The stem cell niche: Lessons from the Drosophila testis

Department of Cell Biology, Johns Hopkins School of Medicine, 725 N. Wolfe Street, Baltimore, MD 21205, USA.
Development (Impact Factor: 6.46). 07/2011; 138(14):2861-9. DOI: 10.1242/dev.056242
Source: PubMed


In metazoans, tissue maintenance and regeneration depend on adult stem cells, which are characterized by their ability to self-renew and generate differentiating progeny in response to the needs of the tissues in which they reside. In the Drosophila testis, germline and somatic stem cells are housed together in a common niche, where they are regulated by local signals, epigenetic mechanisms and systemic factors. These stem cell populations in the Drosophila testis have the unique advantage of being easy to identify and manipulate, and hence much progress has been made in understanding how this niche operates. Here, we summarize recent work on stem cells in the adult Drosophila testis and discuss the remarkable ability of these stem cells to respond to change within the niche.

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    • "We particularly focused on the role of the 6-O sulfate group, a key component of the binding sites on HS for most protein ligands (Ai et al., 2003;Wojcinski et al., 2011;Kleinschmit et al., 2013). Consistent with previous studies, wild-type testes had an average of 9-10 GSCs at 1-3 days post-eclosion (Figure 1, A and D) (Yamashita et al., 2005;de Cuevas and Matunis, 2011). Interestingly, homozygous Hs6st null mutants had a significantly higher number of GSCs (Figure 1, B and D), but normal hub size and structure (Figure 1E), compared to both wild-type and heterozygous control flies. "
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    ABSTRACT: Stem cell division is tightly controlled via secreted signaling factors and cell adhesion molecules provided from local niche structures. Molecular mechanisms by which each niche component regulates stem cell behaviors remain to be elucidated. Here we show that heparan sulfate (HS), a class of glycosaminoglycan chains, regulates the number and asymmetric division of germline stem cells (GSCs) in the Drosophila testis. We found that GSC number is sensitive to the levels of 6-O sulfate groups on HS. Loss of 6-O sulfation also disrupted normal positioning of centrosomes, a process required for asymmetric division of GSCs. Blocking HS sulfation specifically in the hub led to increased GSC numbers and mispositioning of centrosomes. The same treatment also perturbed the enrichment of Apc2, a component of the centrosome anchoring machinery, at the hub-GSC interface. This perturbation of the centrosome anchoring process ultimately led to an increase in the rate of spindle misorientation and symmetric GSC division. Our study shows that specific HS modifications provide a novel regulatory mechanism for stem cell asymmetric division. Our results also suggest that HS-mediated niche signaling acts upstream of GSC division orientation control.
    Preview · Article · Jan 2016 · Molecular Biology of the Cell
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    • "The somatic cyst stem cells (CySCs) serve as a component of the niche for the germline stem cells (GSCs). In fact, it is a combination of signals derived from the terminally differentiated hub cells to which CySCs and GSCs are adhered and the CySCs themselves that are necessary for GSC maintenance (de Cuevas and Matunis, 2011; Leatherman and Dinardo, 2008, 2010; Figure 1A). Similar to regulation in the hair follicle niche, the generation of daughter cells by GSCs and CySCs in the testis must be tightly controlled. "
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    ABSTRACT: In many tissues, the stem cell niche must coordinate behavior across multiple stem cell lineages. How this is achieved is largely unknown. We have identified delayed completion of cytokinesis in germline stem cells (GSCs) as a mechanism that regulates the production of stem cell daughters in the Drosophila testis. Through live imaging, we show that a secondary F-actin ring is formed through regulation of Cofilin activity to block cytokinesis progress after contractile ring disassembly. The duration of this block is controlled by Aurora B kinase. Additionally, we have identified a requirement for somatic cell encystment of the germline in promoting GSC abscission. We suggest that this non-autonomous role promotes coordination between stem cell lineages. These findings reveal the mechanisms by which cytokinesis is inhibited and reinitiated in GSCs and why such complex regulation exists within the stem cell niche. Copyright © 2015 Elsevier Inc. All rights reserved.
    Full-text · Article · Jul 2015 · Developmental Cell
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    • "Several signaling pathways have been shown to be involved in testis development, including TGF-b signaling for the maintenance of germline stem cells and the restriction of spermatogonial proliferation (Loveland and Hime, 2005), as well as Jak/Stat signaling which contributes to stem cell self-renewal (Hombria and Brown, 2002; de Cuevas and Matunis, 2011). On the other hand, the mechanisms underlying asymmetric coiling have not yet been addressed. "
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    ABSTRACT: Drosophila is a classical model to study body patterning, however Left-Right (L/R) asymmetry had remained unexplored, until recently. The discovery of the conserved myosin ID gene as a major determinant of L/R asymmetry has revealed a novel L/R pathway involving the actin cytoskeleton and the adherens junction. In this process, the HOX gene Abdominal-B plays a major role through the control of myosin ID expression and therefore symmetry breaking. In this review, we present organs and markers showing L/R asymmetry in Drosophila and discuss our current understanding of the underlying molecular genetic mechanisms. Drosophila represents a valuable model system revealing novel strategies to establish L/R asymmetry in invertebrates and providing an evolutionary perspective to the problem of laterality in bilateria. © 2014 Wiley Periodicals, Inc.
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