12: 461-468, 1993.
24. Wu X, Bayle JH, Olson D and Levine AJ: The p53-mdm2 autoregulatory feedback loop. Gene Develop 7: 1126-1132, 1993.
25. Haupt Y, Rowan S, Shaulian E, Vousden K and Oren M: Induction of apoptosis in HeLa cells by transactivation-deficient p53. Gene Develop 9: 2170-2183, 1995.
26. Brain R and Jenkins JR: Human p53 directs DNA strand reassociation and is photolabelled by 8-azido ATP. Oncogene 9: 1775-1780, 1994.
27. Oberosler P, Hloch P, Ramsperger U and Stahl H: P53-catalized annealing of complementary single-stranded nucleic acids. EMBO J 12: 2389-2396, 1993.
28. Dutta A, Ruppert SM, Aster JC and Winchester E: Inhibition of DNA replication factor RP-A by p53. Nature 365: 79-82, 1993.
29. Li R and Botchan MR: 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, 1993.
30. Stürzbecher HW, Donzelmann B, Henning W and Knippschild U: p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction. EMBO J 15: 1992-2002, 1996.
31. Wang XW, Yeh H, Schaeffer L, Roy R, Moncollin V, Egly J-M, Wang Z, Friedberg EC, Evans MK, Taffe BG, Bohr VA, Weeda G, Hoeijmakers JHJ, Forrester K and Harris CC: p53 modulation of TFIIH-associated nucleotide excision repair 55 activity. Nature Genet 10: 188-195, 1995.
32. Drapkin R, Reardon JT, Ansari A, Huang J-C, Zawel L, Ahn K, Sancar A and Reinberg D: Dual role of TFIIH in DNA excision repair and in transcription by RNA polymerase II. Nature 368: 769-772, 1994.
33. Fuchs B, Hecker D and Scheidtmann KH: Phosphorylation studies on rat p53 using the baculovirus system: manipulation of the phosphorylation state with okadaic acid and influence on DNA binding. Eur J Biochem 228: 625-639, 1995.
34. Hupp TR and Lane DP: 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, 1995.
35. Selkirk JK, Merrick BA, Stackhouse BL and He C: Multiple p53 protein isoforms and formation of oligomeric complexes with heat shock proteins Hsp70 and Hsp90 in the human mammary tumor, T47D, cell line. Appl Theor Electroph 4: 11-18, 1994.
36. Meek DW: Post-translational modification of p53. Semin Cancer Biol 5: 203-210, 1994.
37. Müller E, Boldyreff B and Scheidtmann KH: Characterization of protein kinase activities associated with p53-large T immune complexes from SV40-transformed rat cells. Oncogene 8: 2193-2205, 1993.
38. Patschinsky T, Knippschild U and Deppert W: Species-specific phosphorylation of mouse and rat p53 in simian virus 40-transformed cells. J Virol 66: 3846-3859, 1992.
39. Milne DM, Palmer RH, Campbell FB and Meek DW: Phosphorylation of the p53 tumour-suppressor protein at three N-terminal sites by a novel casein kinase I-like enzyme. Oncogene 7: 1361-1369, 1992.
40. Herrmann CPE, Kraiss S and Montenarh M: Association of casein kinase II with immunopurified p53. Oncogene 6: 877-884, 1991.
41. Meek DW, Simon S, Kikkawa U and Eckhart W: The p53 tumor suppressor protein is phosphorylated at serine 386 by casein kinase II. EMBO J 9: 3253-3260, 1990.
42. Jamal S and Ziff EB: Raf phosphorylates p53 in vitro and potentiates p53-dependent transcriptional transactivation in vivo. Oncogene 10: 2095-2101, 1995.
43. Bischoff JR, Friedman PN, Marshak DR, Prives C and Beach D: Human p53 is phosphorylated by p60-cdc2 and cyclin B-cdc2. Proc Natl Acad Sci USA 87: 4766-4770, 1990.
44. cdc2 in transformed cells. EMBO J 9: 2885-2889, 1990.
45. cdc2 in mammalian cells: implications for cell cycle control and oncogenesis. Oncogene 5: 795-801, 1990.
46. Lees-Miller S, Sakaguchi K, Ullrich SJ, Appella E and Anderson CW: Human DNA-activated protein kinase phosphorylates serine 15 and 37 in the amino-terminal transactivation domain of human p53. Mol Cell Biol 12: 5041-5049, 1992.
47. Milne DM, Campbell DG, Caudwell FB and Meek DW: Phosphorylation of the tumor suppressor protein p53 by mitogen-activated protein kinases. J Biol Chem 269: 9253-9260, 1994.
48. Milne DM, Campbell LE, Campbell DG and Meek DW: p53 is phosphorylated in vitro and in vivo by an ultraviolet radiation-induced protein kinase characteristic of the c-jun kinase. J Biol Chem 270: 5511-5518, 1995.
49. Baudier J, Delphin C, Grunwald D, Khochbin S and Lawrence JJ: Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc Natl Acad Sci USA 89: 11627-11631, 1992.
50. Hupp TR and Lane DP: Allosteric activation of latent p53 tetramers. Curr Biol 4: 865-875, 1994.
51. Müller E and Scheidtmann KH: Purification and characterization of a protein kinase which is activated by SV40 large T-antigen and phosphorylates the tumor suppressor protein p53. Oncogene 10: 1175-1185, 1995.
52. Fritsche M, Haessler C and Brandner G: Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene 8: 307-318, 1993.
53. Hall P, McKee PH, Menage HP, Dover R and Lane DP: High levels of p53 protein in UV-induced normal human skin. Oncogene 8: 203-207, 1993.
54. Mosner B, Mummenbrauer T, Bauer C, Sczakiel G, Grosse F and Deppert W: Negative feedback regulation of wild-type p53 biosynthesis. EMBO J 14: 4442-4449, 1995.
55. Lu X and Lane DP: Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell 75: 765-778, 1993.
56. Hecker D, Page G, Lohrum M, Weiland S and Scheidtmann KH: Complex regulation of the DNA-binding activity of p53 by phosphorylation: differential effects of individual phosphorylation sites on the interaction with different binding motifs. Oncogene 12: 953-961, 1996.
57. Hupp TR, Meek DW, Midgley CA and Lane DP: Regulation of the specific DNA binding function of p53. Cell 71: 875-886, 1992.
58. 1 cyclin-dependent kinases. Nature 367: 88-91, 1995.
59. 2 terminus facilitates transactivation. Cancer Res 55: 2410-2417, 1995.
60. Zhang W, McClain C, Gau J-P, Guo X-YD and Deisseroth AB: Hyperphosphorylation of p53 induced by okadaic acid attenuates its transcriptional activation function. Cancer Res 54: 4448-4453, 1994.
61. Lohrum M and Scheidtmann KH: Differential effects of phosphorylation of rat p53 on transactivation of promoters derived from different p53 responsive genes. Oncogene (In press).
62. Scheidtmann KH and Haber A: Simian virus 40 large T-antigen induces or activates a protein kinase which phosphorylates the transformation-associated protein p53. J Virol 64: 672-679, 1990.
63. Gurney EG, Harrison RO and Fenno J: Monoclonal antibodies against simian virus 40 T-antigen: evidence for distinct subclasses of large T-antigen and for similarities among nonviral T-antigens. J Virol 34: 752-763, 1980.
64. Luo K, Hurley RT and Sefton BM: Transfer of proteins to membranes facilitates both cyanogen bromide cleavage and two-dimensional proteolytic mapping. Oncogene 5: 921-923, 1990.
65. Scheidtmann KH, Landsberg G and Graessmann A: Enhanced kinase activity in SV40-transformed cells may be compensated by enhanced phosphatase activity in revertants as reflected by phosphorylation of p53. Int J Oncol 5: 1353-1362, 1994.
66. 1 cell-cycle arrest. Gene Develop 9: 204-217, 1995.
67. Fiscella M, Zambrano N, Ullrich SJ, Unger T, Lin D, Cho B, Mercer WE, Anderson CW and Appella E: Mutation of the serine 15 phosphorylation site of human p53 reduces the ability to inhibit cell cycle progression. Oncogene 8: 1519-1528, 1994.
68. Deffi A, Wu H, Reinke V and Lozano G: The tumor suppressor p53 regulates its own transcription. Mol Cell Biol 13: 3415-3423, 1993.
69. Jayaraman L and Prives C: Activation of p53 sequence-specific DNA binding by short single strands of DNA requires the p53 C-terminus. Cell 81: 1021-1029, 1995.
70. Knippschild U, Milne D, Campbell L and Meek D: p53 N-terminus-targeted protein kinase activity is stimulated in response to wild-type p53 and DNA damage. Oncogene (In press).
71. Elledge SJ and Harper JW: Cdk inhibitors: on the threshold of checkpoints and development. Curr Opin Cell Biol 6: 847-852, 1994.
72. wafI is required for survival of differentiating neuroblastoma cells. Mol Cell Biol 16: 1335-1341, 1996.
73. Polyak K, Waldman T, He T-C, Kinzler KW and Vogelstein B: Genetic determinants of p53-induced apoptosis and growth arrest. Gene Develop 10: 1945-1952, 1996.
74. 1 checkpoint control. Cell 82: 675-684, 1995.
75. Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, Kinzler K, Vogelstein B and Jacks T: p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Gene Develop 9: 935-944, 1995.
76. Wang XW, Vermeulen W, Coursen JD, Gibson M, Lupold SE, Forrester K, Xu G, Elmore L, Yeh H, Hoeijmakers JHJ and Harris CC: The XPB and XPD DNA helicases are components of the p53-mediated apoptosis pathway. Gene Develop 10: 1219-1232, 1996.