Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis.

The function of the stem cell system is supported by a stereotypical shape of the niche structure. In Drosophila ovarian germarium, somatic cap cells form a dish-like niche structure that allows only two or three germ-line stem cells (GSCs) reside in the niche. Despite extensive studies on the mecha...

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Main Authors: Kiichiro Taniguchi, Tatsushi Igaki
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-03-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1010684
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author Kiichiro Taniguchi
Tatsushi Igaki
author_facet Kiichiro Taniguchi
Tatsushi Igaki
author_sort Kiichiro Taniguchi
collection DOAJ
description The function of the stem cell system is supported by a stereotypical shape of the niche structure. In Drosophila ovarian germarium, somatic cap cells form a dish-like niche structure that allows only two or three germ-line stem cells (GSCs) reside in the niche. Despite extensive studies on the mechanism of stem cell maintenance, the mechanisms of how the dish-like niche structure is shaped and how this structure contributes to the stem cell system have been elusive. Here, we show that a transmembrane protein Stranded at second (Sas) and its receptor Protein tyrosine phosphatase 10D (Ptp10D), effectors of axon guidance and cell competition via epidermal growth factor receptor (Egfr) inhibition, shape the dish-like niche structure by facilitating c-Jun N-terminal kinase (JNK)-mediated apoptosis. Loss of Sas or Ptp10D in gonadal apical cells, but not in GSCs or cap cells, during the pre-pupal stage results in abnormal shaping of the niche structure in the adult, which allows excessive, four to six GSCs reside in the niche. Mechanistically, loss of Sas-Ptp10D elevates Egfr signaling in the gonadal apical cells, thereby suppressing their naturally-occurring JNK-mediated apoptosis that is essential for the shaping of the dish-like niche structure by neighboring cap cells. Notably, the abnormal niche shape and resulting excessive GSCs lead to diminished egg production. Our data propose a concept that the stereotypical shaping of the niche structure optimizes the stem cell system, thereby maximizing the reproductive capacity.
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spelling doaj.art-6e3ac37ea76d44e69432a8facc1f76252023-04-13T05:31:06ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042023-03-01193e101068410.1371/journal.pgen.1010684Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis.Kiichiro TaniguchiTatsushi IgakiThe function of the stem cell system is supported by a stereotypical shape of the niche structure. In Drosophila ovarian germarium, somatic cap cells form a dish-like niche structure that allows only two or three germ-line stem cells (GSCs) reside in the niche. Despite extensive studies on the mechanism of stem cell maintenance, the mechanisms of how the dish-like niche structure is shaped and how this structure contributes to the stem cell system have been elusive. Here, we show that a transmembrane protein Stranded at second (Sas) and its receptor Protein tyrosine phosphatase 10D (Ptp10D), effectors of axon guidance and cell competition via epidermal growth factor receptor (Egfr) inhibition, shape the dish-like niche structure by facilitating c-Jun N-terminal kinase (JNK)-mediated apoptosis. Loss of Sas or Ptp10D in gonadal apical cells, but not in GSCs or cap cells, during the pre-pupal stage results in abnormal shaping of the niche structure in the adult, which allows excessive, four to six GSCs reside in the niche. Mechanistically, loss of Sas-Ptp10D elevates Egfr signaling in the gonadal apical cells, thereby suppressing their naturally-occurring JNK-mediated apoptosis that is essential for the shaping of the dish-like niche structure by neighboring cap cells. Notably, the abnormal niche shape and resulting excessive GSCs lead to diminished egg production. Our data propose a concept that the stereotypical shaping of the niche structure optimizes the stem cell system, thereby maximizing the reproductive capacity.https://doi.org/10.1371/journal.pgen.1010684
spellingShingle Kiichiro Taniguchi
Tatsushi Igaki
Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis.
PLoS Genetics
title Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis.
title_full Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis.
title_fullStr Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis.
title_full_unstemmed Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis.
title_short Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis.
title_sort sas ptp10d shapes germ line stem cell niche by facilitating jnk mediated apoptosis
url https://doi.org/10.1371/journal.pgen.1010684
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