Coordinated sequential action of EGFR and Notch signaling pathways regulates proneural wave progression in the<i>Drosophila</i>optic lobe

Yasugi, Tetsuo; Sugie, Atsushi; Umetsu, Daiki; Tabata, Tetsuya

doi:10.1242/dev.048058

Cited by 97 publications

(210 citation statements)

References 73 publications

(44 reference statements)

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“…E(spl)md, E(spl)m7, and Tom are direct targets of the Notch pathway (Bray 2006), while H is a transcription corepressor involved in repression of Notch signaling activity (Bang et al 1995). The Notch pathway is required for neuroepithelial maintenance and expansion (Egger et al 2010;Ngo et al 2010;Reddy et al 2010;Yasugi et al 2010;Orihara-Ono et al 2011;Wang et al 2011b;Weng et al 2012). Our microarray data support a model in which JAK/STAT acts upstream of Notch signaling in the optic lobe (Wang et al 2011a).…”

Section: Discussionsupporting

confidence: 68%

Evidence for Tissue-Specific JAK/STAT Target Genes inDrosophilaOptic Lobe Development

et al. 2013

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The evolutionarily conserved JAK/STAT pathway plays important roles in development and disease processes in humans. Although the signaling process has been well established, we know relatively little about what the relevant target genes are that mediate JAK/STAT activation during development. Here, we have used genome-wide microarrays to identify JAK/STAT targets in the optic lobes of the Drosophila brain and identified 47 genes that are positively regulated by JAK/STAT. About two-thirds of the genes encode proteins that have orthologs in humans. The STAT targets in the optic lobe appear to be different from the targets identified in other tissues, suggesting that JAK/STAT signaling may regulate different target genes in a tissue-specific manner. Functional analysis of Nop56, a cell-autonomous STAT target, revealed an essential role for this gene in the growth and proliferation of neuroepithelial stem cells in the optic lobe and an inhibitory role in lamina neurogenesis.

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Section: Discussionsupporting

confidence: 68%

Evidence for Tissue-Specific JAK/STAT Target Genes inDrosophilaOptic Lobe Development

et al. 2013

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“…Notch signaling is required to regulate the progression of the proneural wave (Egger et al, 2010;Ngo et al, 2010;Reddy et al, 2010;Wang et al, 2011;Weng et al, 2012;Yasugi et al, 2010). Given that Cno and Notch functionally interact in other systems (Carmena et al, 2006;Miyamoto et al, 1995) and that cno mutant phenotypes were very reminiscent of those previously described for Notch mutants in the neuroepithelium (Yasugi et al, 2010), we decided to analyze the relative localization of Cno and Notch in the optic lobe.…”

Section: Cno Colocalizes With Notch At the Ajs Of Ne Cellsmentioning

confidence: 99%

“…Differentiation of NE cells to medulla NBs progresses from the medial to the lateral edge of the OPC in a 'proneural wave', which was recently identified by the transient and local expression at the wave front of the proneural gene lethal of scute (l9sc) (Yasugi et al, 2008). Over the past few years multiple signaling pathways have proved to be essential for regulating the proneural wave progression within the neuroepithelium in a tissue-autonomous way, including Notch, JAK-STAT, EGFRRas-PointedP1 (PntP1) and Fat-Hippo signaling pathways (Egger et al, 2010;Ngo et al, 2010;Reddy et al, 2010;Yasugi et al, 2010;Yasugi et al, 2008). However, not much is known about non-autonomous regulatory mechanisms.…”

Section: Introductionmentioning

confidence: 99%

“…In addition, Cno acts as an integration hub of different signaling pathways, including Ras and Notch during muscle and heart progenitor specification (Carmena et al, 2006). The Ras pathway triggered by the EGFR ultimately activates the ETS transcription factor Pnt that exists in two isoforms, PntP1 and PntP2, the former acting in the optic lobe (Klämbt, 1993;Yasugi et al, 2010). PntP1 is very locally activated at the transition zone, where, in turn, it induces the local expression of L9sc (Yasugi et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…The Ras pathway triggered by the EGFR ultimately activates the ETS transcription factor Pnt that exists in two isoforms, PntP1 and PntP2, the former acting in the optic lobe (Klämbt, 1993;Yasugi et al, 2010). PntP1 is very locally activated at the transition zone, where, in turn, it induces the local expression of L9sc (Yasugi et al, 2010). The Notch receptor is activated by two different ligands, Delta (Dl) and Serrate (Ser), which trigger the proteolytic cleavage of the intracellular domain of Notch.…”

Section: Introductionmentioning

confidence: 99%

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A Serrate-Notch-Canoe complex mediates glial-neuroepithelial cell interactions essential during Drosophila optic lobe development

Pérez-Gómez

Slováková

Rives-Quinto

et al. 2013

Journal of Cell Science

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It is firmly established that neuron-glia interactions are fundamental across species for the correct establishment of a functional brain. Here, we found that the glia of the Drosophila larval brain display an essential non-autonomous role during the development of the optic lobe. The optic lobe develops from neuroepithelial cells that proliferate by dividing symmetrically until they switch to asymmetric/differentiative divisions generating neuroblasts. The proneural gene lethal of scute (l'sc) is transiently activated by the Epidermal Growth Factor Receptor (EGFR)/Ras signal transduction pathway at the leading edge of a proneural wave that sweeps from medial to lateral neuroepithelium promoting this switch. This process is tightly regulated by the tissue-autonomous function within the neuroepithelium of multiple signaling pathways, including EGFR/Ras and Notch. This study shows that the Notch ligand Serrate (Ser) is expressed in the glia and it forms a complex in vivo with Notch and Canoe, which colocalize at the adherens junctions of neuroepithelial cells. This complex is crucial for glial-neuroepithelial cell interactions during optic lobe development. Ser is tissue-autonomously required in the glia where it activates Notch to regulate its proliferation, and non-autonomously in the neuroepithelium where Ser induces Notch signaling to avoid the premature activation of the EGFR/Ras pathway and hence of L'sc. Interestingly, different Notch activity reporters showed very different expression patterns in the glia and in the neuroepithelium, suggesting the existence of tissue-specific factors that promote the expression of particular Notch target genes or/and a reporter response dependent on different thresholds of Notch signaling.

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Programmed cell death acts at different stages of Drosophila neurodevelopment to shape the central nervous system

2016

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Edited by Wilhelm JustNervous system development is a process that integrates cell proliferation, differentiation, and programmed cell death (PCD). PCD is an evolutionary conserved mechanism and a fundamental developmental process by which the final cell number in a nervous system is established. In vertebrates and invertebrates, PCD can be determined intrinsically by cell lineage and age, as well as extrinsically by nutritional, metabolic, and hormonal states. Drosophila has been an instrumental model for understanding how this mechanism is regulated. We review the role of PCD in Drosophila central nervous system development from neural progenitors to neurons, its molecular mechanism and function, how it is regulated and implemented, and how it ultimately shapes the fly central nervous system from the embryo to the adult. Finally, we discuss ideas that emerged while integrating this information.Keywords: apoptosis; Drosophila; neurodevelopment Apoptosis shapes Drosophila neural development from the emergence of neuroectoderm in the embryo to the eclosing adult. The earliest indication of programmed cell death (PCD) during neurodevelopment is at embryonic stages 11-12 [1-3], when the first neurons and epidermal cells die [4,5]. Neuronal apoptosis then increases dramatically peaking at embryonic stages 16-17, when the ventral nerve cord (VNC) condenses [3] and the embryo produces its first twitching movements [1]. Although the observed amount of neuronal death differs from embryo to embryo [5], symmetry in neuronal PCD is often observed between the right and left sides of a single embryo [1], indicating that both deterministic and 'random' processes participate in the selection of surviving neurons.Programmed cell death in Drosophila neural development comes in different flavors. It can be triggered by spatial, temporal, nutritional, hormonal, and metabolic signals; it can be regulated by Hox genes, Notch, and other signaling pathways; it can be mediated by one or more proapoptotic genes; and it can act at the stage of neural precursors, of newly born or of mature neurons/glia. What is clear is that dying is not trivial for a cell. Many layers of regulation exist that ensure

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

Cited by 97 publications

References 73 publications

Evidence for Tissue-Specific JAK/STAT Target Genes inDrosophilaOptic Lobe Development

Evidence for Tissue-Specific JAK/STAT Target Genes inDrosophilaOptic Lobe Development

A Serrate-Notch-Canoe complex mediates glial-neuroepithelial cell interactions essential during Drosophila optic lobe development

Programmed cell death acts at different stages of Drosophila neurodevelopment to shape the central nervous system

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