Effects of glossopharyngeal nerve section on the expression of neurotrophins and their receptors in lingual taste buds of adult mice

Abstract

The expression of neurotrophins and neurotrophin receptors is essential for the proper establishment and function of many sensory systems. To determine which neurotrophins and neurotrophin receptors are expressed in taste buds, and in taste buds of mice following denervation, antibodies directed against the neurotrophins and their receptors were applied to adult mouse gustatory tissue. Immunohistochemistry reveals that nerve growth factor (NGF)-like immunoreactive (LIR), tyrosine kinase (trk) A-LIR, trkB-LIR, and p75-LIR elongated, differentiated taste cells are present within all lingual taste buds, whereas neither neurotrophin (NT)-3- nor trkC-LIR was detected in taste cells. Double-label immunohistochemistry using markers of different taste cell types in brain-derived neurotrophic factor (BDNF)LacZ mice reveals that BDNF (beta-gal) and trkB colocalize, mainly in type III taste cells. NGF, pro-NGF, and trkA coexist in type II taste cells, i.e., those expressing phospholipase Cbeta2 (PLCbeta2). p75-LIR also is present in both BDNF and NGF taste cell populations. To determine the neural dependence of neurotrophin expression in adult taste buds, glossopharyngeal nerves were cut unilaterally. During the period of denervation (10 days to 3 weeks), taste buds largely disappear, and few neurotrophin-expressing cells are present. Three weeks after nerve transection, nerve fascicles on the operated side of the tongue exhibit BDNF-LIR, NGF-LIR, and ubiquitin carboxyl terminal hydrolase (PGP 9.5)-LIR. However, BDNF-LIR staining intensity but not NGF-LIR or PGP 9.5-LIR is increased in nerve fascicles on the operated compared with the unoperated side. Five weeks following nerve transection, NT and NT receptor expression resumes and appears normal in taste buds and nerves. These results indicate that neurotrophin expression in taste buds is dependent on gustatory innervation, but expression in nerves is not dependent on contact with taste buds.

Mice lacking the p75 receptor fail to acquire a normal complement of taste buds and geniculate ganglion neurons by adulthood

“…This type of nerve-independent mechanism functions to maintain adult Merkel cells (English et al, 1994;Kinkelin et al, 1999;SieberBlum et al, 2004). However, it is unlikely that neurotrophins act directly on taste buds via p75, since unlike previous reports (Fan et al, 2004;Yee et al, 2005), no p75-like immunoreactivity was observed in taste cells. Rather, it is possible that taste buds are lost in p75 À/À mice because p75 expressing gustatory neurons are lost.…”

“…It has been reported that the p75 receptor is present not only in peripheral sensory neurons, but also in somatosensory receptor cells (i.e., Merkel cells) and taste cells (Fan et al, 2004;Yee et al, 2005). To verify these findings in the taste system, tongue sections were immunohistochemically labeled for the p75 receptor.…”

“…The p75 receptor is expressed in taste bud cells (Fan et al, 2004;Yee et al, 2005), and a small proportion of taste buds in the circumvallate papillae are lost by postnatal day 7 (P7) in p75 À/À mice (Fan et al, 2004). However, most peripheral somatosensory deficits in p75 À/À mice (e.g., Merkel cell loss and deficits in whisker pad sensory innervation) do not occur until after PN7.…”

Roles of innervation in developing and regenerating orofacial tissues

“…In rodents, bilateral resection of the glossopharyngeal nerves impairs taste bud growth [21,22], while re-establishment of innervation allows continuation of their development [21]. Additionally, innervation is required for the maintenance of taste buds: resection of the glossopharyngeal nerves in adult rodents leads to taste bud degeneration within a few weeks [21,22].…”

“…Additionally, innervation is required for the maintenance of taste buds: resection of the glossopharyngeal nerves in adult rodents leads to taste bud degeneration within a few weeks [21,22]. This effect is reversible since the regeneration of nerve fibres permits the formation of functional new taste buds [21,22].…”