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

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.

Regulation of Mating-Induced Increase in Female Germline Stem Cells in the Fruit Fly Drosophila melanogaster

“…It is speculated that NPF, OA, and ecdysteroids promote symmetric, rather than asymmetric cell division of female GSCs, causing to mating-inducible increase in number of female GSCs. Previous research also suggest that the Dpp niche signaling is essential for the mating-induced increase in female GSC number (Ameku and Niwa, 2016;Ameku et al, 2018;Yoshinari et al, 2020). However, it is yet unknown how the humoral factors accelerate cell divisions and regulate the polarity of female GSC cell division by modulating the niche signal.…”

“…Therefore, it is expected that humoral factors, such as hormones and neurotransmitters, may also contribute to the mating-induced increase in female GSCs. After our genetic approaches ( Ameku and Niwa, 2016 ; Ameku et al, 2017 , 2018 ; Yoshinari et al, 2019 , 2020 ), the three humoral factors have been identified: ecdysteroids, NPF, and octopamine (OA), originating from the ovary itself, the gut, and the central nervous system, respectively ( Figures 2A,B ). These factors are received by the GSC niche, and downstream signaling is essential for the increase in female GSCs and their maintenance.…”

“…In addition, dsx + Tdc2 neurons are responsible for the regulation of egg-laying behavior ( Monastirioti, 2003 ; Rezával et al, 2014 ; Deady and Sun, 2015 ; White et al, 2021b ). Forced activation of these neurons results in an increase in the number of GSCs even in the virgin state ( Yoshinari et al, 2020 ). Conversely, inactivation of dsx + Tdc2 neurons suppresses the mating-induced increase in female GSCs.…”

“…Since the discovery of post-mating increase in female GSCs, our group has intensively studied how SP-mediated mating information can affect the increase in number of female GSCs. We have successfully identified essential neuroendocrine factors, such as steroid hormones, neuropeptides, and monoaminergic neurotransmitters ( Ameku and Niwa, 2016 ; Ameku et al, 2018 ; Yoshinari et al, 2020 ). In this review, we focus on the role of the neuroendocrine system in transmitting mating stimuli to female GSCs and discuss the future direction of our research.…”

Knockdown of a β-Adrenergic-Like Octopamine Receptor Affects Locomotion and Reproduction of Tribolium castaneum

“…High concentrations of OA have been found in the neuronal and nonneuronal tissues of most invertebrate species [ 2 ]. OA acts as a neurohormone, neuromodulator, and neurotransmitter in invertebrates [ 3 ], with essential functions and regulation of many physiological processes, including olfactory sensitivity [ 4 , 5 , 6 ], endocrine regulation [ 7 ], learning and memory [ 8 , 9 ], locomotion [ 10 , 11 , 12 , 13 ], sleep [ 14 ], induction of germline stem cell increase [ 15 ], and ovulation [ 16 , 17 , 18 , 19 ].…”