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. 2015 Mar;94(3):421-9.
doi: 10.1177/0022034514566030. Epub 2015 Jan 9.

Different requirements for Wnt signaling in tongue myogenic subpopulations

Z Zhong  1 , H Zhao  2 , J Mayo  2 , Y Chai  3
Affiliations

Different requirements for Wnt signaling in tongue myogenic subpopulations

Z Zhong et al. J Dent Res. 2015 Mar.

Abstract

The tongue is a muscular organ that is essential in vertebrates for important functions, such as food intake and communication. Little is known about regulation of myogenic progenitors during tongue development when compared with the limb or trunk region. In this study, we investigated the relationship between different myogenic subpopulations and the function of canonical Wnt signaling in regulating these subpopulations. We found that Myf5- and MyoD-expressing myogenic subpopulations exist during embryonic tongue myogenesis. In the Myf5-expressing myogenic progenitors, there is a cell-autonomous requirement for canonical Wnt signaling for cell migration and differentiation. In contrast, the MyoD-expressing subpopulation does not require canonical Wnt signaling during tongue myogenesis. Taken together, our results demonstrate that canonical Wnt signaling differentially regulates the Myf5- and MyoD-expressing subpopulations during tongue myogenesis.

Keywords: Myf5; MyoD; Wnt/β-catenin; craniofacial muscles; myogenesis; progenitors.

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Conflict of interest statement

The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

Figures

Figure 1.
Figure 1.
Myf5- and MyoD-expressing cells are distinct subpopulations during tongue myogenesis. (A–D) Detection of Myf5- and MyoD-derived cells in E10.5 Myf5-Cre;Tdtomatofl/+ (A, C) and MyoD-Cre;Tdtomatofl/+ (B, D) reporter mice, respectively. Myf5-derived cells are detectable in the hypoglossal cord (white arrows), whereas few MyoD-derived cells are detectable (open arrows). (E, F) Myf5 immunostaining (green, arrowheads) in the hypoglossal cord region of E10.5 MyoD-Cre;Tdtomatofl/+ reporter mice (MyoD-derived myogenic cells indicated by red, open arrow). Boxed area (E) is shown magnified (F). (G, H) Double immunostaining of MyoD (red) and Myf5 (green) in the hypoglossal cord at E10.5 (G) and the tongue bud at E11.0 (H) of wild-type mice. (I–L) Hematoxylin and eosin staining (I, K) and myosin heavy chain (MHC) immunostaining (J, L) of tongues from newborn (NB) Myf5-Cre;R26RDTA/+ and R26RDTA/+ control mice. (M–P) Hematoxylin and eosin staining (M, O) and MHC immunostaining (N, P) of tongues from NB MyoD-Cre;R26RDTA/+ and R26RDTA/+ control mice. Scale bars, 200 µm.
Figure 2.
Figure 2.
Activation of canonical Wnt signaling in myogenic progenitors during tongue myogenesis. (A) Whole-mount X-gal staining of E10.5 Myf5-Cre;R26R embryos. Red arrow indicates Myf5-derived cells in the hypoglossal cord. (B) Whole-mount X-gal staining of E10.5 Axin2LacZ/+ embryos. Red arrow indicates activation of the canonical Wnt signaling pathway in the hypoglossal cord region. (C–E) Visualization of Myf5-derived cells (C; red) and lacZ staining indicating activation of canonical Wnt signaling (D; blue) in adjacent sections of Myf5-Cre;Tdtomatofl/+;Axin2LacZ/+ mice. White arrow indicates Myf5 derived cells. Red arrow indicates Axin2+ cells. Colocalization is indicated by the black arrow (E). (F–H) Immunohistochemical staining of β-galactosidase (F; asterisks) and MyoD (G; white arrows) in E11.5 Axin2LacZ/+ mice embryos. Blue arrows (H) indicate colocalization. (I–L) X-gal staining of tongue buds in Axin2LacZ/+ mice at E10.5 (I), E11.5 (J), E12.5 (K), and E14.5 (L) shows activation of canonical Wnt signaling pathway. Black arrow indicates the hypoglossal cord (I). Scale bars, 200 µm.
Figure 3.
Figure 3.
Loss of β-catenin leads to migration and differentiation defects in the Myf5-expressing subpopulation. (A–D) Whole tongues (A) and hematoxylin and eosin staining of tongue sections (C, D) from E18.5 Myf5-Cre;β-cateninfl/fl (mutant) and Myf5-Cre; β-cateninfl/+ (control) mice. Quantification of the tongue area confirmed a significant difference in tongue size between Myf5-Cre;β-cateninfl/fl and control mice at E18.5 (B). *P < 0.05, n = 3. (E–H) X-gal staining of sections of tongues from E14.5 (E, F) and E18.5 (G, H) Myf5-Cre;β-cateninfl/fl;R26R and Myf5-Cre;β-cateninfl/+;R26R control mice. (I–L) Whole-mount X-gal staining (I, J) and X-gal staining of sections (K, L) of E10.5 Myf5-Cre;β-cateninfl/fl;R26R and Myf5-Cre;β-cateninfl/+;R26R control mice. Red arrows indicate migration defects of Myf5-derived cells in the hypoglossal cord (I, J). Black arrows highlight migration defects in sections from Myf5-Cre;β-cateninfl/fl; R26R mice (K, L). (M–P) Double immunostaining of MyoD (green) and β-gal (red) in E11.5 Myf5-Cre;β-cateninfl/fl;R26R and Myf5-Cre;β-cateninfl/+;R26R control mice. Boxed areas (M, N) are shown magnified (O, P). Scale bars, 200 µm.
Figure 4.
Figure 4.
Canonical Wnt signaling is not required in the MyoD-expressing subpopulation. (A–D) Whole tongues (A, C) and hematoxylin and eosin staining (B, D) of tongue sections from newborn (NB) MyoD-Cre;β-cateninfl/fl and MyoD-Cre;β-cateninfl/+ control mice. (E–H) X-gal staining of E16.5 (E, G) and NB (F, H) MyoD-Cre;β-cateninfl/fl;R26R and MyoD-Cre;β-cateninfl/+;R26R control mice. (I–L) Double immunostaining of MyoD (green) and β-gal (red) in E11.5 MyoD-Cre;β-cateninfl/fl;R26R and MyoD-Cre;β-cateninfl/+;R26R control mice. Boxed areas (I, K) are shown magnified (J, L). (M–P) Myosin heavy chain (MHC) immunostaining of NB MyoD-Cre;β-cateninfl/fl and MyoD-Cre;β-cateninfl/+ control mice. Boxed areas (M, O) are shown magnified (N, P). Scale bars, 200 µm.
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