The endocrinology of taste receptors

Abstract

Levels of obesity have reached epidemic proportions on a global scale, which has led to considerable increases in health problems and increased risk of several diseases, including cardiovascular and pulmonary diseases, cancer and diabetes mellitus. People with obesity consume more food than is needed to maintain an ideal body weight, despite the discrimination that accompanies being overweight and the wealth of available information that overconsumption is detrimental to health. The relationship between energy expenditure and energy intake throughout an individual's lifetime is far more complicated than previously thought. An improved comprehension of the relationships between taste, palatability, taste receptors and hedonic responses to food might lead to increased understanding of the biological underpinnings of energy acquisition, as well as why humans sometimes eat more than is needed and more than we know is healthy. This Review discusses the role of taste receptors in the tongue, gut, pancreas and brain and their hormonal involvement in taste perception, as well as the relationship between taste perception, overeating and the development of obesity.

Figure 1

Localization and structure of taste buds in the human tongue. a | Schematic representation of a taste bud and intragemmal nerve fibres. By convention, four subtypes of taste bud cells are present in taste buds. Of the four subtypes, only type III taste bud cells form recognizable synapses with the afferent nerve fibres. b | Localization of taste papillae. Circumvallate (back of tongue), foliate (sides of tongue) and fungiform (middle and front of tongue).

Figure 2

Expression of hormones and their receptors in the three subtypes of taste bud cells that perceive the five prototypic tastants, as well as fat. The specific taste perceptions are represented as sweet, bitter, umami, sour, salt and fat. Abbreviations: CCK, cholecystokinin; CCK-AR, cholecystokinin-A receptor; CD36, platelet glycoprotein 4; GAL, galanin; GAL2-R, galanin receptor type 2; GHRP, ghrelin receptor; GLP-1, glucagon-like peptide 1; GLP-1R, glucagon-like peptide 1 receptor; GLP-2, glucagon-like peptide 2; GPR120, free fatty acid receptor 4; Lep-R, leptin receptor; NPY, neuropeptide Y; NPY1-R, neuropeptide Y receptor type 1; NPY4-R, neuropeptide Y receptor type 4; PYY, peptide tyrosine tyrosine; VIP, vasoactive intestinal peptide; VIP-R, vasoactive intestinal peptide receptor.

Figure 3

Localization of selected hormones along the gut. Hormones that are expressed in the gut and that are also present in the taste bud cells within taste buds. CCK and ghrelin are found in the upper gastrointestinal tract; CCK is secreted by I-cells and ghrelin is secreted by X/A-like cells. In the middle gastrointestinal tract, K-cells secrete GIP. In the lower gastrointestinal tract, L-cells secrete PYY, GLP-1 and GLP-2. Abbreviations: CCK, cholecystokinin; GIP, gastric inhibitory polypeptide; GLP-1, glucagon-like peptide 1; GLP-2, glucagon-like peptide 2; PYY, peptide tyrosine tyrosine.

Figure 4

Relationship of organ systems with taste-sensing machinery. Nerve fibres that transmit taste information from the taste papillae converge in the NTS in the brainstem; taste perception signals are then routed to the PBN (shown only in rodents), toward the thalamus and terminating in the primary gustatory cortex in the insula. Beyond the pons, one-third of the fibres ascend and crossover in the thalamus such that taste is represented bilaterally in the insulae. Local projections from the NTS mediate salivation from salivary glands and serous secretions from Von Ebner’s glands. α-gustducin is expressed in the brush cells of the pancreatic ducts and intestine; however, its function in these cells in not yet known. α-gustducin and TAS1Rs are also expressed in β cells in islets of Langerhans, where they might be involved in regulating basal insulin secretion. Additionally, TAS1Rs in islets are activated by fructose, which leads to enhanced glucose-mediated insulin secretion. In enteroendocrine cells, receptors for sweet (TAS1R2/TAS1R3 or a putative TAS1R3/TAS1R3 dimer), umami (TAS1R1/TAS1R3), bitter (TAS2R) and long-chain fatty acids (GPR120, GPR40 and CD36) are expressed and are involved in secretion of GLP-1, CCK and ghrelin. Glucose and fat are absorbed into enterocytes: glucose absorption is through sodium-dependent SGLT1 channels and fat molecules freely diffuse across the luminal surface. Abbreviations: CCK, cholecystokinin; CD36; platelet glycoprotein 4; GLP-1, glucagon-like peptide 1; GPR40, free fatty acid receptor 1; GPR120, free fatty acid receptor 4; NTS, nucleus tractus solitarius; PBN, parabrachial nucleus; SGLT1, sodium/ glucose cotransporter 1; TAS1R1, taste receptor type 1 member 1; TAS1R2, taste receptor type 1 member 2; TAS1R3, taste receptor type 1 member 3; TAS2R, taste receptor type 2.