Rewiring the taste system

Abstract

In mammals, taste buds typically contain 50-100 tightly packed taste receptor cells (TRCs) representing all five basic qualities: sweet, sour, bitter, salty and umami1,2. Notably, mature taste cells have life spans of only 5-20 days, and consequently, are constantly replenished by differentiation of taste stem cells3. Given the importance of establishing and maintaining appropriate connectivity between TRCs and their partner ganglion neurons (i.e. ensuring that a labeled line from sweet TRCs connects to sweet neurons, bitter TRCs to bitter neurons, sour to sour, etc.), we examined how new connections are specified to retain fidelity of signal transmission. Our results show that bitter and sweet TRCs provide instructive signals to bitter and sweet target neurons via different guidance molecules (Sema3A and Sema7A)4-6. Here, we demonstrate that targeted expression of Sema3A or Sema7A in different classes of TRCs produce peripheral taste systems with miswired sweet or bitter cells. Indeed, we engineered animals whereby bitter neurons now respond to sweet tastants, sweet neurons respond to bitter, or with sweet neurons responding to sour stimuli. Together, these results uncover the basic logic of the wiring of the taste system at the periphery, and illustrate how a labeled-line sensory circuit preserves signaling integrity despite rapid and stochastic turnover of receptor cells.

The Taste of Blood in Mosquitoes

“…How is information from this network of blood-sensitive neurons integrated to form the perception of blood? Experiments in Drosophila melanogaster and mice found that information from each taste quality remains segregated as each population projects to discrete regions in central taste-processing centers and activates different higher order neuronal populations (Chen et al, 2011;Harris et al, 2015;Lee et al, 2017;Marella et al, 2006). It will be interesting to see how signals from blood-sensitive subpopulations converge and if this processing stream is segregated from other subpopulations of stylet sensory neurons that do not respond to blood.…”

Wiring taste receptor cells to the central gustatory system

“…How can ever‐changing bitter or sweet receptors find never‐changing neurons that must match the specificity of the signal? This article reviews a recent paper published in Nature (Lee, MacPherson, Parada, Zuker, & Ryba, , 548:330‐333) that identified two molecules belonging to the semaphorin axon guidance family of molecules ( SEMA 3A and SEMA 7A) that help maintain the “labeled line principle” between peripheral bitter or sweet receptors and their respective central projection area in the gustatory center.…”

“…That question was answered in an elegant study from Charles Zuker and Nick Ryba's laboratories published in a recent paper in Nature (Lee et al., ). The authors have systematically looked for potential molecules among the gene expression profile of taste cells related to either adhesion molecules, growth factors, axon guidance molecules, or synaptic components.…”

Opening a “Wide” Window onto Taste Signal Transmission

“…However, it also opens up a new avenue to tackle important problems to be solved in the future. Taste buds are densely packed with functionally distinct TBCs, each of which is innervated by secondary taste neurons in a quality-specific manner (Lee et al, 2017). How does a given nerve fiber selectively respond to ATP release from the target TBC, but not from adjacent cells?…”