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Ecdysteroids affect Drosophila ovarian stem cell niche formation and early germline differentiation.

König A, Yatsenko AS, Weiss M, Shcherbata HR - EMBO J. (2011)

Bottom Line: This differentiation impediment is associated with reduced TGF-β signalling in the germline and increased levels of cell adhesion complexes and cytoskeletal proteins in somatic escort cells.A co-activator of the ecdysone receptor, Taiman is the spatially restricted regulator of the ecdysone signalling pathway in soma.Additionally, when ecdysone signalling is perturbed during the process of somatic stem cell niche establishment enlarged functional niches able to host additional stem cells are formed.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Research Group of Gene Expression and Signaling, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany.

ABSTRACT
Previously, it has been shown that in Drosophila steroid hormones are required for progression of oogenesis during late stages of egg maturation. Here, we show that ecdysteroids regulate progression through the early steps of germ cell lineage. Upon ecdysone signalling deficit germline stem cell progeny delay to switch on a differentiation programme. This differentiation impediment is associated with reduced TGF-β signalling in the germline and increased levels of cell adhesion complexes and cytoskeletal proteins in somatic escort cells. A co-activator of the ecdysone receptor, Taiman is the spatially restricted regulator of the ecdysone signalling pathway in soma. Additionally, when ecdysone signalling is perturbed during the process of somatic stem cell niche establishment enlarged functional niches able to host additional stem cells are formed.

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Related in: MedlinePlus

The ecdysone receptor co-activator Taiman controls the number of ovarian germline stem cell niche cells. (A) Schematic view of a wild-type germarium: germline stem cells (GSCs, pink) marked by anterior spectrosomes (SS, red dots) are located at the apex of the germarium next to the niche cap cells (CpCs, grey). Further noted are terminal filament (TF; dark blue), escort stem cells (ESCs, olive), differentiating cystoblasts (CBs, blue), escort cells (ECs, lime), 4, 8 (bright green) and 16 cell (green) cysts in region 2A, indicated by the presence of fusomes (FS, red branched structures), follicle stem cells (FSCs, violet) and follicle cells (FC, light grey) in regions 2B and 3. (B) Schematic view of a tai mutant germarium with an increased number of single spectrosome containing cells (SSCs, pink and blue), CpCs (grey) and additional somatic cells (plum). (C, E) In wild-type germaria, two GSCs marked by the presence of the stem cell marker pMad (C), spectrosomes (stained with Adducin) and the absence of the differentiation factor BamC (E) are directly attached to the niche (marked with LaminC, arrows). (D, F) In the tai61G1/taiBG02711 transheterozygous mutant germarium, the enlarged niche is coupled with an increased number of GSCs that are pMad positive (D) and BamC negative (F). In addition, extra somatic cells are present at the anterior (marked with brackets). CpC (G) and GSC (H) numbers are increased in tai mutant germaria. (I) Scheme illustrating that Tai is a co-activator of the EcR/USP nuclear receptor complex that is activated upon binding of its ligand ecdysone; Ab negatively regulates the ecdysone signalling by direct binding to Tai (based on Bai et al (2000) and Jang et al (2009)). (J) EcRQ50st/tai61G1 transheterozygous germaria also contain an increased number of GSCs and CpCs, indicating that tai genetically interacts with EcR (see Supplementary Table S1). (D–F, J) Projections of optical sections assembled through the germarial tissue; GSCs are outlined with yellow dashed lines, niche cells are marked with white arrows; Red, Adducin+LaminC; blue, DAPI; and green, pMad (C, D), BamGFP (E), BamC (F) and Vasa (J); Error bars represent s.e.m. *P<0.05, **P<0.005, ***P<0.0005.
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f1: The ecdysone receptor co-activator Taiman controls the number of ovarian germline stem cell niche cells. (A) Schematic view of a wild-type germarium: germline stem cells (GSCs, pink) marked by anterior spectrosomes (SS, red dots) are located at the apex of the germarium next to the niche cap cells (CpCs, grey). Further noted are terminal filament (TF; dark blue), escort stem cells (ESCs, olive), differentiating cystoblasts (CBs, blue), escort cells (ECs, lime), 4, 8 (bright green) and 16 cell (green) cysts in region 2A, indicated by the presence of fusomes (FS, red branched structures), follicle stem cells (FSCs, violet) and follicle cells (FC, light grey) in regions 2B and 3. (B) Schematic view of a tai mutant germarium with an increased number of single spectrosome containing cells (SSCs, pink and blue), CpCs (grey) and additional somatic cells (plum). (C, E) In wild-type germaria, two GSCs marked by the presence of the stem cell marker pMad (C), spectrosomes (stained with Adducin) and the absence of the differentiation factor BamC (E) are directly attached to the niche (marked with LaminC, arrows). (D, F) In the tai61G1/taiBG02711 transheterozygous mutant germarium, the enlarged niche is coupled with an increased number of GSCs that are pMad positive (D) and BamC negative (F). In addition, extra somatic cells are present at the anterior (marked with brackets). CpC (G) and GSC (H) numbers are increased in tai mutant germaria. (I) Scheme illustrating that Tai is a co-activator of the EcR/USP nuclear receptor complex that is activated upon binding of its ligand ecdysone; Ab negatively regulates the ecdysone signalling by direct binding to Tai (based on Bai et al (2000) and Jang et al (2009)). (J) EcRQ50st/tai61G1 transheterozygous germaria also contain an increased number of GSCs and CpCs, indicating that tai genetically interacts with EcR (see Supplementary Table S1). (D–F, J) Projections of optical sections assembled through the germarial tissue; GSCs are outlined with yellow dashed lines, niche cells are marked with white arrows; Red, Adducin+LaminC; blue, DAPI; and green, pMad (C, D), BamGFP (E), BamC (F) and Vasa (J); Error bars represent s.e.m. *P<0.05, **P<0.005, ***P<0.0005.

Mentions: The Drosophila ovary contains distinct populations of stem cells: GSCs, which give rise to the gametes, and two types of somatic stem cells: ESCs and follicle stem cells (FSCs) (Figure 1A). These stem cells reside in stereotyped positions inside the germarium, a specialised structure at the anterior end of the Drosophila ovary. Both GSCs and ESCs are adjacent to somatic signalling centres or niches consisting of the terminal filament (TF) and cap cells (CpCs), which promote stem cell identity. ESCs produce squamous daughters with long processes that encase developing cysts to protect them from niche signalling and allow differentiation. These different cell types have distinct morphologies and molecular markers (Figure 1C and E).


Ecdysteroids affect Drosophila ovarian stem cell niche formation and early germline differentiation.

König A, Yatsenko AS, Weiss M, Shcherbata HR - EMBO J. (2011)

The ecdysone receptor co-activator Taiman controls the number of ovarian germline stem cell niche cells. (A) Schematic view of a wild-type germarium: germline stem cells (GSCs, pink) marked by anterior spectrosomes (SS, red dots) are located at the apex of the germarium next to the niche cap cells (CpCs, grey). Further noted are terminal filament (TF; dark blue), escort stem cells (ESCs, olive), differentiating cystoblasts (CBs, blue), escort cells (ECs, lime), 4, 8 (bright green) and 16 cell (green) cysts in region 2A, indicated by the presence of fusomes (FS, red branched structures), follicle stem cells (FSCs, violet) and follicle cells (FC, light grey) in regions 2B and 3. (B) Schematic view of a tai mutant germarium with an increased number of single spectrosome containing cells (SSCs, pink and blue), CpCs (grey) and additional somatic cells (plum). (C, E) In wild-type germaria, two GSCs marked by the presence of the stem cell marker pMad (C), spectrosomes (stained with Adducin) and the absence of the differentiation factor BamC (E) are directly attached to the niche (marked with LaminC, arrows). (D, F) In the tai61G1/taiBG02711 transheterozygous mutant germarium, the enlarged niche is coupled with an increased number of GSCs that are pMad positive (D) and BamC negative (F). In addition, extra somatic cells are present at the anterior (marked with brackets). CpC (G) and GSC (H) numbers are increased in tai mutant germaria. (I) Scheme illustrating that Tai is a co-activator of the EcR/USP nuclear receptor complex that is activated upon binding of its ligand ecdysone; Ab negatively regulates the ecdysone signalling by direct binding to Tai (based on Bai et al (2000) and Jang et al (2009)). (J) EcRQ50st/tai61G1 transheterozygous germaria also contain an increased number of GSCs and CpCs, indicating that tai genetically interacts with EcR (see Supplementary Table S1). (D–F, J) Projections of optical sections assembled through the germarial tissue; GSCs are outlined with yellow dashed lines, niche cells are marked with white arrows; Red, Adducin+LaminC; blue, DAPI; and green, pMad (C, D), BamGFP (E), BamC (F) and Vasa (J); Error bars represent s.e.m. *P<0.05, **P<0.005, ***P<0.0005.
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f1: The ecdysone receptor co-activator Taiman controls the number of ovarian germline stem cell niche cells. (A) Schematic view of a wild-type germarium: germline stem cells (GSCs, pink) marked by anterior spectrosomes (SS, red dots) are located at the apex of the germarium next to the niche cap cells (CpCs, grey). Further noted are terminal filament (TF; dark blue), escort stem cells (ESCs, olive), differentiating cystoblasts (CBs, blue), escort cells (ECs, lime), 4, 8 (bright green) and 16 cell (green) cysts in region 2A, indicated by the presence of fusomes (FS, red branched structures), follicle stem cells (FSCs, violet) and follicle cells (FC, light grey) in regions 2B and 3. (B) Schematic view of a tai mutant germarium with an increased number of single spectrosome containing cells (SSCs, pink and blue), CpCs (grey) and additional somatic cells (plum). (C, E) In wild-type germaria, two GSCs marked by the presence of the stem cell marker pMad (C), spectrosomes (stained with Adducin) and the absence of the differentiation factor BamC (E) are directly attached to the niche (marked with LaminC, arrows). (D, F) In the tai61G1/taiBG02711 transheterozygous mutant germarium, the enlarged niche is coupled with an increased number of GSCs that are pMad positive (D) and BamC negative (F). In addition, extra somatic cells are present at the anterior (marked with brackets). CpC (G) and GSC (H) numbers are increased in tai mutant germaria. (I) Scheme illustrating that Tai is a co-activator of the EcR/USP nuclear receptor complex that is activated upon binding of its ligand ecdysone; Ab negatively regulates the ecdysone signalling by direct binding to Tai (based on Bai et al (2000) and Jang et al (2009)). (J) EcRQ50st/tai61G1 transheterozygous germaria also contain an increased number of GSCs and CpCs, indicating that tai genetically interacts with EcR (see Supplementary Table S1). (D–F, J) Projections of optical sections assembled through the germarial tissue; GSCs are outlined with yellow dashed lines, niche cells are marked with white arrows; Red, Adducin+LaminC; blue, DAPI; and green, pMad (C, D), BamGFP (E), BamC (F) and Vasa (J); Error bars represent s.e.m. *P<0.05, **P<0.005, ***P<0.0005.
Mentions: The Drosophila ovary contains distinct populations of stem cells: GSCs, which give rise to the gametes, and two types of somatic stem cells: ESCs and follicle stem cells (FSCs) (Figure 1A). These stem cells reside in stereotyped positions inside the germarium, a specialised structure at the anterior end of the Drosophila ovary. Both GSCs and ESCs are adjacent to somatic signalling centres or niches consisting of the terminal filament (TF) and cap cells (CpCs), which promote stem cell identity. ESCs produce squamous daughters with long processes that encase developing cysts to protect them from niche signalling and allow differentiation. These different cell types have distinct morphologies and molecular markers (Figure 1C and E).

Bottom Line: This differentiation impediment is associated with reduced TGF-β signalling in the germline and increased levels of cell adhesion complexes and cytoskeletal proteins in somatic escort cells.A co-activator of the ecdysone receptor, Taiman is the spatially restricted regulator of the ecdysone signalling pathway in soma.Additionally, when ecdysone signalling is perturbed during the process of somatic stem cell niche establishment enlarged functional niches able to host additional stem cells are formed.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Research Group of Gene Expression and Signaling, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany.

ABSTRACT
Previously, it has been shown that in Drosophila steroid hormones are required for progression of oogenesis during late stages of egg maturation. Here, we show that ecdysteroids regulate progression through the early steps of germ cell lineage. Upon ecdysone signalling deficit germline stem cell progeny delay to switch on a differentiation programme. This differentiation impediment is associated with reduced TGF-β signalling in the germline and increased levels of cell adhesion complexes and cytoskeletal proteins in somatic escort cells. A co-activator of the ecdysone receptor, Taiman is the spatially restricted regulator of the ecdysone signalling pathway in soma. Additionally, when ecdysone signalling is perturbed during the process of somatic stem cell niche establishment enlarged functional niches able to host additional stem cells are formed.

Show MeSH
Related in: MedlinePlus