The Drosophila Arf GEF Steppke controls MAPK activation in EGFR signaling

Journal of Cell Science

Volumn 126, Issue 11, 2013, Pages 2470-2479

  Hahn, Ines ^a   Fuss, Bernhard ^a   Peters, Annika ^a   Werner, Tamara ^a   Sieberg, Andrea ^a   Gosejacob, Dominic ^a   Hoch, Michael ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Arf GEF Steppke; Drosophila; EGFR signalling; MAP kinase; RAS

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; COMPLEMENTARY DNA; CYTOHESIN 1; EPIDERMAL GROWTH FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; SCAFFOLD PROTEIN; VASCULOTROPIN RECEPTOR;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ADOLESCENT; ALLELE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CHEMICAL ANALYSIS; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVATION; EYE DEVELOPMENT; FORELIMB; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE LOSS; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; KNOCKOUT MOUSE; LOSS OF FUNCTION MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA INTERFERENCE; RNA ISOLATION; SIGNAL TRANSDUCTION; TRANSGENIC ORGANISM;

ARF GEF STEPPKE; DROSOPHILA; EGFR SIGNALLING; MAP KINASE; RAS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MAP KINASE SIGNALING SYSTEM; MICE; MUTATION; RECEPTORS, FIBROBLAST GROWTH FACTOR;

EID: 84880034073     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.120964     Document Type: Article

References (49)

1. Alvarez, R. H., Valero, V. and Hortobagyi, G. N. (2010). Emerging targeted therapies for breast cancer. J. Clin. Oncol. 28, 3366-3379.
2. Antonarakis, E. S., Carducci, M. A. and Eisenberger, M. A. (2010). Novel targeted therapeutics for metastatic castration-resistant prostate cancer. Cancer Lett. 291, 1-13.
3. Arndt, V., Daniel, C., Nastainczyk, W., Alberti, S. and Höhfeld, J. (2005). BAG-2 acts as an inhibitor of the chaperone-associated ubiquitin ligase CHIP. Mol. Biol. Cell 16, 5891-5900.
4. Arkenau, H.-T. (2009). Gastric cancer in the era of molecularly targeted agents: current drug development strategies. J. Cancer Res. Clin. Oncol. 135, 855-866.
5. Bauer, R., Voelzmann, A., Breiden, B., Schepers, U., Farwanah, H., Hahn, I., Eckardt, F., Sandhoff, K. and Hoch, M. (2009). Schlank, a member of the ceramide synthase family controls growth and body fat in Drosophila. EMBO J. 28, 3706-3716.
6. Becker, T., Loch, G., Beyer, M., Zinke, I., Aschenbrenner, A. C., Carrera, P., Inhester, T., Schultze, J. L. and Hoch, M. (2010). FOXO-dependent regulation of innate immune homeostasis. Nature 463, 369-373.
7. Bier, E. (2000). Drawing lines in the Drosophila wing: initiation of wing vein development. Curr. Opin. Genet. Dev. 10, 393-398.
8. Bill, A., Schmitz, A., Albertoni, B., Song, J.-N., Heukamp, L. C., Walrafen, D., Thorwirth, F., Verveer, P. J., Zimmer, S., Meffert, L. et al. (2010). Cytohesins are cytoplasmic ErbB receptor activators. Cell 143, 201-211.
9. Blair, S. S. (2007). Wing vein patterning in Drosophila and the analysis of intercellular signaling. Annu. Rev. Cell Dev. Biol. 23, 293-319.
10. Böhni, R., Riesgo-Escovar, J., Oldham, S., Brogiolo, W., Stocker, H., Andruss, B. F., Beckingham, K. and Hafen, E. (1999). Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97, 865-875.
11. Britton, J. S., Lockwood, W. K., Li, L., Cohen, S. M. and Edgar, B. A. (2002). Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2, 239-249.
12. Brogiolo, W., Stocker, H., Ikeya, T., Rintelen, F., Fernandez, R. and Hafen, E. (2001). An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11, 213-221.
13. Brunet, A., Roux, D., Lenormand, P., Dowd, S., Keyse, S. and Pouysségur, J. (1999). Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J. 18, 664-674.
14. Carnero, A. (2010). The PKB/AKT pathway in cancer. Curr. Pharm. Des. 16, 34-44.
15. Chen, R. H., Sarnecki, C. and Blenis, J. (1992). Nuclear localization and regulation of erk- and rsk-encoded protein kinases. Mol. Cell. Biol. 12, 915-927.
16. Clapéron, A. and Therrien, M. (2007). KSR and CNK: two scaffolds regulating RASmediated RAF activation. Oncogene 26, 3143-3158.
17. Cobb, M. H. and Goldsmith, E. J. (2000). Dimerization in MAP-kinase signaling. Trends Biochem. Sci. 25, 7-9.
18. De Celis, J. F. (2003). Pattern formation in the Drosophila wing: The development of the veins. Bioessays 25, 443-451.
19. Dietzl, G., Chen, D., Schnorrer, F., Su, K.-C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S. et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
20. Douziech, M., Roy, F., Laberge, G., Lefrançois, M., Armengod, A.-V. and Therrien, M. (2003). Bimodal regulation of RAF by CNK in Drosophila. EMBO J. 22, 5068-5078.
21. Douziech, M., Sahmi, M., Laberge, G. and Therrien, M. (2006). A KSR/CNK complex mediated by HYP, a novel SAM domain-containing protein, regulates RASdependent RAF activation in Drosophila. Genes Dev. 20, 807-819.
22. Fuss, B., Becker, T., Zinke, I. and Hoch, M. (2006). The cytohesin Steppke is essential for insulin signalling in Drosophila. Nature 444, 945-948.
23. 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.
24. Gaengel, K. and Mlodzik, M. (2003). Egfr signaling regulates ommatidial rotation and cell motility in the Drosophila eye via MAPK/Pnt signaling and the Ras effector Canoe/AF6. Development 130, 5413-5423.
25. Hafner, M., Schmitz, A., Grüne, I., Srivatsan, S. G., Paul, B., Kolanus, W., Quast, T., Kremmer, E., Bauer, I. and Famulok, M. (2006). Inhibition of cytohesins by SecinH3 leads to hepatic insulin resistance. Nature 444, 941-944.
26. Huang, J., Zhou, W., Watson, A. M., Jan, Y.-N. and Hong, Y. (2008). Efficient endsout gene targeting in Drosophila. Genetics 180, 703-707.
27. Jünger, M. A., Rintelen, F., Stocker, H., Wasserman, J. D., Végh, M., Radimerski, T., Greenberg, M. E. and Hafen, E. (2003). The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J. Biol. 2, 20.
28. 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.
29. Kolanus, W. (2007). Guanine nucleotide exchange factors of the cytohesin family and their roles in signal transduction. Immunol. Rev. 218, 102-113.
30. Laberge, G., Douziech, M. and Therrien, M. (2005). Src42 binding activity regulates Drosophila RAF by a novel CNK-dependent derepression mechanism. EMBO J. 24, 487-498.
31. Lenormand, P., Brondello, J. M., Brunet, A. and Pouysségur, J. (1998). Growth factor-induced p42/p44 MAPK nuclear translocation and retention requires both MAPK activation and neosynthesis of nuclear anchoring proteins. J. Cell Biol. 142, 625-633.
32. Lim, J., Zhou, M., Veenstra, T. D. and Morrison, D. K. (2010). The CNK1 scaffold binds cytohesins and promotes insulin pathway signaling. Genes Dev. 24, 1496-1506.
33. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
34. Mannell, H. K., Pircher, J., Chaudhry, D. I., Alig, S. K. C., Koch, E. G., Mettler, R., Pohl, U. and Krötz, F. (2012). ARNO regulates VEGF-dependent tissue responses by stabilizing endothelial VEGFR-2 surface expression. Cardiovasc. Res. 93, 111-119.
35. Martín-Blanco, E., Roch, F., Noll, E., Baonza, A., Duffy, J. B. and Perrimon, N. (1999). A temporal switch in DER signaling controls the specification and differentiation of veins and interveins in the Drosophila wing. Development 126, 5739-5747.
36. McNeill, H., Craig, G. M. and Bateman, J. M. (2008). Regulation of neurogenesis and epidermal growth factor receptor signaling by the insulin receptor/target of rapamycin pathway in Drosophila. Genetics 179, 843-853.
37. Rajakulendran, T., Sahmi, M., Kurinov, I., Tyers, M., Therrien, M. and Sicheri, F. (2008). CNK and HYP form a discrete dimer by their SAM domains to mediate RAF kinase signaling. Prxoc. Natl. Acad. Sci. USA 105, 2836-2841.
38. Rong, Y. S. and Golic, K. G. (2001). A targeted gene knockout in Drosophila. Genetics 157, 1307-1312.
39. Roy, F., Laberge, G., Douziech, M., Ferland-McCollough, D. and Therrien, M. (2002). KSR is a scaffold required for activation of the ERK/MAPK module. Genes Dev. 16, 427-438.
40. Schlessinger, J. (2004). Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 306, 1506-1507.
41. Simpson, P. (2007). The stars and stripes of animal bodies: evolution of regulatory elements mediating pigment and bristle patterns in Drosophila. Trends Genet. 23, 350-358.
42. Tabata, T., Schwartz, C., Gustavson, E., Ali, Z. and Kornberg, T. B. (1995). Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development 121, 3359-3369.
43. Teleman, A. A. (2010). Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochem. J. 425, 13-26.
44. Therrien, M., Wong, A. M. and Rubin, G. M. (1998). CNK, a RAF-binding multidomain protein required for RAS signaling. Cell 95, 343-353.
45. Voelzmann, A. and Bauer, R. (2011). Embryonic expression of Drosophila ceramide synthase schlank in developing gut, CNS and PNS. Gene Expr. Patterns 11, 501-510.
46. Wasserman, J. D. and Freeman, M. (1997). Control of EGF receptor activation in Drosophila. Trends Cell Biol. 7, 431-436.
47. Wasserman, J. D. and Freeman, M. (1998). An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell 95, 355-364.
48. Witte, H. T., Jeibmann, A., Klämbt, C. and Paulus, W. (2009). Modeling glioma growth and invasion in Drosophila melanogaster. Neoplasia 11, 882-888.
49. Yoshida, H., Kwon, E., Hirose, F., Otsuki, K., Yamada, M. and Yamaguchi, M. (2004). DREF is required for EGFR signalling during Drosophila wing vein development. Genes Cells 9, 935-944.