P2X₂‐ and P2X₃‐positive fibers in fungiform papillae originate from the chorda tympani but not the trigeminal nerve in rats and mice

Abstract

The subtype 2 and subtype 3 ionotropic purinergic receptors (P2X receptors) are crucial for gustation, but the distribution of these receptors in the geniculate ganglion (GG) and their colocalization in tongue papillae remain unknown. Here we investigated the expression and colocalization of P2X(2) and P2X(3) receptors in the GG and fungiform papillae in rats and mice by using in situ hybridization and immunohistochemistry. In both species, P2X(2) transcripts and immunoreactivity were detected in approximately 50-60% of GG neuronal somata, whereas those of P2X(3) were observed in almost all neurons. In each fungiform papilla, immunoreactivity for both receptors was mostly colocalized and was seen in nerve fibers and their bundles concentrated in the taste buds. Because it is well known that the P2X receptors are involved in not only taste but also nociception, we determined whether the expression originated from the chorda tympani nerve (CT, gustatory) or trigeminal nerve (somatosensory) by cutting the CT in both animals. Most P2X(2) and P2X(3) immunoreactivity in the fungiform papillae was abolished after transection, although the nerve fiber immunoreactivity of transient receptor potential V1 (a marker of somatosensory nerve fibers) remained unchanged, indicating that most fungiform papillae nerve fibers with P2X(2) and P2X(3) receptors were derived from CT. Taken together, these findings suggest that most P2X(2) and P2X(3) receptors in fungiform papillae are used for gustation rather than somatosensation.

Role of the ectonucleotidase NTPDase2 in taste bud function

“…Although both P2X2 and P2X3 can form homotrimeric receptors, they also tend to form heteromers when coexpressed in a single cell. P2X3 is expressed by nearly all ganglionic neurons of the chorda tympani nerve, whereas P2X2 is expressed on only 50-60% of these ganglion cells (28). Thus, ganglion cells expressing only P2X23 produce P2X3 homomeric receptors, whereas other cells expressing both P2X2 and P2X3 generate mostly heteromeric receptors (29).…”

Targeted Taste Cell-specific Overexpression of Brain-derived Neurotrophic Factor in Adult Taste Buds Elevates Phosphorylated TrkB Protein Levels in Taste Cells, Increases Taste Bud Size, and Promotes Gustatory Innervation

“…Interestingly, the increase in the gustatory innervation constitutes a major part of the general innervation density, as evaluated by immunohistochemistry to P2X3 ATP receptors. P2X3 antibodies have been suggested to identify gustatory nerve fibers in taste buds as well as some taste cells (38). In addition, there are a significantly lager number of NCAM-and pTrkB-positive cells in taste buds.…”

“…P2X3 has been proposed to function as a specific marker for gustatory nerve fibers (38). Nerve fibers innervating the circumvallate taste buds stained intensely with P2X3 receptor antibodies in both wild-type and high BDNF-expressing Gust-BDNF mice (Fig.…”

Role of neurotrophin in the taste system following gustatory nerve injury

“…By 7 days after chorda tympani nerve section, P2X3 (ATP receptor) positive fibers and taste buds both disappear from fungiform papillae in rat (Ishida et al 2009). Similarly, in mice, nerve fibers were absent from fungiform papillae within 14 days after chorda tympani and lingual nerve section (Guagliardo and Hill 2007).…”

“…Following gustatory nerve sectioning, nerve fibers inside of the taste bud disappear and taste evoked responses from nerve are absent (Cain et al 1996;Guagliardo and Hill 2007;Ishida et al 2009). By 7 days after chorda tympani nerve section, P2X3 (ATP receptor) positive fibers and taste buds both disappear from fungiform papillae in rat (Ishida et al 2009).…”