Intracolonic infusion of fecal supernatants from ulcerative colitis patients triggers altered permeability and inflammation in mice: role of cathepsin G and protease-activated receptor-4

Inflamm Bowel Dis. 2011 Jun;17(6):1409-14. doi: 10.1002/ibd.21454. Epub 2010 Dec 22.

Abstract

Background: Cathepsin G (Cat-G) is a neutrophil serine-protease found in the colonic lumen of ulcerative colitis (UC) patients. Cat-G is able to activate protease-activated receptor-4 (PAR(4) ) located at the apical side of enterocytes, leading to epithelial barrier disruption. However, the mechanisms through which Cat-G triggers inflammation are not fully elucidated. The aims of our study were to evaluate in vivo the effects of UC fecal supernatants and Cat-G on epithelial barrier function and inflammation, and the connection between these two parameters.

Methods: Male balb/c mice were used in this study. We evaluated the effect of a 2-hour intracolonic infusion of 1) fecal supernatants from UC patients pretreated or not with specific Cat-G inhibitor (SCGI); 2) PAR(4) -activating peptide (PAR(4) -AP); and 3) Cat-G on colonic myeloperoxidase (MPO) activity and paracellular permeability (CPP). The involvement of PAR(4) was assessed by pretreating animals with pepducin P4pal-10, which blocks PAR(4) signaling. We investigated the role of myosin light chain (MLC) kinase by using its inhibitor, ML-7, and we determined phosphorylated MLC (pMLC) levels in mice colonic mucosa.

Results: UC fecal supernatants, Cat-G, and PAR(4) agonist increased both CPP and MPO activity in comparison with healthy subjects fecal supernatants. ML-7 inhibited the CPP increase triggered by Cat-G by 92.3%, and the enhanced MPO activity by 43.8%. Intracolonic infusion of UC fecal supernatant determined an increased phosphorylation level of MLC.

Conclusions: These observations support that luminal factors such as Cat-G play an important proinflammatory role in the pathogenesis of colitis, mainly depending on CPP increase by MLC phosphorylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Administration, Rectal
  • Adolescent
  • Adult
  • Aged
  • Animals
  • Blotting, Western
  • Cathepsin G / physiology*
  • Cell Membrane Permeability / physiology
  • Colitis / etiology*
  • Colitis / physiopathology
  • Colitis, Ulcerative / etiology*
  • Colitis, Ulcerative / physiopathology
  • Colon / physiopathology
  • Feces
  • Humans
  • Intestinal Mucosa / physiopathology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Middle Aged
  • Peroxidase / metabolism
  • Receptors, Thrombin / physiology*
  • Young Adult

Substances

  • Receptors, Thrombin
  • Peroxidase
  • Cathepsin G
  • protease-activated receptor 4