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Embryonic frog epidermis: a model for the study of cell-cell interactions in the development of mucociliary disease.

Dubaissi E, Papalopulu N - Dis Model Mech (2010)

Bottom Line: These cells express high levels of ion channels and transporters; therefore, we suggest that they are analogous to ionocytes found in transporting epithelia such as the mammalian kidney.Depletion of ionocytes by foxi1e knockdown has detrimental effects on the development of multiciliated cells, which show fewer and aberrantly beating cilia.These results reveal a newly identified role for ionocytes and suggest that the frog embryonic skin is a model system that is particularly suited to studying the interactions of different cell types in mucociliary, as well as in secretory and transporting, epithelia.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, University of Manchester, Manchester, UK.

ABSTRACT
Specialised epithelia such as mucociliary, secretory and transporting epithelia line all major organs, including the lung, gut and kidney. Malfunction of these epithelia is associated with many human diseases. The frog embryonic epidermis possesses mucus-secreting and multiciliated cells, and has served as an excellent model system for the biogenesis of cilia. However, ionic regulation is important for the function of all specialised epithelia and it is not clear how this is achieved in the embryonic frog epidermis. Here, we show that a third cell type develops alongside ciliated and mucus-secreting cells in the tadpole skin. These cells express high levels of ion channels and transporters; therefore, we suggest that they are analogous to ionocytes found in transporting epithelia such as the mammalian kidney. We show that frog ionocytes express the transcription factor foxi1e, which is required for the development of these cells. Depletion of ionocytes by foxi1e knockdown has detrimental effects on the development of multiciliated cells, which show fewer and aberrantly beating cilia. These results reveal a newly identified role for ionocytes and suggest that the frog embryonic skin is a model system that is particularly suited to studying the interactions of different cell types in mucociliary, as well as in secretory and transporting, epithelia.

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Ionocytes (cells expressing ion modulators) show a scattered epidermal distribution. (A) Images of whole-mounted X. tropicalis tadpole skin (stage 27) showing that ciliated cells, visualised with an α1-tubulin probe, and goblet cells, recognised by staining with an anti-lectin antibody, anti-xeel (red), account for the majority of cells in this tissue. However, a cell type that does not express either α1-tubulin nor xeel is also present (arrow). Approximately 60% of cells in this tissue are goblet cells, 18% are ciliated cells and approximately 22% represent an uncharacterised cell type(s). (B) Model for the development of the mucociliary epidermis of Xenopus. During the early neurula stage, ciliated cells (red) and other INCs (green) are specified in the inner epidermal layer (1; yellow). By the late neurula stage, both cell types intercalate into the outer layer (2; blue), where ciliated cells undergo ciliogenesis (3) [modified from Stubbs et al. (Stubbs et al., 2006)]. (C) Several ion transporters and enzymes show a scattered, punctate expression pattern in the epidermis by in situ hybridisation. This includes three subunits of the v-atpase enzyme complex (v1a, v1g and v0d), ca12 (also expressed in the otic vesicle and olfactory placode), slc26a4 (pendrin) and mct4 (also expressed in the somites). ov, otic vesicle; op, olfactory placode; s, somites. (D) Sectioning of embryos probed for v1a or ca12 (red) by fluorescent in situ hybridisation and DAPI staining for nuclei (blue). At the neurula stage (stage 14), cells expressing v1a and ca12 are located in the inner layer of the epidermis and then move into the outer layer by tailbud stage (stage 25). Scale bars: 50 μm (A,D); 250 μm (C).
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f1-0040179: Ionocytes (cells expressing ion modulators) show a scattered epidermal distribution. (A) Images of whole-mounted X. tropicalis tadpole skin (stage 27) showing that ciliated cells, visualised with an α1-tubulin probe, and goblet cells, recognised by staining with an anti-lectin antibody, anti-xeel (red), account for the majority of cells in this tissue. However, a cell type that does not express either α1-tubulin nor xeel is also present (arrow). Approximately 60% of cells in this tissue are goblet cells, 18% are ciliated cells and approximately 22% represent an uncharacterised cell type(s). (B) Model for the development of the mucociliary epidermis of Xenopus. During the early neurula stage, ciliated cells (red) and other INCs (green) are specified in the inner epidermal layer (1; yellow). By the late neurula stage, both cell types intercalate into the outer layer (2; blue), where ciliated cells undergo ciliogenesis (3) [modified from Stubbs et al. (Stubbs et al., 2006)]. (C) Several ion transporters and enzymes show a scattered, punctate expression pattern in the epidermis by in situ hybridisation. This includes three subunits of the v-atpase enzyme complex (v1a, v1g and v0d), ca12 (also expressed in the otic vesicle and olfactory placode), slc26a4 (pendrin) and mct4 (also expressed in the somites). ov, otic vesicle; op, olfactory placode; s, somites. (D) Sectioning of embryos probed for v1a or ca12 (red) by fluorescent in situ hybridisation and DAPI staining for nuclei (blue). At the neurula stage (stage 14), cells expressing v1a and ca12 are located in the inner layer of the epidermis and then move into the outer layer by tailbud stage (stage 25). Scale bars: 50 μm (A,D); 250 μm (C).

Mentions: The Xenopus larval epidermis is known to consist of mucus-secreting goblet cells and ciliated cells, bearing multiple beating cilia (Billett and Gould, 1971). However, double staining with a ciliated-cell marker and a goblet-cell marker revealed the presence of additional cells that are found in almost equal numbers as the ciliated cells (Fig. 1A, arrow) but their molecular profile and physiological properties are not known. Previous studies have reported a population of uncharacterised intercalating non-ciliated cells (INCs) that intercalate in an irregular pattern (Stubbs et al., 2006) (Fig. 1B). Such an uncharacterised population has also been shown, or inferred, in previous studies as developing alongside mucus-secreting goblet cells (Billett and Gould, 1971; Hayes et al., 2007; Mitchell et al., 2009; Montorzi et al., 2000; Nickells et al., 1988; Stubbs et al., 2006).


Embryonic frog epidermis: a model for the study of cell-cell interactions in the development of mucociliary disease.

Dubaissi E, Papalopulu N - Dis Model Mech (2010)

Ionocytes (cells expressing ion modulators) show a scattered epidermal distribution. (A) Images of whole-mounted X. tropicalis tadpole skin (stage 27) showing that ciliated cells, visualised with an α1-tubulin probe, and goblet cells, recognised by staining with an anti-lectin antibody, anti-xeel (red), account for the majority of cells in this tissue. However, a cell type that does not express either α1-tubulin nor xeel is also present (arrow). Approximately 60% of cells in this tissue are goblet cells, 18% are ciliated cells and approximately 22% represent an uncharacterised cell type(s). (B) Model for the development of the mucociliary epidermis of Xenopus. During the early neurula stage, ciliated cells (red) and other INCs (green) are specified in the inner epidermal layer (1; yellow). By the late neurula stage, both cell types intercalate into the outer layer (2; blue), where ciliated cells undergo ciliogenesis (3) [modified from Stubbs et al. (Stubbs et al., 2006)]. (C) Several ion transporters and enzymes show a scattered, punctate expression pattern in the epidermis by in situ hybridisation. This includes three subunits of the v-atpase enzyme complex (v1a, v1g and v0d), ca12 (also expressed in the otic vesicle and olfactory placode), slc26a4 (pendrin) and mct4 (also expressed in the somites). ov, otic vesicle; op, olfactory placode; s, somites. (D) Sectioning of embryos probed for v1a or ca12 (red) by fluorescent in situ hybridisation and DAPI staining for nuclei (blue). At the neurula stage (stage 14), cells expressing v1a and ca12 are located in the inner layer of the epidermis and then move into the outer layer by tailbud stage (stage 25). Scale bars: 50 μm (A,D); 250 μm (C).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC3046089&req=5

f1-0040179: Ionocytes (cells expressing ion modulators) show a scattered epidermal distribution. (A) Images of whole-mounted X. tropicalis tadpole skin (stage 27) showing that ciliated cells, visualised with an α1-tubulin probe, and goblet cells, recognised by staining with an anti-lectin antibody, anti-xeel (red), account for the majority of cells in this tissue. However, a cell type that does not express either α1-tubulin nor xeel is also present (arrow). Approximately 60% of cells in this tissue are goblet cells, 18% are ciliated cells and approximately 22% represent an uncharacterised cell type(s). (B) Model for the development of the mucociliary epidermis of Xenopus. During the early neurula stage, ciliated cells (red) and other INCs (green) are specified in the inner epidermal layer (1; yellow). By the late neurula stage, both cell types intercalate into the outer layer (2; blue), where ciliated cells undergo ciliogenesis (3) [modified from Stubbs et al. (Stubbs et al., 2006)]. (C) Several ion transporters and enzymes show a scattered, punctate expression pattern in the epidermis by in situ hybridisation. This includes three subunits of the v-atpase enzyme complex (v1a, v1g and v0d), ca12 (also expressed in the otic vesicle and olfactory placode), slc26a4 (pendrin) and mct4 (also expressed in the somites). ov, otic vesicle; op, olfactory placode; s, somites. (D) Sectioning of embryos probed for v1a or ca12 (red) by fluorescent in situ hybridisation and DAPI staining for nuclei (blue). At the neurula stage (stage 14), cells expressing v1a and ca12 are located in the inner layer of the epidermis and then move into the outer layer by tailbud stage (stage 25). Scale bars: 50 μm (A,D); 250 μm (C).
Mentions: The Xenopus larval epidermis is known to consist of mucus-secreting goblet cells and ciliated cells, bearing multiple beating cilia (Billett and Gould, 1971). However, double staining with a ciliated-cell marker and a goblet-cell marker revealed the presence of additional cells that are found in almost equal numbers as the ciliated cells (Fig. 1A, arrow) but their molecular profile and physiological properties are not known. Previous studies have reported a population of uncharacterised intercalating non-ciliated cells (INCs) that intercalate in an irregular pattern (Stubbs et al., 2006) (Fig. 1B). Such an uncharacterised population has also been shown, or inferred, in previous studies as developing alongside mucus-secreting goblet cells (Billett and Gould, 1971; Hayes et al., 2007; Mitchell et al., 2009; Montorzi et al., 2000; Nickells et al., 1988; Stubbs et al., 2006).

Bottom Line: These cells express high levels of ion channels and transporters; therefore, we suggest that they are analogous to ionocytes found in transporting epithelia such as the mammalian kidney.Depletion of ionocytes by foxi1e knockdown has detrimental effects on the development of multiciliated cells, which show fewer and aberrantly beating cilia.These results reveal a newly identified role for ionocytes and suggest that the frog embryonic skin is a model system that is particularly suited to studying the interactions of different cell types in mucociliary, as well as in secretory and transporting, epithelia.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, University of Manchester, Manchester, UK.

ABSTRACT
Specialised epithelia such as mucociliary, secretory and transporting epithelia line all major organs, including the lung, gut and kidney. Malfunction of these epithelia is associated with many human diseases. The frog embryonic epidermis possesses mucus-secreting and multiciliated cells, and has served as an excellent model system for the biogenesis of cilia. However, ionic regulation is important for the function of all specialised epithelia and it is not clear how this is achieved in the embryonic frog epidermis. Here, we show that a third cell type develops alongside ciliated and mucus-secreting cells in the tadpole skin. These cells express high levels of ion channels and transporters; therefore, we suggest that they are analogous to ionocytes found in transporting epithelia such as the mammalian kidney. We show that frog ionocytes express the transcription factor foxi1e, which is required for the development of these cells. Depletion of ionocytes by foxi1e knockdown has detrimental effects on the development of multiciliated cells, which show fewer and aberrantly beating cilia. These results reveal a newly identified role for ionocytes and suggest that the frog embryonic skin is a model system that is particularly suited to studying the interactions of different cell types in mucociliary, as well as in secretory and transporting, epithelia.

Show MeSH
Related in: MedlinePlus