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Signalling from the Gut Lumen

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Signalling from the Gut Lumen CSIRO PUBLISHING Animal Production Science, 2017, 57, 2175–2187 Review http://dx.doi.org/10.1071/AN17276 Signalling from the gut lumen John B. Furness A,B,C and Jeremy J. Cottrell A ADepartment of Agriculture and Food, The University of Melbourne, Parkville, Vic. 3010, Australia. BFlorey Institute of Neuroscience and Mental Health, Parkville, Vic. 3010, Australia. CCorresponding author. Email: [email protected] Abstract. The lining of the gastrointestinal tract needs to be easily accessible to nutrients and, at the same time, defend against pathogens and chemical challenges. This lining is the largest and most vulnerable surface that faces the outside world. To manage the dual problems of effective nutrient conversion and defence, the gut lining has a sophisticated system for detection of individual chemical entities, pathogenic organisms and their products, and physico-chemical properties of its contents. Detection is through specific receptors that signal to the gut endocrine system, the nervous system, the immune system and local tissue defence systems. These effectors, in turn, modify digestive functions and contribute to tissue defence. Receptors for nutrients include taste receptors for sweet, bitter and savoury, free fatty acid receptors, peptide and phytochemical receptors, that are primarily located on enteroendocrine cells. Hormones released by enteroendocrine cells act locally, through the circulation and via the nervous system, to optimise digestion and mucosal health. Pathogen detection is both through antigen presentation to T-cells and through pattern-recognition receptors (PRRs). Activation of PRRs triggers local tissue defence, for example, by causing release of antimicrobials from Paneth cells. Toxic chemicals, including plant toxins, are sensed and then avoided, expelled or metabolised. It continues to be a major challenge to develop a comprehensive understanding of the integrated responses of the gastrointestinal tract to its luminal contents. Additional keywords: microbiota, mucosal biology, nutrient receptors. Received 2 May 2017, accepted 3 July 2017, published online 19 July 2017 Introduction cells in other gut regions, hormones from other sources, and The gastrointestinal tract exists in a state of hypervigilance. neural signals including those from the central nervous system It contains a rich assortment of chemicals and microorganisms, (CNS). separated from the body’s internal milieu by only a single layer Roles of gastro-entero-pancreatic hormone-producing of epithelial cells for most of its length. This single layer of cells (enteroendocrine) cells in determining digestive in the small intestine is the largest vulnerable surface of the efficiency body, with a surface area of ~60 m2 (Ferraris et al. 1989). The total external (luminal) surface of the gastrointestinal tract is Optimal conversion of food to essential nutrients, including energy ~100–400 m2, compared with ~2 m2 of skin (MacDonald and substrates and structural and regulatory proteins, depends on the Monteleone 2005; Artis 2008). The lining of the gut is continually control of a range of digestive and digestion-related functions, exposed to food, drink and contaminants they may bring with many of which are influenced by the hormones released by them, to a multitude of microorganisms and their products, to enteroendocrine cells (EEC). These functions include appetite enzymatic and chemical breakdown products of complex and satiety, the rate of gastric emptying, intestinal transit, release molecules, to gastrointestinal secretions, to potentially toxic of digestive enzymes, induction of nutrient transporters, fluid and chemicals and to food additives. electrolyte transport across the mucosa, local blood flow, pancreatic The intestine continuously monitors its contents so as to insulin secretion, modulation of immune responses and tissue optimise nutrient conversion and defend against threats to its growth. The EEC release their hormones in response to integrity. For these purposes it possesses a range of sensory chemicals in the gut lumen, mechanical forces and the bulk receptors and mechanisms (Table 1) that activate four major properties of the luminal contents, such as pH. effector systems: the enteroendocrine system, the nervous fi system, the gut immune system and the non-immune defence Classi cation of EEC systems of the gut, including mucosal repair (Fig. 1). Enteroendocrine cells (EEC) are scattered as single cells in the This review concerns exteroception, particularly sensing of lining epithelium of the stomach, and small and large intestine, chemicals that are in the luminal contents or arise from the which collectively form the largest endocrine organ of the body luminal contents. The digestive tract also senses messages from (Rehfeld 2004; Janssen and Depoortere 2013). Closely related the internal environment. These include hormones released by cells are found in the biliary tract and in the pancreatic islets; Journal compilation Ó CSIRO 2017 www.publish.csiro.au/journals/an 2176 Animal Production Science J. B. Furness and J. J. Cottrell Table 1. Some factors that are sensed in the gut lumen and the associated receptors (italic) The table lists the major known properties of the contents and states of the gastrointestinal tract that are specifically sensed and that lead to endocrine, neural or other signals that change organ or body states. FFAR, free fatty acid receptor; GPCR, G protein-coupled receptor; Nod, nucleotide-binding oligomerisation domain; PRR, pattern-recognition receptor; TGR, Takeda G protein receptor; T1R–T2R, Tastant 1 receptor–Tastant 2 receptor; TRP, transient receptor-potential; 5-HT, 5-hydroxytryptamine Nutrients and food components The taste receptors: simple sugars, the sweet taste receptor, T1R2–T1R3; aminoacids, the umami (savoury) receptor, T1R1–T1R3; the bitter receptor family, T2Rs; the sour (acid) receptor, TRPP2. Protein breakdown products (peptones and amino acids): GPR92/93, GPRC6A, T1R1–T1R3 Free fatty acid receptors: FFARs 1–3, GPR119, GPR120 Phytochemicals (specific chemical entities of herbs and spices): TRP receptors, including TRPV1, TRPV2, TRPV5, TRPV6, TRPA1, TRPP2; the bitter receptor, T2R; olfactory receptors Mechanical distortion, stretch and tension Mechanosensitive channels of nerve endings and enteroendocrine cells Other physico-chemical attributes Temperature, osmolarity, acidity Internal secretions Bile acid receptors, TGR5 Bacteria, viruses, fungi, protozoa and helminths: their antigens and products Pattern-recognition receptors (PRRs): toll-like receptors 1–9, Nod1, 2. T-cell receptors: peptides, lipopolysaccharides, vitamin B metabolites. Toxins and emetogenic compounds Receptors for emetogenic toxins on 5-HT-containing enteroendocrine cells in the stomach and proximal small intestine. Receptors for advanced glycation end products (RAGE). Foreign compound transporters/receptors that recognise foreign compounds including pharmaceuticals: peptide transporter (PTR) family members, oligopeptide transporters and organic anion transporters (OATPs). together with EEC, these form the gastro-entero-pancreatic and that there is both diversity of 5-HT-containing EEC and a endocrine system. Until very recently, EEC were classified into wide range of roles of gut-derived 5-HT (Diwakarla et al. 2017; 12 types, each with a single letter code representing the hormone Martin et al. 2017). Although the classification of EEC needs that the cells contain and release, for example, G cells being gastrin substantial revision, the major roles of the hormones in the containing, S cells being secretin containing and I cells being control of digestive function can be identified (Table 2). cholecystokinin (CCK)-containing. The exception was L cells Nutrient receptors are mostly, but not exclusively, located on that contain both glucagon gene products (glucagon-like peptides EEC cells. A summary of the nutrient receptor types that (GLP-1, GLP-2), glicentin and oxyntomodulin) and peptide influence the release of the different hormones is included in tyrosine–tyrosine (PYY). It is now clear that the one cell–one Table 2. The patterns of co-expression of hormones, and the hormone (or hormone combination) classificationisnolonger differences along the gut, provide a much greater complexity tenable (Helander and Fändriks 2012; Gribble and Reimann than is represented in the table, and that has been covered in 2015;Fothergillet al. 2017). For example, when cells expressing depth in recent reviews (Psichas et al. 2015; Husted et al. 2017). a reporter transgene under CCK promotor control are isolated and The hormones released from the EEC can act locally on other molecularly analysed, it is found that CCK gene transcripts are cells, including immune cells, on nerve endings, or at a distance co-expressed with secretin, glucagon-like insulinotropic peptide on other organs, including the pancreatic islets and the CNS. It (GIP), GLP-1, PYY and neurotensin transcripts in subsets of is notable that the hormones do not act alone; for example, CCK EEC, and co-expression of the peptide hormones has been and 5-HT both increase the release of digestive enzymes from confirmed by mass spectrometry and immunohistochemistry the pancreas (Li et al. 2000) and CCK, GLP-1 and PYY are all (Egerod et al. 2012). Isolation of GIP-expressing and GLP- satiety factors. GLP-1 and PYY, which are commonly localised expressing EEC and correlated immunohistochemical analysis in the same cells, have synergistic effects. Infusion of GLP-1 or has
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