Fate mapping of mammalian embryonic taste bud progenitors

Abstract

Mammalian taste buds have properties of both epithelial and neuronal cells, and are thus developmentally intriguing. Taste buds differentiate at birth within epithelial appendages, termed taste papillae, which arise at mid-gestation as epithelial thickenings or placodes. However, the embryonic relationship between placodes, papillae and adult taste buds has not been defined. Here, using an inducible Cre-lox fate mapping approach with the ShhcreER T2 mouse line, we demonstrate that Shh-expressing embryonic taste placodes are taste bud progenitors, which give rise to at least two different adult taste cell types, but do not contribute to taste papillae. Strikingly, placodally descendant taste cells disappear early in adult life. As placodally derived taste cells are lost, we used Wnt1Cre mice to show that the neural crest does not supply cells to taste buds, either embryonically or postnatally, thus ruling out a mesenchymal contribution to taste buds. Finally, using Bdnf null mice, which lose neurons that innervate taste buds, we demonstrate that Shh-expressing taste bud progenitors are specified and produce differentiated taste cells normally, in the absence of gustatory nerve contact. This resolution of a direct relationship between embryonic taste placodes with adult taste buds, which is independent of mesenchymal contribution and nerve contact, allows us to better define the early development of this important sensory system. These studies further suggest that mammalian taste bud development is very distinct from that of other epithelial appendages.

Neuronal delivery of Hedgehog directs spatial patterning of taste organ regeneration

“…2F and Fig. S3A), as also noted by others (21)(22)(23)(24). Note that the mG marking of Shh-expressing cells within the taste bud is driven by the CAG promoter inserted at the R26 locus.…”

Progress and renewal in gustation: new insights into taste bud development

“…tongues, and in embryos lacking gustatory innervation immature taste buds are comparable in size and number to those of controls (Hall et al, 2003;Mistretta et al, 2003;Thirumangalathu et al, 2009), leading to the conclusion that, in mammals, the embryonic development of taste buds, as well as papilla morphogenesis, are nerve independent.…”

“…Taste placodes express sonic hedgehog (Shh) (Bitgood and McMahon, 1995;Hall et al, 1999;Jung et al, 1999), and cell lineage progression can thus be traced genetically by turning on indelible reporter gene expression in these cells (Buckingham and Meilhac, 2011). Following induction of a tamoxifen-sensitive Cre allele driven by the Shh promoter (Harfe et al, 2004), Shh + placode cells gave rise exclusively to differentiated taste cells, but not to taste papilla epithelium, functionally defining Shh + taste placodes as taste bud precursor cells (Thirumangalathu et al, 2009 Lingual taste buds are housed in distributed fungiform papillae (FFP; blue) in the anterior region of the tongue, which is otherwise covered with mechanosensory filiform papillae (flp in lower inset). Bilateral foliate papillae (FolP; blue) and a single midline circumvallate papilla (CVP; blue) are located posteriorly in the tongue.…”

Roles of innervation in developing and regenerating orofacial tissues

“…Taste buds reside in three types of taste papillae of the tongue and palate [15,16] (Fig 2a): fungiform papillae are concentrated in the anterior part of the tongue, while foliate papillae and circumvallate papillae reside in the posterior region. A fourth type of papillae, the foliate papillae, does not contain taste buds.…”

“…Nevertheless, taste bud receptor cells express voltage-gated channels and release neurotransmitters onto postsynaptic neurons [15,17]. Unlike neurons and other receptor cells, bud cells are continuously regenerating [15,18].…”