Alteration of cholinergic and peptidergic neurotransmitters in rat ileum induced by acute stress following transient intestinal infection is mast cell dependent

Background Mast cells are implicated in the development of irritable bowel syndrome (IBS), which is associated with the activation of the "neural-immune" system. The aim of this study was to investigate the role of mast cells in the remodeling of cholinergic and peptidergic neurotransmitters induced by acute cold restriction stress (ACRS) post infection (PI) using mast cell deficient rats (Ws/Ws) and their wild-type controls (+/+). Methods Transient intestinal infection was initiated by giving 1500 Trichinella spiralis (TS.) larvae by gavage. ACRS was induced for 2 hours at day 100 PI. Samples of terminal ilea were prepared for H&E staining, mast cell counting and activation and assessment of IL-1 beta and IL-10. Results When infected, both strains of rats experienced an acute infectious stage followed by a recovery. Histological scores were significantly higher in infected rats compared with those of the non-infected controls at day 10 PI (10 day-PI vs. control: +/+: 2.75 +/- 0.17 vs. 0.42 +/- 0.09; Ws/Ws: 2.67 +/- 0.67 vs. 0.50 +/- 0.34; P <0.01). In +/+ rats, post-infection ACRS induced the formation of low-grade inflammation, represented by the imbalance of IL-1 beta and IL-10 (IL-1 beta: PI+ACRS vs. control: (1812.24 +/- 561.61) vs. (1275.97 +/- 410.21) pg/g, P <0.05; IL-10: PI+ACRS vs. control: (251.9 +/- 39.8) vs. (255.3 +/- 24.7) pg/g, P >0.05), accompanied by hyperplasia and activation of mast cells (PI+ACRS vs. control: 58.8 +/- 19.2 vs. 28.0 +/- 7.6; P <0.01). The balance between acetylcholine (ACh) and substance P (SP) was also disturbed (ACh: PI+ACRS vs. control: (743.94 +/- 238.72) vs. (1065.68 +/- 256.46) pg/g, P <0.05; SP: PI+ACRS vs. control: (892.60 +/- 231.12) vs. (696.61 +/- 148.61) pg/g, P <0.05). Nevertheless, similar changes of IL-1 beta/IL-10 and ACh/SP were not detected in Ws/Ws rats. Conclusion The imbalance of ACh/SP, together with the activation of mucosal immunity induced by post-infection ACRS were lacking in mast cell deficient rats, which supports the premise that mast cells play an important role in cholinergic and peptidergic remodeling in the ileum of rats. Chin Med J 2010;123(2):227-233