Abstract
Author SummaryThe Drosophila ovary contains a well-defined stem cell niche that hosts 2–3 germline stem cells (GSCs). The Hedgehog (Hh) family of signalling proteins mediates cellular homeostasis in several adult tissues, and here we decipher the detailed mechanism of action of Hh in the adult female GSC niche. We demonstrate that Hh acts in a juxtacrine manner (i.e., it requires physical contact between the cells involved) to maintain the normal pool of GSCs in the ovarian niche. Hh is produced in one type of niche support cell (the cap cells), and it is received, upon secretion, by a second, neighbouring population of niche cells (the escort cells). In the latter, we show that the Hh signalling pathway regulates the expression of the Drosophila Bone Morphogenetic Protein (BMP) homologues and essential stem cell factors decapentaplegic (dpp) and glass bottom boat (gbb). We also find that Hh distribution in the GSC niche is mediated by short cellular projections, reminiscent of wing disc cytonemes, although they grow from the (Hh) signal-producing cells towards the receiving cells. Under conditions of low levels of Hh protein and/or Hh signalling within the niche, cap cells emit up to 6-fold longer Hh-decorated cytonemes towards the signalling-deficient area of the niche. Our data reveal that stem cell niches are dynamic structures that can sense, and react to, changes in the activity of essential stem cell factors to prevent stem cell differentiation.
Highlights
Stem cells are responsible for the integrity of tissues during growth, ageing, and repair
The Hedgehog (Hh) family of signalling proteins mediates cellular homeostasis in several adult tissues, and here we decipher the detailed mechanism of action of Hh in the adult female germline stem cell (GSC) niche
We demonstrate that Hh acts in a juxtacrine manner to maintain the normal pool of GSCs in the ovarian niche
Summary
Stem cells are responsible for the integrity of tissues during growth, ageing, and repair. They reside in specialised microenvironments, or niches, which frequently comprise support cells that control stem cell self-renewal, proliferation, and differentiation [1,2]. Stem cell niche regulation often involves short-range signalling between stem cells themselves and the surrounding microenvironment. One such short-range signal is the Hedgehog (Hh) family of proteins, which mediates homeostasis in several adult tissues, including the gastrointestinal tract, the hematopoietic system, and the vertebrate central nervous system [3,4,5,6,7]. The detailed mechanisms by which Hh acts in stem cell maintenance remain elusive
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