The distribution of PGP9.5, BDNF and NGF in the vallate papilla of adult and developing mice

Abstract

The development and innervation of vallate papillae and taste buds in mice were studied using antibodies against the neuronal marker, protein gene product 9.5 (PGP 9.5), and against nerve growth factor (NGF) and brain-derived neurotrophic factor (BDNF). PGP 9.5 immunohistochemical studies revealed that the earliest sign of median vallate papilla formation was an epithelial bulge at embryonic day 13 (E13), and at E14, a dense nerve plexus was found within the connective tissue core of the papilla. Thin nerve fibers penetrated the apical and medial trench wall epithelium of the papilla at E16 and a few of these began to invade the lateral trench wall epithelium at E17. At postnatal day 1 (P1), the newly formed taste buds were recognizable and a small number of PGP 9.5-immunoreactive (IR) cells appeared on the medial trench wall epithelium. The number of PGP 9.5-IR taste bud cells then increased gradually and reached the adult level at postnatal week 2. PGP 9.5 immunoreactivity increased systematically with age. NGF and BDNF immunoreactivity was first seen at the boundary between the columnar cells in the apical epithelium of the developing vallate papilla at E13, then in the medial and lateral trench walls at E15 (BDNF) or E18 (NGF). At P1, BDNF immunoreactivity was exclusively present in the newly formed taste buds of the medial trench wall. The number of BDNF-IR taste bud cells then increased gradually, reaching the adult level at P7. Similar degrees of NGF and BDNF immunoreactivity were seen in the developing vallate papilla. In the present study, we found that the vallate papilla was formed prior to its innervation, and we propose that initiation of papilla formation does not require any direct influence from the specific gustatory nerve. We also suggest that neurotrophins in the early developing vallate papillae might act as local tropic factors for the embryonic growth of nerve fibers to induce differentiation of the taste buds.

Brain‐derived neurotrophic factor‐, neurotrophin‐3‐, and tyrosine kinase receptor‐like immunoreactivity in lingual taste bud fields of mature hamster

“…In addition, Table 3 shows that for each neurotrophin, the mean number of NT-3-like, or, BDNF-like immunopositive cells/bud in fungiform, foliate, and circumvallate buds is not significantly different. These immunofluorescent data are generally consistent with results obtained for rat (Nosrat et al, 1996;Cho and Farbman, 1999), mouse (Chou et al, 2001), and human (Nosrat et al, 2000) taste buds using in situ hybridization, RT-PCR, or immunocytochemical methods, in which expression of these neurotrophins was also evident in anterior or posterior lingual taste buds. However, notwithstanding the methodolgic differences employed, the present results for the mature hamster (Table 3) also reflect nuances in species difference with respect to the age at which and the degree to which each neurotrophin is expressed in mammalian tongue taste buds.…”

“…In developing rodent and human taste systems, BDNF and NT-3 mRNA are present in incipient fungiform and circumvallate papillae prior to and pari passu the appearance of their resident taste bud primordia, possibly signaling future loci of gustatory peripheral receptor innervation as well as peribud somatosensory innervation (Nosrat andOlson, 1995, 1998;Nosrat et al, 2000Nosrat et al, , 2001; see also Chou et al, 2001). In the adult, within the context of normal gemmal cell turnover and guiding of bud (re)innervation, their expression may possibly relate to the balance among cell proliferation, normal cell death, and cell survival necessary for maintaining constant bud size as well as receptoneural connectivity.…”

“…In previous studies, ubiquitin c-terminal hydrolase L-1 [i.e., protein gene product (PGP) 9.5] has been shown to label neurons of the central nervous system and peripheral nerve fibers including intragemmal and perigemmal fibers (Nosrat et al, 2000, Chou et al, 2001, Yee et al, 2001. In the present study, it is used as a general neural indicator.…”

Neuronal intermediate filaments in the developing tongue of the frog Rana esculenta

“…However, immunohistochemical data concerning the development of gustatory organs are generally scarce and mainly concern the localisation of neuropeptides (Wakisaka et al 1996;Kusakabe et al 1996;Witt et al 2000;Chou et al 2001;Zuwala 2002a).…”

Spacing patterns on tongue surface-gustatory papilla.

“…2 E-G). Although the temporal sequence of papilla development has been established in several species, the mechanisms involved in papilla differentiation, patterning, growth and morphogenesis are not elucidated (Bao et al, 1995;Chou et al, 2001;Krimm et al, 2001;Mbiene and Roberts, 2003;Mistretta et al, 2003). It should be noted that the signalling molecules, growth factors, transcription factors, cell surface receptors and extracellular matrix proteins, which have been implicated in the morphogenetic regulation of many other epithelial appendages, are also associated with the initiation of the tongue papillae formation.…”