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Review
. 2024 May 9;390(18):1699-1710.
doi: 10.1056/NEJMra2304578.

Physiological Integration of Taste and Metabolism

Josephine M Egan  1
Affiliations
Review

Physiological Integration of Taste and Metabolism

Josephine M Egan. N Engl J Med. .
No abstract available

PubMed Disclaimer

Figures

Figure 1
Figure 1. Anatomy and Physiology of the Tongue and Taste Buds.
There are three types of papillae (Panel A): fungiform (FFP), foliate (FLP), and circumvallate (CVP). CVP, up to 11 in number, are the largest and are easily visualized on the back of the tongue. FLP are parallel folds on the sides of the tongue. FFP, several hundred in number and just visible to the naked eye, are scattered on the anterior tongue, interspersed with a fourth papilla type, filiform, that do not contain taste buds; they help cleanse the mouth, move food around, and serve mechanosensory functions by responding to touch, pain, and temperature. Each taste bud has a pore surrounded by a bushy network of villi of the taste receptor cells (TRCs). Humans may have up to 4500 taste buds, but the number varies greatly, and 50 to 60% of them are in CVP. Each taste bud, regardless of location, contains about 60 TRCs (morphologic types I, II, and III) and precursor cells (type IV). Types I, II, and III can be subclassified on the basis of differences in TRC function, molecular markers, or both (Panel B). Type I TRCs, which wrap around the other TRCs, contain NTPDase2 on their plasma membrane, which degrades ATP released from type II TRCs. The G protein–coupled receptors, necessary for sweet taste (TAS1R3 and TAS1R2), umami taste (TAS1R3 and TAS1R1), and bitter taste (TAS2Rs) are present on type II TRCs. In response to their respective tastants, they release ATP as their signaling molecule through CALHM1/3 channels onto purinergic receptors on intragemmal nerve fibers throughout taste buds. Sodium ions, responsible for a pleasant salty taste, enter through epithelial sodium channels (ENaCs) on TRCs, and also use ATP as their signaling molecule. Type III TRCs, the only TRC type with classical neuronal synapses, contain a proton channel (OTOP1) that detects sour or acidic tastants leading to neurotransmitter release, such as 5-hydroxytryptamine (5-HT).
Figure 2.
Figure 2.. Transmission of Taste Information.
Fibers innervating the taste buds transmit signals to the gustatory region of the nucleus of the tractus solitarius (NTS), then to the thalamus and the gustatory cortex (pathway depicted in red). Each taste bud is innervated by primary intragemmal gustatory fibers, which extensively branch and connect with multiple taste buds, interacting with many TRCs. This results in electrical activity that reflects the input from numerous TRCs. Taste buds in the fungiform papillae are innervated by sensory neurons of the geniculate ganglion, traveling through the chorda tympani branch of the facial nerve (cranial nerve [CN] VII). Taste buds in the posterior third of the tongue are innervated by sensory neurons of the petrosal ganglion, traveling through the lingual branch of the glossopharyngeal nerve (CN IX). Isolated taste buds in the palate are innervated by the greater superficial petrosal branch of CN VII, whereas those on the epiglottis and esophagus receive innervation from the superior laryngeal branch of the vagus nerve (CN X). Sensory fibers from CNs VII, IX, and X enter the medulla, synapsing on a slender column of cells within the gustatory region situated in the rostral and lateral part of the NTS. From there, neurons project to the ventral posteromedial nucleus of the thalamus. Next, neurons project to the anterior insula and frontal operculum in the cerebral cortex, which facilitates the conscious perception and discrimination of tastes. Taste sensations often include somatosensory aspects like texture, temperature, and responses to spicy and minty foods. This component is transmitted by the branches of the trigeminal nerve (CN V), originating in the trigeminal ganglion. From there, information goes to the principal nucleus in the caudal pons, which also projects to the ventral posteromedial nucleus of the thalamus, and finally to the somatosensory cortex in the brain’s parietal lobe (pathway depicted in blue).
Figure 3.
Figure 3.. Immunohistochemical Features and Examples of Hormones in Human FFP.
Two typical-appearing taste buds are present in an FFP (Panel A, hematoxylin and eosin), and GLP-1 and neuropeptide Y (NPY) are present in type II TRCs in taste buds (Panels B and C, respectively, immunofluorescence staining). In mice, GLP-1 maintains or enhances sweet perception through GLP-1 receptors on the intragemmal nerve fibers, and NPY enhances sweet and bitter perception through Y1 receptors. In FFP from humans, there are approximately 60 TRCs in each bud, at least 50% of which are type II. However, as shown in these examples, the size of the cells varies greatly between persons and even varies among individual taste buds.
Figure 4.
Figure 4.. Extraoral Taste Receptors.
TAS1Rs are present not just on the tongue but throughout the body in tissues such as the gut, brain, pancreas, bladder, bone, adipose tissue, airway epithelium, skeletal muscle, and testes. There are also extraoral TAS2Rs in the larynx, gut, and brain and on immune cells, as well as throughout the respiratory and genitourinary systems. TAS2Rs, along with TAS1R3 and α-gustducin, are also present in testes. Animals in which TAS2Rs are used to avoid noxious foods also appear to have highly efficient spermatogenesis and, as a consequence, may produce more offspring. OTOP1, the proton channel in type III TRCs, was first identified in the vestibular system, where it is necessary for the formation of calcium carbonate–based otoconia and otoliths. It is also expressed in brown adipose cells.
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References

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