Stem Cell Niches in Drosophila


A precise balance between stem cell self‐renewal and differentiation drives normal maintenance of many adult tissues. One mechanism that achieves this balance is through asymmetric cell division (ACD). During ACD, two daughter cells with distinct fates are generated by asymmetric inheritance of many cellular components. The stem cell microenvironment, called the stem cell niche, contributes to the regulation of this balance. The niche serves as an anchoring point, while also contributing extrinsic cues that orchestrate the polarised distribution of intrinsic cellular components to ensure their asymmetric inheritance. Investigating how the niche communicates with stem cells works toward the goal of understanding stem cell biology, developmental biology and regenerative medicine. This article summarises our current knowledge of different adult stem cell lineages in Drosophila melanogaster, highlighting common threads found in regulating their maintenance and proper differentiation.

Key Concepts

  • A balance between adult stem cell self‐renewal and differentiation is necessary for tissue homeostasis.
  • Asymmetric cell division of adult stem cells produces daughter cells with distinct cell fates.
  • Spindle orientation regulates asymmetric versus symmetric cell division in intestinal stem cells and germline stem cells.
  • Sister chromatids in male germline stem cells are differentially enriched with either previously synthesised (old) or newly synthesised (new) histones.
  • Polarised segregation of epigenetically different sister chromatids in male germline stem cells is achieved through temporally regulated spindle activity.
  • Stromal and nonstromal stem cell niches are sources of signalling molecules and physical anchoring.
  • Adherens junctions anchor stem cells to their niche.
  • Signalling pathways like JAK‐STAT, BMP, Hippo, EGF and Wnt all contribute to self‐renewal of many stem cell lineages.

Keywords: asymmetric cell division; stem cell niche; germline stem cell; intestinal stem cell; renal and nephric stem cell; cell fate determinants; spindle orientation; nonrandom chromosome segregation

Figure 1. Stem cell populations in D. melanogaster. (a) The female germarium contains the germline stem cell (GSC) niche, composed of terminal filament cells, cap cells and escort cells. GSCs attached to the niche undergo asymmetric cell division (ACD) to produce another GSC and a daughter cystoblast (CB). The CB undergoes mitotic divisions to form germline cysts that are connected by the fusome (purple). Follicle stem cells (FSC) are located midway in the germarium and contribute to the epithelial lining of the developing germline cyst. (b) The male GSC niche is composed of the hub, surrounding GSCs and cyst stem cells (CySC). GSCs divide to produce an additional GSC and a gonialblast that undergoes mitosis to form germline cysts connected by the fusome (purple). The CySC also divides to produce a cyst cell that encapsulates the differentiating germline cyst. In both male and female GSCs, the fusome is called the spectrosome (purple). (c) The intestinal epithelial lining is maintained by intestinal stem cells (ISCs). ISCs differentiate to produce the other cells composing the epithelium: enterocytes (EC), enteroblasts (EB) and enteroendocrine cells (EE). (d) Malpighian tubules are composed of three main cell types, stellate cells, principal cells and renal and nephric stem cells.
Figure 2. Asymmetric cell division of intestinal stem cells (ISC). (a) Asymmetric cell division of an ISC produces an additional ISC and either an enteroendocrine cell (EE) or an enteroblast (EB) that further differentiates into an enterocyte (EC). (b) Spindle orientation determines the cell division plane. Spindles oriented perpendicular to the basement membrane (orange) result in asymmetric cell division. In contrast, spindles oriented parallel to the basement membrane promote symmetric cell division. Symmetric cell division can either produce two ISCs (shown here) or EEs (not pictured). The centrosomes are shown in purple.
Figure 3. Segregation of cell fate determinants. (a) In male GSCs, the mother centrosome projects spindles that attach to sister chromatids with old histone (green) and higher CID (blue) enrichment. This directs inheritance of sister chromatids enriched with old histone to the self‐renewing stem cell. New histone‐enriched sisters (red) are inherited by the differentiating daughter cell. Based on Ranjan et al., . (b) A model demonstrating chromatid‐specific deposition of old and new histones during DNA replication. In this model, old histones (green) are recycled onto the leading strand, whereas new histones (red) are incorporated into chromatin of the lagging strand. (c) The distribution of Numb (dark green at cell membrane) inheritance influences the Notch signalling cascade to determine cell fate following ACD of the ISC. Based on Sallé et al., .
Figure 4. Signalling pathways involved in stem cell regulation. (a) Ligands from the BMP signalling pathway originate from cap cells to regulate GSC activity. Polar cells contribute to FSC activity as a source of the JAK‐STAT ligand. FSC activity is further regulated by Hh and Wnt ligands emanating from cap cells and escort cells. (b) BMP and JAK‐STAT ligands emanating from the hub maintain GSC and CySC activity. CySCs also contribute to GSC maintenance through providing BMP ligands. (c) ISC activity is regulated through many signalling ligands originating from the visceral muscle (VM) and differentiated ECs and EBs. (d) RNSCs contribute to their own activity while also regulating differentiation of their daughter cells.


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Further Reading

Guo Z, Lucchetta E, Rafel N and Ohlstein B (2016) Maintenance of the adult Drosophila intestine: all roads lead to homeostasis. Current Opinion in Genetics and Development 40: 81–86.

Gallaud E, Pham T and Cabernard C (2017) Drosophila melanogaster neuroblasts: a model for asymmetric stem cell divisions. In: Jean‐Pierre Tassan and Jacek Z. Kubiak (eds) Results and Problems in Cell Differentiation, vol. 61, chap. 8, pp 183–210.

Kahney EW, Snedeker JC and Chen X (2019) Regulation of Drosophila germline stem cells. Current Opinion in Cell Biology 60: 27–35.

Losick VP, Morris LX, Fox DT and Spradling A (2011) Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Developmental Cell 21 (1): 159–171.

Loyer N and Januschke J (2020) Where does asymmetry come from? Illustrating principles of polarity and asymmetry establishment in Drosophila neuroblasts. Current Opinion in Cell Biology 62: 70–77.

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Sahai‐Hernandez P, Castanieto A and Nystul TG (2012) Drosophila models of epithelial stem cells and their niches. Wiley Interdisciplinary Reviews: Developmental Biology 1: 447–457.

Wooten M, Ranjan R and Chen X (2020) Asymmetric histone inheritance in asymmetrically dividing stem cells. Trends in Genetics 36 (1): 30–43.

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Urban, Jennifer, and Chen, Xin(Jun 2020) Stem Cell Niches in Drosophila. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0021854.pub2]