Endocrinol Metab.  2021 Jun;36(3):469-477. 10.3803/EnM.2021.302.

Recent Advances in Understanding Peripheral Taste Decoding I: 2010 to 2020

Affiliations
  • 1BK21 Graduate Program, Department of Biomedical Sciences, Korea University College of Medicine, Seoul, Korea
  • 2Department of Pharmacology, Korea University College of Medicine, Seoul, Korea
  • 3Department of Biochemistry and Molecular Biology, Seoul National University College of Medicine, Seoul, Korea
  • 4Department of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Korea
  • 5Department of Oral Biology, BK21 FOUR Project, Yonsei University College of Dentistry, Seoul, Korea

Abstract

Taste sensation is the gatekeeper for direct decisions on feeding behavior and evaluating the quality of food. Nutritious and beneficial substances such as sugars and amino acids are represented by sweet and umami tastes, respectively, whereas noxious substances and toxins by bitter or sour tastes. Essential electrolytes including Na+ and other ions are recognized by the salty taste. Gustatory information is initially generated by taste buds in the oral cavity, projected into the central nervous system, and finally processed to provide input signals for food recognition, regulation of metabolism and physiology, and higher-order brain functions such as learning and memory, emotion, and reward. Therefore, understanding the peripheral taste system is fundamental for the development of technologies to regulate the endocrine system and improve whole-body metabolism. In this review article, we introduce previous widely-accepted views on the physiology and genetics of peripheral taste cells and primary gustatory neurons, and discuss key findings from the past decade that have raised novel questions or solved previously raised questions.

Keyword

Taste; Taste buds; Geniculate ganglion; Synaptic transmission; Signal transduction; Hormones

Figure

  • Fig. 1 The peripheral gustatory system in humans and mice. (A) The location of three types of papillae and the structure of the taste buds. The fungiform papilla (FuP) are distributed over the anterior two-thirds of the tongue, the foliate papilla are located on the lateral sides of the posterior tongue, and the circumvallate papilla (CVP) are mostly located on the center of the posterior one-third of the tongue. Each papilla contains one or more taste buds consisting of four types of taste cells: type I supporting (glial-like) cells, type II receptor cells, type III synaptic cells, and type IV basal (progenitor) cells. (B) The gustatory pathway from the taste buds to the brainstem in humans (left) and mice (right). Taste buds in the FuP are innervated by the chorda tympani, cranial nerve (CN) VII, and the taste buds in the FuP and CVP are innervated by the glossopharyngeal, cranial nerve IX. Taste impulses carried by CN VII and CN IX synapse in the solitary tract nucleus in the medulla oblongata of the brainstem.

  • Fig. 2 Comparison of past and current understanding of taste transduction in type II and type III taste cells. (A) Past proposed model. Type II taste cells transmit sweet, umami, or bitter taste signals to afferent nerve fibers in a type III taste cell-dependent manner, while type III taste cells transmit either salt or sour taste signals to afferent nerve fibers. (B) Current proposed model. Type II taste cells, salt cells, and type III taste cells individually transmit taste signals of sweet or bitter, salt, and sour tastes, respectively, to the afferent nerve fibers paired with each taste cell. Type II taste cells detect sweet, umami, or bitter taste by G-protein coupled receptors (GPCRs) that act in pairs (T1R2+T1R3 for sweet, and T1R1+T1R3 for umami) or act alone (T2Rs for bitter). GPCR-mediated signal transduction elevates the cytoplasmic Ca2+ concentration by releasing Ca2+ from the intracellular stores. Elevation of cytoplasmic Ca2+ in turn activates transient receptor potential cation channel subfamily m member 5 (TRPM5), depolarizes the cell to generate action potentials through voltage-gated sodium channel (VGNC), and releases adenosine triphosphate (ATP) through calcium homeostasis modulator 1/3 (CALHM1/3). Semaphorin 7A (SEMA7A) secreted by sweet taste receptor cells (TRCs) and SEMA3A secreted by bitter TRCs guide sweet and bitter ganglion neurons to the sweet and the bitter TRCs, respectively. Sodium cells are depolarized by the influx of Na+ through amiloride-sensitive epithelial sodium channel alpha subunit (ENACα). Action potentials are generated by an additional Na+ influx through voltage-gated sodium channel (VGNA) activation, independently of the intracellular Ca2+ signaling pathway, eventually releasing ATP through CALHM1/3. Type III taste cells detect sour taste by H+ influx through Otop1 channels. Intracellular acidification inhibits Kir2.1, and sequentially activates VGNA and voltage-gated calcium channel (VGCC), leading to neurotransmitter (NT) release using synaptic vesicles. Gαgust, Gα-gustducin; PDE, phosphodiesterase; PLCβ2, phospholipase Cβ2; IP3, inositol trisphosphate; DAG, diacylglycerol; Panx1, pannexin-1; PKD2L1, polycystin 2 like 1; 5-HT, 5-hydroxytryptamine; GABA, γ-aminobutyric acid; P2X2, P2X purinoceptor 2; P2X3, P2X purinoceptor 3; ER, endoplasmic reticulum; Otop1, otopetrin-1; Kir2.1, inward rectifier K+ channel.


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