The cells and logic for mammalian sour taste detection

Abstract

Mammals taste many compounds yet use a sensory palette consisting of only five basic taste modalities: sweet, bitter, sour, salty and umami (the taste of monosodium glutamate). Although this repertoire may seem modest, it provides animals with critical information about the nature and quality of food. Sour taste detection functions as an important sensory input to warn against the ingestion of acidic (for example, spoiled or unripe) food sources. We have used a combination of bioinformatics, genetic and functional studies to identify PKD2L1, a polycystic-kidney-disease-like ion channel, as a candidate mammalian sour taste sensor. In the tongue, PKD2L1 is expressed in a subset of taste receptor cells distinct from those responsible for sweet, bitter and umami taste. To examine the role of PKD2L1-expressing taste cells in vivo, we engineered mice with targeted genetic ablations of selected populations of taste receptor cells. Animals lacking PKD2L1-expressing cells are completely devoid of taste responses to sour stimuli. Notably, responses to all other tastants remained unaffected, proving that the segregation of taste qualities even extends to ionic stimuli. Our results now establish independent cellular substrates for four of the five basic taste modalities, and support a comprehensive labelled-line mode of taste coding at the periphery. Notably, PKD2L1 is also expressed in specific neurons surrounding the central canal of the spinal cord. Here we demonstrate that these PKD2L1-expressing neurons send projections to the central canal, and selectively trigger action potentials in response to decreases in extracellular pH. We propose that these cells correspond to the long-sought components of the cerebrospinal fluid chemosensory system. Taken together, our results suggest a common basis for acid sensing in disparate physiological settings.

Taste perception, associated hormonal modulation, and nutrient intake

“…18 In addition to their neuronal actions, type III cells also respond to sour taste and carbonation. [55][56][57][58] Interestingly, data from functional magnetic resonance imaging in humans suggest carbonation attenuates brain activity in gustatory brain regions, thus reducing sweetness perception. 59 Attenuated sweetness perception may trigger sweetseeking behaviors in some individuals and may potentially increase the risk of overconsumption of high-energy foods and development of obesity.…”

Genetics of Taste and Smell

“…Although genetically distinct strains of inbred mice are known to differ in sour preference, 77 no genes have been identified that account for these differences. One candidate is the polycystic kidney disease 2-like 1 gene (Pkd2l1), which is involved in sour taste in mice 78 and possibly in humans. 79 Whether naturally occurring allelic variation in this gene is responsible for differential sour perception (in mice or humans) is not known.…”

Proton production, regulation and pathophysiological roles in the mammalian brain

“…Studies from Drosophila and the mammalian sour taste detection system also highlighted channels from the transient receptor potential (TRP) family, such as PKD2L1 and TRPA1, as sensors for acid or CO 2 [62,63] . To fully illustrate proton-sensing pathways in the brain, we will discuss some typical receptors which are directly gated or modulated by protons ( Table 2, Fig.…”

“…Animals lacking PKD2L1-expressing cells are completely devoid of taste responses to sour stimuli [63] . A follow-up study showed that PKD2L1 is directly activated by exposure to solutions of low pH.…”