Enteroendocrine cells and 5-HT availability are altered in mucosa of guinea pigs with TNBS ileitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 287, Issue 5 50-5, 2004, Pages

  O'Hara, Jennifer R ^a   Ho, Winnie ^a   Linden, David R ^b   Mawe, Gary M ^b   Sharkey, Keith A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Inflammatory bowel disease; Motility; Neurotensin; Secretion; Sensory transduction; Somatostatin

Indexed keywords

CHOLECYSTOKININ; DEOXYCHOLATE SODIUM; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 2; NEUROTENSIN; PEPTIDE YY; SEROTONIN; SEROTONIN UPTAKE INHIBITOR; SOMATOSTATIN; TRINITROBENZENESULFONIC ACID;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOCRINE CELL; GUINEA PIG; ILEITIS; IMMUNOCOMPETENT CELL; INTESTINE CELL; INTESTINE INNERVATION; INTESTINE MOTILITY; INTESTINE SECRETION; MALE; MECHANICAL STIMULATION; MUCOSA INFLAMMATION; NONHUMAN; PERISTALSIS; PRIORITY JOURNAL; SEROTONIN RELEASE; SIGNAL TRANSDUCTION; SMALL INTESTINE MUCOSA;

ANIMALS; BIOLOGICAL AVAILABILITY; CELL COUNT; ENTEROENDOCRINE CELLS; GUINEA PIGS; ILEITIS; INTESTINAL MUCOSA; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; NERVE TISSUE PROTEINS; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; TRINITROBENZENESULFONIC ACID;

EID: 7044246141     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.00090.2004     Document Type: Article

References (62)

1. Asfaha S, Bell CJ, Wallace JL, and MacNaughton WK. Prolonged colonic epithelial hyporesponsiveness after colitis: role of inducible nitric oxide synthase. Am J Physiol Gastrointest Liver Physiol 276: G703-G710, 1999.
2. Bertrand PP, Kunze WA, Furness JB, and Bornstein JC. The terminals of myenteric intrinsic primary afferent neurons of the guinea-pig ileum are excited by 5-hydroxytryptamine acting at 5-hydroxytryptamine-3 receptors. Neuroscience 101: 459-469, 2000.
3. Bishop AE, Pietroletti R, Taat CW, Brummelkamp WH, and Polak JM. Increased populations of endocrine cells in Crohn's ileitis. Virchows Arch A Pathol Anat Histopathol 410: 391-396, 1987.
4. Blaschko H and Levine WG. Metabolism of indolealkylamines. In: 5-Hydroxytryptamine and Related Indolealkylamines, edited by Erspamer V. Berlin: Springer-Verlag, 1966, p. 212-239.
5. Bose M, Nickols C, and Greenwald S. 5-Hydroxytryptamine (5-HT) levels in colonic mucosa in irritable bowel syndrome (IBS): assessment by high performance liquid chromatography (HPLC) (Abstract). Gut 48: A57, 2001.
6. Bülbring E and Crema A. The release of 5-hydroxytryptamine in relation to pressure exerted on the intestinal mucosa. J Physiol 146: 18-28, 1959.
7. Bülbring E and Lin R. The effect of intraluminal application of 5-hydroxytryptamine and 5-hydroxytryptophan on peristalsis; the local production of 5-HT and its release in relation to intraluminal pressure and propulsive activity. J Physiol 140: 381-407, 1958.
8. Carlton SM, Du J, Davidson E, Zhou S, and Coggeshall RE. Somatostatin receptors on peripheral primary afferent terminals: inhibition of sensitized nociceptors. Pain 90: 233-244, 2001.
9. Castagliuolo I, Wang CC, Valenick L, Pasha A, Nikulasson S, Carraway RE, and Pothoulakis C. Neurotensin is a proinflammatory neuropeptide in colonic inflammation. J Clin Invest 103: 843-849, 1999.
10. Chang L, Munakata J, Mayer EA, Schmulson MJ, Johnson TD, Bernstein CN, Saba L, Naliboff B, Anton PA, and Matin K. Perceptual responses in patients with inflammatory and functional bowel disease. Gut 47: 497-505, 2000.
11. Chen JJ, Li Z, Pan H, Murphy DL, Tamir H, Koepsell H, and Gershon MD. Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the high-affinity serotonin transporter: abnormal intestinal motility and the expression of cation transporters. J Neurosci 21: 6348-6361, 2001.
12. Chen JX, Pan H, Rothman TP, Wade PR, and Gershon MD. Guinea pig 5-HT transporter: cloning, expression, distribution, and function in intestinal sensory reception. Am J Physiol Gastrointest Liver Physiol 275: G433-G448, 1998.
13. Coates MD, Mahoney CR, Linden DR, Sampson JE, Chen J, Blaszyk H, Crowell MD, Sharkey KA, Gershon MD, Mawe GM, and Moses PL. Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 126: 1657-1664, 2004.
14. Collins SM. The immunomodulation of enteric neuromuscular function: implications for motility and inflammatory disorders. Gastroenterology 111: 1683-1699, 1996.
15. Cooke HJ, Wunderlich J, and Christofi FL. "The force be with you": ATP in gut mechanosensory transduction. News Physiol Sci 18: 43-49, 2003.
16. Damholt AB, Kofod H, and Buchan AM. Immunocytochemical evidence for a paracrine interaction between GIP and GLP-1-producing cells in canine small intestine. Cell Tissue Res 298: 287-293, 1999.
17. Dave S, Liu S, Bogunovic M, and Plevy S. Toll-like receptors on enteroendocrine cells: role and function in gut homeostasis (Abstract). Gastroenterology 126, Suppl 2: A-573. 2004.
18. De Jonge F, Van Nassauw L, De Man JG, De Winter BY, Van Meir F, Depoortere I, Peeters TL, Pelckmans PA, Van Marck E, and Timmermans JP. Effects of Schistosoma mansoni infection on somatostatin and somatostatin receptor 2A expression in mouse ileum. Neurogastroenterol Motil 15: 149-159, 2003.
19. Drucker DJ, Yusta B, Boushey RP, DeForest L, and Brubaker PL. Human [Gly2]GLP-2 reduces the severity of colonic injury in a murine model of experimental colitis. Am J Physiol Gastrointest Liver Physiol 276: G79-G91, 1999.
20. El Salhy M, Danielsson A, Stenling R, and Grimelius L. Colonic endocrine cells in inflammatory bowel disease. J Intern Med 242: 413-419, 1997.
21. Furness JB, Kunze WAA, and 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 Gastrointest Liver Physiol 277: G922-G928, 1999.
22. Gershon MD. Roles played by 5-hydroxytryptamine in the physiology of the bowel. Aliment Pharmacol Ther 13, Suppl 2: 15-30, 1999.
23. Gershon MD. Plasticity in serotonin control mechanisms in the gut. Curr Opin Pharmacol 3: 600-607, 2003.
24. Grider JR, Kuemmerle JF, and Jin JG. 5-HT released by mucosal stimuli initiates peristalsis by activating 5-HT4/5-HT1p receptors on sensory CGRP neurons. Am J Physiol Gastrointest Liver Physiol 270: G778-G782, 1996.
25. Grundy D, Blaekshaw LA, and Hillsley K. Role of 5-hydroxytryptamine in gastrointestinal chemosensitivity. Dig Dis Sci 39: 44S-47S, 1994.
26. Hillsley K and Grundy D. Sensitivity to 5-hydroxytryptamine in different afferent subpopulations within mesenteric nerves supplying the rat jejunum. J Physiol 509: 717-727, 1998.
27. Hillsley K, Kirkup AJ, and Grundy D. Direct and indirect actions of 5-hydroxytryptamine on the discharge of mesenteric afferent fibres innervating the rat jejunum. J Physiol 506: 551-561, 1998.
28. Jin JG, Foxx-Orenstein AE, and Grider JR. Propulsion in guinea pig colon induced by 5-hydroxytryptamine (HT) via 5-HT4 and 5-HT3 receptors. J Pharmacol Exp Ther 288: 93-97, 1999.
29. Kirchgessner AL, Tamir H, and Gershon MD. Identification and stimulation by serotonin of intrinsic sensory neurons of the submucosal plexus of the guinea pig gut: activity-induced expression of Fos immunoreactivity. J Neurosci 12: 235-248, 1992.
30. Liddle RA. Cholecystokinin cells. Annu Rev Physiol 59: 221-242, 1997.
31. Linden DR, Chen JX, Gershon MD, Sharkey KA, and Mawe GM. Serotonin availability is increased in mucosa of guinea pigs with TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol 285: G207-G216, 2003.
32. Liu MT, Rayport S, Jiang Y, Murphy DL, and Gershon MD. Expression and function of 5-HT3 receptors in the enteric neurons of mice lacking the serotonin transporter. Am J Physiol Gastrointest Liver Physiol 283: G1398-G1411, 2002.
33. Lovshin J and Drucker DJ. New frontiers in the biology of GLP-2. Regul Pept 90: 27-32, 2000.
34. MacNaughton WK, Lowe SS, and Gushing K. Role of nitric oxide in inflammation-induced suppression of secretion in a mouse model of acute colitis. Am J Physiol Gastrointest Liver Physiol 275: G1353-G1360, 1998.
35. Magro F, Vieira-Coelho MA, Fraga S, Serrao MP, Veloso FT, Ribeiro T, and Soares-da-Silva P. Impaired synthesis or cellular storage of norepinephrine, dopamine, and 5-hydroxytryptamine in human inflammatory bowel disease. Dig Dis Sci 47: 216-224, 2002.
36. Martinolle JP, Garcia-Villar R, Fioramonti J, and Bueno L. Altered contractility of circular and longitudinal muscle in TNBS-inflamed guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 272: G1258-G1267, 1997.
37. Meier JJ, Nauck MA, Schmidt WE, and Gallwitz B. Gastric inhibitory polypeptide: the neglected incretin revisited. Regul Pept 107: 1-13, 2002.
38. Miceli P, Morris GP, MacNaughton WK, and Vanner S. Alterations in capsaicin-evoked electrolyte transport during the evolution of guinea pig TNBS ileitis. Am J Physiol Gastrointest Liver Physiol 282: G972-G980, 2002.
39. Miller LJ. Gastrointestinal hormones and receptors. In: Textbook of Gastroenterology, edited by Yamada T. Philadelphia, PA: Lippincott, Williams & Wilkins, 1999, p. 35-59.
40. Miller MJ, Sadowska-Krowicka H, Chotinaruemol S, Kakkis JL, and Clark DA. Amelioration of chronic ileitis by nitric oxide synthase inhibition. J Pharmacol Exp Ther 264: 11-16, 1993.
41. Miller MJ, Sadowska-Krowicka H, Jeng AY, Chotinaruemol S, Wong M, Clark DA, Ho W, and Sharkey KA. Substance P levels in experimental ileitis in guinea pigs: effects of misoprostol. Am J Physiol Gastrointest Liver Physiol 265: G321-G330, 1993.
42. Moreels TG, De Man JG, Dick JM, Nieuwendijk RJ, De Winter BY, Lefebvre RA, Herman AG, and Pelckmans PA. Effect of TNBS-induced morphological changes on pharmacological contractility of the rat ileum. Eur J Pharmacol 423: 211-222, 2001.
43. Morris GP, Beck PL, Herridge MS, Depew WT, Szewczuk MR, and Wallace JL. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96: 795-803, 1989.
44. Onaga T, Zabielski R, and Kato S. Multiple regulation of peptide YY secretion in the digestive tract. Peptides 23: 279-290, 2002.
45. Oshima S, Fujimura M, and Fukimiya M. Changes in number of serotonin-containing cells and serotonin levels in the intestinal mucosa of rats with colitis induced by dextran sodium sulfate. Histochem Cell Biol 112: 257-263, 1999.
46. Pan H and Gershon MD. Activation of intrinsic afferent pathways in submucosal ganglia of the guinea pig small intestine. J Neurosci 20: 3295-3309, 2000.
47. Peregrin AT, Ahlman H, Jodal M, and Lundgren O. Involvement of serotonin and calcium channels in the intestinal fluid secretion evoked by bile salt and cholera toxin. Br J Pharmacol 127: 887-894, 1999.
48. Racké K, Reimann A, Schworer H, and Kilbinger H. Regulation of 5-HT release from enterochromaffin cells. Behav Brain Res 73: 83-87, 1996.
49. Racké K and Schworer H. Regulation of serotonin release from the intestinal mucosa. Pharmacol Res 23: 13-25, 1991.
50. Rath HC, Ikeda JS, Linde HJ, Scholmerich J, Wilson KH, and Sartor RB. Varying cecal bacterial loads influences colitis and gastritis in HLA-B27 transgenic rats. Gastroenterology 116: 310-319, 1999.
51. Raybould HE. Visceral perception: sensory transduction in visceral afferents and nutrients. Gut 51, Suppl 1: i11-i14, 2002.
52. Raybould HE, Cooke HJ, and Christofi FL. Sensory mechanisms: transmitters, modulators and reflexes. Neurogastroenterol Motil 16, Suppl 1: 60-63, 2004.
53. Rubin DC, Zhang H, Qian P, Lorenz RG, Hutton K, and Peters MG. Altered enteroendocrine cell expression in T cell receptor alpha chain knock-out mice. Microsc Res Tech 51: 112-120, 2000.
54. Sartor RB. Pathogenesis and immune mechanisms of chronic inflammatory bowel diseases. Am J Gastroenterol 92, Suppl 12: 5S-11S, 1997.
55. Solcia E, Capella C, Buffa R, Usellini L, Fiocca R, Frigerio B, Tenti P, and Sessa F. The diffuse endocrine-paracrine system of the gut in health and disease: ultrastructural features. Scand J Gastroenterol Suppl 70: 25-36, 1981.
56. Solcia E, Capella C, Buffa R, Usellini L, Fiocca R, and Sessa F. Endocrine cells of the digestive system. In: Physiology of the Gastrointestinal Tract, edited by Johnson LR. New York: Raven, 1987, p. 111-130.
57. Tulassay Z. Somatostatin and the gastrointestinal tract. Scand J Gastroenterol, Suppl 228: 115-121, 1998.
58. Vermillion DL, Huizinga JD, Riddell RH, and Collins SM. Altered small intestinal smooth muscle function in Crohn's disease. Gastroenterology 104: 1692-1699, 1993.
59. Wade PR, Chen J, Jaffe B, Kassem IS, Blakely RD, and Gershon MD. Localization and function of a 5-HT transporter in crypt epithelia of the gastrointestinal tract. J Neurosci 16: 2352-2364, 1996.
60. Walsh JH. Gastrointestinal hormones. In: Physiology of the Gastrointestinal Tract, edited by Johnson LR. New York: Raven, 1987, p. 324-340.
61. Watanabe T, Kubota Y, Sawada T, and Muto T. Distribution and quantification of somatostatin in inflammatory disease. Dis Colon Rectum 35: 488-494, 1992.
62. Zhu JX, Zhu XY, Owyang C, and Li Y. Intestinal serotonin acts as a paracrine substance to mediate vagal signal transmission evoked by luminal factors in the rat. J Physiol 530: 431-442, 2001.