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A Gene Expression Screen in Drosophila melanogaster Identifies Novel JAK/STAT and EGFR Targets During Oogenesis

Julia Wittes¹, Trudi Schüpbach²

¹Department of Molecular Biology, Princeton University, Princeton, NJ 08544.

G3 (Bethesda, Md.)

|November 3, 2018

Abstract:

The Janus Kinase/Signal Transducer and Activator of Transcription (JAK/STAT) and epidermal growth factor receptor (EGFR) signaling pathways are conserved regulators of tissue patterning, morphogenesis, and other cell biological processes. During Drosophila oogenesis, these pathways determine the fates of epithelial follicle cells (FCs). JAK/STAT and EGFR together specify a population of cells called the posterior follicle cells (PFCs), which signal to the oocyte to establish the embryonic axes. In this study, whole genome expression analysis was performed to identify genes activated by JAK/STAT and/or EGFR. We observed that 317 genes were transcriptionally upregulated in egg chambers with ectopic JAK/STAT and EGFR activity in the FCs. The list was enriched for genes encoding extracellular matrix (ECM) components and ECM-associated proteins. We tested 69 candidates for a role in axis establishment using RNAi knockdown in the FCs. We report that the signaling protein Semaphorin 1b becomes enriched in the PFCs in response to JAK/STAT and EGFR. We also identified ADAM metallopeptidase with thrombospondin type 1 motif A (AdamTS-A) as a novel target of JAK/STAT in the FCs that regulates egg chamber shape. AdamTS-A mRNA becomes enriched at the anterior and posterior poles of the egg chamber at stages 6 to 7 and is regulated by JAK/STAT. Altering AdamTS-A expression in the poles or middle of the egg chamber produces rounder egg chambers. We propose that AdamTS-A regulates egg shape by remodeling the basement membrane.

Insights

The Janus Kinase/Signal Transducer and Activator of Transcription (JAK/STAT) and epidermal growth factor receptor (EGFR) pathways regulate cell fates during Drosophila oogenesis. This study identified novel genes, including AdamTS-A, involved in egg chamber shape and axis establishment.

Area of Science:

Developmental Biology
Cell Signaling
Genomics

Background:

Janus Kinase/Signal Transducer and Activator of Transcription (JAK/STAT) and epidermal growth factor receptor (EGFR) pathways are crucial for tissue patterning and cell fate determination.
During Drosophila oogenesis, these pathways specify posterior follicle cells (PFCs) essential for embryonic axis establishment.

Purpose of the Study:

To identify genes regulated by JAK/STAT and/or EGFR signaling in Drosophila follicle cells.
To investigate the role of identified genes in axis establishment and egg chamber morphogenesis.

Main Methods:

Whole genome expression analysis to identify upregulated genes.
RNA interference (RNAi) knockdown to test candidate genes.
Localization studies to determine protein and mRNA enrichment.

Main Results:

317 genes were upregulated by ectopic JAK/STAT and EGFR activity, enriched for extracellular matrix (ECM) components.
Semaphorin 1b was identified as a signaling protein enriched in PFCs.
ADAM metallopeptidase with thrombospondin type 1 motif A (AdamTS-A) was identified as a novel JAK/STAT target regulating egg chamber shape, with its mRNA enriched at egg chamber poles.

Conclusions:

JAK/STAT and EGFR signaling pathways coordinately regulate gene expression in follicle cells, impacting axis establishment and egg chamber morphology.
AdamTS-A plays a role in regulating egg chamber shape, potentially through basement membrane remodeling.
This study provides insights into the molecular mechanisms governing oogenesis and embryonic axis formation in Drosophila.

Read full analysis

Keywords:

AdamTS-A Drosophila EGFR JAK/STAT Sema1b oogenesis

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