Time-course analysis of counts and degranulation of mast cells during early intestinal ischemia-reperfusion injury in mice

Ge,Mian; Gan,Xiaoliang; Liu,Dezhao; Zhang,Wenhua; Gao,Wanling; Huang,Pinjie; Hei,Ziqing

doi:10.3892/mmr.2013.1530

Time-course analysis of counts and degranulation of mast cells during early intestinal ischemia-reperfusion injury in mice

Authors:
- Mian Ge
- Xiaoliang Gan
- Dezhao Liu
- Wenhua Zhang
- Wanling Gao
- Pinjie Huang
- Ziqing Hei
View Affiliations

Affiliations: Department of Anesthesiology, The Third Affiliated Hospital of Sun Yat-sen University, Guangzhou 510630, P.R. China
Published online on: June 18, 2013 https://doi.org/10.3892/mmr.2013.1530
Pages: 401-406

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Findings of previous studies have revealed that intestinal mucosal mast cells (IMMCs) are involved in small intestinal ischemia‑reperfusion injury (IIRI). However, time-course changes of mast cell counts and mast cell function in this process remain unclear. The present study aimed to observe the number of IMMCs and to investigate the correlation between their activation and small intestine injury at various time points during the period of small intestinal ischemia reperfusion (IIR). Healthy male Kunming mice were randomly divided into five groups, and were subjected to occlusion of the superior mesenteric artery (SMA) for 30 min and followed by reperfusion for 1, 3, 6 and 12 h. By contrast, the SMA was isolated but not clamped in the baseline group. Chiu's scores were assessed by light microscopy, tryptase protein and MCP7 protein expression in the intestine were quantified, and mast cell counts and levels of histamine and TNF-α in the intestine were measured. The results showed that IIR induced severe intestine injury within 12 h as demonstrated by Chiu's scores that was greatly increased as compared to the baseline group, accompanied by increased mast cell counts, histamine and TNF-α levels. However, the Chiu's scores were reduced in the IIR 12 h group compared with the IIR 1 h, IIR 3 h and IIR 6 h groups, with concomitant decreased mast cell counts, histamine and TNF-α levels. The tryptase and MCP7 protein expression was markedly increased in the IIR 1 h and IIR 3 h groups as compared with the baseline group, whereas this expression was gradually decreased at 6 and 12 h after reperfusion. The results of the present study suggest that IIR results in severe mucosal destruction within 6 h after reperfusion, associated with mast cell activation and substantial increases in the mast cell counts.

View Figures

View References

1	Schoots IG, Koffeman GI, Legemate DA, Levi M and van Gulik TM: Systematic review of survival after acute mesenteric ischaemia according to disease aetiology. Br J Surg. 91:17–27. 2004. View Article : Google Scholar : PubMed/NCBI
2	Acosta-Merida MA, Marchena-Gomez J, Hemmersbach-Miller M, Roque-Castellano C and Hernandez-Romero JM: Identification of risk factors for perioperative mortality in acute mesenteric ischemia. World J Surg. 30:1579–1585. 2006. View Article : Google Scholar : PubMed/NCBI
3	Pierro A and Eaton S: Intestinal ischemia reperfusion injury and multisystem organ failure. Semin Pediatr Surg. 13:11–17. 2004. View Article : Google Scholar : PubMed/NCBI
4	Kassahun WT, Schulz T, Richter O and Hauss J: Unchanged high mortality rates from acute occlusive intestinal ischemia: six year review. Langenbecks Arch Surg. 393:163–171. 2008.PubMed/NCBI
5	Cerqueira NF, Hussni CA and Yoshida WB: Pathophysiology of mesenteric ischemia/reperfusion: a review. Acta Cir Bras. 20:336–343. 2005. View Article : Google Scholar : PubMed/NCBI
6	Haddad JJ: Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors. Cell Signal. 14:879–897. 2002. View Article : Google Scholar : PubMed/NCBI
7	Vollmar B and Menger MD: Intestinal ischemia/reperfusion: microcirculatory pathology and functional consequences. Langenbecks Arch Surg. 396:13–29. 2011. View Article : Google Scholar : PubMed/NCBI
8	Andoh A, Kimura T, Fukuda M, Araki Y, Fujiyama Y and Bamba T: Rapid intestinal ischaemia-reperfusion injury is suppressed in genetically mast cell-deficient Ws/Ws rats. Clin Exp Immunol. 116:90–93. 1999. View Article : Google Scholar : PubMed/NCBI
9	Kalia N, Brown NJ, Wood RF and Pockley AG: Ketotifen abrogates local and systemic consequences of rat intestinal ischemia-reperfusion injury. J Gastroenterol Hepatol. 20:1032–1038. 2005. View Article : Google Scholar : PubMed/NCBI
10	Hei ZQ, Gan XL, Huang PJ, Wei J, Shen N and Gao WL: Influence of ketotifen, cromolyn sodium, and compound 48/80 on the survival rates after intestinal ischemia reperfusion injury in rats. BMC Gastroenterol. 8:422008. View Article : Google Scholar
11	Boros M, Takaichi S, Masuda J, Newlands GF and Hatanaka K: Response of mucosal mast cells to intestinal ischemia-reperfusion injury in the rat. Shock. 3:125–131. 1995. View Article : Google Scholar : PubMed/NCBI
12	Chang JX, Chen S, Ma LP, et al: Functional and morphological changes of the gut barrier during the restitution process after hemorrhagic shock. World J Gastroenterol. 11:5485–5491. 2005.
13	Noda T, Iwakiri R, Fujimoto K, Matsuo S and Aw TY: Programmed cell death induced by Ischemia-reperfusion in rat intestinal mucosa. Am J Physiol. 274(2 Pt 1): G270–G276. 1998.PubMed/NCBI
14	Chiu CJ, Mcardle AH, Brown R, Scott HJ and Gurd FN: Intestinal mucosal lesion in low flow states. Arch Surg. 101:478–483. 1970. View Article : Google Scholar : PubMed/NCBI
15	Thakurdas SM, Melicoff E, Sanscores-Garcia L, Moreira DC, Petrova Y, Stevens RL and Adachi R: The mast cell-restricted tryptase mMCP-6 has a critical immunoprotective role in bacterial infections. J Biol Chem. 282:20809–20815. 2007. View Article : Google Scholar : PubMed/NCBI
16	Kemna E, Pickkers P, Nemeth E, van der Hoeven H and Swinkels D: Time-course analysis of hepcidin, serum iron, and plasma cytokine levels in humans injected with LPS. Blood. 106:1864–1866. 2005. View Article : Google Scholar : PubMed/NCBI
17	Bischoff SC: Physiological and pathophysiological functions of intestinal mast cells. Semin Immunopathol. 31:185–205. 2009. View Article : Google Scholar : PubMed/NCBI
18	Wierzbicki M and Brzezińska-Błaszczyk E: The role of mast cells in the development of inflammatory bowel diseases. Postepy Hig Med Dosw (Online). 62:642–650. 2008.PubMed/NCBI
19	Bischoff SC and Kramer S: Human mast cells, bacteria, and intestinal immunity. Immunol Rev. 217:329–337. 2007. View Article : Google Scholar : PubMed/NCBI
20	Hei ZQ, Gan XL, Luo GJ, Li SR and Cai J: Pretreatment of cromolyn sodium prior to reperfusion attenuates early reperfusion injury after the small intestine ischemia in rats. World J Gastroenterol. 13:5139–5146. 2007.PubMed/NCBI
21	Lindsberg PJ, Strbian D and Karjalainen-Lindsberg ML: Mast cells as early responders in the regulation of acute blood-brain barrier changes after cerebral ischemia and hemorrhage. J Cereb Blood Flow Metab. 30:689–702. 2010. View Article : Google Scholar : PubMed/NCBI
22	Morii E: Development of mast cells: analysis with mutant mice. Int J Hematol. 86:22–26. 2007. View Article : Google Scholar
23	Okayama Y and Kawakami T: Development, migration, and survival of mast cells. Immunol Res. 34:97–115. 2006. View Article : Google Scholar : PubMed/NCBI
24	McNeil HP, Reynolds DS, Schiller V, et al: Isolation, characterization, and transcription of the gene encoding mouse mast cell protease 7. Proc Natl Acad Sci USA. 89:11174–11178. 1992. View Article : Google Scholar : PubMed/NCBI
25	Funaba M, Ikeda T, Murakami M, et al: Transcriptional activation of mouse mast cell protease-7 by activin and transforming growth factor-beta is inhibited by microphthalmia-associated transcription factor. J Biol Chem. 278:52032–52041. 2003. View Article : Google Scholar
26	Caughey GH: Mast cell tryptases and chymases in inflammation and host defense. Immunol Rev. 217:141–154. 2007. View Article : Google Scholar : PubMed/NCBI
27	He S, Gaca MD and Walls AF: A role for tryptase in the activation of human mast cells: modulation of histamine release by tryptase and inhibitors of tryptase. J Pharmacol Exp Ther. 286:289–297. 1998.PubMed/NCBI
28	Gan XL, Hei ZQ, Huang HQ, Chen LX, Li SR and Cai J: Effect of Astragalus membranaceus injection on the activity of the intestinal muscosal mast cells after hemorrhagic shock-reperfusion in rats. Chin Med J. 119:1892–1898. 2006.PubMed/NCBI
29	Pascher A and Klupp J: Biologics in the treatment of transplant rejection and ischemia/reperfusion injury: new applications for TNFalpha inhibitors? BioDrugs. 19:211–231. 2005. View Article : Google Scholar : PubMed/NCBI
30	Bischoff SC, Lorentz A, Schwengberg S, Weier G, Raab R and Manns MP: Mast cells are an important cellular source of tumour necrosis factor alpha in human intestinal tissue. Gut. 44:643–652. 1999.PubMed/NCBI