Competition between SOCS36E and Drk modulates sevenless receptor tyrosine kinase activity

Journal of Cell Science

Volumn 123, Issue 22, 2010, Pages 3857-3862

  Almudi, Isabel ^a   Corominas, Montserrat ^a   Serras, Florenci ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Receptor regulation; Sevenless; SOCS36E

Indexed keywords

ADAPTOR PROTEIN; DOWNSTREAM OF RECEPTOR KINASE; PROTEIN SEVENLESS; PROTEIN TYROSINE KINASE; SUPPRESSOR OF CYTOKINE SIGNALING; SUPPRESSOR OF CYTOKINE SIGNALING 36E; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING COMPETITION; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; INSECT CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSFECTION;

DROSOPHILA MELANOGASTER; MAMMALIA;

EID: 78649753400     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.071134     Document Type: Article

References (41)

1. Almudi, I., Stocker, H., Hafen, E., Corominas, M. and Serras, F. (2009). SOCS36E specifically interferes with Sevenless signaling during Drosophila eye development. Dev. Biol. 326, 212-223.
2. Bache, K. G., Slagsvold, T. and Stenmark, H. (2004). Defective downregulation of receptor tyrosine kinases in cancer. EMBO J. 23, 2707-2712. (Pubitemid 39013543)
3. Baetz, A., Frey, M., Heeg, K. and Dalpke, A. H. (2004). Suppressor of cytokine signaling (SOCS) proteins indirectly regulate toll-like receptor signaling in innate immune cells. J. Biol. Chem. 279, 54708-54715.
4. Banerjee, U., Renfranz, P. J., Pollock, J. A. and Benzer, S. (1987). Molecular characterization and expression of sevenless, a gene involved in neuronal pattern formation in the Drosophila eye. Cell 49, 281-291.
5. Basler, K., Christen, B. and Hafen, E. (1991). Ligand-independent activation of the Sevenless receptor tyrosine kinase changes the fate of cells in the developing Drosophila eye. Cell 64, 1069-1081. (Pubitemid 121001194)
6. Beltran, S., Angulo, M., Pignatelli, M., Serras, F. and Corominas, M. (2007). Functional dissection of the ash2 and ash1 transcriptomes provides insights into the transcriptional basis of wing phenotypes and reveals conserved protein interactions. Genome Biol. 8, R67. (Pubitemid 351859195)
7. Biggs, W. H., 3rd, Zavitz, K. H., Dickson, B., van der Straten, A., Brunner, D., Hafen, E. and Zipursky, S. L. (1994). The Drosophila rolled locus encodes a MAP kinase required in the sevenless signal transduction pathway. EMBO J. 13, 1628-1635.
8. Blume-Jensen, P. and Hunter, T. (2001). Oncogenic kinase signalling. Nature 411, 355-365.
9. Cagan, R. L., Kramer, H., Hart, A. C. and Zipursky, S. L. (1992). The Bride of Sevenless and Sevenless interaction: internalization of a transmembrane ligand. Cell 69, 393-399.
10. Callus, B. A. and Mathey-Prevot, B. (2002). SOCS36E, a novel Drosophila SOCS protein, suppresses JAK/STAT and EGF-R signalling in the imaginal wing disc. Oncogene 21, 4812-4821.
11. Campbell, R. E., Tour, O., Palmer, A. E., Steinbach, P. A., Baird, G. S., Zacharias, D. A. and Tsien, R. Y. (2002). A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 7877-7882.
12. Choi, Y. B., Son, M., Park, M., Shin, J. and Yun, Y. (2010). SOCS-6 negatively regulates T cell activation through targeting p56LCK to proteasomal degradation. J. Biol. Chem. 285, 7271-7280.
13. Ciruela, F. (2008). Fluorescence-based methods in the study of protein-protein interactions in living cells. Curr. Opin. Biotechnol. 19, 338-343.
14. Endo, T. A., Masuhara, M., Yokouchi, M., Suzuki, R., Sakamoto, H., Mitsui, K., Matsumoto, A., Tanimura, S., Ohtsubo, M., Misawa, H. et al. (1997). A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387, 921-924.
15. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651-660.
16. Galperin, E., Verkhusha, V. V. and Sorkin, A. (2004). Three-chromophore FRET microscopy to analyze multiprotein interactions in living cells. Nat. Methods 1, 209-217.
17. Gordon, G. W., Berry, G., Liang, X. H., Levine, B. and Herman, B. (1998). Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys. J. 74, 2702-2713. (Pubitemid 28225264)
18. Hafen, E., Basler, K., Edstroem, J. E. and Rubin, G. M. (1987). Sevenless, a cell-specific homeotic gene of Drosophila, encodes a putative transmembrane receptor with a tyrosine kinase domain. Science 236, 55-63.
19. Hart, A. C., Kramer, H., Van Vactor, D. L., Jr, Paidhungat, M. and Zipursky, S. L. (1990). Induction of cell fate in the Drosophila retina: the Bride Of Sevenless protein is predicted to contain a large extracellular domain and seven transmembrane segments. Genes Dev. 4, 1835-1847.
20. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
21. Hilton, D. J., Richardson, R. T., Alexander, W. S., Viney, E. M., Willson, T. A., Sprigg, N. S., Starr, R., Nicholson, S. E., Metcalf, D. and Nicola, N. A. (1998). Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc. Natl. Acad. Sci. USA 95, 114-119.
22. Jiang, X. and Sorkin, A. (2002). Coordinated traffic of Grb2 and Ras during epidermal growth factor receptor endocytosis visualized in living cells. Mol. Biol. Cell 13, 1522-1535.
23. Kario, E., Marmor, M. D., Adamsky, K., Citri, A., Amit, I., Amariglio, N., Rechavi, G. and Yarden, Y. (2005). Suppressors of cytokine signaling 4 and 5 regulate epidermal growth factor receptor signaling. J. Biol. Chem. 280, 7038-7048. (Pubitemid 40341260)
24. Karsten, P., Häder, S. and Zeidler, M. P. (2002) Cloning and expression of Drosophila SOCS36E and its potential regulation by the JAK/STAT pathway. Mech. Dev. 117, 343-346.
25. Krebs, D. L. and Hilton, D. J. (2003). A new role for SOCS in insulin action. Suppressor of cytokine signaling. Sci. STKE 2003, PE6.
26. Nicholson, S. E., Metcalf, D., Sprigg, N. S., Columbus, R., Walker, F., Silva, A., Cary, D., Willson, T. A., Zhang, J. G., Hilton, D. J. et al. (2005). Suppressor of cytokine signaling (SOCS)-5 is a potential negative regulator of epidermal growth factor signaling. Proc. Natl. Acad. Sci. USA 102, 2328-2333.
27. Olivier, J. P., Raabe, T., Henkemeyer, M., Dickson, B., Mbamalu, G., Margolis, B., Schlessinger, J., Hafen, E. and Pawson, T. (1993). A Drosophila SH2-SH3 adaptor protein implicated in coupling the Sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73, 179-191.
28. Raabe, T., Olivier, J. P., Dickson, B., Liu, X., Gish, G. D., Pawson, T. and Hafen, E. (1995). Biochemical and genetic analysis of the Drk SH2/SH3 adaptor protein of Drosophila. EMBO J. 14, 2509-2518.
29. Rawlings, J. S., Rennebeck, G., Harrison, S. M., Xi, R. and Harrison, D. A. (2004). Two Drosophila suppressors of cytokine signaling (SOCS) differentially regulate JAK and EGFR pathway activities. BMC Cell Biol. 5, 38.
30. Reinke, R. and Zipursky, S. L. (1988). Cell-cell interaction in the Drosophila retina: the bride of sevenless gene is required in photoreceptor cell R8 for R7 cell development. Cell 55, 321-330.
31. Sese, M., Corominas, M., Stocker, H., Heino, T. I., Hafen, E. and Serras, F. (2006). The Cdi/TESK1 kinase is required for Sevenless signaling and epithelial organization in the Drosophila eye. J. Cell Sci. 119, 5047-5056.
32. Simon, M. A., Bowtell, D. D., Dodson, G. S., Laverty, T. R. and Rubin, G. M. (1991). Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67, 701-716.
33. Simon, M. A., Dodson, G. S. and Rubin, G. M. (1993). An SH3-SH2-SH3 protein is required for p21Ras1 activation and binds to Sevenless and Sos proteins in vitro. Cell 73, 169-177.
34. Sorkin, A., McClure, M., Huang, F. and Carter, R. (2000). Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr. Biol. 10, 1395-1398.
35. Starr, R., Willson, T. A., Viney, E. M., Murray, L. J., Rayner, J. R., Jenkins, B. J., Gonda, T. J., Alexander, W. S., Metcalf, D., Nicola, N. A. et al. (1997). A family of cytokine-inducible inhibitors of signalling. Nature 387, 917-921.
36. Tomlinson, A. and Ready, D. F. (1986). Sevenless: a cell-specific homeotic mutation of the Drosophila eye. Science 231, 400-402.
37. Tomlinson, A. and Ready, D. F. (1987). Cell fate in the Drosophila ommatidium. Dev. Biol. 123, 264-275.
38. Tomlinson, A., Kimmel, B. E. and Rubin, G. M. (1988). rough, a Drosophila homeobox gene required in photoreceptors R2 and R5 for inductive interactions in the developing eye. Cell 55, 771-784.
39. van der Krogt, G. N., Ogink, J., Ponsioen, B. and Jalink, K. (2008). A comparison of donor-acceptor pairs for genetically encoded FRET sensors: application to the Epac cAMP sensor as an example. PLoS ONE 3, e1916.
40. Yoshimura, A., Ohkubo, T., Kiguchi, T., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., Hara, T. and Miyajima, A. (1995). A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J. 14, 2816-2826.
41. Zhang, J. G., Farley, A., Nicholson, S. E., Willson, T. A., Zugaro, L. M., Simpson, R. J., Moritz, R. L., Cary, D., Richardson, R., Hausmann, G. et al. (1999). The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc. Natl. Acad. Sci. USA 96, 2071-2076.