Mast cells trigger epithelial barrier dysfunction, bacterial translocation and postoperative ileus in a mouse model

Neurogastroenterology and Motility

Volumn 24, Issue 2, 2012, Pages

  Snoek, S A ^a   Dhawan, S ^a   van Bree, S H ^a   Cailotto, C ^a   van Diest, S A ^a   Duarte, J M ^a   Stanisor, O I ^a   Hilbers, F W ^a   Nijhuis, L ^a   Koeman, A ^a   van den Wijngaard, R M ^a   Zuurbier, C J ^a   Boeckxstaens, G E ^a,b   de Jonge, W J ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Barrier function; C Kit; Macrophages; Mast cells; Postoperative ileus

Indexed keywords

CHEMOKINE; NEOMYCIN; POLYMYXIN B;

ABDOMINAL SURGERY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; BIOMANIPULATION; C57BL 6 MOUSE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIGESTIVE SYSTEM FUNCTION DISORDER; EPITHELIUM; EXTRAVASATION; FEMALE; GASTRITIS; ILEUS; INFLAMMATORY INFILTRATE; LAPAROTOMY; MAST CELL; MEAN ARTERIAL PRESSURE; MESENTERIC VEIN; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PERFUSION; PERMEABILITY BARRIER; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SMALL INTESTINE;

ANIMALS; BACTERIAL TRANSLOCATION; DISEASE MODELS, ANIMAL; FEMALE; GASTROINTESTINAL MOTILITY; ILEUS; INFLAMMATION; INTESTINAL MUCOSA; INTESTINE, SMALL; LAPAROTOMY; MAST CELLS; MICE; MICE, INBRED C57BL; PERMEABILITY; STEM CELLS;

EID: 84855913474     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2011.01820.x     Document Type: Article

References (49)

1. Boeckxstaens GE, de Jonge WJ. Neuroimmune mechanisms in postoperative ileus. Gut 2009; 58: 1300-11.
2. Kehlet H. Postoperative ileus - an update on preventive techniques. Nat Clin Pract Gastroenterol Hepatol 2008; 5: 552-8.
3. Kalff JC, Carlos TM, Schraut WH, Billiar TR, Simmons RL, Bauer AJ. Surgically induced leukocytic infiltrates within the rat intestinal muscularis mediate postoperative ileus. Gastroenterology 1999; 117: 378-87.
4. The FO, Bennink RJ, Ankum WM et al. Intestinal handling-induced mast cell activation and inflammation in human postoperative ileus. Gut 2008; 57: 33-40.
5. Bauer AJ, Schwarz NT, Moore BA, Turler A, Kalff JC. Ileus in critical illness: mechanisms and management. Curr Opin Crit Care 2002; 8: 152-7.
6. Kreiss C, Toegel S, Bauer AJ. Alpha2-adrenergic regulation of NO production alters postoperative intestinal smooth muscle dysfunction in rodents. Am J Physiol Gastrointest Liver Physiol 2004; 287: G658-66.
7. Turler A, Kalff JC, Moore BA et al. Leukocyte-derived inducible nitric oxide synthase mediates murine postoperative ileus. Ann Surg 2006; 244: 220-9.
8. de Jonge WJ, van den Wijngaard RM, The FO et al. Postoperative ileus is maintained by intestinal immune infiltrates that activate inhibitory neural pathways in mice. Gastroenterology 2003; 125: 1137-47.
9. The FO, de Jonge WJ, Bennink RJ, van den Wijngaard RM, Boeckxstaens GE. The ICAM-1 antisense oligonucleotide ISIS-3082 prevents the development of postoperative ileus in mice. Br J Pharmacol 2005; 146: 252-8.
10. Cicalese L, Aitouche A, Ploskina TM, Ford HR, Rao AS. The role of laparotomy, gut manipulation and immunosuppression on bacterial translocation from the intestinal tract. Transplant Proc 1999; 31: 1922-3.
11. Wehner S, Buchholz BM, Schuchtrup S et al. Mechanical strain and TLR4 synergistically induce cell-specific inflammatory gene expression in intestinal smooth muscle cells and peritoneal macrophages. Am J Physiol Gastrointest Liver Physiol 2010; 299: G1187-97.
12. Turler A, Schnurr C, Nakao A et al. Endogenous endotoxin participates in causing a panenteric inflammatory ileus after colonic surgery. Ann Surg 2007; 245: 734-44.
13. de Jonge WJ, The FO, van der CD et al. Mast cell degranulation during abdominal surgery initiates postoperative ileus in mice. Gastroenterology 2004; 127: 535-45.
14. The FO, Buist MR, Lei A et al. The role of mast cell stabilization in treatment of postoperative ileus: a pilot study. Am J Gastroenterol 2009; 104: 2257-66.
15. Santos J, Perdue MH. Stress and neuroimmune regulation of gut mucosal function. Gut 2000; 47(Suppl 4): iv49-51.
16. Soderholm JD, Yang PC, Ceponis P et al. Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine. Gastroenterology 2002; 123: 1099-108.
17. Yang PC, Berin MC, Yu L, Perdue MH. Mucosal pathophysiology and inflammatory changes in the late phase of the intestinal allergic reaction in the rat. Am J Pathol 2001; 158: 681-90.
18. McDermott JR, Bartram RE, Knight PA, Miller HR, Garrod DR, Grencis RK. Mast cells disrupt epithelial barrier function during enteric nematode infection. Proc Natl Acad Sci USA 2003; 100: 7761-6.
19. Moriez R, Leveque M, Salvador-Cartier C et al. Mucosal mast cell proteases are involved in colonic permeability alterations and subsequent bacterial translocation in endotoxemic rats. Shock 2007; 28: 118-24.
20. Zuurbier CJ, Emons VM, Ince C. Hemodynamics of anesthetized ventilated mouse models: aspects of anesthetics, fluid support, and strain. Am J Physiol Heart Circ Physiol 2002; 282: H2099-105.
21. The FO, Boeckxstaens GE, Snoek SA et al. Activation of the cholinergic anti-inflammatory pathway ameliorates postoperative ileus in mice. Gastroenterology 2007; 133: 1219-28.
22. Mikkelsen HB. Macrophages in the external muscle layers of mammalian intestines. Histol Histopathol 1995; 10: 719-36.
23. Wehner S, Schwarz NT, Hundsdoerfer R et al. Induction of IL-6 within the rodent intestinal muscularis after intestinal surgical stress. Surgery 2005; 137: 436-46.
24. De Backer O, Elinck E, Blanckaert B, Leybaert L, Motterlini R, Lefebvre RA. Water-soluble CO-releasing molecules reduce the development of postoperative ileus via modulation of MAPK/HO-1 signalling and reduction of oxidative stress. Gut 2009; 58: 347-56.
25. Engel DR, Koscielny A, Wehner S et al. T helper type 1 memory cells disseminate postoperative ileus over the entire intestinal tract. Nat Med 2010; 16: 1407-13.
26. Tono T, Tsujimura T, Koshimizu U et al. c-kit Gene was not transcribed in cultured mast cells of mast cell-deficient Wsh/Wsh mice that have a normal number of erythrocytes and a normal c-kit coding region. Blood 1992; 80: 1448-53.
27. Galli SJ, Tsai M, Gordon JR, Geissler EN, Wershil BK. Analyzing mast cell development and function using mice carrying mutations at W/c-kit or Sl/MGF (SCF) loci. Ann N Y Acad Sci 1992; 664: 69-88.
28. Balzan S, de Almeida QC, de CR, Zilberstein B, Cecconello I. Bacterial translocation: overview of mechanisms and clinical impact. J Gastroenterol Hepatol 2007; 22: 464-71.
29. Derikx JP, van Waardenburg DA, Thuijls G et al. New insight in loss of gut barrier during major non-abdominal surgery. PLoS ONE 2008; 3: e3954.
30. de Haan JJ, Lubbers T, Derikx JP et al. Rapid development of intestinal cell damage following severe trauma: a prospective observational cohort study. Crit Care 2009; 13: R86.
31. MacFie J, Reddy BS, Gatt M, Jain PK, Sowdi R, Mitchell CJ. Bacterial translocation studied in 927 patients over 13years. Br J Surg 2006; 93: 87-93.
32. O'Boyle CJ, MacFie J, Mitchell CJ, Johnstone D, Sagar PM, Sedman PC. Microbiology of bacterial translocation in humans. Gut 1998; 42: 29-35.
33. Reddy BS, Gatt M, Sowdi R, MacFie J. Surgical manipulation of the large intestine increases bacterial translocation in patients undergoing elective colorectal surgery. Colorectal Dis 2006; 8: 596-600.
34. Wallon C, Persborn M, Jonsson M et al. Eosinophils express muscarinic receptors and corticotropin-releasing factor to disrupt the mucosal barrier in ulcerative colitis. Gastroenterology 2011; 140: 1597-607.
35. Wallon C, Yang PC, Keita AV et al. Corticotropin-releasing hormone (CRH) regulates macromolecular permeability via mast cells in normal human colonic biopsies in vitro. Gut 2008; 57: 50-8.
36. Jacob C, Yang PC, Darmoul D et al. Mast cell tryptase controls paracellular permeability of the intestine. Role of protease-activated receptor 2 and beta-arrestins. J Biol Chem 2005; 280: 31936-48.
37. O'Boyle CJ, MacFie J, Dave K, Sagar PS, Poon P, Mitchell CJ. Alterations in intestinal barrier function do not predispose to translocation of enteric bacteria in gastroenterologic patients. Nutrition 1998; 14: 358-62.
38. Schwarz NT, Beer-Stolz D, Simmons RL, Bauer AJ. Pathogenesis of paralytic ileus: intestinal manipulation opens a transient pathway between the intestinal lumen and the leukocytic infiltrate of the jejunal muscularis. Ann Surg 2002; 235: 31-40.
39. Niess JH, Brand S, Gu X et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005; 307: 254-8.
40. Pabst O, Bernhardt G. The puzzle of intestinal lamina propria dendritic cells and macrophages. Eur J Immunol 2010; 40: 2107-11.
41. Zhou JS, Xing W, Friend DS, Austen KF, Katz HR. Mast cell deficiency in Kit(W-sh) mice does not impair antibody-mediated arthritis. J Exp Med 2007; 204: 2797-802.
42. Berrozpe G, Timokhina I, Yukl S et al. The W(sh), W(57), and Ph Kit expression mutations define tissue-specific control elements located between -23 and -154kb upstream of Kit. Blood 1999; 94: 2658-66.
43. Iino S, Horiguchi K, Nojyo Y. W(sh)/W(sh) c-Kit mutant mice possess interstitial cells of Cajal in the deep muscular plexus layer of the small intestine. Neurosci Lett 2009; 459: 123-6.
44. Grimbaldeston MA, Chen CC, Piliponsky AM, Tsai M, Tam SY, Galli SJ. Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am J Pathol 2005; 167: 835-48.
45. Watanabe H, Numata K, Ito T, Takagi K, Matsukawa A. Innate immune response in Th1- and Th2-dominant mouse strains. Shock 2004; 22: 460-6.
46. Anup R, Susama P, Balasubramanian KA. Role of xanthine oxidase in small bowel mucosal dysfunction after surgical stress. Br J Surg 2000; 87: 1094-101.
47. Simmy T, Anup R, Prabhu R, Balasubramanian KA. Effect of surgical manipulation of the rat intestine on enterocyte populations. Surgery 2001; 130: 479-88.
48. Dickinson E, Tuncer R, Nadler E et al. NOX, a novel nitric oxide scavenger, reduces bacterial translocation in rats after endotoxin challenge. Am J Physiol 1999; 277: G1281-7.
49. Nadler EP, Ford HR. Regulation of bacterial translocation by nitric oxide. Pediatr Surg Int 2000; 16: 165-8.