JAK/STAT autocontrol of ligand-producing cell number through apoptosis

Author:

Borensztejn Antoine12,Boissoneau Elisabeth1,Fernandez Guillaume1,Agnès François13,Pret Anne-Marie14

Affiliation:

1. Centre de Génétique Moléculaire (UPR3404), Centre National de la Recherche Scientifique, 1 avenue de la Terrasse, 91198 Gif-Sur-Yvette, France.

2. Université Pierre et Marie Curie Paris 6, Ecole Doctorale Complexité du Vivant, 4 Place Jussieu, 75005 Paris, France.

3. Université Paris-Sud 11, UFR des Sciences, 91405 Orsay, France.

4. Université de Versailles/St Quentin, UFR des Sciences, 78035 Versailles, France.

Abstract

During development, specific cells are eliminated by apoptosis to ensure that the correct number of cells is integrated in a given tissue or structure. How the apoptosis machinery is activated selectively in vivo in the context of a developing tissue is still poorly understood. In the Drosophila ovary, specialised follicle cells [polar cells (PCs)] are produced in excess during early oogenesis and reduced by apoptosis to exactly two cells per follicle extremity. PCs act as an organising centre during follicle maturation as they are the only source of the JAK/STAT pathway ligand Unpaired (Upd), the morphogen activity of which instructs distinct follicle cell fates. Here we show that reduction of Upd levels leads to prolonged survival of supernumerary PCs, downregulation of the pro-apoptotic factor Hid, upregulation of the anti-apoptotic factor Diap1 and inhibition of caspase activity. Upd-mediated activation of the JAK/STAT pathway occurs in PCs themselves, as well as in adjacent terminal follicle and interfollicular stalk cells, and inhibition of JAK/STAT signalling in any one of these cell populations protects PCs from apoptosis. Thus, a Stat-dependent unidentified relay signal is necessary for inducing supernumerary PC death. Finally, blocking apoptosis of PCs leads to specification of excess adjacent border cells via excessive Upd signalling. Our results therefore show that Upd and JAK/STAT signalling induce apoptosis of supernumerary PCs to control the size of the PC organising centre and thereby produce appropriate levels of Upd. This is the first example linking this highly conserved signalling pathway with developmental apoptosis in Drosophila.

Publisher

The Company of Biologists

Subject

Developmental Biology,Molecular Biology

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