Differential molecular and cellular immune mechanisms of postoperative and LPS-induced ileus in mice and rats

Cytokine. 2012 Jul;59(1):49-58. doi: 10.1016/j.cyto.2012.03.012. Epub 2012 Apr 12.

Abstract

Ileus is caused by the initiation of a complex cascade of molecular and cellular inflammatory responses within the intestinal muscularis, which might be species specific. Our objective was to investigate a possible immunological divergence in the mechanisms of postoperative- and endotoxin-induced ileus in C57BL/6 mice and Sprague-Dawley rats. Gastrointestinal transit (GIT) was measured at 24 h after the injurious stimulus. MPO-staining and F4/80 immunohistochemistry were used to quantify polymorphonuclear and monocyte infiltration of jejunal muscularis whole-mounts, and intestinal muscularis MCP-1, ICAM-1 and iNOS gene expression was assessed by RT-PCR. Intestinal muscularis subjected to in vivo surgical manipulation (SM) or LPS treatment was cultured for 24 h, and the liberation of nitric oxide and chemokines/cytokines into the culture medium was analyzed by Griess reaction and Luminex multiplex assay. Intestinal SM and lipopolysaccharide (LPS) (15 mg/kg) caused a significant delay in gastrointestinal transit, which was more severe in mice compared to rats in both injury models. Both SM- and LPS-triggered neutrophil and monocytic extravasation into the rat jejunal muscularis exceeded the cellular infiltration seen in mice. These results correlated with significantly greater increases in rat muscularis MCP-1 (syn. CCL2), ICAM-1 and iNOS message with more subsequent NO production after SM or LPS compared to mouse. The cultured muscularis obtained from SM mice released significantly more inflammatory proteins such as TNF-α, IL-1-α, IL-4 and GM-CSF compared to the manipulated rat muscularis. In contrast, LPS initiated the secretion of significantly more IL-1β by the inflamed rat muscularis compared to the mouse, but GM-CSF (syn. CSF2) liberation from mouse muscularis was markedly higher compared to LPS-treated rat muscularis. The data indicate that mechanistically the development of ileus in rat is mediated predominately through a leukocytic pathway consisting of chemotaxis, cellular extravasation and NO liberation. Whereas, the more intense mouse ileus evolves via a potent but injury-specific local cytokine response.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism
  • Gene Expression Regulation
  • Ileus / chemically induced
  • Ileus / genetics*
  • Ileus / immunology*
  • Ileus / physiopathology
  • Inflammation Mediators / metabolism
  • Intercellular Adhesion Molecule-1 / metabolism
  • Lipopolysaccharides
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Monocytes / immunology
  • Muscles / enzymology
  • Muscles / physiopathology
  • Neutrophil Infiltration / immunology
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / metabolism
  • Postoperative Complications / genetics*
  • Postoperative Complications / immunology*
  • Postoperative Complications / physiopathology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Sepsis / complications
  • Sepsis / genetics
  • Sepsis / pathology
  • Sepsis / physiopathology
  • Time Factors

Substances

  • Chemokine CCL2
  • Inflammation Mediators
  • Lipopolysaccharides
  • RNA, Messenger
  • Intercellular Adhesion Molecule-1
  • Nitric Oxide
  • Nitric Oxide Synthase Type II