Abstract
Stem cell maintenance is established by neighboring niche cells that promote stem cell self-renewal. However, it is poorly understood how stem cell activity is regulated by systemic, tissue-extrinsic signals in response to environmental cues and changes in physiological status. Here, we show that neuropeptide F (NPF) signaling plays an important role in the pathway regulating mating-induced germline stem cell (GSC) proliferation in the fruit fly Drosophila melanogaster. NPF expressed in enteroendocrine cells (EECs) of the midgut is released in response to the seminal-fluid protein sex peptide (SP) upon mating. This midgut-derived NPF controls mating-induced GSC proliferation via ovarian NPF receptor (NPFR) activity, which modulates bone morphogenetic protein (BMP) signaling levels in GSCs. Our study provides a molecular mechanism that describes how a gut-derived systemic factor couples stem cell behavior to physiological status, such as mating, through interorgan communication.
Highlights
Maintenance and regeneration of adult tissues requires a robust stem cell system that balances self-renewal with differentiation [1]
We show that a peptide hormone called neuropeptide F (NPF) is a key player in this process
We found that genetic null mutant flies of short neuropeptide F precursor, encoding an RxRFamide neuropeptide related to NPF, showed a normal increase in germline stem cell (GSC) number after mating (Fig 1D), suggesting that the GSC-suppression phenotype is specific to NPF signaling
Summary
Maintenance and regeneration of adult tissues requires a robust stem cell system that balances self-renewal with differentiation [1]. Because abnormalities in stem cell regulation may result in loss of tissue integrity or tumorigenesis, this robust stem cell system is precisely modulated by local and systemic signals [2]. A number of studies have demonstrated the importance of local niche signals in regulating stem cell identity. The Drosophila ovary is one of the most powerful models for studying adult stem cell behavior in vivo [3,5]. This tissue is composed of many chains of developing egg chambers called ovarioles [6]. The balance between self-renewal and differentiation of GSCs plays a pivotal role in regulating oogenesis because disruption of this balance may cause germ cell depletion, infertility, or tumorigenesis [1]
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