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WIREs Dev Biol
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Control of germline stem cell self‐renewal and differentiation in the Drosophila ovary: concerted actions of niche signals and intrinsic factors

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In the Drosophila ovary, germline stem cells (GSCs) physically interact with their niche composed of terminal filament cells, cap cells, and possibly GSC‐contacting escort cells (ECs). A GSC divides to generate a self‐renewing stem cell that remains in the niche and a differentiating daughter that moves away from the niche. The GSC niche provides a bone morphogenetic protein (BMP) signal that maintains GSC self‐renewal by preventing stem cell differentiation via repression of the differentiation‐promoting gene bag of marbles (bam). In addition, it expresses E‐cadherin, which mediates cell adhesion for anchoring GSCs in the niche, enabling continuous self‐renewal. GSCs themselves also express different classes of intrinsic factors, including signal transducers, transcription factors, chromatin remodeling factors, translation regulators, and miRNAs, which control self‐renewal by strengthening interactions with the niche and repressing various differentiation pathways. Differentiated GSC daughters, known as cystoblasts (CBs), also express distinct classes of intrinsic factors to inhibit self‐renewal and promote germ cell differentiation. Surprisingly, GSC progeny are also dependent on their surrounding ECs for proper differentiation at least partly by preventing BMP from diffusing to the differentiated germ cell zone and by repressing ectopic BMP expression. Therefore, both GSC self‐renewal and CB differentiation are controlled by collaborative actions of extrinsic signals and intrinsic factors. WIREs Dev Biol 2013, 2:261–273. doi: 10.1002/wdev.60

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Figure 1.

The Drosophila ovarian germline stem cell (GSC) system. (a) A schematic diagram of a Drosophila germarium, which is divided into three regions based on germ cell developmental stages. Region 1 contains mitotic germ cells including GSCs, cystoblasts (CBs) and mitotic cysts (2‐cell, 4‐cell, and 8‐cell cysts). Region 2 contains ball‐like 16‐cell cysts wrapped by escort cells (2a) and lens‐shaped 16‐cell cysts surrounded by follicle cells (2b); Region 3 contains a stage 1 egg chamber. Abbreviations: TF, terminal filament; CPC, cap cell; GEC, GSC‐contacting escort cell; DEC, differentiated germ cell‐contacting escort cell; SS, spectrosome; FS, fusome; DC, differentiated cyst; FSC, follicular stem cell; and FC, follicle cells. (b) A GSC (harboring an anteriorly anchored SS) undergoes self‐renewing division to generate a GSC and a CB (carrying a SS) (highlighted by broken lines). The CB divides four times without cytokinesis to form a 16‐cell cyst. 2‐cell, 4‐cell, 8‐cell, and 16‐cell cysts can be easily identified by their branched fusome morphology.

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Figure 2.

Extrinsic and intrinsic factors work concertedly to control germline stem cell (GSC) self‐renewal. (a) A schematic diagram shows how known intrinsic factors in GSCs and niche signaling work together to control GSC self‐renewal by repressing Bam‐dependent and Bam‐independent differentiation pathways. Solid green arrows indicate known positive regulations, while solid red inhibition signs denote known inhibitory relationships. The broken green arrows indicate that the regulations have been inhibited, while the broken lines with a question mark show speculative relationships. (b) A summary on relationships among systemic factors, niche signaling and intrinsic factors in the regulation of GSC self‐renewal.

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Figure 3.

Escort cell (EC) signaling and intrinsic factors control cystoblast (CB) differentiation. (a) A schematic diagram shows that known intrinsic factors in CBs promote differentiation by repressing self‐renewal factors or work with EC signaling to block bone morphogenetic protein (BMP) signaling. (b) A summary of the relationships among EC signaling and intrinsic factors in the regulation of CB differentiation.

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Invertebrate Organogenesis > Flies
Adult Stem Cells, Tissue Renewal, and Regeneration > Tissue Stem Cells and Niches

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