A gradient of epidermal growth factor receptor signaling determines the sensitivity of rbf1 mutant cells to E2F-dependent apoptosis

Molecular and Cellular Biology

Volumn 26, Issue 20, 2006, Pages 7601-7615

  Moon, Nam Sung ^a   Di Stefano, Luisa ^a   Dyson, Nicholas ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; INSECT PROTEIN; PROTEIN ARGOS; PROTEIN RBF1; RAF PROTEIN; RAS PROTEIN; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; UNCLASSIFIED DRUG;

APOPTOSIS; ARGOS GENE; ARTICLE; CELL CYCLE PROGRESSION; CELL DEATH; CELL MUTANT; CELL TYPE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; EYE DEVELOPMENT; GAP1 GENE; GENE; GENE ACTIVATION; GENE INACTIVATION; GENE LOSS; GENE MUTATION; GENE REPRESSION; IN VIVO STUDY; INSECT GENETICS; LARVAL STAGE; MORPHOGENESIS; MORPHOGENETIC FURROW; NEGATIVE FEEDBACK; NONHUMAN; ONCOGENE RAS; OPTIC DISK; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAF GENE; RBF1 GENE; SENSITIZATION; SIGNAL TRANSDUCTION; SPROUTY GENE; TISSUE SPECIFICITY; TUMOR CELL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; E2F1 TRANSCRIPTION FACTOR; EYE; GENE EXPRESSION REGULATION; MUTATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 33749592371     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00836-06     Document Type: Article

References (76)

1. Abrams, J. M. 1999. An emerging blueprint for apoptosis in Drosophila. Trends Cell Biol. 9:435-40.
2. Asano, M., J. R. Nevins, and R. P. Wharton. 1996. Ectopic E2F expression induces S phase and apoptosis in Drosophila imaginal discs. Genes Dev. 10:1422-1432.
3. Attwooll, C., E. L. Denchi, and K. Helin. 2004. The E2F family, specific functions and overlapping interests. EMBO J. 23:4709-4716.
4. Baker, N. E., and S. Y. Yu. 2001. The EGF receptor defines domains of cell cycle progression and survival to regulate cell number in the developing Drosophila eye. Cell 104:699-708.
5. Baonza, A., T. Casci, and M. Freeman. 2001. A primary role for the epidermal growth factor receptor in ommatidial spacing in the Drosophila eye. Curr. Biol. 11:396-404.
6. Bergmann, A., J. Agapite, K. McCall, and H. Steller. 1998. The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95:331-341.
7. Bookstein, R., and W. H. Lee. 1991. Molecular genetics of the retinoblastoma suppressor gene. Crit. Rev. Oncog. 2:211-227.
8. Brook, A., J. E. Xie, W. Du, and N. Dyson. 1996. Requirements for dE2F function in proliferating cells and in post-mitotic differentiating cells. EMBO J. 15:3676-3683.
9. Chau, B. N., and J. Y. Wang. 2003. Coordinated regulation of life and death by RB. Nat. Rev. Cancer 3:130-138.
10. Chaussepied, M., and D. Ginsberg. 2004. Transcriptional regulation of AKT activation by E2F. Mol. Cell 16:831-837.
11. Chen, D., I. Livne-Bar, J. L. Vanderluit, R. S. Slack, M. Agochiya, and R. Bremner. 2004. Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell 5:539-551.
12. Clarke, A. R., E. R. Maandag, M. van Roon, N. M. van der Lugt, M. van der Valk, M. L. Hooper, A. Berns, and H. te Riele. 1992. Requirement for a functional Rb-1 gene in murine development. Nature 359:328-330.
13. Classon, M., and E. Harlow. 2002. The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer 2:910-917.
14. de Bruin, A., L. Wu, H. I. Saavedra, P. Wilson, Y. Yang, T. J. Rosol, M. Weinstein, M. L. Robinson, and G. Leone. 2003. Rb function in extraembryonic lineages suppresses apoptosis in the CNS of Rb-deficient mice. Proc. Natl. Acad. Sci. USA 100:6546-6551.
15. DeGregori, J. 2002. The genetics of the E2F family of transcription factors: shared functions and unique roles. Biochim. Biophys. Acta 1602:131-150.
16. Dominguez, M., J. D. Wasserman, and M. Freeman. 1998. Multiple functions of the EGF receptor in Drosophila eye development. Curr. Biol. 8:1039-1048.
17. Du, W. 2000. Suppression of the rbf null mutants by a de2f1 allele that lacks transactivation domain. Development 127:367-379.
18. Du, W., and N. Dyson. 1999. The role of RBF in the introduction of G1 regulation during Drosophila embryogenesis. EMBO J. 18:916-925.
19. Du, W., M. Vidal, J. E. Xie, and N. Dyson. 1996. RBF, a novel RB-related gene that regulates E2F activity and interacts with cyclin E in Drosophila. Genes Dev. 10:1206-1218.
20. Dyer, M. A., and R. Bremner. 2005. The search for the retinoblastoma cell of origin. Nat. Rev. Cancer 5:91-101.
21. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245-2262.
22. Freeman, M. 1997. Cell determination strategies in the Drosophila eye. Development 124:261-270.
23. Freeman, M. 1994. Misexpression of the Drosophila argos gene, a secreted regulator of cell determination. Development 120:2297-2304.
24. Freeman, M. 1996. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87:651-660.
25. Frolov, M. V., N.-S. Moon, and N. J. Dyson. 2005. dDP is needed for normal cell proliferation. Mol. Cell. Biol. 25:3027-3039.
26. Gabay, L., R. Seger, and B. Z. Shilo. 1997. In situ activation pattern of Drosophila EGF receptor pathway during development. Science 277:1103-1106.
27. Gallic, B. L., C. Campbell, H. Devlin, A. Duckett, and J. A. Squire. 1999. Developmental basis of retinal-specific induction of cancer by RB mutation. Cancer Res. 59:1731s-1735s.
28. Golembo, M., R. Schweitzer, M. Freeman, and B. Z. Shilo. 1996. Argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 122:223-230.
29. Grether, M. E., J. M. Abrams, J. Agapite, K. White, and H. Steller. 1995. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9:1694-1708.
30. Hacohen, N., S. Kramer, D. Sutherland, Y. Hiromi, and M. A. Krasnow. 1998. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92:253-263.
31. Hallstrom, T. C., and J. R. Nevins. 2003. Specificity in the activation and control of transcription factor E2F-dependent apoptosis. Proc. Natl. Acad. Sci. USA 100:10848-10853.
32. Harvey, M., H. Vogel, E. Y. Lee, A. Bradley, and L. A. Donehower. 1995. Mice deficient in both p53 and Rb develop tumors primarily of endocrine origin. Cancer Res. 55:1146-1151.
33. Hershko, T., and D. Ginsberg. 2004. Up-regulation of Bcl-2 homology 3 (BH3)-only proteins by E2F1 mediates apoptosis. J. Biol. Chem. 279:8627-8634.
34. Hsiung, F., and K. Moses. 2002. Retinal development in Drosophila: specifying the first neuron. Hum. Mol. Genet. 11:1207-1214.
35. Jacks, T., A. Fazeli, E. M. Schmitt, R. T. Bronson, M. A. Goodell, and R. A. Weinberg. 1992. Effects of an Rb mutation in the mouse. Nature 359:295-300.
36. Jarman, A. P., Y. Grau, L. Y. Jan, and Y. N. Jan. 1993. atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307-1321.
37. Klein, D. E., V. M. Nappi, G. T. Reeves, S. Y. Shvartsman, and M. A. Lemmon. 2004. Argos inhibits epidermal growth factor receptor signalling by ligand sequestration. Nature 430:1040-1044.
38. Kornbluth, S., and K. White. 2005. Apoptosis in Drosophila: neither fish nor fowl (nor man, nor worm). J. Cell Sci. 118:1779-1787.
39. 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.
40. Kumar, J. P., M. Tio, F. Hsiung, S. Akopyan, L. Gabay, R. Seger, B. Z. Shilo, and K. Moses. 1998. Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125:3875-3885.
41. Kurada, P., and K. White. 1998. Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95:319-329.
42. Lee, E. Y., C. Y. Chang, N. Hu, Y. C. Wang, C. C. Lai, K. Herrup, W. H. Lee, and A. Bradley. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288-294.
43. Lesokhin, A. M., S. Y. Yu, J. Katz, and N. E. Baker. 1999. Several levels of EGF receptor signaling during photoreceptor specification in wild-type, Ellipse, and null mutant Drosophila. Dev. Biol. 205:129-144.
44. Ley, R., K. E. Ewings, K. Hadfield, and S. J. Cook. 2005. Regulatory phosphorylation of Bim: sorting out the ERK from the JNK. Cell Death Differ. 12:1008-1014.
45. Lipinski, M. M., K. F. Macleod, B. O. Williams, T. L. Mullaney, D. Crowley, and T. Jacks. 2001. Cell-autonomous and non-cell-autonomous functions of the Rb tumor suppressor in developing central nervous system. EMBO J. 20:3402-3413.
46. MacPherson, D., J. Sage, T. Kim, D. Ho, M. E. McLaughlin, and T. Jacks. 2004. Cell type-specific effects of Rb deletion in the murine retina. Genes Dev. 18:1681-1694.
47. Moon, N. S., M. V. Frolov, E. J. Kwon, L. Di Stefano, D. K. Dimova, E. J. Morris, B. Taylor-Harding, K. White, and N. J. Dyson. 2005. Drosophila E2F1 has context-specific pro- and antiapoptotic properties during development. Dev. Cell 9:463-475.
48. Muller, H., and K. Helin. 2000. The E2F transcription factors: key regulators of cell proliferation. Biochim. Biophys. Acta 1470:M1-M12.
49. Nevins, J. R. 1998. Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9:585-593.
50. Phillips, A. C., and K. H. Vousden. 2001. E2F-1 induced apoptosis. Apoptosis 6:173-182.
51. Richardson, H., and S. Kumar. 2002. Death to flies: Drosophila as a model system to study programmed cell death. J. Immunol. Methods 265:21-38.
52. Robanus-Maandag, E., M. Dekker, M. van der Valk, M. L. Carrozza, J. C. Jeanny, J. H. Dannenberg, A. Berns, and H. te Riele. 1998. p107 is a suppressor of retinoblastoma development in pRb-deficient mice. Genes Dev. 12:1599-1609.
53. Royzman, I., R. J. Austin, G. Bosco, S. P. Bell, and T. L. Orr-Weaver. 1999. ORC localization in Drosophila follicle cells and the effects of mutations in dE2F and dDP. Genes Dev. 13:827-840.
54. Royzman, I., A. J. Whittaker, and T. L. Orr-Weaver. 1997. Mutations in Drosophila DP and E2F distinguish G1-S progression from an associated transcriptional program. Genes Dev. 11:1999-2011.
55. Sawamoto, K., A. Taguchi, Y. Hirota, C. Yamada, M. H. Jin, and H. Okano. 1998. Argos induces programmed cell death in the developing Drosophila eye by inhibition of the Ras pathway. Cell Death Differ. 5:262-270.
56. Sears, R. C., and J. R. Nevins. 2002. Signaling networks that link cell proliferation and cell fate. J. Biol. Chem. 277:11617-11620.
57. Sherr, C. J. 1996. Cancer cell cycles. Science 274:1672-1677.
58. Stevaux, O., and N. J. Dyson. 2002. A revised picture of the E2F transcriptional network and RB function. Curr. Opin. Cell Biol. 14:684-691.
59. Takahashi, C., R. T. Bronson, M. Socolovsky, B. Contreras, K. Y. Lee, T. Jacks, M. Noda, R. Kucherlapati, and M. E. Ewen. 2003. Rb and N-ras function together to control differentiation in the mouse. Mol. Cell. Biol. 23:5256-5268.
60. Takahashi, C., B. Contreras, R. T. Bronson, M. Loda, and M. E. Ewen. 2004. Genetic interaction between Rb and K-ras in the control of differentiation and tumor suppression. Mol. Cell. Biol. 24:10406-10415.
61. Tio, M., and K. Moses. 1997. The Drosophila TGF alpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124: 343-351.
62. Trimarchi, J. M., and J. A. Lees. 2002. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell. Biol. 3:11-20.
63. Tsai, K. Y., Y. Hu, K. F. Macleod, D. Crowley, L. Yamasaki, and T. Jacks. 1998. Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol. Cell 2:293-304.
64. Voas, M. G., and I. Rebay. 2003. The novel plant homeodomain protein rhinoceros antagonizes Ras signaling in the Drosophila eye. Genetics 165: 1993-2006.
65. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
66. White, K., E. Tahaoglu, and H. Steller. 1996. Cell killing by the Drosophila gene reaper. Science 271:805-807.
67. Williams, B. O., L. Remington, D. M. Albert, S. Mukai, R. T. Bronson, and T. Jacks. 1994. Cooperative tumorigenic effects of germline mutations in Rb and p53. Nat. Genet. 7:480-484.
68. Wu, L., A. de Bruin, H. I. Saavedra, M. Starovic, A. Trimboli, Y. Yang, J. Opavska, P. Wilson, J. C. Thompson, M. C. Ostrowski, T. J. Rosol, L. A. Woollett, M. Weinstein, J. C. Cross, M. L. Robinson, and G. Leone. 2003. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421:942-947.
69. Xie, W., P. Jiang, L. Miao, Y. Zhao, Z. Zhimin, L. Qing, W. G. Zhu, and M. Wu. 2006. Novel link between E2F1 and Smac/DIABLO: proapoptotic Smac/DIABLO is transcriptionally upregulated by E2F1. Nucleic Acids Res. 34:2046-2055.
70. Xu, D., Y. Li, M. Arcaro, M. Lackey, and A. Bergmann. 2005. The CARD-carrying caspase Drone is essential for most, but not all, developmental cell death in Drosophila. Development 132:2125-2134.
71. Yang, L., and N. E. Baker. 2003. Cell cycle withdrawal, progression, and cell survival regulation by EGFR and its effectors in the differentiating Drosophila eye. Dev. Cell 4:359-369.
72. Yang, L., and N. E. Baker. 2001. Role of the EGFR/Ras/Raf pathway in specification of photoreceptor cells in the Drosophila retina. Development 128:1183-1191.
73. Young, A. P., and G. D. Longmore. 2004. Ras protects Rb family null fibroblasts from cell death: a role for AP-1. J. Biol. Chem. 279:10931-10938.
74. Zhang, J., J. Gray, L. Wu, G. Leone, S. Rowan, C. L. Cepko, X. Zhu, C. M. Craft, and M. A. Dyer. 2004. Rb regulates proliferation and rod photoreceptor development in the mouse retina. Nat. Genet. 36:351-360.
75. Zhou, L., and H. Steller. 2003. Distinct pathways mediate UV-induced apoptosis in Drosophila embryos. Dev. Cell 4:599-605.
76. Ziebold, U., T. Reza, A. Caron, and J. A. Lees. 2001. E2F3 contributes both to the inappropriate proliferation and to the apoptosis arising in Rb mutant embryos. Genes Dev. 15:386-391.