Free fatty acid receptor 3 activation suppresses neurogenic motility in rat proximal colon

Neurogastroenterology and Motility

Volumn 30, Issue 1, 2018, Pages

  Kaji, I ^a,b   Akiba, Y ^a,b   Furuyama, T ^c,d   Adelson, D W ^a   Iwamoto, K ^e   Watanabe, M ^f   Kuwahara, A ^e   Kaunitz, J D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^c DOSHISHA UNIVERSITY   (Japan)

^d JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^e UNIVERSITY OF SHIZUOKA   (Japan)

^f HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

circular muscle contraction; defecation; enteric neural pathway; free fatty acid receptor 3; proximal colon

Indexed keywords

BETHANECHOL; FREE FATTY ACID RECEPTOR 3; G PROTEIN COUPLED RECEPTOR 40; NICOTINE; SEROTONIN; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; GPR30 PROTEIN, RAT; NICOTINIC AGENT; SEROTONIN ANTAGONIST;

AGONIST; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASCENDING COLON; CHOLINERGIC NERVE CELL; COLON MOTILITY; CONTROLLED STUDY; DEFECATION; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE CONTRACTION; MUSCLE RELAXATION; MYENTERIC PLEXUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; AGONISTS; ANIMAL; COLON; GASTROINTESTINAL MOTILITY; METABOLISM; NERVE CELL; NITRERGIC NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CHOLINERGIC NEURONS; COLON; DEFECATION; GASTROINTESTINAL MOTILITY; MALE; MUSCLE CONTRACTION; MYENTERIC PLEXUS; NEURONS; NICOTINE; NICOTINIC AGONISTS; NITRERGIC NEURONS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; SEROTONIN; SEROTONIN ANTAGONISTS;

EID: 85024497985     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.13157     Document Type: Article

References (46)

1. Matsuoka K, Mizuno S, Hayashi A, Hisamatsu T, Naganuma M, Kanai T. Fecal microbiota transplantation for gastrointestinal diseases. Keio J Med. 2014;63:69-74.
2. Rossen NG, MacDonald JK, de Vries EM, et al. Fecal microbiota transplantation as novel therapy in gastroenterology: a systematic review. World J Gastroenterol. 2015;21:5359-5371.
3. Hungin AP, Mulligan C, Pot B, et al. Systematic review: probiotics in the management of lower gastrointestinal symptoms in clinical practice – an evidence-based international guide. Aliment Pharmacol Ther. 2013;38:864-886.
4. Ahmad OF, Akbar A. Microbiome, antibiotics and irritable bowel syndrome. Br Med Bull. 2016;120:91-99.
5. Balestra B, Vicini R, Cremon C, et al. Colonic mucosal mediators from patients with irritable bowel syndrome excite enteric cholinergic motor neurons. Neurogastroenterol Motil. 2012;24:1118-e570.
6. Cenac N, Andrews CN, Holzhausen M, et al. Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest. 2007;117:636-647.
7. Buhner S, Li Q, Vignali S, et al. Activation of human enteric neurons by supernatants of colonic biopsy specimens from patients with irritable bowel syndrome. Gastroenterology. 2009;137:1425-1434.
8. Cummings JH. Short chain fatty acids in the human colon. Gut. 1981;22:763-779.
9. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990;70:567-590.
10. Takahashi T, Nakade Y, Fukuda H, Tsukamoto K, Mantyh C, Pappas TN. Daily intake of high dietary fiber slows accelerated colonic transit induced by restrain stress in rats. Dig Dis Sci. 2008;53:1271-1277.
11. Treem WR, Ahsan N, Kastoff G, Hyams JS. Fecal short-chain fatty acids in patients with diarrhea-predominant irritable bowel syndrome: in vitro studies of carbohydrate fermentation. J Pediatr Gastroenterol Nutr. 1996;23:280-286.
12. Mortensen PB, Clausen MR. Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenterol Suppl. 1996;216:132-148.
13. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28:1221-1227.
14. Brown AJ, Goldsworthy SM, Barnes AA, et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem. 2003;278:11312-11319.
15. Le PE, Loison C, Struyf S, et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem. 2003;278:25481-25489.
16. Pluznick J. A novel SCFA receptor, the microbiota, and blood pressure regulation. Gut Microbes. 2014;5:202-207.
17. Iwanaga T, Kishimoto A. Cellular distributions of monocarboxylate transporters: a review. Biomed Res. 2015;36:279-301.
18. Yokokura T, Yajima T, Hashimoto S. Effect of organic acid on gastrointestinal motility of rat in vitro. Life Sci. 1977;21:59-62.
19. Yajima T. Contractile effect of short-chain fatty acids on the isolated colon of the rat. J Physiol. 1985;368:667-678.
20. Richardson A, Delbridge AT, Brown NJ, Rumsey RD, Read NW. Short chain fatty acids in the terminal ileum accelerate stomach to caecum transit time in the rat. Gut. 1991;32:266-269.
21. Mitsui R, Ono S, Karaki S, Kuwahara A. Neural and non-neural mediation of propionate-induced contractile responses in the rat distal colon. Neurogastroenterol Motil. 2005;17:585-594.
22. Dass NB, John AK, Bassil AK, et al. The relationship between the effects of short-chain fatty acids on intestinal motility in vitro and GPR43 receptor activation. Neurogastroenterol Motil. 2007;19:66-74.
23. Kaji I, Akiba Y, Konno K, et al. Neural FFA3 activation inversely regulates nicotinic ACh receptor-mediated secretion in rat proximal colon. J Physiol. 2016;594:3339-3352.
24. Ulven T. Short-chain free fatty acid receptors FFA2/GPR43 and FFA3/GPR41 as new potential therapeutic targets. Front Endocrinol (Lausanne). 2012;3:111.
25. Engelstoft MS, Park WM, Sakata I, et al. Seven transmembrane G protein-coupled receptor repertoire of gastric ghrelin cells. Mol Metab. 2013;2:376-392.
26. Johnson DS, Heinemann SF. Detection of 5-HT3R-A, a 5-HT3 receptor subunit, in submucosal and myenteric ganglia of rat small intestine using in situ hybridization. Neurosci Lett. 1995;184:67-70.
27. Poole DP, Xu B, Koh SL, et al. Identification of neurons that express 5-hydroxytryptamine4 receptors in intestine. Cell Tissue Res. 2006;325:413-422.
28. Prior A, Read NW. Reduction of rectal sensitivity and post-prandial motility by granisetron, a 5 HT3-receptor antagonist, in patients with irritable bowel syndrome. Aliment Pharmacol Ther. 1993;7:175-180.
29. Miyata K, Kamato T, Nishida A, et al. Role of the serotonin3 receptor in stress-induced defecation. J Pharmacol Exp Ther. 1992;261:297-303.
30. Furness JB, Poole DP, Cho HJ, Callaghan BP, Rivera LR. The innervation of the gastrointestinal tract. Yamada's Textbook of Gastroenterology. John Wiley & Sons Ltd: Oxford, UK; 2015:239-258.
31. Takahashi T, Owyang C. Characterization of vagal pathways mediating gastric accommodation reflex in rats. J Physiol. 1997;504(Pt 2):479-488.
32. Schneider DA, Perrone M, Galligan JJ. Nicotinic acetylcholine receptors at sites of neurotransmitter release to the guinea pig intestinal circular muscle. J Pharmacol Exp Ther. 2000;294:363-369.
33. Borjesson L, Nordgren S, Delbro DS. DMPP causes relaxation of rat distal colon by a purinergic and a nitrergic mechanism. Eur J Pharmacol. 1997;334:223-231.
34. Patel BA, Galligan JJ, Swain GM, Bian X. Electrochemical monitoring of nitric oxide released by myenteric neurons of the guinea pig ileum. Neurogastroenterol Motil. 2008;20:1243-1250.
35. Zhou X, Ren J, Brown E, Schneider D, Caraballo-Lopez Y, Galligan JJ. Pharmacological properties of nicotinic acetylcholine receptors expressed by guinea pig small intestinal myenteric neurons. J Pharmacol Exp Ther. 2002;302:889-897.
36. Griffin MT, Ehlert FJ. Specific inhibition of isoproterenol-stimulated cyclic AMP accumulation by M2 muscarinic receptors in rat intestinal smooth muscle. J Pharmacol Exp Ther. 1992;263:221-225.
37. Tallent M, Liapakis G, O'Carroll AM, Lolait SJ, Dichter M, Reisine T. Somatostatin receptor subtypes SSTR2 and SSTR5 couple negatively to an L-type Ca2+ current in the pituitary cell line AtT-20. Neuroscience. 1996;71:1073-1081.
38. Hein L, Altman JD, Kobilka BK. Two functionally distinct alpha2-adrenergic receptors regulate sympathetic neurotransmission. Nature. 1999;402:181-184.
39. D'Agostino G, Barbieri A, Chiossa E, Tonini M. M4 muscarinic autoreceptor-mediated inhibition of -3H-acetylcholine release in the rat isolated urinary bladder. J Pharmacol Exp Ther. 1997;283:750-756.
40. Nohr MK, Pedersen MH, Gille A, et al. GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinol. 2013;154:3552-3564.
41. Samuel BS, Shaito A, Motoike T, et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci USA. 2008;105:16767-16772.
42. Canavan C, West J, Card T. The epidemiology of irritable bowel syndrome. Clin Epidemiol. 2014;6:71-80.
43. Ozaki A, Yoshidomi M, Sukamoto T. Effect of the 5-hydroxytryptamine3 (5-HT3)-receptor antagonist KB-R6933 on experimental diarrhea models. Jpn J Pharmacol. 1999;80:93-96.
44. Taché Y, Million M. Role of corticotropin-releasing factor signaling in stress-related alterations of colonic motility and hyperalgesia. J Neurogastroenterol Motil. 2015;21:8-24.
45. Wang L, Martinez V, Kimura H, Taché Y. 5-Hydroxytryptophan activates colonic myenteric neurons and propulsive motor function through 5-HT4 receptors in conscious mice. Am J Physiol Gastrointest Liver Physiol. 2007;292:G419-G428.
46. Gelal A, Guven H. Characterization of 5-HT receptors in rat proximal colon. Gen Pharmacol. 1998;30:343-346.