Apoptosis Associated with Deregulated E2F Activity Is Dependent on E2F1 and Atm/Nbs1/Chk2

Molecular and Cellular Biology

Volumn 24, Issue 7, 2004, Pages 2968-2977

  Rogoff, Harry A ^a   Pickering, Mary T ^a   Frame, Fiona M ^a   Debatis, Michelle E ^a   Sanchez, Yolanda ^b   Jones, Stephen ^a   Kowalik, Timothy F ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 2; GENE PRODUCT; NIBRIN; PROTEIN E7; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; ATAXIA TELANGIECTASIA; CANCER PREVENTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GROWTH REGULATION; HUMAN; HUMAN CELL; NIJMEGEN BREAKAGE SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SENSITIZATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WART VIRUS;

ANIMALS; APOPTOSIS; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; E2F1 TRANSCRIPTION FACTOR; E2F2 TRANSCRIPTION FACTOR; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, TRANSGENIC; NUCLEAR PROTEINS; ONCOGENE PROTEINS, VIRAL; PROTEIN-SERINE-THREONINE KINASES; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPES; PAPILLOMAVIRUS;

EID: 1642270611     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.7.2968-2977.2004     Document Type: Article

References (90)

1. Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
2. Agarwal, M. L., W. R. Taylor, M. V. Chernov, O. B. Chernova, and G. R. Stark. 1998. The p53 network. J. Biol. Chem. 273:1-4.
3. Ahn, J., and C. Prives. 2002. Checkpoint kinase 2 (Chk2) monomers or dimers phosphorylate Cdc25C after DNA damage regardless of threonine 68 phosphorylation. J. Biol. Chem. 277:48418-48426.
4. Appella, E., and C. W. Anderson. 2001. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268:2764-2772.
5. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506.
6. Banin, S., L. Moyal, S. Shieh, Y. Taya, C. W. Anderson, L. Chessa, N. I. Smorodinsky, C. Prives, Y. Reiss, Y. Shiloh, and Y. Ziv. 1998. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281:1674-1677.
7. Barlow, C., K. D. Brown, C. X. Deng, D. A. Tagle, and A. Wynshaw-Boris. 1997. Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat. Genet. 17:453-456.
8. Bates, S., A. C. Phillips, P. A. Clark, F. Stott, G. Peters, R. L. Ludwig, and K. H. Vousden. 1998. p14ARF links the tumour suppressors RB and p53. Nature 395:124-125.
9. Bernstein, C., H. Bernstein, C. M. Payne, and H. Garewal. 2002. DNA repair/pro-apoptotic dual-role proteins in five major DNA repair pathways: fail-safe protection against carcinogenesis. Mutat. Res. 511:145-178.
10. Blattner, C., A. Sparks, and D. Lane. 1999. Transcription factor E2F-1 is upregulated in response to DNA damage in a manner analogous to that of p53. Mol. Cell. Biol. 19:3704-3713.
11. Brown, A. L., C. H. Lee, J. K. Schwarz, N. Mitiku, H. Piwnica-Worms, and J. H. Chung. 1999. A human Cds1-related kinase that functions downstream of ATM protein in the cellular response to DNA damage. Proc. Natl. Acad. Sci. USA 96:3745-3750.
12. Brown, E. J., and D. Baltimore. 2000. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14:397-402.
13. Buscemi, G., C. Savio, L. Zannini, F. Micciche, D. Masnada, M. Nakanishi, H. Tauchi, K. Komatsu, S. Mizutani, K. Khanna, P. Chen, P. Concannon, L. Chessa, and D. Delia. 2001. Chk2 activation dependence on Nbs1 after DNA damage. Mol. Cell. Biol. 21:5214-5222.
14. Canman, C. E., D. S. Lim, K. A. Cimprich, Y. Taya, K. Tamai, K. Sakaguchi, E. Appella, M. B. Kastan, and J. D. Siliciano. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281:1677-1679.
15. Castillo, J. P., A. D. Yurochko, and T. F. Kowalik. 2000. Role of human cytomegalovirus immediate-early proteins in cell growth control. J. Virol. 74:8028-8037.
16. Chaturvedi, P., W. K. Eng, Y. Zhu, M. R. Mattern, R. Mishra, M. R. Hurle, X. Zhang, R. S. Annan, Q. Lu, L. F. Faucette, G. F. Scott, X. Li, S. A. Carr, R. K. Johnson, J. D. Winkler, and B. B. Zhou. 1999. Mammalian Chk2 is a downstream effector of the ATM-dependent DNA damage checkpoint pathway. Oncogene 18:4047-4054.
17. Chehab, N. H., A. Malikzay, M. Appel, and T. D. Halazonetis. 2000. Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev. 14:278-288.
18. Debbas, M., and E. White. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546-554.
19. DeGregori, J., G. Leone, A. Miron, L. Jakoi, and J. R. Nevins. 1997. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA 94:7245-7250.
20. de Klein, A., M. Muijtjens, R. van Os, Y. Verhoeven, B. Smit, A. M. Carr, A. R. Lehmann, and J. H. Hoeijmakers. 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:479-482.
21. Duensing, S., and K. Munger. 2002. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res. 62:7075-7082.
22. Freedman, D. A., and A. J. Levine. 1998. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 18:7288-7293.
23. Fuchs, S. Y., V. Adler, T. Buschmann, X. Wu, and Z. Ronai. 1998. Mdm2 association with p53 targets its ubiquitination. Oncogene 17:2543-2547.
24. Giaccia, A. J., and M. B. Kastan. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12:2973-2983.
25. Guo, Z., A. Kumagai, S. X. Wang, and W. G. Dunphy. 2000. Requirement for Atr in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev. 14:2745-2756.
26. Hall-Jackson, C. A., D. A. Cross, N. Morrice, and C. Smythe. 1999. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 18:6707-6713.
27. Harbour, J. W., and D. C. Dean. 2000. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev. 14:2393-2409.
28. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387:296-299.
29. He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509-2514.
30. Hekmat-Nejad, M., Z. You, M. C. Yee, J. W. Newport, and K. A. Cimprich. 2000. Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Curr. Biol. 10:1565-1573.
31. Hermeking, H., and D. Eick. 1994. Mediation of c-Myc-induced apoptosis by p53. Science 265:2091-2093.
32. Herzog, K. H., M. J. Chong, M. Kapsetaki, J. I. Morgan, and P. J. McKinnon. 1998. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280:1089-1091.
33. Hirao, A., Y. Y. Kong, S. Matsuoka, A. Wakeham, J. Ruland, H. Yoshida, D. Liu, S. J. Elledge, and T. W. Mak. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287:1824-1827.
34. Hofferer, M., C. Wlrbelauer, B. Humar, and W. Krek. 1999. Increased levels of E2F-1-dependent DNA binding activity after UV- or gamma-irradiation. Nucleic Acids Res. 27:491-495.
35. Honda, R., H. Tanaka, and H. Yasuda. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420:25-27.
36. Huang, Y., T. Ishiko, S. Nakada, T. Utsugisawa, T. Kato, and Z. M. Yuan. 1997. Role for E2F in DNA damage-induced entry of cells into S phase. Cancer Res. 57:3640-3643.
37. Inoue, K., M. F. Roussel, and C. J. Sherr. 1999. Induction of ARF tumor suppressor gene expression and cell cycle arrest by transcription factor DMP1. Proc. Natl. Acad. Sci. USA 96:3993-3998.
38. Ishida, S., E. Huang, H. Zuzan, R. Spang, G. Leone, M. West, and J. R. Nevins. 2001. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol. Cell. Biol. 21: 4684-4699.
39. 1 arrest but is required for a latent p53-mediated apoptotic response. Proc. Natl. Acad. Sci. USA 99:9825-9829.
40. Jin, S., and A. J. Levine. 2001. The p53 functional circuit. J. Cell Sci. 114:4139-4140.
41. Johnson, D. G., J. K. Schwarz, W. D. Cress, and J. R. Nevins. 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 365:349-352.
42. Kalma, Y., L. Marash, Y. Lamed, and D. Ginsberg. 2001. Expression analysis using DNA microarrays demonstrates that E2F-1 up-regulates expression of DNA replication genes including replication protein A2. Oncogene 20:1379-1387.
43. Kamijo, T., F. Zindy, M. F. Roussel, D. E. Quelle, J. R. Downing, R. A. Ashmun, G. Grosveld, and C. J. Sherr. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91:649-659.
44. Kastan, M. B., and D. S. Lim. 2000. The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol. 1:179-186.
45. Vim, S. T., D. S. Lim, C. E. Canman, and M. B. Kastan. 1999. Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274:37538-37543.
46. Kowalik, T. F., J. DeGregori, G. Leone, L. Jakoi, and J. R. Nevins. 1998. E2F1-specific induction of apoptosis and p53 accumulation, which is blocked by Mdm2. Cell Growth Differ. 9:113-118.
47. Kowalik, T. F., J. DeGregori, J. K. Schwarz, and J. R. Nevins. 1995. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 69:2491-2500.
48. Lakin, N. D., B. C. Hann, and S. P. Jackson. 1999. The ataxia-telangiectasia related protein ATR mediates DNA-dependent phosphorylation of p53. Oncogene 18:3989-3995.
49. Leone, G., R. Sears, E. Huang, R. Rempel, F. Nuckolls, C. H. Park, P. Giangrande, L. Wu, H. I. Saavedra, S. J. Field, M. A. Thompson, H. Yang, Y. Fujiwara, M. E. Greenberg, S. Orkin, C. Smith, and J. R. Nevins. 2001. Myc requires distinct E2F activities to induce S phase and apoptosis. Mol. Cell 8:105-113.
50. Liao, M. J., C. Yin, C. Barlow, A. Wynshaw-Boris, and T. van Dyke. 1999. Atm is dispensable for p53 apoptosis and tumor suppression triggered by cell cycle dysfunction. Mol. Cell. Biol. 19:3095-3102.
51. Lim, D. S., S. T. Kim, B. Xu, R. S. Maser, J. Lin, J. H. Petrini, and M. B. Kastan. 2000. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613-617.
52. Lin, W. C., F. T. Lin, and J. R. Nevins. 2001. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev. 15:1833-1844.
53. Ma, Y., R. Croxton, R. L. Moorer, Jr., and W. D. Cress. 2002. Identification of novel E2F1-regulated genes by microarray. Arch. Biochem. Biophys. 399:212-224.
54. Macleod, K. F., Y. Hu, and T. Jacks. 1996. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J. 15:6178-6188.
55. Matsuoka, S., M. Huang, and S. J. Elledge. 1998. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282:1893-1897.
56. Matsuoka, S., G. Rotman, A. Ogawa, Y. Shiloh, K. Tamai, and S. J. EIledge. 2000. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl. Acad. Sci. USA 97:10389-10394.
57. Melchionna, R., X. B. Chen, A. Blasina, and C. H. McGowan. 2000. Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat. Cell Biol. 2:762-765.
58. Meng, R. D., P. Phillips, and W. S. El-Deiry. 1999. p53-independent increase in E2F-1 expression enhances the cytotoxic effects of etoposide and of adriamycin. Int. J. Oncol. 14:5-14.
59. Morris, J. D., T. Crook, L. R. Bandara, R. Davies, N. B. LaThangue, and K. H. Vousden. 1993. Human papillomavirus type 16 E7 regulates E2F and contributes to mitogenic signalling. Oncogene 8:893-898.
60. Muller, H., A. P. Bracken, R. Vernell, M. C. Moroni, F. Christians, E. Grassilli, E. Prosperini, E. Vigo, J. D. Oliner, and K. Helin. 2001. E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev. 15:267-285.
61. Muller, H., and K. Helin. 2000. The E2F transcription factors: key regulators of cell proliferation. Biochim. Biophys. Acta 1470:M1-M12.
62. Nahle, Z., J. Polakoff, R. V. Davuluri, M. E. McCurrach, M. D. Jacobson, M. Narita, M. Q. Zhang, Y. Lazebnik, D. Bar-Sagi, and S. W. Lowe. 2002. Direct coupling of the cell cycle and cell death machinery by E2F. Nat. Cell Biol. 4:859-864.
63. Nevins, J. R. 1998. Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9:585-593.
64. 1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98:9092-9097.
65. O'Connor, D. J., and X. Lu. 2000. Stress signals induce transcriptionally inactive E2F-1 independently of p53 and Rb. Oncogene 19:2369-2376.
66. Pan, H., C. Yin, N. J. Dyson, E. Harlow, L. Yamasaki, and T. Van Dyke. 1998. Key roles for E2F1 in signaling p53-dependent apoptosis and in cell division within developing tumors. Mol. Cell 2:283-292.
67. Phillips, A. C., and K. H. Vousden. 2001. E2F-1 induced apoptosis. Apoptosis 6:173-182.
68. Pierce, A. M., I. B. Gimenez-Conti, R. Schneider-Broussard, L. A. Martinez, C. J. Conti, and D. G. Johnson. 1998. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc. Natl. Acad. Sci. USA 95:8858-8863.
69. Prives, C. 1998. Signaling to p53: breaking the MDM2-p53 circuit. Cell 95:5-8.
70. Qin, X. Q., D. M. Livingston, W. G. Kaelin, Jr., and P. D. Adams. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918-10922.
71. Ren, B., H. Cam, Y. Takahashi, T. Volkert, J. Terragni, R. A. Young, and B. D. Dynlacht. 2002. E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. Genes Dev. 16:245-256.
72. Robertson, K. D., and P. A. Jones. 1998. The human ARF cell cycle regulatory gene promoter is a CpG island which can be silenced by DNA methylation and down-regulated by wild-type p53. Mol. Cell. Biol. 18:6457-6473.
73. Rogoff, H. A., M. T. Pickering, M. E. Debatis, S. Jones, and T. F. Kowalik. 2002. E2F1 induces phosphorylation of p53 that is coincident with p53 accumulation and apoptosis. Mol. Cell. Biol. 22:5308-5318.
74. Russell, J. L., J. T. Powers, R. J. Rounbehler, P. M. Rogers, C. J. Conti, and D. G. Johnson. 2002. ARF differentially modulates apoptosis induced by E2F1 and Myc. Mol. Cell. Biol. 22:1360-1368.
75. Schwarz, J. K., C. H. Bassing, I. Kovesdi, M. B. Datto, M. Blazing, S. George, X. F. Wang, and J. R. Nevins. 1995. Expression of the E2F1 transcription factor overcomes type beta transforming growth factor-mediated growth suppression. Proc. Natl. Acad. Sci. USA 92:483-487.
76. Schwarz, J. K., C. M. Lovly, and H. Piwnica-Worms. 2003. Regulation of the Chk2 protein kinase by oligomerization-mediated cis- and trans-phosphorylation. Mol. Cancer Res. 1:598-609.
77. Shieh, S. Y., J. Ahn, K. Tamai, Y. Taya, and C. Prives. 2000. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 14:289-300.
78. Shiloh, Y. 2001. ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. 11:71-77.
79. Siliciano, J. D., C. E. Canman, Y. Taya, K. Sakaguchi, E. Appella, and M. B. Kastan. 1997. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 11:3471-3481.
80. Stanelle, J., T. Stiewe, C. C. Theseling, M. Peter, and B. M. Putzer. 2002. Gene expression changes in response to E2F1 activation. Nucleic Acids Res. 30:1859-1867.
81. Stevens, C., L. Smith, and N. B. La Thangue. 2003. Chk2 activates E2F-1 in response to DNA damage. Nat. Cell Biol. 5:401-409.
82. Takai, H., K. Naka, Y. Okada, M. Watanabe, N. Harada, S. Saito, C. W. Anderson, E. Appella, M. Nakanishi, H. Suzuki, K. Nagashima, H. Sawa, K. Ikeda, and N. Motoyama. 2002. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 21:5195-5205.
83. Tolbert, D., X. Lu, C. Yin, M. Tantama, and T. Van Dyke. 2002. p19(ARF) is dispensable for oncogenic stress-induced p53-mediated apoptosis and tumor suppression in vivo. Mol. Cell. Biol. 22:370-377.
84. Tsai, K. Y., D. MacPherson, D. A. Rubinson, D. Crowley, and T. Jacks. 2002. ARF is not required for apoptosis in Rb mutant mouse embryos. Curr. Biol. 12:159-163.
85. Vousden, K. H. 2000. p53: death star. Cell 103:691-694.
86. Weinmann, A. S., S. M. Bartley, T. Zhang, M. Q. Zhang, and P. J. Farnham. 2001. Use of chromatin immunoprecipitation to clone novel E2F target promoters. Mol. Cell. Biol. 21:6820-6832.
87. Wu, X., and J. Chen. 2003. Autophosphorylation of checkpoint kinase 2 at serine 516 is required for radiation-induced apoptosis. J. Biol. Chem. 278: 36163-36168.
88. Wu, X., and A. J. Levine. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91:3602-3606.
89. Xie, S., H. Wu, Q. Wang, J. P. Cogswell, I. Husain, C. Conn, P. Stambrook, M. Jhanwar-Uniyal, and W. Dai. 2001. Plk3 functionally links DNA damage to cell cycle arrest and apoptosis at least in part via the p53 pathway. J. Biol. Chem. 276:43305-43312.
90. Zhao, S., Y. C. Weng, S. S. Yuan, Y. T. Lin, H. C. Hsu, S. C. Lin, E. Gerbino, M. H. Song, M. Z. Zdzienicka, R. A. Gatti, J. W. Shay, Y. Ziv, Y. Shiloh, and E. Y. Lee. 2000. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405:473-477.