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Nutrient Sensing of Gut Luminal Environment Proceedings of The Proceedings of the Nutrition Society (2021), 80,29–36 doi:10.1017/S0029665120007120 © The Author(s), 2020. Published by Cambridge University Press on behalf of The Nutrition Society. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. First published online 20 August 2020 The Nutrition Society Winter Meeting was held at the Royal Society of Medicine, London on 2–4 December 2019 Conference on ‘Diet and digestive disease’ Symposium 2: Sensing and signalling of the gut environment Nutrient sensing of gut luminal environment A. W. Moran1, K. Daly1, M. A. Al-Rammahi1,2 and S. P. Shirazi-Beechey1* 1Epithelial Function and Development Group, Faculty of Health and Life Sciences, University of Liverpool, Liverpool L69 7ZB, UK 2Zoonotic Disease Research Unit, College of Veterinary Medicine, University of Al-Qadisiyah, Al-Diwaniyah, Iraq Sensing of nutrients by chemosensory cells in the gastrointestinal tract plays a key role in transmitting food-related signals, linking information about the composition of ingested foods to digestive processes. In recent years, a number of G protein-coupled receptors (GPCR) responsive to a range of nutrients have been identified. Many are localised to intes- tinal enteroendocrine (chemosensory) cells, promoting hormonal and neuronal signalling locally, centrally and to the periphery. The field of gut sensory systems is relatively new and still evolving. Despite huge interest in these nutrient-sensing GPCR, both as sensors for nutritional status and targets for preventing the development of metabolic diseases, major challenges remain to be resolved. However, the gut expressed sweet taste receptor, resident in L-enteroendocrine cells and responsive to dietary sweetener additives, has already been successfully explored and utilised as a therapeutic target, treating weaning-related dis- orders in young animals. In addition to sensing nutrients, many GPCR are targets for drugs used in clinical practice. As such these receptors, in particular those expressed in L-cells, are currently being assessed as potential new pathways for treating diabetes and obesity. Furthermore, growing recognition of gut chemosensing of microbial-produced SCFA acids has led further attention to the association between nutrition and development of Proceedings of the Nutrition Society chronic disorders focusing on the relationship between nutrients, gut microbiota and health. The central importance of gut nutrient sensing in the control of gastrointestinal physiology, health promotion and gut–brain communication offers promise that further therapeutic suc- cesses and nutritional recommendations will arise from research in this area. Nutrient sensing: Enteroendocrine cell: G protein-coupled receptors The intestinal epithelium is a major boundary with the that increasing the acidity in the lumen of the small intes- outside world. Epithelial cells lining the surface of the tine elicited pancreatic secretions, and that this was intestinal epithelium are in direct contact with a luminal mediated, not via the nervous system, but by a humoral environment, the composition of which varies dramatically. factor produced by the gut epithelium that they termed It has long been recognised that the gut is capable of sens- secretin. ing changes in its luminal content and responding by releas- Indeed, we now know that the nerve endings that ing chemical signals. In 1902, Bayliss and Starling(1) noted transmit signals evoked by changes in the gut luminal Abbreviations: cAMP, cyclic adenosine monophosphate; CaSR, calcium-sensing receptor; CCK, cholecystokinin; EEC, enteroendocrine cell; GI, gastrointestinal; GIP, glucose-dependent insulinotropic peptide; GLP, glucagon-like peptide; GPCR, G protein-coupled receptors; PYY, peptide YY; SGLT 1, sodium glucose co-transporter isoform 1; STC 1, secretin tumour cell line; T1R, taste 1 family receptor. *Corresponding author: S. P. Shirazi-Beechey, fax +44 151 795 4408, email [email protected] Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 26 Sep 2021 at 05:22:19, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0029665120007120 30 A. W. Moran et al. contents do not reach the intestinal lumen and that infor- seven transmembrane domains coupled with a large mation about the chemical nature of the luminal contents extracellular domain (Venus flytrap module) and is transmitted to neurons via enteroendocrine cells (EEC) C-terminal cytoplasmic domain. Class A receptors such linking the gut, brain and peripheral tissues. as fatty acid receptors also have seven transmembrane EEC, scattered amongst the cells lining the intestinal domains, but lack the Venus flytrap module(9). In gen- epithelium, are pivotal to the chemosensing pathways eral, nutrient-sensing GPCR are classified based on of the intestinal tract. They are flask-shaped, with the their α-subunits and the corresponding downstream sig- majority having open-type morphology with apically nalling pathways they recruit. They are grouped into extended processes making direct contact with ingested families Gαs,Gαi,Gαq,Gα12/13, and gustducin. The nutrients and microbial products in the gut lumen. physiological effects produced by these receptors in These cells respond to changes in luminal contents by response to nutrients are mainly mediated via cyclic releasing gut hormones into systemic circulation via adenosine monophosphate (cAMP) and Ca2+ signalling their basolateral membrane domain. There are at least cascades. Gαs stimulates adenylate cyclase leading to an sixteen discrete cell types that make up the enteroendo- increase in intracellular concentration of cAMP. Gαi inhi- crine family (generally named after letters of alphabet) bits adenylate cyclase resulting in decreased intracellular and collectively they produce over twenty different hor- cAMP. Gαq stimulates phospholipase C resulting in the mones(2). These include cholecystokinin (CCK), peptide generation of diacylglycerol and inositol triphosphate, YY (PYY) and glucagon-like peptides 1 and 2 (GLP-1, which respectively activate protein kinase C triggering 2+ GLP-2). CCK is released by I-cells predominantly Ca release from intracellular stores. Gα12/13 couples to located in the proximal intestine, whereas PYY, GLP-1 the activation of the small G-protein Rho. Gustducin, a and GLP-2 are secreted mostly by L-cells residing fre- heterotrimeric G protein and mainly a member of Gαi fam- quently in the distal gut. However, L-cells have also ily, can stimulate phosphodiesterase resulting in cAMP been identified in the duodenum albeit in lower number degradation, but in parallel the co-released Gβγ subunits than observed in jejunum and ileum(3). Secretion of activate phospholipase C-β2 leading to inositol CCK, GLP-1 or PYY slows down gastric emptying, as triphosphate-mediated Ca2+ release. The consequent eleva- well as reducing appetite and food intake. GLP-1 also tion of cytoplasmic Ca2+ activates the Ca2+sensitive transi- functions as an incretin hormone, stimulating insulin ent receptor potential channel M5 triggering membrane secretion from pancreatic β-cells, improving meal-related depolarisation and opening of voltage-gated Ca2+ chan- glycaemia. GLP-2, coproduced with GLP-1, promotes nels(9,10). It has also been reported that gustducin activa- intestinal epithelial cell growth and increased nutrient tion stimulates adenylate cyclase, increasing cAMP absorption(4,5). directly or indirectly closing basolateral K+ channels and Although it was believed that gut hormone secretion triggering membrane depolarisation(11). was the result of direct EEC sensing of nutrients in the Several nutrient-sensing GPCR have been identified in lumen of the intestine, until recently little was known the intestinal epithelium. They are expressed mainly on about the initial molecular recognition events involved the apical membrane domain of EEC and are directly in the enteroendocrine luminal sensing. activated by a variety of nutrients. These include recep- tors for glucose, amino acids, peptides, protein hydroly- sates, calcium and both long-chain fatty acids and G protein-coupled receptors and intestinal nutrient SCFA (Fig. 1)(12). Nutrient sensing initiates a cascade Proceedings of the Nutrition Society sensing of events involving hormonal and neural pathways. This culminates in functional responses that ultimately G protein-coupled receptors (GPCR) represent the lar- regulate vital physiological processes including food gest family of cell-surface mediators of signal transduc- intake (appetite and satiety), nutrient digestion and tion(6). They are encoded by about 800 different genes absorption, intestinal barrier function, gut motility, and in human subjects(7), enabling cells to respond to many insulin secretion. diverse sensory inputs. Hence, GPCR are well- This review focuses on GPCR responsive to digestive established targets for almost half of all therapeutic products of macronutrients. drugs, yet many are denominated as ‘orphan receptors’ whose physiological agonists remain unknown. As such these receptors have attracted significant attention in Carbohydrates terms of continued identification and characterisation, with the recognition that they are potential targets for One of the primary functions
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