argos is required for projection of photoreceptor axons during optic lobe development in Drosophila

Sawamoto, Kazunobu; Okabe, Masataka; Tanimura, Teiichi; Hayashi, Shigeo; Mikoshiba, Katsuhiko

doi:10.1002/(sici)1097-0177(199602)205:2<162::aid-aja7>3.0.co;2-g

Cited by 10 publications

(3 citation statements)

References 47 publications

(68 reference statements)

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“…1C). We searched for genes that might promote the proneural wave and focused on the EGFR signal, because it was reported that the projections of photoreceptor axons (R axons) were disorganized in optic lobes of aos mutants, a gene encoding an antagonist of the EGFR signaling pathway (Sawamoto et al, 1996). Relative to wild-type flies, the number of Dpn-expressing medulla neuroblasts…”

Section: Resultsmentioning

confidence: 99%

“…The Janus kinase/Signal transducer and activator of transcription (JAK/STAT) pathway is activated in lateral neuroepithelial cells and negatively regulates proneural wave progression (Yasugi et al, 2008). We also studied the role of the EGFR and Notch signaling pathways in proneural wave progression because the impairment of the pathways has previously been suggested to cause abnormal optic lobe development (Sawamoto et al, 1996;Toriya et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Coordinated sequential action of EGFR and Notch signaling pathways regulates proneural wave progression in theDrosophilaoptic lobe

et al. 2010

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SUMMARYDuring neurogenesis in the medulla of the Drosophila optic lobe, neuroepithelial cells are programmed to differentiate into neuroblasts at the medial edge of the developing optic lobe. The wave of differentiation progresses synchronously in a row of cells from medial to the lateral regions of the optic lobe, sweeping across the entire neuroepithelial sheet; it is preceded by the transient expression of the proneural gene lethal of scute [l(1)sc] and is thus called the proneural wave. We found that the epidermal growth factor receptor (EGFR) signaling pathway promotes proneural wave progression. EGFR signaling is activated in neuroepithelial cells and induces l(1)sc expression. EGFR activation is regulated by transient expression of Rhomboid (Rho), which is required for the maturation of the EGF ligand Spitz. Rho expression is also regulated by the EGFR signal. The transient and spatially restricted expression of Rho generates sequential activation of EGFR signaling and assures the directional progression of the differentiation wave. This study also provides new insights into the role of Notch signaling. Expression of the Notch ligand Delta is induced by EGFR, and Notch signaling prolongs the proneural state. Notch signaling activity is downregulated by its own feedback mechanism that permits cells at proneural states to subsequently develop into neuroblasts. Thus, coordinated sequential action of the EGFR and Notch signaling pathways causes the proneural wave to progress and induce neuroblast formation in a precisely ordered manner.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Coordinated sequential action of EGFR and Notch signaling pathways regulates proneural wave progression in theDrosophilaoptic lobe

et al. 2010

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“…Aos is the first reported extracellular factor shown to inhibit an RTK (54). Genetic interactions between Aos and members of the DER signaling pathway have indicated that Aos functions as an inhibitor of the DER signaling pathway to repress cell fate determination during eye, wing, and chordotonal organ development (37,38,(45)(46)(47)54). Aos overexpression induces programmed cell death in the developing eye by inhibiting the DER/Ras pathway (48).…”

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The Interaction between the Drosophila Secreted Protein Argos and the Epidermal Growth Factor Receptor Inhibits Dimerization of the Receptor and Binding of Secreted Spitz to the Receptor

Jin

Sawamoto

Ito

et al. 2000

Molecular and Cellular Biology

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Drosophila Argos (Aos), a secreted protein with an epidermal growth factor (EGF)-like domain, has been shown to inhibit the activation of the Drosophila EGF receptor (DER). However, it has not been determined whether Aos binds directly to DER or whether regulation of the DER activation occurs through some other mechanism. Using DER-expressing cells (DER/S2) and a recombinant DER extracellular domain-Fc fusion protein (DER-Fc), we have shown that Aos binds directly to the extracellular domain of DER with its carboxyl-terminal region, including the EGF-like domain. Furthermore, Aos can block the binding of secreted Spitz (sSpi), a transforming growth factor ␣-like ligand of DER, to the extracellular domain of DER. We observed that sSpi stimulates the dimerization of both the soluble DER extracellular domain (sDER) and the intact DER in the DER/S2 cells and that Aos can block the sSpi-induced dimerization of both sDER and intact DER. Moreover, we have shown that, by directly interacting with DER, Aos and SpiAos (a chimeric protein that is composed of the N-terminal region of Spi and the C-terminal region of Aos) inhibit the dimerization and phosphorylation of DER that are induced by DER's overexpression in the absence of sSpi. These results indicate that Aos exerts its inhibitory function through dual molecular mechanisms: by blocking both the receptor dimerization and the binding of activating ligand to the receptor. This is the first description of this novel inhibitory mechanism for receptor tyrosine kinases.The epidermal growth factor (EGF) receptor (EGFR) is a member of the ErbB family of receptor tyrosine kinases (RTKs), which are composed of an extracellular domain, a transmembrane region, and a cytoplasmic domain, which includes a tyrosine kinase domain (5, 20) (see Fig. 1A). The binding of EGF to its receptor induces conformational changes in the extracellular domain (18), resulting in rapid dimerization of the receptor (3,8,25). In its dimerized state, the activated tyrosine kinase phosphorylates tyrosine in the carboxyl-terminal region of the adjacent receptor through an intermolecular mechanism (23,29,57).Like its vertebrate homologues, the Drosophila EGFR (DER) mediates various inductive signaling events in several tissues to regulate normal development (1,42,50,55). DER signaling functions principally through the Ras/mitogen-activated protein kinase (MAPK) signal transduction pathway, which is highly conserved between Drosophila and mammals (14, 40). The loss-of-function mutant phenotypes of DER indicate that DER regulates a variety of developmental processes, including the survival of embryonic ectodermal tissues, the proliferation of imaginal discs, the morphogenesis of several adult ectodermal structures, and neural differentiation (7, 55). Since DER signaling is involved in many different aspects of development, like other members of the ErbB family, its activation must be controlled precisely. Evidence from genetic and biochemical analyses indicates that both activating and inhibitory ligands reg...

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Genetical analysis ofvisual system disorganizer (vid), a new gene involved in normal development of eye and optic lobe of the brain inDrosophila melanogaster

1997

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A neuroanatomical screening of a collection of P-element mutagenized flies has been carried out with the aim of finding new mutants affecting the optic lobe of the adult brain in Drosophila melanogaster. We have identified a new gene that is involved in the development of the adult axon array in the optic ganglia and in the ommatidia assembly. We have named this locus visual system disorganizer (vid). Reversional mutagenesis demonstrated that the vid mutant was the result of a P-element insertion in the Drosophila genome and allowed us to generate independent alleles, some of which resulted in semilethality, like the vid original mutant, while the others were completely lethal. A genetic somatic mosaic analysis indicated that the vid gene is required in the eye for its normal development by inductive effects. This analysis also suggests an inductive effect of the vid gene on the distal portion of the optic lobe, particularly the lamina and the first optic chiasma. Moreover, the absence of mutant phenotype in the proximal region of the optic ganglia, including the medulla, the second optic chiasma, and the lobula complex underlying mosaic eyes, is suggestive of an autonomously acting mechanism of the vid gene in the optic lobe. The complete or partial lethality generated by different mutations at the vid locus suggests that this gene's role may not be limited to the visual system, but may also affect a vital function during Drosophila development.

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argos is required for projection of photoreceptor axons during optic lobe development in Drosophila

Cited by 10 publications

References 47 publications

Coordinated sequential action of EGFR and Notch signaling pathways regulates proneural wave progression in theDrosophilaoptic lobe

Coordinated sequential action of EGFR and Notch signaling pathways regulates proneural wave progression in theDrosophilaoptic lobe

The Interaction between the Drosophila Secreted Protein Argos and the Epidermal Growth Factor Receptor Inhibits Dimerization of the Receptor and Binding of Secreted Spitz to the Receptor

Genetical analysis ofvisual system disorganizer (vid), a new gene involved in normal development of eye and optic lobe of the brain inDrosophila melanogaster

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