C-Fos Repression by Piwi Regulates Drosophila Ovarian Germline Formation and Tissue Morphogenesis.

Jonathon D Klein,Xiaoyang Yang,Jamy C Peng,Chunxu Qu,Yiping Fan,Chunlao Tang,Mónica P Colaiácovo

doi:10.1371/journal.pgen.1006281

Jonathon D Klein, Xiaoyang Yang + Show 5 more

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https://doi.org/10.1371/journal.pgen.1006281

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Journal: PLoS Genetics	Publication Date: Sep 13, 2016
Citations: 31	License type: CC BY 4.0

Affiliation: St. Jude Children's Research Hospital

Abstract

Drosophila melanogaster Piwi functions within the germline stem cells (GSCs) and the somatic niche to regulate GSC self-renewal and differentiation. How Piwi influences GSCs is largely unknown. We uncovered a genetic interaction between Piwi and c-Fos in the somatic niche that influences GSCs. c-Fos is a proto-oncogene that influences many cell and developmental processes. In wild-type ovarian cells, c-Fos is post-transcriptionally repressed by Piwi, which destabilized the c-Fos mRNA by promoting the processing of its 3′ untranslated region (UTR) into Piwi-interacting RNAs (piRNAs). The c-Fos 3′ UTR was sufficient to trigger Piwi-dependent destabilization of a GFP reporter. Piwi represses c-Fos in the somatic niche to regulate GSC maintenance and differentiation and in the somatic follicle cells to affect somatic cell disorganization, tissue dysmorphogenesis, oocyte maturation arrest, and infertility.

Highlights

Two major stem cell types are present in the Drosophila ovary: germline stem cells (GSCs) and somatic stem cells
The Drosophila melanogaster ovary is consisted of germ cells differentiated from GSCs and ovarian somatic cells that provide structural support to the organ
Piwi is a ribonucleoprotein required for GSC maintenance and differentiation in the Drosophila ovary

Summary

Introduction

Two major stem cell types are present in the Drosophila ovary: germline stem cells (GSCs) and somatic stem cells. The somatic niche (or the GSC microenvironment) promotes GSC maintenance via signaling factors such as dpp/BMP [1, 2]. Piwi in GSCs and in the somatic niche promotes GSC maintenance and differentiation [3,4,5,6,7]. Piwi mutant flies have no or markedly underdeveloped ovaries. Phenotypic studies of piwi mutant mosaic clones suggest that Piwi affects oogenesis [3, 4, 8]. A genome-wide screen identified genetic interactors of Piwi [9], and follow-up studies revealed that Piwi interacts with Corto and Polycomb Group proteins to regulate GSCs [10, 11]. The molecular mechanism by which Piwi regulates GSC maintenance and differentiation is not well understood

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