Sequential activation of ETS proteins provides a sustained transcriptional response to EGFR signaling

Development (Cambridge)

Volumn 140, Issue 13, 2013, Pages 2746-2754

  Shwartz, Arkadi ^a   Yogev, Shaul ^a   Schejter, Eyal D ^a   Shilo, Ben Zion ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

EGFR signaling; ETS proteins; Eye development; MAP kinase; Pointed

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE;

ARTICLE; DROSOPHILA; GENE LOCUS; GENETIC TRANSCRIPTION; NONHUMAN; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EGFR SIGNALING; ETS PROTEINS; EYE DEVELOPMENT; MAP KINASE; POINTED;

ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; NERVE TISSUE PROTEINS; PROTO-ONCOGENE PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84878863089     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.093138     Document Type: Article

References (44)

1. Alvarez, A. D., Shi, W., Wilson, B. A. and Skeath, J. B. (2003). pannier and pointedP2 act sequentially to regulate Drosophila heart development. Development 130, 3015-3026.
2. Aza-Blanc, P., Ramírez-Weber, F. A., Laget, M. P., Schwartz, C. and Kornberg, T. B. (1997). Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89, 1043-1053.
3. Banerjee, U. and Zipursky, S. L. (1990). The role of cell-cell interaction in the development of the Drosophila visual system. Neuron 4, 177-187.
4. Brunner, D., Dücker, K., Oellers, N., Hafen, E., Scholz, H. and Klämbt, C. (1994). The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature 370, 386-389.
5. Casci, T., Vinós, J. and Freeman, M. (1999). Sprouty, an intracellular inhibitor of Ras signaling. Cell 96, 655-665.
6. Cavallo, R. A., Cox, R. T., Moline, M. M., Roose, J., Polevoy, G. A., Clevers, H., Peifer, M. and Bejsovec, A. (1998). Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395, 604-608.
7. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651-660.
8. Freeman, M., Kimmel, B. E. and Rubin, G. M. (1992a). Identifying targets of the rough homeobox gene of Drosophila: evidence that rhomboid functions in eye development. Development 116, 335-346.
9. Freeman, M., Klämbt, C., Goodman, C. S. and Rubin, G. M. (1992b). The argos gene encodes a diffusible factor that regulates cell fate decisions in the Drosophila eye. Cell 69, 963-975.
10. Gabay, L., Scholz, H., Golembo, M., Klaes, A., Shilo, B. Z. and Klämbt, C. (1996). EGF receptor signaling induces pointed P1 transcription and inactivates Yan protein in the Drosophila embryonic ventral ectoderm. Development 122, 3355-3362.
11. Gabay, L., Seger, R. and Shilo, B. Z. (1997). In situ activation pattern of Drosophila EGF receptor pathway during development. Science 277, 1103-1106.
12. Ginsberg, M., James, D., Ding, B. S., Nolan, D., Geng, F., Butler, J. M., Schachterle, W., Pulijaal, V. R., Mathew, S., Chasen, S. T. et al. (2012). Efficient direct reprogramming of mature amniotic cells into endothelial cells by ETS factors and TGFβ suppression. Cell 151, 559-575.
13. Hart, A. H., Reventar, R. and Bernstein, A. (2000). Genetic analysis of ETS genes in C. elegans. Oncogene 19, 6400-6408.
14. Helman, A., Cinnamon, E., Mezuman, S., Hayouka, Z., Von Ohlen, T., Orian, A., Jiménez, G. and Paroush, Z. (2011). Phosphorylation of Groucho mediates RTK feedback inhibition and prolonged pathway target gene expression. Curr. Biol. 21, 1102-1110.
15. Hsiung, F. and Moses, K. (2002). Retinal development in Drosophila: specifying the first neuron. Hum. Mol. Genet. 11, 1207-1214.
16. Hsu, T. and Schulz, R. A. (2000). Sequence and functional properties of Ets genes in the model organism Drosophila. Oncogene 19, 6409-6416.
17. Kauffmann, R. C., Li, S., Gallagher, P. A., Zhang, J. and Carthew, R. W. (1996). Ras1 signaling and transcriptional competence in the R7 cell of Drosophila. Genes Dev. 10, 2167-2178.
18. Kim, M., Cha, G. H., Kim, S., Lee, J. H., Park, J., Koh, H., Choi, K. Y. and Chung, J. (2004). MKP-3 has essential roles as a negative regulator of the Ras/mitogenactivated protein kinase pathway during Drosophila development. Mol. Cell. Biol. 24, 573-583.
19. Klaes, A., Menne, T., Stollewerk, A., Scholz, H. and Klämbt, C. (1994). The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78, 149-160.
20. Klämbt, C. (1993). The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glial cells. Development 117, 163-176.
21. Klein, D. E., Nappi, V. M., Reeves, G. T., Shvartsman, S. Y. and Lemmon, M. A. (2004). Argos inhibits epidermal growth factor receptor signalling by ligand sequestration. Nature 430, 1040-1044.
22. Kramer, S., Okabe, M., Hacohen, N., Krasnow, M. A. and Hiromi, Y. (1999). Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126, 2515-2525.
23. Kumar, J. P. (2012). Building an ommatidium one cell at a time. Dev. Dyn. 241, 136-149.
24. Lai, E. C. (2002). Keeping a good pathway down: transcriptional repression of Notch pathway target genes by CSL proteins. EMBO Rep. 3, 840-845.
25. Lai, Z. C. and Rubin, G. M. (1992). Negative control of photoreceptor development in Drosophila by the product of the yan gene, an ETS domain protein. Cell 70, 609-620.
26. McGuire, S. E., Mao, Z. and Davis, R. L. (2004). Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci. STKE 2004, pl6.
27. Morimoto, A. M., Jordan, K. C., Tietze, K., Britton, J. S., O'Neill, E. M. and Ruohola-Baker, H. (1996). Pointed, an ETS domain transcription factor, negatively regulates the EGF receptor pathway in Drosophila oogenesis. Development 122, 3745-3754.
28. Müller, B., Hartmann, B., Pyrowolakis, G., Affolter, M. and Basler, K. (2003). Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient. Cell 113, 221-233.
29. O'Neill, E. M., Rebay, I., Tjian, R. and Rubin, G. M. (1994). The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78, 137-147.
30. Ohlmeyer, J. T. and Kalderon, D. (1998). Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature 396, 749-753.
31. Rebay, I. and Rubin, G. M. (1995). Yan functions as a general inhibitor of differentiation and is negatively regulated by activation of the Ras1/MAPK pathway. Cell 81, 857-866.
32. Reich, A., Sapir, A. and Shilo, B. (1999). Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 126, 4139-4147.
33. Rogers, E. M., Brennan, C. A., Mortimer, N. T., Cook, S., Morris, A. R. and Moses, K. (2005). Pointed regulates an eye-specific transcriptional enhancer in the Drosophila hedgehog gene, which is required for the movement of the morphogenetic furrow. Development 132, 4833-4843.
34. Samakovlis, C., Hacohen, N., Manning, G., Sutherland, D. C., Guillemin, K. and Krasnow, M. A. (1996). Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122, 1395-1407.
35. Scholz, H., Deatrick, J., Klaes, A. and Klämbt, C. (1993). Genetic dissection of pointed, a Drosophila gene encoding two ETS-related proteins. Genetics 135, 455-468.
36. Tio, M. and Moses, K. (1997). The Drosophila TGF alpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124, 343-351.
37. Tweedie, S., Ashburner, M., Falls, K., Leyland, P., McQuilton, P., Marygold, S., Millburn, G., Osumi-Sutherland, D., Schroeder, A., Seal, R. et al.; FlyBase Consortium (2009). FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res. 37 Database issue, D555-D559.
38. Yang, L. and Baker, N. E. (2001). Role of the EGFR/Ras/Raf pathway in specification of photoreceptor cells in the Drosophila retina. Development 128, 1183-1191.
39. Yang, L. and Baker, N. E. (2003). Cell cycle withdrawal, progression, and cell survival regulation by EGFR and its effectors in the differentiating Drosophila eye. Dev. Cell 4, 359-369.
40. Yogev, S., Schejter, E. D. and Shilo, B. Z. (2008). Drosophila EGFR signalling is modulated by differential compartmentalization of Rhomboid intramembrane proteases. EMBO J. 27, 1219-1230.
41. Yordy, J. S. and Muise-Helmericks, R. C. (2000). Signal transduction and the Ets family of transcription factors. Oncogene 19, 6503-6513.
42. Zhu, S., Barshow, S., Wildonger, J., Jan, L. Y. and Jan, Y. N. (2011). Ets transcription factor Pointed promotes the generation of intermediate neural progenitors in Drosophila larval brains. Proc. Natl. Acad. Sci. USA 108, 20615-20620.
43. zur Lage, P. and Jarman, A. P. (1999). Antagonism of EGFR and notch signalling in the reiterative recruitment of Drosophila adult chordotonal sense organ precursors. Development 126, 3149-3157.
44. zur Lage, P. I., Powell, L. M., Prentice, D. R., McLaughlin, P. and Jarman, A. P. (2004). EGF receptor signaling triggers recruitment of Drosophila sense organ precursors by stimulating proneural gene autoregulation. Dev. Cell 7, 687-696.