Neural crest contribution to lingual mesenchyme, epithelium and developing taste papillae and taste buds

Abstract

The epithelium of mammalian tongue hosts most of the taste buds that transduce gustatory stimuli into neural signals. In the field of taste biology, taste bud cells have been described as arising from “local epithelium”, in distinction from many other receptor organs that are derived from neurogenic ectoderm including neural crest (NC). In fact, contribution of NC to both epithelium and mesenchyme in the developing tongue is not fully understood. In the present study we used two independent, well-characterized mouse lines, Wnt1-Cre and P0-Cre that express Cre recombinase in a NC-specific manner, in combination with two Cre reporter mouse lines, R26R and ZEG, and demonstrate a contribution of NC-derived cells to both tongue mesenchyme and epithelium including taste papillae and taste buds. In tongue mesenchyme, distribution of NC-derived cells is in close association with taste papillae. In tongue epithelium, labeled cells are observed in an initial scattered distribution and progress to a clustered pattern between papillae, and within papillae and early taste buds. This provides evidence for a contribution of NC to lingual epithelium. Together with previous reports for the origin of taste bud cells from local epithelium in postnatal mouse, we propose that NC cells migrate into and reside in the epithelium of the tongue primordium at an early embryonic stage, acquire epithelial cell phenotypes, and undergo cell proliferation and differentiation that is involved in the development of taste papillae and taste buds. Our findings lead to a new concept about derivation of taste bud cells that include a NC origin.

Localization and osteoblastic differentiation potential of neural crest-derived cells in oral tissues of adult mice

“…We also found GFP-positive regions in the tongues of adult P0 mice. In agreement with this observation, Liu et al [33] noted contributions of NCDCs to both tongue mesenchyme and epithelium in 2 independent mouse lines, Wnt1-Cre and P0-Cre, which express Cre recombinase in an NC-specific manner. They also reported that NCDCs are distributed within lingual epithelium and in mesenchyme in close association with embryonic taste papillae.…”

Coevolutionary patterning of teeth and taste buds

“…In contrast all three pathways synergistically support the maturation of tooth placodes distally. It is well established in other model organisms that teeth and taste buds are derived in part from ectomesenchyme of neural crest origin (43,44). In cichlids, neural crest-derived ectomesenchyme is likely induced to the placodes under a BMP + tooth environment expressing bmp2/4 and a BMP − taste environment, restricted by repressors like osr2 and possibly bmper.…”

Neural Crest-derived Cells in the Oral and Maxillofacial Regions of Adult Mice: Isolation and Application for Regenerative Medicine

“…GFP-positive regions, noted as green dots, were also seen on the surface of the tongue. In addition, Liu et al noted contributions of NCDCs to both tongue mesenchyme and epithelium development in 2 independent mouse lines, Wnt1-Cre and P0-Cre ; both express Cre-recombinase in an NC-speci c manner 25 . They also reported that NCDCs are distributed within the lingual epithelium and mesenchyme in close association with embryonic taste papillae formation.…”