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...
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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 |
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