Taste transduction and channel synapses in taste buds

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INVITED REVIEW

Taste transduction and channel synapses in taste buds Akiyuki Taruno 1,2 J. Kevin Foskett 4,5

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Kengo Nomura 1

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Tsukasa Kusakizako 3

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Zhongming Ma 4

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Osamu Nureki 3

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Received: 29 July 2020 / Revised: 29 July 2020 / Accepted: 7 September 2020 # Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract The variety of taste sensations, including sweet, umami, bitter, sour, and salty, arises from diverse taste cells, each of which expresses specific taste sensor molecules and associated components for downstream signal transduction cascades. Recent years have witnessed major advances in our understanding of the molecular mechanisms underlying transduction of basic tastes in taste buds, including the identification of the bona fide sour sensor H+ channel OTOP1, and elucidation of transduction of the amiloride-sensitive component of salty taste (the taste of sodium) and the TAS1R-independent component of sweet taste (the taste of sugar). Studies have also discovered an unconventional chemical synapse termed “channel synapse” which employs an action potential-activated CALHM1/3 ion channel instead of exocytosis of synaptic vesicles as the conduit for neurotransmitter release that links taste cells to afferent neurons. New images of the channel synapse and determinations of the structures of CALHM channels have provided structural and functional insights into this unique synapse. In this review, we discuss the current view of taste transduction and neurotransmission with emphasis on recent advances in the field. Keywords Taste . Sensory . Synapse . Ion channel . CALHM

Introduction Taste is a chemosensation perceived on the tongue and provoked by chemical compounds contained in food and drinks. A chemical that produces a taste sensation is called a tastant. A vast variety of tastants can be categorized into five groups depending on the quality of the evoked taste sensation: sweet, umami, bitter, salty, and sour. Animals are attracted to sweet and umami tastes produced by caloric nutrients, sugars, and

* Akiyuki Taruno [email protected] 1

Department of Molecular Cell Physiology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Japan

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Japan Science and Technology Agency, PRESTO, Kawaguchi, Saitama, Japan

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Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan

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Department of Physiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

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Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

amino acids, respectively. Bitter and sour tastes are indicative of potentially toxic and spoiled ingredients, respectively, and cause innate avoidance. The salty taste of NaCl can be attractive or aversive depending on its concentration in order to fine-tune the body electrolyte homeostasis. Thus, taste plays pivotal roles in survival by controlling dietary choices. Because the epidemic of overnutriti