Gustatory papillae and taste bud development and maintenance in the absence of TrkB ligands BDNF and NT-4

Ito, Akira; Nosrat, Christopher A.

doi:10.1007/s00441-009-0833-7

Cited by 28 publications

(30 citation statements)

References 52 publications

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“…2010). Although immature taste buds are detectable in embryonic taste papillae by K8-ir (Ito and Nosrat, 2009;Thirumangalathu et al, 2009), most fungiform taste buds do not express markers of specific taste cell types until the first postnatal week (Kapsimali and Barlow, 2013). Previously, we found that activation of β-catenin in K14 + embryonic epithelium caused precocious differentiation of a small number of Type II taste cells .…”

Section: Resultsmentioning

confidence: 89%

ß-Catenin signaling regulates temporally discrete phases of anterior taste bud development

Thirumangalathu

Barlow

2015

Development

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The sense of taste is mediated by multicellular taste buds located within taste papillae on the tongue. In mice, individual taste buds reside in fungiform papillae, which develop at mid-gestation as epithelial placodes in the anterior tongue. Taste placodes comprise taste bud precursor cells, which express the secreted factor sonic hedgehog (Shh) and give rise to taste bud cells that differentiate around birth. We showed previously that epithelial activation of β-catenin is the primary inductive signal for taste placode formation, followed by taste papilla morphogenesis and taste bud differentiation, but the degree to which these later elements were direct or indirect consequences of β-catenin signaling was not explored. Here, we define discrete spatiotemporal functions of β-catenin in fungiform taste bud development. Specifically, we show that early epithelial activation of β-catenin, before taste placodes form, diverts lingual epithelial cells from a taste bud fate. By contrast, β-catenin activation a day later within Shh + placodes, expands taste bud precursors directly, but enlarges papillae indirectly. Further, placodal activation of β-catenin drives precocious differentiation of Type I glial-like taste cells, but not other taste cell types. Later activation of β-catenin within Shh + precursors during papilla morphogenesis also expands taste bud precursors and accelerates Type I cell differentiation, but papilla size is no longer enhanced. Finally, although Shh regulates taste placode patterning, we find that it is dispensable for the accelerated Type I cell differentiation induced by β-catenin.

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Section: Resultsmentioning

confidence: 89%

ß-Catenin signaling regulates temporally discrete phases of anterior taste bud development

Thirumangalathu

Barlow

2015

Development

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“…Several studies suggest that the initial stages of taste papillae development are nerveindependent (Fritzsch et al 1997;Barlow and Northcutt 1998;Ito and Nosrat 2009). However, poorly innervated papillae are distorted or malformed at late embryonic and early postnatal stages (Fritzsch et al 1997;Nosrat et al 1997;Zhang et al 1997;Nosrat et al 2004;Ito and Nosrat 2009). Therefore, we have focused on the initial stages of papillary formation, when the structure of papillae is not affected by innervation.…”

Section: Discussionmentioning

confidence: 98%

“…*Statistically significant difference at P<0.05 decreased nerve supply. Smaller and sparser fungiform papillae compared with the wild-type have been reported to occur in mice deficient in brain-derived neurotropic factor (BDNF) and neurotrophin (NT), viz., BDNF -/-NT-4 -/- (Ito and Nosrat 2009), in BDNF -/-NT-3 -/-mice (Nosrat et al 2004), and in mice deficient in neurotrophin receptor TrkB (TrkB -/-; Fritzsch et al 1997) with various degrees of geniculate ganglion cell loss.…”

Section: Discussionmentioning

confidence: 99%

Regulatory role of Six1 in the development of taste papillae

Ikeda

Kawakami

2010

Cell Tissue Res

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The Six family genes encode homeobox transcription factors, and their deficiency leads to abnormal sensory organ structures. We analyzed the expression patterns of Six1 and its role in the morphogenesis of taste bud-bearing lingual papillae during mouse embryonic development. Six1 was expressed in the mesenchyme of the lateral lingual swellings at embryonic day (E) 11.5 and in the epithelium of fungiform papillae during E14.5-E17.5. In the posterior region of the tongue, Six1 expression appeared in the epithelial thickenings in the center of the dorsal surface at E13.5-E14.5 and was observed in the trench wall of circumvallate and foliate papillae at E15.5-postnatal day 0. Six1-deficient mice (Six1 (-/-)) showed distinct morphological changes: the fungiform papillae increased in size and number, and their distribution in the tongue differed from that of wild-type mice. The number of primordia of fungiform papillae marked by Shh and Wnt10b appeared to increase in Six1 ( -/- ). With regard to circumvallate papillae, more extensive invagination of epithelial thickenings, earlier formation of papillae, and stunted trenches were noted in Six1 ( -/- ); the expression of Shh was altered, consistent with these anomalies. The foliate papillae were elevated initially and showed stunted trenches in Six1 ( -/- ). Thus, the modulation of signaling events in Six1 ( -/- ) leads to the earlier formation of the gustatory papillae, the abnormal distribution of fungiform papillae, and malformed trenches in circumvallate and foliate papillae.

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“…Not all neurotrophin knockout and receptor mice lose the same number of taste buds; for example, TrkB −/− mice possess more taste buds than hybrid Bdnf −/− / Nt4 −/− mice at birth [15,17,58]. The reason for this is unclear but we speculated that the additional taste buds might be supported by BDNF or NT4 functioning via p75.…”

Section: Discussionmentioning

confidence: 99%

The neurotrophin receptor p75 regulates gustatory axon branching and promotes innervation of the tongue during development

Huang

Krimm

2014

Neural Dev

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BackgroundBrain-derived neurotrophic factor (BDNF) and neurotrophin-4 (NT4) regulate the survival of gustatory neurons, axon growth and branching, and innervation of taste buds during development. These actions are largely, but not completely, mediated through the tyrosine kinase receptor, TrkB. Here, we investigated the role of p75, the other major receptor for BDNF and NT4, in the development of the taste system.ResultsWe found that p75−/−mice showed delayed axon outgrowth and reduced branching of gustatory axons at embryonic day (E)13.5. From E14.5 to E18.5, gustatory neurons innervated fewer papillae and completely failed to innervate the mid-region of the tongue in p75−/−mice. These early effects of the p75 mutation on gustatory axons preceded the loss of geniculate ganglion neurons starting at E14.5 and also contributed to a loss of taste buds at and after birth. Because knockouts for the TrkB receptor (TrkB−/−) do not lose as many taste buds as hybrid knockouts for its two ligands (BDNF and NT4), we asked if p75 maintains those additional taste buds in the absence of TrkB. It does not; hybrid TrkB−/−/p75−/−mice had more taste buds than TrkB−/−mice; these additional taste buds were not due to an increase in neurons or innervation.Conclusionsp75 regulates gustatory neuron axon branching and tongue innervation patterns during taste system development. This function is likely accomplished independently of BDNF, NT4, and TrkB. In addition, p75 does not support the remaining neurons or taste buds in TrkB−/−mice.

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Gustatory papillae and taste bud development and maintenance in the absence of TrkB ligands BDNF and NT-4

Cited by 28 publications

References 52 publications

ß-Catenin signaling regulates temporally discrete phases of anterior taste bud development

ß-Catenin signaling regulates temporally discrete phases of anterior taste bud development

Regulatory role of Six1 in the development of taste papillae

The neurotrophin receptor p75 regulates gustatory axon branching and promotes innervation of the tongue during development

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