FGF Signaling Regulates the Number of Posterior Taste Papillae by Controlling Progenitor Field Size

Camille I Petersen,Ophir D Klein,Andrew H Jheon,Pasha Mostowfi,Cyril Charles,Shoba Thirumangalathu,Linda A Barlow,Saunders Ching,Irma Thesleff

doi:10.1371/journal.pgen.1002098

Abstract

The sense of taste is fundamental to our ability to ingest nutritious substances and to detect and avoid potentially toxic ones. Sensory taste buds are housed in papillae that develop from epithelial placodes. Three distinct types of gustatory papillae reside on the rodent tongue: small fungiform papillae are found in the anterior tongue, whereas the posterior tongue contains the larger foliate papillae and a single midline circumvallate papilla (CVP). Despite the great variation in the number of CVPs in mammals, its importance in taste function, and its status as the largest of the taste papillae, very little is known about the development of this structure. Here, we report that a balance between Sprouty (Spry) genes and Fgf10, which respectively antagonize and activate receptor tyrosine kinase (RTK) signaling, regulates the number of CVPs. Deletion of Spry2 alone resulted in duplication of the CVP as a result of an increase in the size of the placode progenitor field, and Spry1−/−;Spry2−/− embryos had multiple CVPs, demonstrating the redundancy of Sprouty genes in regulating the progenitor field size. By contrast, deletion of Fgf10 led to absence of the CVP, identifying FGF10 as the first inductive, mesenchyme-derived factor for taste papillae. Our results provide the first demonstration of the role of epithelial-mesenchymal FGF signaling in taste papilla development, indicate that regulation of the progenitor field size by FGF signaling is a critical determinant of papilla number, and suggest that the great variation in CVP number among mammalian species may be linked to levels of signaling by the FGF pathway.

Highlights

Taste sensory capability is mediated by aggregates of receptor cells, called taste buds, which reside within the oral and pharyngeal cavities
We propose that perturbations to the Fibroblast Growth Factors (FGFs) signaling pathway may have been involved in the dramatic differences in circumvallate papilla (CVP) number that arose during mammalian evolution
Deletion of Spry2 leads to a duplication of the CVP Wild-type mice possess a single CVP in the midline of the posterior tongue; foliate papillae reside on the lateral tongue and multiple fungiform papillae populate the anterior tongue (Figure 1A, 1B)

Summary

Introduction

Taste sensory capability is mediated by aggregates of receptor cells, called taste buds, which reside within the oral and pharyngeal cavities. Fungiform papillae initially form as placodes that subsequently undergo epithelial morphogenesis and acquire a mesenchymal core [5] in a process that is similar to morphogenesis of other vertebrate epithelial specializations, such as hair, teeth, and mammary glands [6,7]. The development of these other organs requires signaling between epithelium and mesenchyme, suggesting that such epithelial-mesenchymal interactions are involved in patterning and morphogenesis of taste placodes. To date, no inductive, mesenchyme-derived factor involved in taste development has been identified

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Conclusion