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Published in: Digestive Diseases and Sciences 12/2008

01-12-2008 | Original Paper

Infiltration of Mast Cells in Rat Colon Is a Consequence of Ischemia/Reperfusion

Authors: Elin Sand, Anna Themner-Persson, Eva Ekblad

Published in: Digestive Diseases and Sciences | Issue 12/2008

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Abstract

Intestinal ischemia as well as mastocytosis occur in patients with inflammatory bowel disease and irritable bowel syndrome. Our aim was to clarify how ischemia with reperfusion (I/R) affects the structure, enteric neurons, and immune cells in the colon. Rats were subjected to colon ischemia for 1 h and reperfused for 1 day up to 20 weeks; sham-operated rats were used as controls. No structural remodeling of the intestinal segment was detected after I/R. The number and distribution of eosinophils were not affected by I/R. Local areas containing numerous mast cells were detected in the muscle layers, the serosa, and in and around the myenteric ganglia 4–20 weeks post ischemia. It was notable that myenteric ganglionic formations within mast-cell-rich areas virtually lacked neurons. Mast cells were rarely found in controls. In conclusion, I/R of the colon attracts mast cells, and death of myenteric neurons occurs in such locations.
Literature
6.
go back to reference Takeyoshi I, Iwanami K, Ohwada S, Kawashima Y, Kawata K, Aiba M, Kobayashi J, Koyama T, Matsumoto K, Satoh S, Morishita Y (1999) Effect of FR167653 on small bowel ischemia-reperfusion injury in dogs. Dig Dis Sci 44:2334–2343. doi:10.1023/A:1026633510390 PubMedCrossRef Takeyoshi I, Iwanami K, Ohwada S, Kawashima Y, Kawata K, Aiba M, Kobayashi J, Koyama T, Matsumoto K, Satoh S, Morishita Y (1999) Effect of FR167653 on small bowel ischemia-reperfusion injury in dogs. Dig Dis Sci 44:2334–2343. doi:10.​1023/​A:​1026633510390 PubMedCrossRef
7.
go back to reference Takada K, Yamashita K, Sakurai-Yamashita Y, Shigematsu K, Hamada Y, Hioki K, Taniyama K (1998) Participation of nitric oxide in the mucosal injury of rat intestine induced by ischemia-reperfusion. J Pharmacol Exp Therap 287:403–407 Takada K, Yamashita K, Sakurai-Yamashita Y, Shigematsu K, Hamada Y, Hioki K, Taniyama K (1998) Participation of nitric oxide in the mucosal injury of rat intestine induced by ischemia-reperfusion. J Pharmacol Exp Therap 287:403–407
8.
go back to reference Takahashi A, Tomomasa T, Kaneko H, Watanabe T, Tabata M, Morikawa H, Tsuchida Y, Kuwano H (2001) Intestinal motility in an in vivo rat model of intestinal ischemia-reperfusion with special reference to the effect of nitric oxide on the motility changes. J Pediatr Gastroenterol Nutr 33:283–288. doi:10.1097/00005176-200109000-00010 PubMedCrossRef Takahashi A, Tomomasa T, Kaneko H, Watanabe T, Tabata M, Morikawa H, Tsuchida Y, Kuwano H (2001) Intestinal motility in an in vivo rat model of intestinal ischemia-reperfusion with special reference to the effect of nitric oxide on the motility changes. J Pediatr Gastroenterol Nutr 33:283–288. doi:10.​1097/​00005176-200109000-00010 PubMedCrossRef
9.
go back to reference Calcina F, Barocelli E, Bertoni S, Furukawa O, Kaunitz J, Impicciatore M, Sternini C (2005) Effect of N-methyl-D-aspartate receptor blockade on neuronal plasticity and gastrointestinal transit delay induced by ischemia/reperfusion in rats. Neuroscience 134:39–49. doi:10.1016/j.neuroscience.2005.03.052 PubMedCrossRef Calcina F, Barocelli E, Bertoni S, Furukawa O, Kaunitz J, Impicciatore M, Sternini C (2005) Effect of N-methyl-D-aspartate receptor blockade on neuronal plasticity and gastrointestinal transit delay induced by ischemia/reperfusion in rats. Neuroscience 134:39–49. doi:10.​1016/​j.​neuroscience.​2005.​03.​052 PubMedCrossRef
11.
go back to reference Piao D, Jiang H, Kosaka M, Shibata T, Ohtsuka A, Murakami T (1999) Cytoplasmic delayed neuronal death in the myenteric plexus of the rat small intestine after ischemia. Arch Histol Cytol 62:383–392. doi:10.1679/aohc.62.383 PubMedCrossRef Piao D, Jiang H, Kosaka M, Shibata T, Ohtsuka A, Murakami T (1999) Cytoplasmic delayed neuronal death in the myenteric plexus of the rat small intestine after ischemia. Arch Histol Cytol 62:383–392. doi:10.​1679/​aohc.​62.​383 PubMedCrossRef
12.
go back to reference Matsuura T, Masumoto K, Ieiri S, Nakatsuji T, Akiyoshi J, Nishimoto Y, Takahashi Y, Hayashida M, Taguchi T (2007) Morphological and physiological changes of interstitial cells of Cajal after small bowel transplantation in rats. Transplant Int 20:616–624. doi:10.1111/j.1432-2277.2007.00475.x CrossRef Matsuura T, Masumoto K, Ieiri S, Nakatsuji T, Akiyoshi J, Nishimoto Y, Takahashi Y, Hayashida M, Taguchi T (2007) Morphological and physiological changes of interstitial cells of Cajal after small bowel transplantation in rats. Transplant Int 20:616–624. doi:10.​1111/​j.​1432-2277.​2007.​00475.​x CrossRef
15.
go back to reference Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM, Corinaldesi R (2004) Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126:693–702. doi:10.1053/j.gastro.2003.11.055 PubMedCrossRef Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM, Corinaldesi R (2004) Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126:693–702. doi:10.​1053/​j.​gastro.​2003.​11.​055 PubMedCrossRef
16.
go back to reference Guilarte M, Santos J, de Torres I, Alonso C, Vicario M, Ramos L, Martínez C, Casellas F, Saperas E, Malagelada JR (2007) Diarrhoea-predominant IBS patients show mast cell activation and hyperplasia in the jejunum. Gut 56:203–209. doi:10.1136/gut.2006.100594 PubMedCrossRef Guilarte M, Santos J, de Torres I, Alonso C, Vicario M, Ramos L, Martínez C, Casellas F, Saperas E, Malagelada JR (2007) Diarrhoea-predominant IBS patients show mast cell activation and hyperplasia in the jejunum. Gut 56:203–209. doi:10.​1136/​gut.​2006.​100594 PubMedCrossRef
17.
go back to reference He SH (2004) Key role of mast cells and their major secretory products in inflammatory bowel disease. World J Gastroenterol 10:309–318PubMed He SH (2004) Key role of mast cells and their major secretory products in inflammatory bowel disease. World J Gastroenterol 10:309–318PubMed
18.
go back to reference Stead R, Dixon M, Bramwell N, Riddell R, Bienenstock J (1989) Mast cells are closely apposed to nerves in the human gastrointestinal mucosa. Gastroenterology 97:575–585PubMed Stead R, Dixon M, Bramwell N, Riddell R, Bienenstock J (1989) Mast cells are closely apposed to nerves in the human gastrointestinal mucosa. Gastroenterology 97:575–585PubMed
19.
21.
go back to reference Kalia N, Brown NJ, Wood RF, Pockley AG (2005) Ketotifen arbrogates local and systemic consequences of rat intestinal ischemia-reperfusion injury. J Gastroenterol Hepatol 20:1032–1038PubMed Kalia N, Brown NJ, Wood RF, Pockley AG (2005) Ketotifen arbrogates local and systemic consequences of rat intestinal ischemia-reperfusion injury. J Gastroenterol Hepatol 20:1032–1038PubMed
22.
go back to reference Santen S, Wang Y, Menger MD, Jeppsson B, Thorlacius H (2007) Mast-cell-dependent secretion of CXC chemokines regulates ischemia-reperfusion-induced recruitment in the colon. Int J Colorectal Dis 23:527–534. doi:10.1007/s00384-007-0436-2 Santen S, Wang Y, Menger MD, Jeppsson B, Thorlacius H (2007) Mast-cell-dependent secretion of CXC chemokines regulates ischemia-reperfusion-induced recruitment in the colon. Int J Colorectal Dis 23:527–534. doi:10.​1007/​s00384-007-0436-2
24.
go back to reference Ekblad E, Mulder H, Sundler F (1996) Vasoactive intestinal peptide expression in enteric neurons is up regulated by both colchicine and axotomy. Regul Pept 63:113–121PubMed Ekblad E, Mulder H, Sundler F (1996) Vasoactive intestinal peptide expression in enteric neurons is up regulated by both colchicine and axotomy. Regul Pept 63:113–121PubMed
25.
go back to reference Ekblad E, Sjuve R, Arner A, Sundler F (1998) Enteric neuronal plasticity and a reduced number of interstitial cells of Cajal in hypertrophic rat ileum. Gut 42:836–844PubMedCrossRef Ekblad E, Sjuve R, Arner A, Sundler F (1998) Enteric neuronal plasticity and a reduced number of interstitial cells of Cajal in hypertrophic rat ileum. Gut 42:836–844PubMedCrossRef
28.
go back to reference Cenac N, Andrews C, Holzhausen M, Chapman K, Cottrell G, Andrade-Gordon P, Steinhoff M, Barbara G, Beck P, Bunnett NW, Sharkey KA, Ferraz JG, Shaffer E, Vergnolle N (2007) Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest 117:636–647. doi:10.1172/JCI29255 PubMedCrossRef Cenac N, Andrews C, Holzhausen M, Chapman K, Cottrell G, Andrade-Gordon P, Steinhoff M, Barbara G, Beck P, Bunnett NW, Sharkey KA, Ferraz JG, Shaffer E, Vergnolle N (2007) Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest 117:636–647. doi:10.​1172/​JCI29255 PubMedCrossRef
29.
go back to reference Barbara G, Wang B, Stanghellini V, Cremon C, Di Nardo G, Trevisani M, Campi B, Geppetti P, Tonini M, Bunnett NW, Grundy D, Corinaldesi R (2007) Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 132:26–37. doi:10.1053/j.gastro.2006.11.039 PubMedCrossRef Barbara G, Wang B, Stanghellini V, Cremon C, Di Nardo G, Trevisani M, Campi B, Geppetti P, Tonini M, Bunnett NW, Grundy D, Corinaldesi R (2007) Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 132:26–37. doi:10.​1053/​j.​gastro.​2006.​11.​039 PubMedCrossRef
34.
go back to reference Schneider J, Jehle E, Starlinger, Neunlist M, Michel K, Hoppe S, Schemann M (2001) Neurotransmitter coding of enteric neurons in the submucous plexus is changed in non-inflamed rectum of patients with Crohn’s disease. Neurogastroenterol Motil 13:255–264. doi:10.1046/j.1365-2982.2001.00265.x PubMedCrossRef Schneider J, Jehle E, Starlinger, Neunlist M, Michel K, Hoppe S, Schemann M (2001) Neurotransmitter coding of enteric neurons in the submucous plexus is changed in non-inflamed rectum of patients with Crohn’s disease. Neurogastroenterol Motil 13:255–264. doi:10.​1046/​j.​1365-2982.​2001.​00265.​x PubMedCrossRef
35.
go back to reference Sandgren K, Lin Z, Fex Svenningsen Å, Ekblad E (2003) Vasoactive intestinal peptide and nitric oxide promote survival of adult rat myenteric neurons in culture. J Neurosci Res 72:595–602. doi:10.1002/jnr.10612 PubMedCrossRef Sandgren K, Lin Z, Fex Svenningsen Å, Ekblad E (2003) Vasoactive intestinal peptide and nitric oxide promote survival of adult rat myenteric neurons in culture. J Neurosci Res 72:595–602. doi:10.​1002/​jnr.​10612 PubMedCrossRef
42.
go back to reference Belai A, Boulos PB, Robson T, Burnstock G (1997) Neurochemical coding in the small intestine of patients with Crohn’s disease. Gut 40:767–774PubMedCrossRef Belai A, Boulos PB, Robson T, Burnstock G (1997) Neurochemical coding in the small intestine of patients with Crohn’s disease. Gut 40:767–774PubMedCrossRef
Metadata
Title
Infiltration of Mast Cells in Rat Colon Is a Consequence of Ischemia/Reperfusion
Authors
Elin Sand
Anna Themner-Persson
Eva Ekblad
Publication date
01-12-2008
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 12/2008
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-008-0279-x

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