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The position and function of the Notch-mediated eye growth organizer: the roles of JAK/STAT and four-jointed.

ABSTRACT: In many animal systems, the local activation of patterning signals in spatially confined regions (organizers) is crucial for promoting the growth of developing organs. Nevertheless, how organizers are set up and how their activity influences global organ growth remains poorly understood. In the Drosophila eye, local Notch activation establishes a conserved dorsal-ventral organizer that promotes growth. The dorsal selector Iroquois complex defines the position of the organizer at the mid-first instar, and through its ligand, unpaired, the Janus kinase (JAK)/signal transducers and activator of transcription (STAT) pathway is thought to mediate global growth downstream of the organizer. However, here we show that the unpaired/JAK/STAT pathway is actually a fundamental element in the spatial control of the organizer, upstream from Notch activation. Furthermore, we identify four-jointed, a target of the Fat and Hippo tumour-suppressor pathways, as a mediator of the growth controlled by the organizer. These findings redefine the process of organizer formation and function, and they identify four-jointed as a regulatory node, integrating multiple growth-control pathways.

SUBMITTER: Gutierrez-Avino FJ

PROVIDER: S-EPMC2750068 | biostudies-literature | 2009 Sep

REPOSITORIES: biostudies-literature

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The position and function of the Notch-mediated eye growth organizer: the roles of JAK/STAT and four-jointed.

Gutierrez-Aviño Francisco Jose FJ Ferres-Marco Dolors D Dominguez Maria M

EMBO reports 20090807 9

In many animal systems, the local activation of patterning signals in spatially confined regions (organizers) is crucial for promoting the growth of developing organs. Nevertheless, how organizers are set up and how their activity influences global organ growth remains poorly understood. In the Drosophila eye, local Notch activation establishes a conserved dorsal-ventral organizer that promotes growth. The dorsal selector Iroquois complex defines the position of the organizer at the mid-first in ...[more]

PMID: 19662079

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Project description:To gain a comprehensive view of the changes in host gene expression underlying Zika virus (ZIKV) pathogenesis, we performed whole-genome RNA sequencing (RNA-seq) of ZIKV-infected Drosophila adult flies. RNA-seq analysis revealed that ZIKV infection alters several and diverse biological processes, including stress, locomotion, lipid metabolism, imaginal disc morphogenesis and regulation of JAK/STAT signaling. To explore the interaction between ZIKV infection and JAK/STAT signaling regulation, we generated genetic constructs overexpressing ZIKV-specific non-structural proteins NS2A, NS2B, NS4A and NS4B. We found that ectopic expression of non-structural proteins in the developing Drosophila eye significantly restricts growth of the larval and adult eye and correlates with considerable repression of the in vivo JAK/STAT reporter, 10XStat92E-GFP At the cellular level, eye growth defects are associated with reduced rate of proliferation without affecting the overall rate of apoptosis. In addition, ZIKV NS4A genetically interacts with the JAK/STAT signaling components; co-expression of NS4A along with the dominant-negative form of domeless or StatRNAi results in aggravated reduction in eye size, while co-expression of NS4A in HopTuml (also known as hopTum ) mutant background partially rescues the h o p-induced eye overgrowth phenotype. The function of ZIKV NS4A in regulating growth is maintained in the wing, where ZIKV NS4A overexpression in the pouch domain results in reduced growth linked with diminished expression of Notch targets, Wingless (Wg) and Cut, and the Notch reporter, NRE-GFP Thus, our study provides evidence that ZIKV infection in Drosophila results in restricted growth of the developing eye and wing, wherein eye phenotype is induced through regulation of JAK/STAT signaling, whereas restricted wing growth is induced through regulation of Notch signaling. The interaction of ZIKV non-structural proteins with the conserved host signaling pathways further advance our understanding of ZIKV-induced pathogenesis.This article has an associated First Person interview with the first author of the paper.

Dataset Information

The position and function of the Notch-mediated eye growth organizer: the roles of JAK/STAT and four-jointed.

Publications

The position and function of the Notch-mediated eye growth organizer: the roles of JAK/STAT and four-jointed.

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