Xenopus embryonic epidermis as a mucociliary cellular ecosystem to assess the effect of sex hormones in a non-reproductive context

Patricia Castillo-Briceno,Laurent Kodjabachian

doi:10.1186/1742-9994-11-9

Patricia Castillo-Briceno, Laurent Kodjabachian

Open Access

https://doi.org/10.1186/1742-9994-11-9

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Abstract

BackgroundHow important are sexual hormones beyond their function in reproductive biology has yet to be understood. In this study, we analyzed the effects of sex steroids on the biology of the embryonic amphibian epidermis, which represents an easily amenable model of non-reproductive mucociliary epithelia (MCE). MCE are integrated systems formed by multiciliated (MC), mucus-secreting (MS) and mitochondrion-rich (MR) cell populations that are shaped by their microenvironment. Therefore, MCE could be considered as ecosystems at the cellular scale, found in a wide array of contexts from mussel gills to mammalian oviduct.ResultsWe showed that the natural estrogen (estradiol, E2) and androgen (testosterone, T) as well as the synthetic estrogen (ethinyl-estradiol, EE2), all induced a significant enhancement of MC cell numbers. The effect of E2, T and EE2 extended to the MS and MR cell populations, to varying degrees. They also modified the expression profile of RNA MCE markers, and induced a range of “non-typical” cellular phenotypes, with mixed identities and aberrant morphologies, as revealed by imaging analysis through biomarker confocal detection and scanning electron microscopy. Finally, these hormones also affected tadpole pigmentation, revealing an effect on the entire cellular ecosystem of the Xenopus embryonic skin.ConclusionsThis study reveals the impact in vivo, at the molecular, cellular, tissue and organism levels, of sex steroids on non-reproductive mucociliary epithelium biogenesis, and validates the use of Xenopus as a relevant model system in this field.

Highlights

An ecosystem is defined as a biological system composed of all the organisms found in a particular physical environment, interacting with it and with each other [1]
We studied the effect of sex steroids on the epidermal mucociliary epithelia (MCE) of Xenopus embryos
Characterization of epidermal MCE architecture and differentiation during embryonic development in Xenopus In the outer layer of the differentiated epidermis of Xenopus embryos, confocal imaging of biomolecular markers specific for MS, MC and MR cells (Additional file 2) revealed a predominance of MS cells, which form a web-like layer (Figure 2A), with intercalating MC (Figure 2A,B) and MR cells (Figure 2B). This MCE arrangement was confirmed by scanning electron microscopy (SEM) morphological analysis, which allowed differentiating between ridged MR and vesicle MR cells (Figure 2C, Additional file 2)

Summary

Introduction

An ecosystem is defined as a biological system composed of all the organisms found in a particular physical environment, interacting with it and with each other [1]. Animal tissues can be considered as complex cellular ecosystems composed of different cell types that can be affected by mutual interactions as well as by the elements of their microenvironment. Under this perspective, the animal skin is interesting because of its direct relationship with endogenous and exogenous environments. Mucociliary epithelia formed by putative MC, MS and MR cell populations. We analyzed the effects of sex steroids on the biology of the embryonic amphibian epidermis, which represents an amenable model of non-reproductive mucociliary epithelia (MCE). MCE are integrated systems formed by multiciliated (MC), mucus-secreting (MS) and mitochondrion-rich (MR) cell populations that are shaped by their microenvironment. MCE could be considered as ecosystems at the cellular scale, found in a wide array of contexts from mussel gills to mammalian oviduct

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