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Mesenchymal to epithelial transition during tissue homeostasis and regeneration: Patching up the Drosophila midgut epithelium.

Antonello ZA, Reiff T, Dominguez M - Fly (Austin) (2015)

Bottom Line: Stem cells divide to self-renew and to generate progenitor cells to sustain cell demand from the tissue throughout the organism's life.In this Extra View article, we discuss the ability of progenitor cells to actively postpone terminal differentiation in the absence of a local demand and how tissue demand activates terminal differentiation via a conserved mesenchymal-epithelial transition program revealed in our recent EMBO J paper and other published and unpublished data.The extent of the significance of these results is discussed for models of tissue dynamics during both homeostasis and regeneration.

View Article: PubMed Central - PubMed

Affiliation: a Instituto de Neurociencias; Consejo Superior de Investigaciones Científicas (CSIC); and Universidad Miguel Hernández (UMH) ; Campus de Sant Joan, Apartado 18, 03550 Sant Joan, Alicante , Spain.

ABSTRACT
Stem cells are responsible for preserving morphology and function of adult tissues. Stem cells divide to self-renew and to generate progenitor cells to sustain cell demand from the tissue throughout the organism's life. Unlike stem cells, the progenitor cells have limited proliferation potential but have the capacity to terminally differentiate and thereby to substitute older or damaged mature cells. Recent findings indicate that adult stem cells can adapt their division kinetics dynamically to match changes in tissue demand during homeostasis and regeneration. However, cell turnover not only requires stem cell division but also needs timed differentiation of the progenitor cells, which has been much less explored. In this Extra View article, we discuss the ability of progenitor cells to actively postpone terminal differentiation in the absence of a local demand and how tissue demand activates terminal differentiation via a conserved mesenchymal-epithelial transition program revealed in our recent EMBO J paper and other published and unpublished data. The extent of the significance of these results is discussed for models of tissue dynamics during both homeostasis and regeneration.

No MeSH data available.


Related in: MedlinePlus

Progenitor cells have a marked planar cell polarity characterized by long protrusions and can sense the surrounding epithelial cells determining where to differentiate. A) Intestinal stem (ISC) and progenitor cells (EB) are marked by escargot-GAL4>UAS-CD8::GFP while EB co-stain with a Su(H)-LacZ reporter. Arrows indicate ISCs, arrowheads EBs. B-B″) Comparative morphological analysis of stem vs. progenitor cells. Bars represent mean and standard deviation of the mean. B) Circularity describes how close the relation between the area and perimeter of the cell shape is to that of a perfect circle. B′) Aspect ratio reflects the degree of elongation. B″) Solidity describes convexity of the cell shape. C-C′) An EB sending a long protrusion (arrowhead) toward a not yet replenished area which has lower density of EBs (red dashed line). D-D′) EBs which protrusions are likely repulsed (arrowheads) from areas which have already been replenished (red dashed area). **** = p-value <0.0001 (2 tails unpaired T-test). Scalebar = 50 µM.
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f0001: Progenitor cells have a marked planar cell polarity characterized by long protrusions and can sense the surrounding epithelial cells determining where to differentiate. A) Intestinal stem (ISC) and progenitor cells (EB) are marked by escargot-GAL4>UAS-CD8::GFP while EB co-stain with a Su(H)-LacZ reporter. Arrows indicate ISCs, arrowheads EBs. B-B″) Comparative morphological analysis of stem vs. progenitor cells. Bars represent mean and standard deviation of the mean. B) Circularity describes how close the relation between the area and perimeter of the cell shape is to that of a perfect circle. B′) Aspect ratio reflects the degree of elongation. B″) Solidity describes convexity of the cell shape. C-C′) An EB sending a long protrusion (arrowhead) toward a not yet replenished area which has lower density of EBs (red dashed line). D-D′) EBs which protrusions are likely repulsed (arrowheads) from areas which have already been replenished (red dashed area). **** = p-value <0.0001 (2 tails unpaired T-test). Scalebar = 50 µM.

Mentions: The escargot-ReDDM marking of stem and progenitor cells takes advantage of a membrane tethered GFP originally designed to highlight neuronal processes.20,21 This approach facilitated the comprehensive analysis of the cellular architectures of intestinal stem cells (ISCs) and committed progenitor cells (enteroblasts, EB). As previously described, ISCs are small round cells that are basally located in the midgut epithelium.22-24 However, in stark contrast, progenitor cells have a front-rear polarity and extend long protrusions and branching, typical of migrating mesenchymal cells (Fig. 1). In addition, using ex-vivo live imaging of whole intestine, we detected occasional movements and repositioning of progenitor cells, further highlighting not only the mesenchymal traits but also the mesenchymal behavior of progenitors. Finally, terminal differentiation involved a mesenchymal-epithelial transition and the repression of the mesenchymal factors escargot and zfh1 and the activation of epithelial markers such as Dlg-1 (Antonello et al. 2015).Figure 1.


Mesenchymal to epithelial transition during tissue homeostasis and regeneration: Patching up the Drosophila midgut epithelium.

Antonello ZA, Reiff T, Dominguez M - Fly (Austin) (2015)

Progenitor cells have a marked planar cell polarity characterized by long protrusions and can sense the surrounding epithelial cells determining where to differentiate. A) Intestinal stem (ISC) and progenitor cells (EB) are marked by escargot-GAL4>UAS-CD8::GFP while EB co-stain with a Su(H)-LacZ reporter. Arrows indicate ISCs, arrowheads EBs. B-B″) Comparative morphological analysis of stem vs. progenitor cells. Bars represent mean and standard deviation of the mean. B) Circularity describes how close the relation between the area and perimeter of the cell shape is to that of a perfect circle. B′) Aspect ratio reflects the degree of elongation. B″) Solidity describes convexity of the cell shape. C-C′) An EB sending a long protrusion (arrowhead) toward a not yet replenished area which has lower density of EBs (red dashed line). D-D′) EBs which protrusions are likely repulsed (arrowheads) from areas which have already been replenished (red dashed area). **** = p-value <0.0001 (2 tails unpaired T-test). Scalebar = 50 µM.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4862424&req=5

f0001: Progenitor cells have a marked planar cell polarity characterized by long protrusions and can sense the surrounding epithelial cells determining where to differentiate. A) Intestinal stem (ISC) and progenitor cells (EB) are marked by escargot-GAL4>UAS-CD8::GFP while EB co-stain with a Su(H)-LacZ reporter. Arrows indicate ISCs, arrowheads EBs. B-B″) Comparative morphological analysis of stem vs. progenitor cells. Bars represent mean and standard deviation of the mean. B) Circularity describes how close the relation between the area and perimeter of the cell shape is to that of a perfect circle. B′) Aspect ratio reflects the degree of elongation. B″) Solidity describes convexity of the cell shape. C-C′) An EB sending a long protrusion (arrowhead) toward a not yet replenished area which has lower density of EBs (red dashed line). D-D′) EBs which protrusions are likely repulsed (arrowheads) from areas which have already been replenished (red dashed area). **** = p-value <0.0001 (2 tails unpaired T-test). Scalebar = 50 µM.
Mentions: The escargot-ReDDM marking of stem and progenitor cells takes advantage of a membrane tethered GFP originally designed to highlight neuronal processes.20,21 This approach facilitated the comprehensive analysis of the cellular architectures of intestinal stem cells (ISCs) and committed progenitor cells (enteroblasts, EB). As previously described, ISCs are small round cells that are basally located in the midgut epithelium.22-24 However, in stark contrast, progenitor cells have a front-rear polarity and extend long protrusions and branching, typical of migrating mesenchymal cells (Fig. 1). In addition, using ex-vivo live imaging of whole intestine, we detected occasional movements and repositioning of progenitor cells, further highlighting not only the mesenchymal traits but also the mesenchymal behavior of progenitors. Finally, terminal differentiation involved a mesenchymal-epithelial transition and the repression of the mesenchymal factors escargot and zfh1 and the activation of epithelial markers such as Dlg-1 (Antonello et al. 2015).Figure 1.

Bottom Line: Stem cells divide to self-renew and to generate progenitor cells to sustain cell demand from the tissue throughout the organism's life.In this Extra View article, we discuss the ability of progenitor cells to actively postpone terminal differentiation in the absence of a local demand and how tissue demand activates terminal differentiation via a conserved mesenchymal-epithelial transition program revealed in our recent EMBO J paper and other published and unpublished data.The extent of the significance of these results is discussed for models of tissue dynamics during both homeostasis and regeneration.

View Article: PubMed Central - PubMed

Affiliation: a Instituto de Neurociencias; Consejo Superior de Investigaciones Científicas (CSIC); and Universidad Miguel Hernández (UMH) ; Campus de Sant Joan, Apartado 18, 03550 Sant Joan, Alicante , Spain.

ABSTRACT
Stem cells are responsible for preserving morphology and function of adult tissues. Stem cells divide to self-renew and to generate progenitor cells to sustain cell demand from the tissue throughout the organism's life. Unlike stem cells, the progenitor cells have limited proliferation potential but have the capacity to terminally differentiate and thereby to substitute older or damaged mature cells. Recent findings indicate that adult stem cells can adapt their division kinetics dynamically to match changes in tissue demand during homeostasis and regeneration. However, cell turnover not only requires stem cell division but also needs timed differentiation of the progenitor cells, which has been much less explored. In this Extra View article, we discuss the ability of progenitor cells to actively postpone terminal differentiation in the absence of a local demand and how tissue demand activates terminal differentiation via a conserved mesenchymal-epithelial transition program revealed in our recent EMBO J paper and other published and unpublished data. The extent of the significance of these results is discussed for models of tissue dynamics during both homeostasis and regeneration.

No MeSH data available.


Related in: MedlinePlus