"Tripartite Synapses" in Taste Buds: A Role for Type I Gliallike Taste Cells

Yuryanni A. Rodriguez, Jennifer K. Roebber, Gennady Dvoryanchikov, Vivien Makhoul, Stephen D. Roper, Nirupa Chaudhari

Research output: Contribution to journalArticlepeer-review

Abstract

In mammalian taste buds, Type I cells comprise half of all cells. These are termed "glial-like" based on morphologic and molecular features, but there are limited studies describing their function. We tested whether Type I cells sense chemosensory activation of adjacent chemosensory (i.e., Types II and III) taste bud cells, similar to synaptic glia. Using Gad2;;GCaMP3 mice of both sexes, we confirmed by immunostaining that, within taste buds, GCaMP expression is predominantly in Type I cells (with no Type II and ≈28% Type III cells expressing weakly). In dissociated taste buds, GCaMP1 Type I cells responded to bath-applied ATP (10-100 lM) but not to 5-HT (transmitters released by Type II or III cells, respectively). Type I cells also did not respond to taste stimuli (5 lM cycloheximide, 1 mM denatonium). In lingual slice preparations also, Type I cells responded to bath-applied ATP (10-100 lM). However, when taste buds in the slice were stimulated with bitter tastants (cycloheximide, denatonium, quinine), Type I cells responded robustly. Taste-evoked responses of Type I cells in the slice preparation were significantly reduced by desensitizing purinoceptors or by purinoceptor antagonists (suramin, PPADS), and were essentially eliminated by blocking synaptic ATP release (carbenoxolone) or degrading extracellular ATP (apyrase). Thus, taste-evoked release of afferent ATP from type II chemosensory cells, in addition to exciting gustatory afferent fibers, also activates glial-like Type I taste cells. We speculate that Type I cells sense chemosensory activation and that they participate in synaptic signaling, similarly to glial cells at CNS tripartite synapses.

Original languageEnglish (US)
Pages (from-to)9860-9871
Number of pages12
JournalJournal of Neuroscience
Volume41
Issue number48
DOIs
StatePublished - Dec 1 2021

Keywords

  • Glia
  • Paracrine
  • Purinoceptor
  • Sensory
  • Synaptic transmission

ASJC Scopus subject areas

  • Neuroscience(all)

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