Diversity in cell motility reveals the dynamic nature of the formation of zebrafish taste sensory organs

Abstract

Taste buds are sensory organs in jawed vertebrates, composed of distinct cell types that detect and transduce specific taste qualities. Taste bud cells differentiate from oropharyngeal epithelial progenitors, which are localized mainly in proximity to the forming organs. Despite recent progress in elucidating the molecular interactions required for taste bud cell development and function, the cell behavior underlying the organ assembly is poorly defined. Here, we used time-lapse imaging to observe the formation of taste buds in live zebrafish larvae. We found that tg(fgf8a.dr17)-expressing cells form taste buds and get rearranged within the forming organs. In addition, differentiating cells move from the epithelium to the forming organs and can be displaced between developing organs. During organ formation, tg(fgf8a.dr17) and type II taste bud cells are displaced in random, directed or confined mode relative to the taste bud they join or by which they are maintained. Finally, ascl1a activity in the 5-HT/type III cell is required to direct and maintain tg(fgf8a.dr17)-expressing cells into the taste bud. We propose that diversity in displacement modes of differentiating cells acts as a key mechanism for the highly dynamic process of taste bud assembly.

Epithelial cell behaviours during neurosensory organ formation

“…Laser ablation of Type III cells has further shown that this cell type is required for the maintenance of Fgf8a-expressing cells by the taste bud. However, none of the motility modes of Type II cells relies on the Ascl1/5-HT/Type III cell, and taste buds do form in Ascl1a −/− larvae (Soulika et al, 2016), suggesting that different molecular mechanisms regulate the motility and assembly of Type II cells into taste buds.…”

“…The cell has directed motility, i.e. it migrates, and this occurs within the epithelium of origin (intraepithelially) (Kuo and Krasnow, 2015;Noguchi et al, 2015;Soulika et al, 2016). It is currently unclear to what extent a slithering cell shares similar molecular characteristics with cohorts of cells undergoing EMT (see below).…”

“…In the example shown, two taste bud organs composed of different cells types (light blue, blue, purple cells) are shown, one of which (left) is in a more mature state than the other (right). A differentiating taste bud cell (dark blue) slithers between the two organs, within the epithelium, joins first the taste bud located on the left, then exits, migrates and integrates into the less mature organ on the right (Soulika et al, 2016).…”

“…fish and cats do not sense sweet) (Ishimaru et al, 2005;Kapsimali and Barlow, 2013;Li et al, 2005;Matsumoto et al, 2013;Oike et al, 2007;Yoshida et al, 2007). In vivo imaging and subsequent analyses of the displacement of two cell populations, one likely representing an intermediate progenitor pool (expressing Fgf8a) and a second consisting of Type II cells, showed that developing taste bud cells exhibit random, confined or directed modes of motility (see Box 2) relative to the cell closest to the centre of mass of the taste bud and, therefore, show heterogeneity in their mode of displacement (Soulika et al, 2016). In particular, within the early developing oral epithelium, Fgf8a-expressing taste bud cells form organs through confined and/or random displacement.…”

“…It has also been noted that the slithering taste bud cells make contacts with more than one cell in more than one neighbouring organs that surround them, as if they are 'choosing' the organ into which they will integrate ( Fig. 4B) (Soulika et al, 2016). The physiological significance and the molecular mechanisms underlying the diversity of cell motility during taste bud assembly remain largely unknown.…”