Taste sensing in the colon

Current Pharmaceutical Design

Volumn 20, Issue 16, 2014, Pages 2766-2774

  Kaji, Izumi ^a,b   Karaki, Shin ichiro ^a   Kuwahara, Atsukazu ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Colonic anion secretion; Luminal chemosensing; Short chain fatty acid receptors; Taste receptors; Transient receptor potential cation channels

Indexed keywords

CALCIUM SENSING RECEPTOR; FREE FATTY ACID RECEPTOR 2; RECEPTOR; SHORT CHAIN FATTY ACID RECEPTOR; TASTE RECEPTOR TYPE 1; TASTE RECEPTOR TYPE 2; TOLL LIKE RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG;

ARTICLE; BRUSH BORDER; CELL DIFFERENTIATION; CELL POPULATION; CELL STRUCTURE; CELL TRANSPORT; CHEMORECEPTOR; COLON; COLON MUCOSA; COLONIC LUMEN; COLONIC SECRETION; COLUMNAR EPITHELIUM; ENTEROENDOCRINE CELL; EX VIVO STUDY; EXTRACELLULAR CALCIUM; GOBLET CELL; HOMEOSTASIS; IN VIVO STUDY; INTESTINE CELL; MEMBRANOUS EPITHELIAL CELL; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY RECEPTOR; SIGNAL TRANSDUCTION; SMALL INTESTINE ABSORPTION; STIMULATION; ANIMAL; CHEMORECEPTOR CELL; CYTOLOGY; HUMAN; INTESTINE MUCOSA; METABOLISM; PHYSIOLOGY; TASTE;

ANIMALS; CHEMORECEPTOR CELLS; COLON; HUMANS; INTESTINAL MUCOSA; TASTE;

EID: 84903743305     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990573     Document Type: Article

References (90)

1. Sbarbati A, Osculati F. A new fate for old cells: brush cells and related elements. J Anat 2005; 206: 349-58.
2. Tsubouchi S, Leblond CP. Migration and turnover of enteroendocrine and caveolated cells in the epithelium of the descending colon, as shown by radioautography after continuous infusion of 3H-thymidine into mice. Am J Anat 1979; 156: 431-51.
3. Kunzelmann K, Mall M. Electrolyte transport in the mammalian colon: mechanisms and implications for disease. Physiol Rev 2002; 82: 245-89.
4. Ito H, Satsukawa M, Arai E, et al. Soluble fiber viscosity affects both goblet cell number and small intestine mucin secretion in rats. J Nutr 2009; 139: 1640-7.
5. Beltowski J. Guanylin and related peptides. J Physiol Pharmacol 2001; 52: 351-375.
6. Owen RL. Uptake and transport of intestinal macromolecules and microorganisms by M cells in Peyer's patches--a personal and historical perspective. Semin Immunol 1999; 11: 157-63.
7. Clark MA, Jepson MA, Simmons NL, Hirst BH. Differential surface characteristics of M cells from mouse intestinal Peyer's and caecal patches. Histochem J 1994; 26: 271-280.
8. Osaka M, Sasagawa T, Kobayashi S, Fujita T. The endocrine cells in the human colon and rectum. An electron microscope study of biopsy materials. Arch Histol Jpn 1971; 33: 247-60.
9. Fujita T. Taste cells in the gut and on the tongue. Their common, paraneuronal features. Physiol Behav 1991; 49: 883-5.
10. Braun T, Voland P, Kunz L, Prinz C, Gratzl M. Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology 2007; 132: 1890-901.
11. Kidd M, Modlin IM, Gustafsson BI, Drozdov I, Hauso O, Pfragner R. Luminal regulation of normal and neoplastic human EC cell serotonin release is mediated by bile salts, amines, tastants, and olfactants. Am J Physiol Gastrointest Liver Physiol 2008; 295: G260-72.
12. Nozawa K, Kawabata Shoda E, Doihara H, et al. TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells. Proc Natl Acad Sci USA 2009; 106: 3408-13.
13. Sjolund K, Sanden G, Hakanson R, Sundler F. Endocrine cells in human intestine: an immunocytochemical study. Gastroenterology 85: 1120-30, 1983.
14. Gerbe F, van Es JH, Makrini L, et al. Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J Cell Biol 2011; 192: 767-80.
15. Glisic R, Koko V, Todorovic V, Drndarevic N, Cvijic G. Serotonin-producing enterochromaffin (EC) cells of gastrointestinal mucosa in dexamethasone-treated rats. Regul Pept 2006; 136: 30-9.
16. Cani PD, Hoste S, Guiot Y, Delzenne NM. Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr 2007; 98: 32-7.
17. Kaji I, Karaki S, Tanaka R, Kuwahara A. Density distribution of free fatty acid receptor 2 (FFA2)-expressing and GLP-1-producing enteroendocrine L cells in human and rat lower intestine, and increased cell numbers after ingestion of fructo-oligosaccharide. J Mol Histol 2011; 42: 27-38.
18. Kuwahara A, Fujimiya M. Luminal release of regulatory peptides and amines: waste or physiological message? In: Zabielski R, Gregory PC, Westrom B. Eds. Biology of the Intestine in Growing Animals, Amsterdam, 2002.
19. Wiegand RC, Kato J, Huang MD, Fok KF, Kachur JF, Currie MG. Human guanylin: cDNA isolation, structure, and activity. FEBS Lett 1992; 311: 150-4.
20. Kugler P, Hofer D, Mayer B, Drenckhahn D. Nitric oxide synthase and NADP-linked glucose-6-phosphate dehydrogenase are colocalized in brush cells of rat stomach and pancreas. J Histochem Cytochem 1994; 42: 1317-21.
21. Bezencon C, Furholz A, Raymond F, et al. Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. J Comp Neurol 2008; 509: 514-25.
22. Kokrashvili Z, Rodriguez D, Yevshayeva V, Zhou H, Margolskee RF, Mosinger B. Release of endogenous opioids from duodenal enteroendocrine cells requires Trpm5. Gastroenterology 2009; 137: 598-606.
23. Hofer D, Puschel B, Drenckhahn D. Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc Natl Acad Sci USA 1996; 93: 6631-4.
24. Bezencon C, le Coutre J, Damak S. Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 2007; 32: 41-9.
25. Dyer J, Salmon KS, Zibrik L, Shirazi Beechey SP. Expression of sweet taste receptors of the T1R family in the intestinal tract and enteroendocrine cells. Biochem Soc Trans 2005; 33: 302-5.
26. Wu SV, Rozengurt N, Yang M, Young SH, Sinnett Smith J, Rozengurt E. Expression of bitter taste receptors of the T2R family in the gastrointestinal tract and enteroendocrine STC-1 cells. Proc Natl Acad Sci USA 2002; 99: 2392-7.
27. Rozengurt N, Wu SV, Chen MC, Huang C, Sternini C, Rozengurt E. Colocalization of the alpha-subunit of gustducin with PYY and GLP-1 in L cells of human colon. Am J Physiol Gastrointest Liver Physiol 2006; 291: G792-802.
28. Sutherland K, Young RL, Cooper NJ, Horowitz M, Blackshaw LA. Phenotypic characterization of taste cells of the mouse small intestine. Am J Physiol Gastrointest Liver Physiol 2007; 292: G1420-8.
29. San Gabriel AM, Maekawa T, Uneyama H, Yoshie S, Torii K. mGluR1 in the fundic glands of rat stomach. FEBS Lett 2007; 581: 1119-23.
30. Chattopadhyay N, Cheng I, Rogers K, et al. Identification and localization of extracellular Ca(2+)-sensing receptor in rat intestine. Am J Physiol 1998; 274: G122-30.
31. Edfalk S, Steneberg P, Edlund H. Gpr40 is expressed in enteroendocrine cells and mediates free fatty acid stimulation of incretin secretion. Diabetes 2008; 57: 2280-7.
32. 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: 16767-72.
33. Karaki S, Mitsui R, Hayashi H, et al. Short-chain fatty acid receptor, GPR43, is expressed by enteroendocrine cells and mucosal mast cells in rat intestine. Cell Tissue Res 2006; 324: 353-60.
34. Hirasawa A, Tsumaya K, Awaji T, et al. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 2005; 11: 90-4.
35. Margolskee RF, Dyer J, Kokrashvili Z, et al. T1R3 and gustducin in gut sense sugars to regulate expression of Na+-glucose cotransporter 1. Proc Natl Acad Sci USA 2007; 104: 15075-80.
36. Mace OJ, Affleck J, Patel N, Kellett GL. Sweet taste receptors in rat small intestine stimulate glucose absorption through apical GLUT2. J Physiol 582: 379-92, 2007.
37. Akiba Y, Kaunitz JD. Luminal chemosensing in the duodenal mucosa. Acta Physiol (Oxf) 2011; 201: 77-84.
38. Umesaki Y, Yajima T, Yokokura T, Mutai M. Effect of organic acid absorption on bicarbonate transport in rat colon. Pflugers Arch 1979; 379: 43-7.
39. Yajima T. Contractile effect of short-chain fatty acids on the isolated colon of the rat. J Physiol 1985; 368: 667-78.
40. Yajima T. Luminal propionate-induced secretory response in the rat distal colon in vitro. J Physiol 1988; 403: 559-75.
41. Tazoe H, Otomo Y, Karaki S, et al. Expression of short-chain fatty acid receptor GPR41 in the human colon. Biomed Res 2009; 30: 149-56.
42. Andres H, Rock R, Bridges RJ, Rummel W, Schreiner J. Submucosal plexus and electrolyte transport across rat colonic mucosa. J Physiol 1985; 364: 301-12.
43. Furness JB, Kunze WA, Clerc N. Nutrient tasting and signaling mechanisms in the gut. II. The intestine as a sensory organ: neural, endocrine, and immune responses. Am J Physiol 1999; 277: G922-8.
44. Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS. A novel family of mammalian taste receptors. Cell 2000; 100: 693-702.
45. Matsunami H. Functional expression of Mammalian odorant receptors. Chem Senses 2005; 30: i95-96.
46. Montmayeur JP, Matsunami H. Receptors for bitter and sweet taste. Curr Opin Neurobiol 2002; 12: 366-71.
47. Meyerhof W, Batram C, Kuhn C, et al. The molecular receptive ranges of human TAS2R bitter taste receptors. Chem Senses 2010; 35: 157-70.
48. Kaji I, Karaki SI, Fukami Y, Terasaki M, Kuwahara A. Secretory effects of a luminal bitter tastant and expressions of bitter taste receptors, T2Rs, in the human and rat large intestine. Am J Physiol Gastrointest Liver Physiol. 2009; 296: G971-81.
49. Nelson TM, Munger SD, Boughter JD Jr. Taste sensitivities to PROP and PTC vary independently in mice. Chem Senses 2003; 28: 695-704.
50. Mueller KL, Hoon MA, Erlenbach I, Chandrashekar J, Zuker CS, Ryba NJ. The receptors and coding logic for bitter taste. Nature 2005; 434: 225-9.
51. Diener M, Rummel W. Distension-induced secretion in the rat colon: mediation by prostaglandins and submucosal neurons. Eur J Pharmacol 1990; 178: 47-57.
52. Sharon P, Stenson WF. Enhanced synthesis of leukotriene B4 by colonic mucosa in inflammatory bowel disease. Gastroenterology 1984; 86: 453-60.
53. Halm DR, Halm ST. Prostanoids stimulate K secretion and Cl secretion in guinea pig distal colon via distinct pathways. Am J Physiol Gastrointest Liver Physiol 2001; 281: G984-96.
54. Karaki SI, Kuwahara A. Regulation of intestinal secretion involved in the interaction between neurotransmitters and prostaglandin E2. Neurogastroenterol Motil 2004; 16 Suppl 1: 96-9.
55. McLaughlin SK, McKinnon PJ, Margolskee RF. Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature 1992; 357: 563-9.
56. Jang HJ, Kokrashvili Z, Theodorakis MJ, et al. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA 104: 15069-74, 2007.
57. Cummings JH. Short chain fatty acids in the human colon. Gut 1981; 22: 763-779.
58. Savage DC. Gastrointestinal microflora in mammalian nutrition. Annu Rev Nutr 1986; 6: 155-78.
59. Yajima T, Inoue R, Matsumoto M, Yajima M. Non-neuronal release of ACh plays a key role in secretory response to luminal propionate in rat colon. J Physiol 2011; 589: 953-962.
60. Diener M, Hug F, Strabel D, Scharrer E. Cyclic AMP-dependent regulation of K+ transport in the rat distal colon. Br J Pharmacol 1996; 118: 1477-87.
61. Karaki S, Kuwahara A. Propionate-induced epithelial K(+) and Cl (-)/HCO (3) (-) secretion and free fatty acid receptor 2 (FFA2, GPR43) expression in the guinea pig distal colon. Pflugers Arch 2011; 461: 141-52.
62. Karaki S, Tazoe H, Kaji I, Otomo Y, Yajima T, Kuwahara A. Contractile and Secretory Responses of Luminal Short-Chain Fatty Acids and the Expression of These Receptors, GPR41 and GPR43, in the Human Small and Large Intestines Gastroenterology 2008; 134: A-368.
63. 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: 11312-9.
64. Le Poul E, 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: 25481-9.
65. Nilsson NE, Kotarsky K, Owman C, Olde B. Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids. Biochem Biophys Res Commun 2003; 303: 1047-52.
66. Stoddart LA, Smith NJ, Milligan G. International Union of Pharmacology. LXXI. Free fatty acid receptors FFA1,-2, and-3: pharmacology and pathophysiological functions. Pharmacol Rev 60: 405-17, 2008.
67. Karaki S, Tazoe H, Hayashi H, et al. Expression of the short-chain fatty acid receptor, GPR43, in the human colon. J Mol Histol 2008; 39: 135-42.
68. Dumoulin V, Moro F, Barcelo A, Dakka T, Cuber JC. Peptide YY, glucagon-like peptide-1, and neurotensin responses to luminal factors in the isolated vascularly perfused rat ileum. Endocrinology 1998; 139: 3780-6.
69. Freeland KR, Wolever TM. Acute effects of intravenous and rectal acetate on glucagon-like peptide-1, peptide YY, ghrelin, adiponectin and tumour necrosis factor-alpha. Br J Nutr 2010; 103: 460-6.
70. Paroder V, Spencer SR, Paroder M, et al. Na(+)/monocarboxylate transport (SMCT) protein expression correlates with survival in colon cancer: molecular characterization of SMCT. Proc Natl Acad Sci USA 2006; 103: 7270-5.
71. Iwanaga T, Takebe K, Kato I, Karaki S, Kuwahara A. Cellular expression of monocarboxylate transporters (MCT) in the digestive tract of the mouse, rat, and humans, with special reference to slc5a8. Biomed Res 2006; 27: 243-54.
72. Umesaki Y, Yajima T, Tohyama K, Mutai M. Characterization of acetate uptake by the colonic epithelial cells of the rat. Pflugers Arch 1980; 388: 205-9.
73. Campbell JM, Fahey GC Jr, Wolf BW. Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J Nutr 1997; 127: 130-6.
74. Ten Bruggencate SJ, Bovee Oudenhoven IM, Lettink Wissink ML, Van der Meer R. Dietary fructooligosaccharides increase intestinal permeability in rats. J Nutr 2005; 135: 837-42.
75. Mitsui R, Karaki SI, Kubo Y, Sugiura Y, Kuwahara A. Fibre-free diet leads to impairment of neuronally mediated muscle contractile response in rat distal colon. Neurogastroenterol Motil 2006; 18: 1093-101.
76. Bulbring E, Crema A. The release of 5-hydroxytryptamine in relation to pressure exerted on the intestinal mucosa. J Physiol 146: 18-28, 1959.
77. Cooke HJ. "Enteric Tears": Chloride Secretion and Its Neural Regulation. News Physiol Sci 1998; 13: 269-74.
78. Hoenderop JG, Vennekens R, Muller D, et al. Function and expression of the epithelial Ca(2+) channel family: comparison of mammalian ECaC1 and 2. J Physiol 2001; 537: 747-61.
79. Ueda T, Yamada T, Ugawa S, Ishida Y, Shimada S. TRPV3, a thermosensitive channel is expressed in mouse distal colon epithelium. Biochem Biophys Res Commun 2009; 383: 130-134.
80. Matsumoto K, Kurosawa E, Terui H, et al. Localization of TRPV1 and contractile effect of capsaicin in mouse large intestine: high abundance and sensitivity in rectum and distal colon. Am J Physiol Gastrointest Liver Physiol 2009; 297: G348-60.
81. Poole DP, Pelayo JC, Cattaruzza F, et al. Transient receptor potential ankyrin 1 is expressed by inhibitory motoneurons of the mouse intestine. Gastroenterology 2011; 141: 565-75.
82. Penuelas A, Tashima K, Tsuchiya S, et al. Contractile effect of TRPA1 receptor agonists in the isolated mouse intestine. Eur J Pharmacol 576: 143-50, 2007.
83. Kaji I, Yasuoka Y, Karaki S, Kuwahara A. Activation of TRPA1 by luminal stimuli induces EP4-mediated anion secretion in human and rat colon. Am J Physiol Gastrointest Liver Physiol 2012; 302: G690-701.
84. Cheng SX, Okuda M, Hall AE, Geibel JP, Hebert SC. Expression of calcium-sensing receptor in rat colonic epithelium: evidence for modulation of fluid secretion. Am J Physiol Gastrointest Liver Physiol 2002; 283: G240-50.
85. Boudry G, Perrier C. Thyme and cinnamon extracts induce anion secretion in piglet small intestine via cholinergic pathways. J Physiol Pharmacol 2008; 59: 543-552.
86. Schulz S, Dickschat JS. Bacterial volatiles: the smell of small organisms. Nat Prod Rep 2007; 24: 814-42.
87. Kaji I, Karaki SI, Kuwahara A. Effects of luminal thymol on epithelial transport in human and rat colon. Am J Physiol Gastrointest Liver Physiol 2011; 300: G1132-43.
88. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 2010; 10: 131-44.
89. Bogunovic M, Dave SH, Tilstra JS, et al. Enteroendocrine cells express functional Toll-like receptors. Am J Physiol Gastrointest Liver Physiol 292: G1770-83, 2007.
90. Fukuda S, Toh H, Hase K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2001; 469: 543-7.