Abstract
The niche controls stem cell self-renewal and progenitor differentiation for maintaining adult tissue homeostasis in various organisms. However, it remains unclear whether the niche is compartmentalized to control stem cell self-renewal and stepwise progeny differentiation. In the Drosophila ovary, inner germarial sheath (IGS) cells form a niche for controlling germline stem cell (GSC) progeny differentiation. In this study, we have identified four IGS subpopulations, which form linearly arranged niche compartments for controlling GSC maintenance and multi-step progeny differentiation. Single-cell analysis of the adult ovary has identified four IGS subpopulations (IGS1-IGS4), the identities and cellular locations of which have been further confirmed by fluorescent in situ hybridization. IGS1 and IGS2 physically interact with GSCs and mitotic cysts to control GSC maintenance and cyst formation, respectively, whereas IGS3 and IGS4 physically interact with 16-cell cysts to regulate meiosis, oocyte development, and cyst morphological change. Finally, one follicle cell progenitor population has also been transcriptionally defined for facilitating future studies on follicle stem cell regulation. Therefore, this study has structurally revealed that the niche is organized into multiple compartments for orchestrating stepwise adult stem cell development and has also provided useful resources and tools for further functional characterization of the niche in the future.
Highlights
Stem cells maintain adult tissue homeostasis through continuous self-renewal and generation of differentiated cells
Those CG7194-expressing clusters are composed of five subpopulations, IGS1–IGS5, suggesting the existence of inner germarial sheath (IGS) subpopulations (Figures 1F and 1G). Those purified 31C09-expressing IGS cells in region 1 are almost exclusively restricted to the IGS1 and IGS2 subpopulations, whereas those purified 25A11-expressing IGS cells in regions 1 and 2a are distributed to IGS1–IGS4 (Figures 1B and 1G). 71E07-expressing IGS cells in region 1 and somatic cells in regions 2b and 3 are allocated into IGS1, IGS2, and IGS5 subpopulations (Figures 1B and 1G). These results suggest that IGS1 and IGS2, IGS3 and IGS4, and IGS5 are located along the anterior-to-posterior germarial axis
By using the UAS-nLacZ reporter, we show that dpr17-Gal[4] exhibits similar dynamic IGS expression patterns to its mRNA, and the percentages of the germaria with the same IGS expression pattern for dpr17-Gal[4] and dpr[17] mRNA are comparable (Figures 3C and 3D). dpr[17] encodes an immunoglobin (Ig)-domain-containing protein involved in synapse recognition and specificity determination by engaging with another Ig-domain-containing protein DIP-ε or Figure 3. dpr[17] Is Dynamically Expressed in Different IGS Subpopulations (A) t-SNE plot showing dpr[17] is enriched in the IGS4 and is expressed in other IGS subpopulations at low levels. (B and C) dpr[17] mRNA fluorescent in situ hybridization (FISH) (B) images and dpr17-Gal4>UAS-nLacZ expression patterns (C) showing variable expression patterns of dpr[17] in Drosophila germaria
Summary
Stem cells maintain adult tissue homeostasis through continuous self-renewal and generation of differentiated cells Their self-renewal is shown to be controlled by the niche in the organisms ranging from Drosophila to mammals.[1,2,3] Recently, stem cell progeny differentiation has been proposed to be regulated by the niche in the Drosophila ovary.[4] The differentiation process often consists of multiple developmental steps for generating one or several functional cell types. It remains largely unclear how the niche controls these differentiation steps at the cellular level. Cap cells and anterior IGS cells form a niche for controlling GSC self-renewal through Dpp/BMPmediated signaling and E-cadherin-mediated cell adhesion,[8,9,10,11,12] whereas IGS cells form a niche for promoting differentiation partly by preventing bone morphogenetic protein (BMP) signaling.[4,12] IGS cells utilize Hh, Wnt, epidermal growth factor receptor (EGFR), and Jak-Stat signaling to prevent BMP signaling in GSC progeny.[11,13,14,15,16,17,18,19,20,21] Long IGS cellular processes are regulated by Hh and Rho-CDC42 small GTPase signaling, and cellular-processmediated direct interactions are important for CB differentiation and cyst formation.[4,14,22] Ecdysone signaling prevents IGS transformation into cap cells during development and is needed in IGS cells for cyst formation, meiosis, and egg chamber formation.[23,24,25] two niches coordinately control GSC development in the Drosophila ovary
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
