Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster

Stem cells fuel the development and maintenance of tissues. Many studies have addressed how local signals from neighboring niche cells regulate stem cell identity and their proliferative potential. However, the regulation of stem cells by tissue-extrinsic signals in response to environmental cues re...

Full description

Bibliographic Details
Main Authors: Yuto Yoshinari, Tomotsune Ameku, Shu Kondo, Hiromu Tanimoto, Takayuki Kuraishi, Yuko Shimada-Niwa, Ryusuke Niwa
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/57101
id doaj-595e75ef41de4f4f9ac4d0723aabf3a1
record_format Article
spelling doaj-595e75ef41de4f4f9ac4d0723aabf3a12021-05-05T21:37:36ZengeLife Sciences Publications LtdeLife2050-084X2020-10-01910.7554/eLife.57101Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogasterYuto Yoshinari0Tomotsune Ameku1Shu Kondo2Hiromu Tanimoto3https://orcid.org/0000-0001-5880-6064Takayuki Kuraishi4Yuko Shimada-Niwa5https://orcid.org/0000-0001-5757-4329Ryusuke Niwa6https://orcid.org/0000-0002-1716-455XGraduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanGraduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanInvertebrate Genetics Laboratory, National Institute of Genetics, Mishima, JapanGraduate School of Life Sciences, Tohoku University, Sendai, JapanFaculty of Pharmacy, Institute of Medical, Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Japan; AMED-PRIME, Japan Agency for Medical Research and Development, Tokyo, JapanLife Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance (TARA), University of Tsukuba, Tsukuba, JapanLife Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance (TARA), University of Tsukuba, Tsukuba, Japan; AMED-CREST, Japan Agency for Medical Research and Development, Tokyo, JapanStem cells fuel the development and maintenance of tissues. Many studies have addressed how local signals from neighboring niche cells regulate stem cell identity and their proliferative potential. However, the regulation of stem cells by tissue-extrinsic signals in response to environmental cues remains poorly understood. Here we report that efferent octopaminergic neurons projecting to the ovary are essential for germline stem cell (GSC) increase in response to mating in female Drosophila. The neuronal activity of the octopaminergic neurons is required for mating-induced GSC increase as they relay the mating signal from sex peptide receptor-positive cholinergic neurons. Octopamine and its receptor Oamb are also required for mating-induced GSC increase via intracellular Ca2+ signaling. Moreover, we identified Matrix metalloproteinase-2 as a downstream component of the octopamine-Ca2+ signaling to induce GSC increase. Our study provides a mechanism describing how neuronal system couples stem cell behavior to environmental cues through stem cell niche signaling.https://elifesciences.org/articles/57101germline stem cellstem cell nichematingoctopamineacetylcholinematrix metalloproteinase
collection DOAJ
language English
format Article
sources DOAJ
author Yuto Yoshinari
Tomotsune Ameku
Shu Kondo
Hiromu Tanimoto
Takayuki Kuraishi
Yuko Shimada-Niwa
Ryusuke Niwa
spellingShingle Yuto Yoshinari
Tomotsune Ameku
Shu Kondo
Hiromu Tanimoto
Takayuki Kuraishi
Yuko Shimada-Niwa
Ryusuke Niwa
Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster
eLife
germline stem cell
stem cell niche
mating
octopamine
acetylcholine
matrix metalloproteinase
author_facet Yuto Yoshinari
Tomotsune Ameku
Shu Kondo
Hiromu Tanimoto
Takayuki Kuraishi
Yuko Shimada-Niwa
Ryusuke Niwa
author_sort Yuto Yoshinari
title Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster
title_short Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster
title_full Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster
title_fullStr Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster
title_full_unstemmed Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster
title_sort neuronal octopamine signaling regulates mating-induced germline stem cell increase in female drosophila melanogaster
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-10-01
description Stem cells fuel the development and maintenance of tissues. Many studies have addressed how local signals from neighboring niche cells regulate stem cell identity and their proliferative potential. However, the regulation of stem cells by tissue-extrinsic signals in response to environmental cues remains poorly understood. Here we report that efferent octopaminergic neurons projecting to the ovary are essential for germline stem cell (GSC) increase in response to mating in female Drosophila. The neuronal activity of the octopaminergic neurons is required for mating-induced GSC increase as they relay the mating signal from sex peptide receptor-positive cholinergic neurons. Octopamine and its receptor Oamb are also required for mating-induced GSC increase via intracellular Ca2+ signaling. Moreover, we identified Matrix metalloproteinase-2 as a downstream component of the octopamine-Ca2+ signaling to induce GSC increase. Our study provides a mechanism describing how neuronal system couples stem cell behavior to environmental cues through stem cell niche signaling.
topic germline stem cell
stem cell niche
mating
octopamine
acetylcholine
matrix metalloproteinase
url https://elifesciences.org/articles/57101
work_keys_str_mv AT yutoyoshinari neuronaloctopaminesignalingregulatesmatinginducedgermlinestemcellincreaseinfemaledrosophilamelanogaster
AT tomotsuneameku neuronaloctopaminesignalingregulatesmatinginducedgermlinestemcellincreaseinfemaledrosophilamelanogaster
AT shukondo neuronaloctopaminesignalingregulatesmatinginducedgermlinestemcellincreaseinfemaledrosophilamelanogaster
AT hiromutanimoto neuronaloctopaminesignalingregulatesmatinginducedgermlinestemcellincreaseinfemaledrosophilamelanogaster
AT takayukikuraishi neuronaloctopaminesignalingregulatesmatinginducedgermlinestemcellincreaseinfemaledrosophilamelanogaster
AT yukoshimadaniwa neuronaloctopaminesignalingregulatesmatinginducedgermlinestemcellincreaseinfemaledrosophilamelanogaster
AT ryusukeniwa neuronaloctopaminesignalingregulatesmatinginducedgermlinestemcellincreaseinfemaledrosophilamelanogaster
_version_ 1721457991643824128