The neurotrophins brain-derived neurotrophic factor (BDNF) and neurotrophin-3 (NT-3), as well as their respective tyrosine kinase (Trk) receptors, TrkB and TrkC, influence peripheral target cell innervation, survival, and proliferation. In the mature taste system the role of neurotrophins and their receptors is not known. The mature hamster is an intriguing model because anterior lingual fungiform, unlike posterior lingual foliate and circumvallate, taste buds survive denervation. In light of this difference, we examined whether the degree of neurotrophin- or neurotrophin receptor-like immunoreactivity (IR) normally differs among lingual gemmal fields. In single- and double-labeled immunofluorescent experiments, 3,209 taste bud sections (profiles) from 13 hamsters were examined for immunopositive gemmal cells or nerve fibers using antibodies to BDNF and NT-3, their respective receptors TrkB and TrkC, and the neural marker ubiquitin c-terminal hydrolase L-1 [protein gene product (PGP) 9.5]. In each gemmal field, more than 75% of taste bud profiles showed immunopositivity to BDNF, NT-3, and TrkB. Across bud fields, BDNF-, TrkB-, and BDNF/TrkB-like IR, as well as PGP 9.5 and PGP 9.5/BDNF-like IR in centrally located, fungiform bud cells was greater (P < 0.0001 to P < 0.002) than in circumvallate or foliate buds. Within bud fields, the number of BDNF-like, labeled bud cells/bud profile was greater than that for NT-3-like IR in fungiform (P < 0.0002) and foliate (P < 0.0001) buds. TrkC was immunonegative in gemmal cells. The average density of TrkB- and TrkC-like fiber IR was more pronounced in fungiform than posterior gemmal-bearing papillae. Thus, fungiform papillae, whose taste buds are least affected by denervation, exhibit specific neurotrophin and receptor enrichment.
Unlike lingual taste buds in most mammals, fungiform buds on the anterior tongue of mature hamster survive sensory denervation. The role of the neurotrophin ligands, brain-derived neurotrophic factor (BDNF) and neurotrophin-3 (NT-3), and their respective tyrosine kinase (Trk) receptors, TrkB and TrkC, in denervated taste buds is not known. The present report investigates changes in the degree of gemmal cell immunoreactivity (IR) (i.e., number of immunoreactive cells/bud profile) and density of nerve fiber-IR of these markers in unilaterally denervated mature hamsters. The fungiform bud field after chorda tympani/lingual nerve resection is compared with the nerve-dependent, posterior tongue foliate and circumvallate bud fields after glossopharyngeal nerve resection. Four weeks post lesion, the number of denervated fungiform buds matched that on the unoperated side, whereas denervated foliate and circumvallate bud counts decreased by 72% and 38%, respectively. In taste buds that survived on the posterior tongue, the degree of foliate bud cell BDNF-, NT-3-, and TrkB-like IR, and circumvallate bud cell BDNF- and NT-3-like IR, significantly decreased compared with the unoperated side. In contrast, for anterior tongue fungiform bud cells, the degree of neurotrophin- and receptor-like IR was relatively less affected: NT-3- and TrkB-like IR were unchanged; BDNF-like IR, although significantly decreased, was also maintained. Moreover, TrkB-like fiber IR was essentially eliminated within and surrounding fungiform buds. Hence, NT-3-, BDNF-, and TrkB-like IR in fungiform gemmal cells may reflect an autocrine capacity promoting survival. Because TrkC-like IR in bud cells is absent (i.e., immunonegative), and sparse in fibers intragemmally and perigemmally, NT-3 may also bind to bud cell TrkB so as to sustain fungiform gemmal cell viability post denervation.
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