Abstract
Zebrafish is a vertebrate teleost widely used in many areas of research. As embryos, they develop quickly and provide unique opportunities for research studies owing to their transparency for at least 48 h post fertilization. Zebrafish have many ciliated organs that include primary cilia as well as motile cilia. Using zebrafish as an animal model helps to better understand human diseases such as Primary Ciliary Dyskinesia (PCD), an autosomal recessive disorder that affects cilia motility, currently associated with more than 50 genes. The aim of this study was to validate zebrafish motile cilia, both in mono and multiciliated cells, as organelles for PCD research. For this purpose, we obtained systematic high-resolution data in both the olfactory pit (OP) and the left–right organizer (LRO), a superficial organ and a deep organ embedded in the tail of the embryo, respectively. For the analysis of their axonemal ciliary structure, we used conventional transmission electron microscopy (TEM) and electron tomography (ET). We characterised the wild-type OP cilia and showed, for the first time in zebrafish, the presence of motile cilia (9 + 2) in the periphery of the pit and the presence of immotile cilia (still 9 + 2), with absent outer dynein arms, in the centre of the pit. In addition, we reported that a central pair of microtubules in the LRO motile cilia is common in zebrafish, contrary to mouse embryos, but it is not observed in all LRO cilia from the same embryo. We further showed that the outer dynein arms of the microtubular doublet of both the OP and LRO cilia are structurally similar in dimensions to the human respiratory cilia at the resolution of TEM and ET. We conclude that zebrafish is a good model organism for PCD research but investigators need to be aware of the specific physical differences to correctly interpret their results.
Highlights
Motile cilia are centriole-derived organelles, surrounded by a membrane and containing microtubules formed by protofilaments that can be longer or shorter, depending on the number of tubulin molecules they contain, according to the function they perform [1,2,3].This structure is called the ciliary axoneme or ciliary shaft [4], a transversal term throughout species, due to the well-conserved ciliary structure [3]
We showed by electron tomography (ET) the variable presence of a central pair (CP) in the left–right organizer (LRO) monocilia, a feature hypothesised in a previous publication by Tavares et al [18]
Zebrafish have motile cilia in many of its organs, that are present since the early stages of development, as depicted in the diagram from Figure 1
Summary
Motile cilia are centriole-derived organelles, surrounded by a membrane and containing microtubules formed by protofilaments that can be longer or shorter, depending on the number of tubulin molecules they contain, according to the function they perform [1,2,3] This structure is called the ciliary axoneme or ciliary shaft [4], a transversal term throughout species, due to the well-conserved ciliary structure [3]. Motile monocilia-lacking CPs were described in the node of mice [7,8,9] These are very different from non-motile primary cilia ( with a 9 + 0 configuration) without dynein motor arms that can be found in almost every cell type having solo sensory functions and lacking the ability to generate movement [10,11]. Speculate that all combinations are present in nature, likely by adaptive evolution
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