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

Citation

Niwa, Ryusuke et al. (2020), Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster, Dryad, Dataset, https://doi.org/10.5061/dryad.zkh189375

Abstract

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.

Methods

Source data file 1. Data of numbers of GSC and other cells. GSC numbers were determined based on the morphology and position of their anteriorly anchored spherical spectrosome visualized by immunostaining with mouse anti-Hts 1B1 (Developmental Studies Hybridoma Bank [DSHB]; 1:50), rat anti-DE-cadherin DCAD2 (DSHB; 1:50). Cap cells were visualized by immunostaining with mouse monoclonal anti-Lamin C antibody LC28.26 (DSHB; 1:10).

Source data file 2: Data of pMad and dad-lacZ signal intensity. pMad was visualized by immunostaining with rabbit monoclonal anti-pMad (Abcam #ab52903; 1:1000). LacZ was visualized by immunostaining with mouse monoclonal anti-LacZ antibody 40-1a (DSHB; 1:50). The fluorescence intensity in confocal sections was measured via ImageJ.

Source data file 3: Data of GCaMP6s intensity in escort cells. We monitored [Ca2+]i using a genetically encoded calcium sensor, GCaMP6s. GCaMP6s transgene was expressed driven by tj-GAL4 or c587-GAL4, which are active in escort cells. GFP fluorescence intensity in confocal sections was measured via ImageJ.

Source data file 4: Data of TRIC intensity in the abdominal ganglions. The transcriptional reporter of intracellular Ca2+ (TRIC) is designed to increase the GFP expression in proportion to [Ca2+]i. The fly genotype was Tdc2>UAS-mCD8::RFP, UAS-p65AD::CaM LexAop2-mCD8::GFP; nSyb-MKII::nlsLexADBDo;UAS-p65AD::CaM. GFP fluorescence intensity in confocal sections was measured via ImageJ.

Funding

Japan Society for the Promotion of Science, Award: 26250001

Japan Society for the Promotion of Science, Award: A17H01378

Japan Society for the Promotion of Science, Award: 18J20572

Japan Society for the Promotion of Science, Award: 15J00652

Japan Agency for Medical Research and Development, Award: 17gm6010011h0001

Japan Agency for Medical Research and Development, Award: 19gm1110001h0003

Takeda Science Foundation, Award: n/a