Abstract
TRPA1 is an ion channel that detects specific chemicals in food and also transduces mechanical, cold and chemical stimulation. Its presence in sensory nerve endings is well known and recent evidence indicates that it is expressed by some gastrointestinal enteroendocrine cells (EEC). The purpose of the present work is to identify and quantify EEC that express TRPA1 in the mouse gastrointestinal tract. Combined in situ hybridisation histochemistry for TRPA1 and immunofluorescence for EEC hormones was used. TRPA1 expressing EEC were common in the duodenum and jejunum, were rare in the distal small intestine and were absent from the stomach and large intestine. In the duodenum and jejunum, TRPA1 occurred in EEC that contained both cholecystokinin (CCK) and 5-hydroxytryptamine (5HT) and in a small number of cells expressing 5HT but not CCK. TRPA1 was absent from CCK cells that did not express 5HT and from EEC containing glucagon-like insulinotropic peptide. Thus TRPA1 is contained in very specific EEC populations. It is suggested that foods such as garlic and cinnamon that contain TRPA1 stimulants may aid digestion by facilitating the release of CCK.
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References
Aiken KD, Kisslinger JA, Roth KA (1994) Immunohistochemical studies indicate multiple enteroendocrine cell differentiation pathways in the mouse proximal small intestine. Dev Dyn 201:63–70
Brierley SM, Hughes PA, Page AJ, Kwan KY, Martin CM, O’Donnell TA, Cooper NJ, Harrington AM, Adam B, Liebregts T, Holtmann G, Corey DP, Rychkov GY, Blackshaw LA (2009) The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 137:2084–2095
de Lange CFM, Pluske J, Gong J, Nyachoti CM (2010) Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livest Sci 134:124–134
Dockray GJ (2013) Enteroendocrine cell signalling via the vagus nerve. Curr Opin Pharm 13:1–5
Doihara H, Nozawa K, Kawabata-Shoda E, Kojima R, Yokoyama T, Ito H (2009) TRPA1 agonists delay gastric emptying in rats through serotonergic pathways. Naunyn-Schmiedeberg’s Arch Pharmacol 380:353–357
Franz C, Baser KHC, Windisch W (2010) Essential oils and aromatic plants in animal feeding – A European perspective. Annu Rev Flavour Fragr J 25:327–340
Furness JB, Rivera LR, Cho HJ, Bravo DM, Callaghan B (2013) The gut as a sensory organ. Nat Rev Gastroenterol Hepatol, published on line, doi:10.1038/nrgastro.2013.180
Gershon MD (2013) 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Curr Op Endoc Diab Obes 20:14–21
Hashemi SR, Davoodi H (2011) Herbal plants and their derivatives as growth and health promoters in animal nutrition. Vet Res Commun 35:169–180
Holzer P (2011) TRP channels in the digestive system. Curr Pharm Biotechnol 12:24–34
Kaji I, S-i K, Kuwahara A (2011) Effects of luminal thymol on epithelial transport in human and rat colon. Am J Physiol 300:G1132–G1143
Kaji I, Yasuoka Y, Karaki S-I, Kuwahara A (2012) Activation of TRPA1 by luminal stimuli induces EP4-mediated anion secretion in human and rat colon. Am J Physiol 302:G690–G701
Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang D-S, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277–289
Li Y, Hao Y, Zhu J, Owyang C (2000) Serotonin released from intestinal enterochromaffin cells mediates luminal non-cholecystokinin-stimulated pancreatic secretion in rats. Gastroenterology 118:1197–1207
Michiels J, Missotten J, Van Hoorick A, Ovyn A, Fremaut D, De Smet S, Dierick N (2010) Effects of dose and formulation of carvacrol and thymol on bacteria and some functional traits of the gut in piglets after weaning. Arch Anim Nutr 64:136–154
Nozawa K, Kawabata-Shoda E, Doihara H, Kojima R, Okada H, Mochizuki S, Sano Y, Inamura K, Matsushime H, Koizumi T, Yokoyama T, Ito H (2009) TRPA 1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells. Proc Natl Acad Sci USA 106:3408–3413
Owyang C (1996) Physiological mechanisms of cholecystokinin action on pancreatic secretion. Am J Physiol 271:G1–G7
Penuelas A, Tashima K, Tsuchiya S, Matsumoto K, Nakamura T, Horie S, Yano S (2007) Contractile effect of TRPA1 receptor agonists in the isolated mouse intestine. Eur J Pharmacol 576:143–150
Poole DP, Pelayo JC, Cattaruzza F, Kuo Y-M, Gai G, Chiu JV, Bron R, Furness JB, Grady EF, Bunnett NW (2011) Transient receptor potential Ankyrin 1 is expressed by inhibitory motoneurons of the mouse intestine. Gastroenterology 141:565–575
Purhonen AK, Louhivuori LM, Kiehne K, Akerman KEO, Herzig KH (2008) TRPA1 channel activation induces cholecystokinin release via extracellular calcium. FEBS Lett 582:229–232
Raybould HE (2007) Mechanisms of CCK signaling from gut to brain. Curr Opin Pharm 7:570–574
Rehfeld JF (2004) A centenary of gastrointestinal endocrinology. Horm Metab Res 36:735–741
Rochfort S, Parker AJ, Dunshea FR (2008) Plant bioactives for ruminant health and productivity. Phytochemistry 69:299–322
Windisch W, Schedle K, Plitzner C, Kroismayr A (2008) Use of phytogenic products as feed additives for swine and poultry. J Anim Sci 86:E140–E148
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We thank Dr. Daniel Poole and Dr. Tinamarie Lieu for providing the TRPA1 KO mice.
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Cho, HJ., Callaghan, B., Bron, R. et al. Identification of enteroendocrine cells that express TRPA1 channels in the mouse intestine. Cell Tissue Res 356, 77–82 (2014). https://doi.org/10.1007/s00441-013-1780-x
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DOI: https://doi.org/10.1007/s00441-013-1780-x