E2F1 and E2F2 have opposite effects on radiation-induced p53-independent apoptosis in Drosophila

Developmental Biology

Volumn 346, Issue 1, 2010, Pages 80-89

  Wichmann, Anita ^a   Uyetake, Lyle ^a   Su, Tin Tin ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Drosophila; E2F; P53; Radiation

Indexed keywords

CHECKPOINT KINASE 2; HEAD INVOLUTION DEFECTIVE PROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F2; DNA BINDING PROTEIN; DP1 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; E2F2 PROTEIN, DROSOPHILA; LOK PROTEIN, DROSOPHILA; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE MUTATION; IONIZING RADIATION; MITOSIS INDEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; RADIATION EXPOSURE; ANIMAL; CYTOLOGY; PHYSIOLOGY; RADIATION RESPONSE;

DROSOPHILA MELANOGASTER;

ANIMALS; APOPTOSIS; CHECKPOINT KINASE 2; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; E2F1 TRANSCRIPTION FACTOR; E2F2 TRANSCRIPTION FACTOR; MITOTIC INDEX; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77956402972     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.07.023     Document Type: Article

References (47)

1. Abrams J.M., White K., Fessler L.I., Steller H. Programmed cell death during Drosophila embryogenesis. Development 1993, 117:29-43.
2. Asano M., Nevins J.R., Wharton R.P. Ectopic E2F expression induces S phase and apoptosis in Drosophila imaginal discs. Genes Dev. 1996, 10:1422-1432.
3. Bandara L.R., Buck V.M., Zamanian M., Johnston L.H., La Thangue N.B. Functional synergy between DP-1 and E2F-1 in the cell cycle-regulating transcription factor DRTF1/E2F. EMBO J. 1993, 12:4317-4324.
4. Beijersbergen R.L., Kerkhoven R.M., Zhu L., Carlee L., Voorhoeve P.M., Bernards R. E2F-4, a new member of the E2F gene family, has oncogenic activity and associates with p107 in vivo. Genes Dev. 1994, 8:2680-2690.
5. Brodsky M.H., Nordstrom W., Tsang G., Kwan E., Rubin G.M., Abrams J.M. Drosophila p53 binds a damage response element at the reaper locus. Cell 2000, 101:103-113.
6. Brodsky M.H., Sekelsky J.J., Tsang G., Hawley R.S., Rubin G.M. mus304 encodes a novel DNA damage checkpoint protein required during Drosophila development. Genes Dev. 2000, 14:666-678.
7. Brodsky M.H., Weinert B.T., Tsang G., Rong Y.S., McGinnis N.M., Golic K.G., Rio D.C., Rubin G.M. Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol. Cell. Biol. 2004, 24:1219-1231.
8. Cayirlioglu P., Bonnette P.C., Dickson M.R., Duronio R.J. Drosophila E2f2 promotes the conversion from genomic DNA replication to gene amplification in ovarian follicle cells. Development 2001, 128:5085-5098.
9. Cuddihy A.R., Bristow R.G. The p53 protein family and radiation sensitivity: yes or no?. Cancer Metastasis Rev. 2004, 23:237-257.
10. DeGregori J. The genetics of the E2F family of transcription factors: shared functions and unique roles. Biochim. Biophys. Acta 2002, 1602:131-150.
11. DeGregori J., Johnson D.G. Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Curr. Mol. Med. 2006, 6:739-748.
12. Du W., Xie J.E., Dyson N. Ectopic expression of dE2F and dDP induces cell proliferation and death in the Drosophila eye. EMBO J. 1996, 15:3684-3692.
13. Duronio R.J., Bonnette P.C., O'Farrell P.H. Mutations of the Drosophila dDP, dE2F, and cyclin E genes reveal distinct roles for the E2F-DP transcription factor and cyclin E during the G1-S transition. Mol. Cell. Biol. 1998, 18:141-151.
14. Duronio R.J., O'Farrell P.H., Xie J.E., Brook A., Dyson N. The transcription factor E2F is required for S phase during Drosophila embryogenesis. Genes Dev. 1995, 9:1445-1455.
15. Dynlacht B.D., Brook A., Dembski M., Yenush L., Dyson N. DNA-binding and trans-activation properties of Drosophila E2F and DP proteins. Proc. Natl Acad. Sci. USA 1994, 91:6359-6363.
16. Frolov M.V., Huen D.S., Stevaux O., Dimova D., Balczarek-Strang K., Elsdon M., Dyson N.J. Functional antagonism between E2F family members. Genes Dev. 2001, 15:2146-2160.
17. Grether M.E., Abrams J.M., Agapite J., White K., Steller H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 1995, 9:1694-1708.
18. Hay B.A., Wolff T., Rubin G.M. Expression of baculovirus P35 prevents cell death in Drosophila. Development 1994, 120:2121-2129.
19. Holmberg C., Helin K., Sehested M., Karlstrom O. E2F-1-induced p53-independent apoptosis in transgenic mice. Oncogene 1998, 17:143-155.
20. Irwin M., Marin M.C., Phillips A.C., Seelan R.S., Smith D.I., Liu W., Flores E.R., Tsai K.Y., Jacks T., Vousden K.H., Kaelin W.G. Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 2000, 407:645-648.
21. La Thangue N.B., Bandara L.R. Targets for cancer chemotherapy: transcription factors and other nuclear proteins 2002, Humana Press, Totowa, NJ.
22. Ma Y., Croxton R., Moorer R.L., Cress W.D. Identification of novel E2F1-regulated genes by microarray. Arch. Biochem. Biophys. 2002, 399:212-224.
23. McNamee L.M., Brodsky M.H. p53-independent apoptosis limits DNA damage-induced aneuploidy. Genetics 2009, 182:423-435.
24. Merritt A.J., Allen T.D., Potten C.S., Hickman J.A. Apoptosis in small intestinal epithelial from p53-null mice: evidence for a delayed, p53-independent G2/M-associated cell death after gamma-irradiation. Oncogene 1997, 14:2759-2766.
25. Milton A., Luoto K., Ingram L., Munro S., Logan N., Graham A.L., Brummelkamp T.R., Hijmans E.M., Bernards R., La Thangue N.B. A functionally distinct member of the DP family of E2F subunits. Oncogene 2006, 25:3212-3218.
26. Moon N.S., Di Stefano L., Morris E.J., Patel R., White K., Dyson N.J. E2F and p53 induce apoptosis independently during Drosophila development but intersect in the context of DNA damage. PLoS Genet. 2008, 4:e1000153.
27. Moon N.S., Frolov M.V., Kwon E.J., Di Stefano L., Dimova D.K., Morris E.J., Taylor-Harding B., White K., Dyson N.J. Drosophila E2F1 has context-specific pro- and antiapoptotic properties during development. Dev. Cell 2005, 9:463-475.
28. Moroni M.C., Hickman E.S., Lazzerini Denchi E., Caprara G., Colli E., Cecconi F., Muller H., Helin K. Apaf-1 is a transcriptional target for E2F and p53. Nat. Cell Biol. 2001, 3:552-558.
29. Morris L., Allen K.E., La Thangue N.B. Regulation of E2F transcription by cyclin E-Cdk2 kinase mediated through p300/CBP co-activators. Nat. Cell Biol. 2000, 2:232-239.
30. Nahle Z., Polakoff J., Davuluri R.V., McCurrach M.E., Jacobson M.D., Narita M., Zhang M.Q., Lazebnik Y., Bar-Sagi D., Lowe S.W. Direct coupling of the cell cycle and cell death machinery by E2F. Nat. Cell Biol. 2002, 4:859-864.
31. Nicholson S.C., Gilbert M.M., Nicolay B.N., Frolov M.V., Moberg K.H. The archipelago tumor suppressor gene limits rb/e2f-regulated apoptosis in developing Drosophila tissues. Curr. Biol. 2009, 19:1503-1510.
32. Ohtani K., Nevins J.R. Functional properties of a Drosophila homolog of the E2F1 gene. Mol. Cell. Biol. 1994, 14:1603-1612.
33. Ollmann M., Young L.M., Di Como C.J., Karim F., Belvin M., Robertson S., Whittaker K., Demsky M., Fisher W.W., Buchman A., Duyk G., Friedman L., Prives C., Kopczynski C. Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 2000, 101:91-101.
34. Rogers K.T., Higgins P.D., Milla M.M., Phillips R.S., Horowitz J.M. DP-2, a heterodimeric partner of E2F: identification and characterization of DP-2 proteins expressed in vivo. Proc. Natl Acad. Sci. USA 1996, 93:7594-7599.
35. Rong Y.S., Titen S.W., Xie H.B., Golic M.M., Bastiani M., Bandyopadhyay P., Olivera B.M., Brodsky M., Rubin G.M., Golic K.G. Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev. 2002, 16:1568-1581.
36. Royzman I., Austin R.J., Bosco G., Bell S.P., Orr-Weaver T.L. ORC localization in Drosophila follicle cells and the effects of mutations in dE2F and dDP. Genes Dev. 1999, 13:827-840.
37. Royzman I., Whittaker A.J., Orr-Weaver T.L. Mutations in Drosophila DP and E2F distinguish G1-S progression from an associated transcriptional program. Genes Dev. 1997, 11:1999-2011.
38. Sawado T., Yamaguchi M., Nishimoto Y., Ohno K., Sakaguchi K., Matsukage A. dE2F2, a novel E2F-family transcription factor in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 1998, 251:409-415.
39. Shu H.K., Julin C.M., Furman F., Yount G.L., Haas-Kogan D., Israel M.A. Overexpression of E2F1 in glioma-derived cell lines induces a p53-independent apoptosis that is further enhanced by ionizing radiation. Neuro-oncology 2000, 2:16-21.
40. Sogame N., Kim M., Abrams J.M. Drosophila p53 preserves genomic stability by regulating cell death. Proc. Natl Acad. Sci. USA 2003, 100:4696-4701.
41. Tanaka-Matakatsu M., Xu J., Cheng L., Du W. Regulation of apoptosis of rbf mutant cells during Drosophila development. Dev. Biol. 2009, 326:347-356.
42. Wichmann A., Jaklevic B., Su T.T. Ionizing radiation induces caspase-dependent but Chk2- and p53-independent cell death in Drosophila melanogaster. PNAS 2006, 103:9952-9957.
43. Wu C.L., Zukerberg L.R., Ngwu C., Harlow E., Lees J.A. In vivo association of E2F and DP family proteins. Mol. Cell. Biol. 1995, 15:2536-2546.
44. Xie W., Jiang P., Miao L., Zhao Y., Zhimin Z., Qing L., Zhu W.G., Wu M. Novel link between E2F1 and Smac/DIABLO: proapoptotic Smac/DIABLO is transcriptionally upregulated by E2F1. Nucleic Acids Res. 2006, 34:2046-2055.
45. Zhang Y., Chellappan S.P. Cloning and characterization of human DP2, a novel dimerization partner of E2F. Oncogene 1995, 10:2085-2093.
46. Zhang Y., Lin N., Carroll P.M., Chan G., Guan B., Xiao H., Yao B., Wu S.S., Zhou L. Epigenetic blocking of an enhancer region controls irradiation-induced proapoptotic gene expression in Drosophila embryos. Dev. Cell 2008, 14:481-493.
47. Zhou L., Steller H. Distinct pathways mediate UV-induced apoptosis in Drosophila embryos. Dev. Cell 2003, 4:599-605.