17
Views
94
CrossRef citations to date
0
Altmetric
DNA Dynamics and Chromosome Structure

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

, , , , , & show all
Pages 2968-2977 | Received 04 Sep 2003, Accepted 02 Jan 2004, Published online: 27 Mar 2023

REFERENCES

  • Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177–2196.
  • Agarwal, M. L., Taylor W. R., Chernov M. V., Chernova O. B., and Stark G. R.. 1998. The p53 network. J. Biol. Chem. 273:1–4.
  • Ahn, J., and Prives C.. 2002. Checkpoint kinase 2 (Chk2) monomers or dimers phosphorylate Cdc25C after DNA damage regardless of threonine 68 phosphorylation. J. Biol. Chem. 277:48418–48426.
  • Appella, E., and Anderson C. W.. 2001. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268:2764–2772.
  • Bakkenist, C. J., and Kastan M. B.. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499–506.
  • Banin, S., Moyal L., Shieh S., Taya Y., Anderson C. W., Chessa L., Smorodinsky N. I., Prives C., Reiss Y., Shiloh Y., and Ziv Y.. 1998. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281:1674–1677.
  • Barlow, C., Brown K. D., Deng C. X., Tagle D. A., and Wynshaw-Boris A.. 1997. Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat. Genet. 17:453–456.
  • Bates, S., Phillips A. C., Clark P. A., Stott F., Peters G., Ludwig R. L., and Vousden K. H.. 1998. p14ARF links the tumour suppressors RB and p53. Nature 395:124–125.
  • Bernstein, C., Bernstein H., Payne C. M., and Garewal H.. 2002. DNA repair/pro-apoptotic dual-role proteins in five major DNA repair pathways: fail-safe protection against carcinogenesis. Mutat. Res. 511:145–178.
  • Blattner, C., Sparks A., and Lane D.. 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.
  • Brown, A. L., Lee C. H., Schwarz J. K., Mitiku N., Piwnica-Worms H., and Chung J. H.. 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.
  • Brown, E. J., and Baltimore D.. 2000. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14:397–402.
  • Buscemi, G., Savio C., Zannini L., Micciche F., Masnada D., Nakanishi M., Tauchi H., Komatsu K., Mizutani S., Khanna K., Chen P., Concannon P., Chessa L., and Delia D.. 2001. Chk2 activation dependence on Nbs1 after DNA damage. Mol. Cell. Biol. 21:5214–5222.
  • Canman, C. E., Lim D. S., Cimprich K. A., Taya Y., Tamai K., Sakaguchi K., Appella E., Kastan M. B., and Siliciano J. D.. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281:1677–1679.
  • Castillo, J. P., Yurochko A. D., and Kowalik T. F.. 2000. Role of human cytomegalovirus immediate-early proteins in cell growth control. J. Virol. 74:8028–8037.
  • Chaturvedi, P., Eng W. K., Zhu Y., Mattern M. R., Mishra R., Hurle M. R., Zhang X., Annan R. S., Lu Q., Faucette L. F., Scott G. F., Li X., Carr S. A., Johnson R. K., Winkler J. D., and Zhou B. B.. 1999. Mammalian Chk2 is a downstream effector of the ATM-dependent DNA damage checkpoint pathway. Oncogene 18:4047–4054.
  • Chehab, N. H., Malikzay A., Appel M., and Halazonetis T. D.. 2000. Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev. 14:278–288.
  • Debbas, M., and White E.. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546–554.
  • DeGregori, J., Leone G., Miron A., Jakoi L., and Nevins J. R.. 1997. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA 94:7245–7250.
  • de Klein, A., Muijtjens M., van Os R., Verhoeven Y., Smit B., Carr A. M., Lehmann A. R., and Hoeijmakers J. H.. 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:479–482.
  • Duensing, S., and Munger K.. 2002. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res. 62:7075–7082.
  • Freedman, D. A., and Levine A. J.. 1998. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 18:7288–7293.
  • Fuchs, S. Y., Adler V., Buschmann T., Wu X., and Ronai Z.. 1998. Mdm2 association with p53 targets its ubiquitination. Oncogene 17:2543–2547.
  • Giaccia, A. J., and Kastan M. B.. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12:2973–2983.
  • Guo, Z., Kumagai A., Wang S. X., and Dunphy W. G.. 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.
  • Hall-Jackson, C. A., Cross D. A., Morrice N., and Smythe C.. 1999. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 18:6707–6713.
  • Harbour, J. W., and Dean D. C.. 2000. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev. 14:2393–2409.
  • Haupt, Y., Maya R., Kazaz A., and Oren M.. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387:296–299.
  • He, T. C., Zhou S., da Costa L. T., Yu J., Kinzler K. W., and Vogelstein B.. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509–2514.
  • Hekmat-Nejad, M., You Z., Yee M. C., Newport J. W., and Cimprich K. A.. 2000. Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Curr. Biol. 10:1565–1573.
  • Hermeking, H., and Eick D.. 1994. Mediation of c-Myc-induced apoptosis by p53. Science 265:2091–2093.
  • Herzog, K. H., Chong M. J., Kapsetaki M., Morgan J. I., and McKinnon P. J.. 1998. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280:1089–1091.
  • Hirao, A., Kong Y. Y., Matsuoka S., Wakeham A., Ruland J., Yoshida H., Liu D., Elledge S. J., and Mak T. W.. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287:1824–1827.
  • Hofferer, M., Wirbelauer C., Humar B., and Krek W.. 1999. Increased levels of E2F-1-dependent DNA binding activity after UV- or gamma-irradiation. Nucleic Acids Res. 27:491–495.
  • Honda, R., Tanaka H., and Yasuda H.. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420:25–27.
  • Huang, Y., Ishiko T., Nakada S., Utsugisawa T., Kato T., and Yuan Z. M.. 1997. Role for E2F in DNA damage-induced entry of cells into S phase. Cancer Res. 57:3640–3643.
  • Inoue, K., Roussel M. F., and Sherr C. J.. 1999. Induction of ARF tumor suppressor gene expression and cell cycle arrest by transcription factor DMP1. Proc. Natl. Acad. Sci. USA 96:3993–3998.
  • Ishida, S., Huang E., Zuzan H., Spang R., Leone G., West M., and Nevins J. R.. 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.
  • Jack, M. T., Woo R. A., Hirao A., Cheung A., Mak T. W., and Lee P. W.. 2002. Chk2 is dispensable for p53-mediated G1 arrest but is required for a latent p53-mediated apoptotic response. Proc. Natl. Acad. Sci. USA 99:9825–9829.
  • Jin, S., and Levine A. J.. 2001. The p53 functional circuit. J. Cell Sci. 114:4139–4140.
  • Johnson, D. G., Schwarz J. K., Cress W. D., and Nevins J. R.. 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 365:349–352.
  • Kalma, Y., Marash L., Lamed Y., and Ginsberg D.. 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.
  • Kamijo, T., Zindy F., Roussel M. F., Quelle D. E., Downing J. R., Ashmun R. A., Grosveld G., and Sherr C. J.. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91:649–659.
  • Kastan, M. B., and Lim D. S.. 2000. The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol. 1:179–186.
  • Kim, S. T., Lim D. S., Canman C. E., and Kastan M. B.. 1999. Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274:37538–37543.
  • Kowalik, T. F., DeGregori J., Leone G., Jakoi L., and Nevins J. R.. 1998. E2F1-specific induction of apoptosis and p53 accumulation, which is blocked by Mdm2. Cell Growth Differ. 9:113–118.
  • Kowalik, T. F., DeGregori J., Schwarz J. K., and Nevins J. R.. 1995. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 69:2491–2500.
  • Lakin, N. D., Hann B. C., and Jackson S. P.. 1999. The ataxia-telangiectasia related protein ATR mediates DNA-dependent phosphorylation of p53. Oncogene 18:3989–3995.
  • Leone, G., Sears R., Huang E., Rempel R., Nuckolls F., Park C. H., Giangrande P., Wu L., Saavedra H. I., Field S. J., Thompson M. A., Yang H., Fujiwara Y., Greenberg M. E., Orkin S., Smith C., and Nevins J. R.. 2001. Myc requires distinct E2F activities to induce S phase and apoptosis. Mol. Cell 8:105–113.
  • Liao, M. J., Yin C., Barlow C., Wynshaw-Boris A., and van Dyke T.. 1999. Atm is dispensable for p53 apoptosis and tumor suppression triggered by cell cycle dysfunction. Mol. Cell. Biol. 19:3095–3102.
  • Lim, D. S., Kim S. T., Xu B., Maser R. S., Lin J., Petrini J. H., and Kastan M. B.. 2000. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613–617.
  • Lin, W. C., Lin F. T., and Nevins J. R.. 2001. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev. 15:1833–1844.
  • Ma, Y., Croxton R., Moorer R. L., Jr., and Cress W. D.. 2002. Identification of novel E2F1-regulated genes by microarray. Arch. Biochem. Biophys. 399:212–224.
  • Macleod, K. F., Hu Y., and Jacks T.. 1996. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J. 15:6178–6188.
  • Matsuoka, S., Huang M., and Elledge S. J.. 1998. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282:1893–1897.
  • Matsuoka, S., Rotman G., Ogawa A., Shiloh Y., Tamai K., and Elledge S. J.. 2000. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl. Acad. Sci. USA 97:10389–10394.
  • Melchionna, R., Chen X. B., Blasina A., and McGowan C. H.. 2000. Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat. Cell Biol. 2:762–765.
  • Meng, R. D., Phillips P., and El-Deiry W. S.. 1999. p53-independent increase in E2F-1 expression enhances the cytotoxic effects of etoposide and of adriamycin. Int. J. Oncol. 14:5–14.
  • Morris, J. D., Crook T., Bandara L. R., Davies R., LaThangue N. B., and Vousden K. H.. 1993. Human papillomavirus type 16 E7 regulates E2F and contributes to mitogenic signalling. Oncogene 8:893–898.
  • Muller, H., Bracken A. P., Vernell R., Moroni M. C., Christians F., Grassilli E., Prosperini E., Vigo E., Oliner J. D., and Helin K.. 2001. E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev. 15:267–285.
  • Muller, H., and Helin K.. 2000. The E2F transcription factors: key regulators of cell proliferation. Biochim. Biophys. Acta 1470:M1–M12.
  • Nahle, Z., Polakoff J., Davuluri R. V., McCurrach M. E., Jacobson M. D., Narita M., Zhang M. Q., Lazebnik Y., Bar-Sagi D., and Lowe S. W.. 2002. Direct coupling of the cell cycle and cell death machinery by E2F. Nat. Cell Biol. 4:859–864.
  • Nevins, J. R. 1998. Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9:585–593.
  • Nghiem, P., Park P. K., Kim Y., Vaziri C., and Schreiber S. L.. 2001. ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98:9092–9097.
  • O'Connor, D. J., and Lu X.. 2000. Stress signals induce transcriptionally inactive E2F-1 independently of p53 and Rb. Oncogene 19:2369–2376.
  • Pan, H., Yin C., Dyson N. J., Harlow E., Yamasaki L., and Van Dyke T.. 1998. Key roles for E2F1 in signaling p53-dependent apoptosis and in cell division within developing tumors. Mol. Cell 2:283–292.
  • Phillips, A. C., and Vousden K. H.. 2001. E2F-1 induced apoptosis. Apoptosis 6:173–182.
  • Pierce, A. M., Gimenez-Conti I. B., Schneider-Broussard R., Martinez L. A., Conti C. J., and Johnson D. G.. 1998. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc. Natl. Acad. Sci. USA 95:8858–8863.
  • Prives, C. 1998. Signaling to p53: breaking the MDM2-p53 circuit. Cell 95:5–8.
  • Qin, X. Q., Livingston D. M., Kaelin W. G., Jr., and Adams P. D.. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918–10922.
  • Ren, B., Cam H., Takahashi Y., Volkert T., Terragni J., Young R. A., and Dynlacht B. D.. 2002. E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. Genes Dev. 16:245–256.
  • Robertson, K. D., and Jones P. A.. 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.
  • Rogoff, H. A., Pickering M. T., Debatis M. E., Jones S., and Kowalik T. F.. 2002. E2F1 induces phosphorylation of p53 that is coincident with p53 accumulation and apoptosis. Mol. Cell. Biol. 22:5308–5318.
  • Russell, J. L., Powers J. T., Rounbehler R. J., Rogers P. M., Conti C. J., and Johnson D. G.. 2002. ARF differentially modulates apoptosis induced by E2F1 and Myc. Mol. Cell. Biol. 22:1360–1368.
  • Schwarz, J. K., Bassing C. H., Kovesdi I., Datto M. B., Blazing M., George S., Wang X. F., and Nevins J. R.. 1995. Expression of the E2F1 transcription factor overcomes type beta transforming growth factor-mediated growth suppression. Proc. Natl. Acad. Sci. USA 92:483–487.
  • Schwarz, J. K., Lovly C. M., and Piwnica-Worms H.. 2003. Regulation of the Chk2 protein kinase by oligomerization-mediated cis- and trans-phosphorylation. Mol. Cancer Res. 1:598–609.
  • Shieh, S. Y., Ahn J., Tamai K., Taya Y., and Prives C.. 2000. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 14:289–300.
  • Shiloh, Y. 2001. ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. 11:71–77.
  • Siliciano, J. D., Canman C. E., Taya Y., Sakaguchi K., Appella E., and Kastan M. B.. 1997. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 11:3471–3481.
  • Stanelle, J., Stiewe T., Theseling C. C., Peter M., and Putzer B. M.. 2002. Gene expression changes in response to E2F1 activation. Nucleic Acids Res. 30:1859–1867.
  • Stevens, C., Smith L., and La Thangue N. B.. 2003. Chk2 activates E2F-1 in response to DNA damage. Nat. Cell Biol. 5:401–409.
  • Takai, H., Naka K., Okada Y., Watanabe M., Harada N., Saito S., Anderson C. W., Appella E., Nakanishi M., Suzuki H., Nagashima K., Sawa H., Ikeda K., and Motoyama N.. 2002. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 21:5195–5205.
  • Tolbert, D., Lu X., Yin C., Tantama M., and Van Dyke T.. 2002. p19(ARF) is dispensable for oncogenic stress-induced p53-mediated apoptosis and tumor suppression in vivo. Mol. Cell. Biol. 22:370–377.
  • Tsai, K. Y., MacPherson D., Rubinson D. A., Crowley D., and Jacks T.. 2002. ARF is not required for apoptosis in Rb mutant mouse embryos. Curr. Biol. 12:159–163.
  • Vousden, K. H. 2000. p53: death star. Cell 103:691–694.
  • Weinmann, A. S., Bartley S. M., Zhang T., Zhang M. Q., and Farnham P. J.. 2001. Use of chromatin immunoprecipitation to clone novel E2F target promoters. Mol. Cell. Biol. 21:6820–6832.
  • Wu, X., and Chen J.. 2003. Autophosphorylation of checkpoint kinase 2 at serine 516 is required for radiation-induced apoptosis. J. Biol. Chem. 278:36163–36168.
  • Wu, X., and Levine A. J.. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91:3602–3606.
  • Xie, S., Wu H., Wang Q., Cogswell J. P., Husain I., Conn C., Stambrook P., Jhanwar-Uniyal M., and Dai W.. 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.
  • Zhao, S., Weng Y. C., Yuan S. S., Lin Y. T., Hsu H. C., Lin S. C., Gerbino E., Song M. H., Zdzienicka M. Z., Gatti R. A., Shay J. W., Ziv Y., Shiloh Y., and Lee E. Y.. 2000. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405:473–477.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.