Concomitant requirement for Notch and Jak/Stat signaling during neuro-epithelial differentiation in the Drosophila optic lobe

Ngo, Kathy T.; Wang, Jay; Junker, Markus; Kriz, Steve; Vo, Gloria; Asem, Bobby; Olson, John M.; Banerjee, Utpal; Hartenstein, Volker

doi:10.1016/j.ydbio.2010.07.036

Cited by 71 publications

(94 citation statements)

References 76 publications

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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%

“…The JAK/STAT pathway is active in the optic lobe (Yasugi et al 2008;Ngo et al 2010;Wang et al 2011a). Overexpression of upd or hop Tum-l , which encodes an activated JAK kinase (Harrison et al 1995;Luo et al 1995), results in neuroepithelial overgrowth whereas loss of hop activity leads to an early depletion of NEs and a small brain lobe (Figure 1, E and F;Wang et al 2011a).…”

Section: Whole-genome Analyses Of Jak/stat Targets In the Drosophila mentioning

confidence: 99%

“…The JAK/STAT pathway plays a wide range of roles in Drosophila development, including embryonic segmentation, blood cell proliferation and differentiation, eye growth and polarity determination, heart development, border cell migration and stalk cell specification in the ovary, stem cell self-renewal in the testis and intestine, long-term memory formation, and circadian behavior (Arbouzova and Zeidler 2006;Jiang et al 2009;Liu et al 2010;Copf et al 2011;Johnson et al 2011;Xu et al 2011;Luo and Sehgal 2012). Recent studies also indicated that the JAK/STAT pathway is required for the development of the larval optic lobe (Yasugi et al 2008;Ngo et al 2010;Wang et al 2011a).…”

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confidence: 99%

“…The maintenance of neuroepithelial stem cells and their differentiation into asymmetrically dividing progenitors must be tightly regulated. In JAK mutant brains, the NEs cannot be maintained and prematurely differentiate into medulla NBs, resulting in severe defects in lamina and medulla development (Yasugi et al 2008;Ngo et al 2010;Wang et al 2011a). It is not well understood how the JAK/STAT pathway regulates neuroepithelial maintenance/expansion and the differentiation from NE to NB.…”

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confidence: 99%

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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%

Section: Whole-genome Analyses Of Jak/stat Targets In the Drosophila mentioning

confidence: 99%

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confidence: 99%

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

et al. 2013

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“…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%

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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Concomitant requirement for Notch and Jak/Stat signaling during neuro-epithelial differentiation in the Drosophila optic lobe

Cited by 71 publications

References 76 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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