Abstract
Stem cells in tissues reside in and receive signals from local microenvironments called niches. Understanding how multiple signals within niches integrate to control stem cell function is challenging. The Drosophila testis stem cell niche consists of somatic hub cells that maintain both germline stem cells and somatic cyst stem cells (CySCs). Here, we show a role for the axon guidance pathway Slit-Roundabout (Robo) in the testis niche. The ligand Slit is expressed specifically in hub cells while its receptor, Roundabout 2 (Robo2), is required in CySCs in order for them to compete for occupancy in the niche. CySCs also require the Slit-Robo effector Abelson tyrosine kinase (Abl) to prevent over-adhesion of CySCs to the niche, and CySCs mutant for Abl outcompete wild type CySCs for niche occupancy. Both Robo2 and Abl phenotypes can be rescued through modulation of adherens junction components, suggesting that the two work together to balance CySC adhesion levels. Interestingly, expression of Robo2 requires JAK-STAT signaling, an important maintenance pathway for both germline and cyst stem cells in the testis. Our work indicates that Slit-Robo signaling affects stem cell function downstream of the JAK-STAT pathway by controlling the ability of stem cells to compete for occupancy in their niche.
Highlights
Adult stem cells are essential for tissue regeneration and are maintained in specialized microenvironments, or niches
The ligand Slit is expressed in the hub, and Slit’s receptor Roundabout 2 (Robo2), which is transcriptionally activated by JAK-STAT signaling, is required in adjacent cyst stem cells (CySCs) to promote ECad-based adhesion to the hub
We found that an enhancer trap inserted in the robo2 gene, encoding the Robo2 axon guidance receptor, is expressed in the hub, CySCs and their immediate daughters (Figure 1B)
Summary
Adult stem cells are essential for tissue regeneration and are maintained in specialized microenvironments, or niches. Many extracellular signals and intrinsic adhesion factors are known to be required for stem cell maintenance, little is known about how they converge to regulate stem cell-niche cell adhesion in vivo [2]. We have approached this question using the well-characterized niche within the Drosophila testis. In this tissue, a cluster of quiescent, somatic hub cells contributes to the stem cell niche by signaling to adjacent germline and somatic stem cells (GSCs and cyst stem cells, or CySCs) (Figure 1A) [3]. CySCs divide asymmetrically, and their differentiating progeny (cyst cells) encase differentiating germ cells and support their differentiation [8,9,10]
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