Abstract
Taste buds, the sensory organs for taste, have been described as arising solely from the surrounding epithelium, which is in distinction from other sensory receptors that are known to originate from neural precursors, i.e., neural ectoderm that includes neural crest (NC). Our previous study suggested a potential contribution of NC derived cells to early immature fungiform taste buds in late embryonic (E18.5) and young postnatal (P1-10) mice. In the present study we demonstrated the contribution of the underlying connective tissue (CT) to mature taste buds in mouse tongue and soft palate. Three independent mouse models were used for fate mapping of NC and NC derived connective tissue cells: (1) P0-Cre/R26-tdTomato (RFP) to label NC, NC derived Schwann cells and derivatives; (2) Dermo1-Cre/RFP to label mesenchymal cells and derivatives; and (3) Vimentin-CreER/mGFP to label Vimentin-expressing CT cells and derivatives upon tamoxifen treatment. Both P0-Cre/RFP and Dermo1-Cre/RFP labeled cells were abundant in mature taste buds in lingual taste papillae and soft palate, but not in the surrounding epithelial cells. Concurrently, labeled cells were extensively distributed in the underlying CT. RFP signals were seen in the majority of taste buds and all three types (I, II, III) of differentiated taste bud cells, with the neuronal-like type III cells labeled at a greater proportion. Further, Vimentin-CreER labeled cells were found in the taste buds of 3-month-old mice whereas Vimentin immunoreactivity was only seen in the CT. Taken together, our data demonstrate a previously unrecognized origin of taste bud cells from the underlying CT, a conceptually new finding in our knowledge of taste bud cell derivation, i.e., from both the surrounding epithelium and the underlying CT that is primarily derived from NC.
Highlights
Sensory receptors, as part of the peripheral nervous system, are known to arise from neurogenic ectoderm that includes the neural tube, neural crest (NC) or ectodermal placodes [1, 2]
A population of taste bud cells originate from underlying connective tissue in tongue and soft palate
Mammalian taste bud cells, specialized gustatory sensory organs that primarily reside in the epithelium of lingual taste papillae and soft palate [32], have both epithelial and neuronal features
Summary
As part of the peripheral nervous system, are known to arise from neurogenic ectoderm that includes the neural tube, neural crest (NC) or ectodermal placodes [1, 2]. The use of a tissue- or inducible tissue-specific Cre/loxP recombinase system has significantly advanced our knowledge pertaining to taste bud precursor/progenitor cell constitutions and how specific tissues/cell populations regulate the formation and maintenance of taste organs. Cell fate mapping using an inducible Cre/loxP system driven by a sonic hedgehog promoter (Shh-CreER) demonstrated that Shh-expressing embryonic taste papilla placodes [16] and basal cells of taste buds [17] are precursors of differentiated taste cells. With a Gli1-CreER mouse, populations of hedgehog-responding and Gli labeled progeny cells in basal epithelium and connective tissue core of the fungiform papilla were shown to contribute to maintenance of fungiform papillae and taste buds [18]. Use of an Lgr5-CreER mouse model provided evidence that Lgr5-expressing cells in the basal region of taste buds are precursors of taste bud cells [19]. Wnt1-Cre, a well characterized and widely used mouse model for labeling NC cells and their derivatives [20], has been a useful tool in demonstrating the contribution of NC to tongue mesenchyme and the important roles of NC derived cells in tongue myogenesis and morphogenesis [21]
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