Antagonistic feedback loops involving rau and sprouty in the drosophila eye control neuronal and glial differentiation

Science Signaling

Volumn 6, Issue 300, 2013, Pages

  Sieglitz, Florian ^a   Matzat, Till ^a   Yuva Adyemir, Yeliz ^b   Neuert, Helen ^a   Altenhein, Benjamin ^c   Klämbt, Christian ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; GUANOSINE TRIPHOSPHATE; PROTEIN; RAS PROTEIN; RAU PROTEIN; SPROUTY PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EYE DEVELOPMENT; FEEDBACK SYSTEM; GLIA; GLIA CELL; NEGATIVE FEEDBACK; NERVE CELL DIFFERENTIATION; NONHUMAN; PDZ DOMAIN; PHENOTYPE; PHOTORECEPTOR; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA NERVE CELL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84888156818     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004651     Document Type: Article

References (57)

1. M. A. Lemmon, J. Schlessinger, Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134 (2010).
2. B. Z. Shilo, Regulating the dynamics of EGF receptor signaling in space and time. Development 132, 4017-4027 (2005).
3. K. Dorey, E. Amaya, FGF signalling: Diverse roles during early vertebrate embryogenesis. Development 137, 3731-3742 (2010).
4. M. Freeman, Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651-660 (1996).
5. J. P. Kumar, Signalling pathways in Drosophila and vertebrate retinal development. Nat. Rev. Genet. 2, 846-857 (2001).
6. J. Y. Roignant, J. E. Treisman, Pattern formation in the Drosophila eye disc. Int. J. Dev. Biol. 53, 795-804 (2009).
7. R. V. Aroian, M. Koga, J. E. Mendel, Y. Ohshima, P. W. Sternberg, The let-23 gene necessary for Caenorhabditis elegans vulval induction encodes a tyrosine kinase of the EGF receptor subfamily. Nature 348, 693-699 (1990).
8. J. P. Kumar, M. Tio, F. Hsiung, S. Akopyan, L. Gabay, R. Seger, B. Z. Shilo, K. Moses, Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125, 3875-3885 (1998).
9. M. Freeman, Cell determination strategies in the Drosophila eye. Development 124, 261-270 (1997).
10. S.R.Franzdóttir, D. Engelen, Y. Yuva-Aydemir, I. Schmidt, A. Aho, C. Klämbt, SwitchinFGF signalling initiates glial differentiation in the Drosophila eye. Nature 460, 758-761 (2009).
11. K. W. Choi, S. Benzer, Migration of glia along photoreceptor axons in the developing Drosophila eye. Neuron 12, 423-431 (1994).
12. T. Hummel, S. Attix, D. Gunning, S. L. Zipursky, Temporal control of glial cell migration in the Drosophila eye requires gilgamesh, hedgehog, and eye specification genes. Neuron 33, 193-203 (2002).
13. R. Rangarajan, Q. Gong, U. Gaul, Migration and function of glia in the developing Drosophila eye. Development 126, 3285-3292 (1999).
14. M. Silies, Y. Yuva, D. Engelen, A. Aho, T. Stork, C. Klämbt, Glial cell migration in the eye disc. J. Neurosci. 27, 13130-13139 (2007).
15. J. Schlessinger, Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 306, 1506-1507 (2004).
16. J. M. Mason, D. J. Morrison, M. A. Basson, J. D. Licht, Sprouty proteins: Multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol. 16, 45-54 (2006).
17. H. J. Kim, D. Bar-Sagi, Modulation of signalling by Sprouty: A developing story. Nat. Rev. Mol. Cell Biol. 5, 441-450 (2004).
18. S. Kramer, M. Okabe, N. Hacohen, M. A. Krasnow, Y. Hiromi, Sprouty: A common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126, 2515-2525 (1999).
19. N. Hacohen, S. Kramer, D. Sutherland, Y. Hiromi, M. A. Krasnow, sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92, 253-263 (1998).
20. G. Minowada, L. A. Jarvis, C. L. Chi, A. Neubüser, X. Sun, N. Hacohen, M. A. Krasnow, G. R. Martin, Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126, 4465-4475 (1999).
21. C. Klämbt, J. R. Jacobs, C. S. Goodman, The midline of the Drosophila central nervous system: A model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64, 801-815 (1991).
22. M. Kim, J. H. Lee, H. Koh, S. Y. Lee, C. Jang, C. J. Chung, J. H. Sung, J. Blenis, J.Chung, Inhibition of ERK-MAP kinase signaling by RSK during Drosophila development. EMBO J. 25, 3056-3067 (2006).
23. B. Altenhein, A. Becker, C. Busold, B. Beckmann, J. D. Hoheisel, G. M. Technau, Expression profiling of glial genes during Drosophila embryogenesis. Dev. Biol. 296, 545-560 (2006).
24. M. Mlodzik, Y. Hiromi, U. Weber, C. S. Goodman, G. M. Rubin, The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60, 211-224 (1990).
25. M. Iwanami, Y. Hiromi, M. Okabe, Cell-type specific utilization of multiple negative feedback loops generates developmental constancy. Genes Cells 10, 743-752 (2005).
26. G. Kalhammer, M. Bähler, F. Schmitz, J. Jöckel, C. Block, Ras-binding domains: Predicting function versus folding. FEBS Lett. 414, 599-602 (1997).
27. K. G. Guruharsha, J. F. Rual, B. Zhai, J. Mintseris, P. Vaidya, N. Vaidya, C. Beekman, C. Wong, D. Y. Rhee, O. Cenaj, E. McKillip, S. Shah, M. Stapleton, K. H. Wan, C. Yu, B. Parsa, J. W. Carlson, X. Chen, B. Kapadia, K. VijayRaghavan, S. P. Gygi, S. E. Celniker, R. A. Obar, S. Artavanis-Tsakonas, A protein complex network of Drosophila melanogaster. Cell 147, 690-703 (2011).
28. R. Avraham, Y. Yarden, Feedback regulation of EGFR signalling: Decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 12, 104-117 (2011).
29. A. Baonza, T. Casci, M. Freeman, A primary role for the epidermal growth factor receptor in ommatidial spacing in the Drosophila eye. Curr. Biol. 11, 396-404 (2001).
30. D. E. Klein, S. E. Stayrook, F. Shi, K. Narayan, M. A. Lemmon, Structural basis for EGFR ligand sequestration by Argos. Nature 453, 1271-1275 (2008).
31. M. Freeman, C.Klämbt, C. S.Goodman, G. M. Rubin, The argos gene encodes a diffusible factor that regulates cell fate decisions in the drosophila eye. Cell 69, 963-975 (1992).
32. J. D. Wasserman, M. Freeman, An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell 95, 355-364 (1998).
33. M. Golembo, R. Schweitzer, M. Freeman, B. Z. Shilo, argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 122, 223-230 (1996).
34. A. Reich, A. Sapir, B. Shilo, Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 126, 4139-4147 (1999).
35. J. J. Zartman, J. S. Kanodia, L. S. Cheung, S. Y. Shvartsman, Feedback control of the EGFR signaling gradient: Superposition of domain-splitting events in Drosophila oogenesis. Development 136, 2903-2911 (2009).
36. C. Ghiglione, K. L. Carraway III, L. T. Amundadottir, R. E. Boswell, N. Perrimon, J. B. Duffy, The transmembrane molecule kekkon 1 acts in a feedback loop to negatively regulate the activity of the Drosophila EGF receptor during oogenesis. Cell 96, 847-856 (1999).
37. M. Golembo, T. Yarnitzky, T. Volk, B. Z. Shilo, Vein expression is induced by the EGF receptor pathway to provide a positive feedback loop in patterning the Drosophila embryonic ventral ectoderm. Genes Dev. 13, 158-162 (1999).
38. A. Dutt, S. Canevascini, E. Froehli-Hoier, A. Hajnal, EGF signal propagation during C. elegans vulval development mediated by ROM-1 rhomboid. PLOSBiol. 2, e334 (2004).
39. C. P. Ponting, D. R. Benjamin, A novel family of Ras-binding domains. Trends Biochem. Sci. 21, 422-425 (1996).
40. W. Kolch, Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6, 827-837 (2005).
41. C. M. Udell, T. Rajakulendran, F. Sicheri, M. Therrien, Mechanistic principles of RAF kinase signaling. Cell. Mol. Life Sci. 68, 553-565 (2011).
42. T. Rajakulendran, M. Sahmi, M. Lefrançois, F. Sicheri, M. Therrien, A dimerizationdependent mechanism drives RAF catalytic activation. Nature 461, 542-545 (2009).
43. T. Tian, A. Harding, K. Inder, S. Plowman, R. G. Parton, J. F. Hancock, Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat. Cell Biol. 9, 905-914 (2007).
44. S. Boykevisch, C. Zhao, H. Sondermann, P. Philippidou, S. Halegoua, J. Kuriyan, D. Bar-Sagi, Regulation of Ras signaling dynamics by Sos-mediated positive feedback. Curr. Biol. 16, 2173-2179 (2006).
45. D. Brunner, K. Dücker, N. Oellers, E. Hafen, H. Scholz, C. Klämbt, The ETS domain protein Pointed-P2 is a target of MAP kinase in the Sevenless signal transduction pathway. Nature 370, 386-389 (1994).
46. C. Cabernard, M. Affolter, Distinct roles for two receptor tyrosine kinases in epithelial branching morphogenesis in Drosophila. Dev. Cell 9, 831-842 (2005).
47. L. Gabay, H. Scholz, M. Golembo, A. Klaes, B. Z. Shilo, C. Klämbt, EGF receptor signaling induces pointed P1 transcription and inactivates Yan protein in the Drosophila embryonic ventral ectoderm. Development 122, 3355-3362 (1996).
48. A. Klaes, T. Menne, A. Stollewerk, H. Scholz, C. Klämbt, The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78, 149-160 (1994).
49. J. R. Leatherbarrow, M. S. Halfon, Identification of receptor-tyrosine- kinase-signaling target genes reveals receptor-specific activities and pathway branchpoints during Drosophila development. Genetics 181, 1335-1345 (2009).
50. F. A. Pereira, M. J. Tsai, S. Y. Tsai, COUP-TF orphan nuclear receptors in development and differentiation. Cell. Mol. Life Sci. 57, 1388-1398 (2000).
51. A. Perilhou, C. Tourrel-Cuzin, I. Kharroubi, C. Henique, V. Fauveau, T. Kitamura, C. Magnan, C. Postic, C. Prip-Buus, M. Vasseur-Cognet, The transcription factor COUP-TFII is negatively regulated by insulin and glucose via Foxo1- And ChREBP-controlled pathways. Mol. Cell. Biol. 28, 6568-6579 (2008).
52. A. Wodarz, U. Hinz, M. Engelbert, E. Knust, Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67-76 (1995).
53. B. P. Lee, B. W. Jones, Transcriptional regulation of the Drosophila glial gene repo. Mech. Dev. 122, 849-862 (2005).
54. K. J. Sepp, V. J. Auld, Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151, 1093-1101 (1999).
55. J. Bischof, R. K. Maeda, M. Hediger, F. Karch, K. Basler, An optimized transgenesis system for Drosophila using germ-line-specific φC31 integrases. Proc. Natl. Acad. Sci. U.S.A. 104, 3312-3317 (2007).
56. T. Stork, D. Engelen, A. Krudewig, M. Silies, R. J. Bainton, C. Klämbt, Organization and function of the blood-brain barrier in Drosophila. J. Neurosci. 28, 587-597 (2008).
57. H. M. Fang, Y. Wang, RA domain-mediated interaction of Cdc35 with Ras1 is essential for increasing cellular cAMP level for Candida albicans hyphal development. Mol. Microbiol. 61, 484-496 (2006).