Bmp signalling in filiform tongue papillae development

Abstract

Objective: Tongue papillae are critical organs in mastication. There are four different types of tongue papillae; fungiform, circumvallate, foliate, and filiform papillae. Unlike the other three taste papillae, non-gustatory papillae, filiform papillae cover the entire dorsal surface of the tongue and are important structures for the mechanical stress of sucking. Filiform papillae are further classified into two subtypes with different morphologies, depending on their location on the dorsum of the tongue. The filiform papillae at the intermolar eminence have pointed tips, whereas filiform papillae with rounded tips are found in other regions (anterior tongue). It remains unknown how the shape of each type of filiform papillae are determined during their development. Bmp signalling pathway has been known to regulate mechanisms that determine the shapes of many ectodermal organs. The aim of this study was to investigate the role of Bmp signalling in filiform papillae development.

Design: Comparative in situ hybridization analysis of six Bmps (Bmp2-Bmp7) and two Bmpr genes (Bmpr1a and Bmpr1b) were carried out in filiform papillae development. We further examined tongue papillae in mice over-expressing Noggin under the keratin14 promoter (K14-Noggin).

Results: We identified a dynamic temporo-spatial expression of Bmps in filiform papillae development. The K14-Noggin mice showed pointed filiform papillae in regions of the tongue normally occupied by the rounded type.

Conclusions: Bmp signalling thus regulates the shape of filiform papillae.

Fig. 1

Mouse tongue papillae. (A) Schematic diagram of mouse tongue papillae. (B) Schematic diagram of the two types of filiform tongue papillae; pointed type in the intermolar eminence and rounded type in the anterior region. (C) Schematic diagram of the direction of sections; sagittal sections including circumvallate papillae of the intermolar eminence.

Fig. 2

P-Smad1/5/8 in filiform papilla development. Immunohistochemistry of p-Smad1/5/8 in frontal head sections of the developing tongue at E13.5 (A), E14.5 (B–D), E16.5 (E–H, J–L) and birth (I). Arrowheads indicating p-Smad1/5/8 positive cells in tongue papillae (B, E, I). Arrow indicating p-Smad1/5/8 positive cells in fungiform papillae (D). DAPI (C, F, J), p-Smad1/5/8 (A, B, D, E, G, I, K), Merge images (H, L). (F–H, J–L) High magnification of E.

Fig. 3

Bmp expression in filiform papilla development at E14.5. In situ hybridization of Bmps (A–L) and Bmp receptors (M–P) showing expression in sagittal head sections of the anterior tongue (A, C, E, G, I, K, M, O) and the intermolar eminence (B, D, F, H, J, L, N, P) at E14.5 Bmp2 (A, B) Bmp3 (C, D) Bmp4 (E, F) Bmp5 (G, H) Bmp6 (I, J) Bmp7 (K, L) Bmpr1a (M, N) and Bmpr1a (O, P). Arrowheads indicating the circumvallate papillae (B, D, F, H, J, L, N, P). (A, B, E, F, H, I–P) Inset is high magnification view of the filiform papillae. Arrowhead indicating the boundary between epithelium and mesenchyme in inset.

Fig. 4

Bmp expression in filiform papilla development at E16.5. In situ hybridization of Bmps (A–L) and Bmp receptors (M–P) showing expression in sagittal head sections of the anterior tongue (A, C, E, G, I, K, M, O) and the intermolar eminence (B, D, F, H, J, L, N, P) at E16.5. Arrowheads indicate the circumvallate papillae Bmp2 (A, B) Bmp3 (C, D) Bmp4 (E, F) Bmp5 (G, H) Bmp6 (I, J) Bmp7 (K, L) Bmpr1a (M, N) and Bmpr1a (O, P) Arrowheads indicating the circumvallate papillae (B, D, F, H, J, L, N, P). (A, B, E, F, H, K–P) Insets are high magnification views of the filiform papillae. Arrowheads indicating the boundary between epithelium and mesenchyme in insets.

Fig. 5

Bmp expression in filiform papilla development at birth. In situ hybridization of Bmps (A–L) and Bmp receptors (M–P) showing expression in sagittal head sections of the anterior tongue (A, C, E, G, I, K, M, O) and the intermolar eminence (B, D, F, H, J, L, N, P) at birth. Arrowheads indicate the circumvallate papillae Bmp2 (A, B) Bmp3 (C, D) Bmp4 (E, F) Bmp5 (G, H) Bmp6 (I, J) Bmp7 (K, L) Bmpr1a (M, N) and Bmpr1a (O, P). Arrowheads indicating the circumvallate papillae (B, D, F, H, J, L, N, P). (A, B, E, H, K, L, O, P) Insets are high magnification views of the filiform papillae. Arrowheads indicating the boundary between epithelium and mesenchyme in insets.

Fig. 6

K14 and Noggin expression and p-Smad1/5/8 localization in tongue papilla of wild-type and K14-Noggin mice. In situ hybridization showing the expression of K14 (A–D) and Noggin (E, F) in frontal head sections (A, D–F) and in sagittal head sections (B, C) of wild-type (A–E) and K14-Noggin (.F) at E12.5 (A), E14.5 (B), E16.5 (C) and five months of age (D–H). Arrowheads indicating the circumvallate papillae (B, C). (G, H) Immunohistochemistry of p-Smad1/5/8 in sagittal head sections of wild-type (G) and K14-Noggin mice (H) at five months of age. Arrowhead indicating p-Smad1/5/8 positive cells (G). T = Tongue.

Fig. 7

SEMs of Filiform papillae in K14-Noggin (A, F) Oral view of the entire tongue. (B, G) Oral view of the anterior part of the tongue. (C, H) High magnification of the intermolar eminence (1 in A, F). (D, I) High magnification of the side edge of the tongue (2 in A, F). (E, J) High magnification of the anterior part of the tongue (3 in A, F). Wild-type (A–E) and K14-Noggin mice (F–J) at five months of age.