Extraintestinal Helminth Infection Limits Pathology and Proinflammatory Cytokine Expression during DSS-Induced Ulcerative Colitis: A Role for Alternatively Activated Macrophages and Prostaglandins

Biomed Res Int. 2015:2015:563425. doi: 10.1155/2015/563425. Epub 2015 May 18.

Abstract

Chronic inflammation of the intestinal mucosa is characteristic of inflammatory bowel diseases such as ulcerative colitis and Crohn's disease. Helminth parasites have developed immunomodulatory strategies that may impact the outcome of several inflammatory diseases. Therefore, we investigated whether Taenia crassiceps infection is able to decrease the inflammatory effects of dextran sulfate sodium- (DSS-) induced ulcerative colitis in BALB/c and C57BL/6 mice. Preinfection significantly reduced the manifestations of DSS-induced colitis, as weight loss and shortened colon length, and decreased the disease activity index independently of the genetic background of the mice. Taenia infection decreased systemic levels of proinflammatory cytokines while increasing levels of IL-4 and IL-10, and the inflammatory infiltrate into the colon was also markedly reduced. RT-PCR assays from colon showed that T. crassiceps-infected mice displayed increased expression of Arginase-1 but decreased expression of iNOS compared to DSS-treated uninfected mice. The percentages of T regulatory cells were not increased. The adoptive transfer of alternatively activated macrophages (AAMФs) from infected mice into mice with DSS-induced colitis reduced the severity of colon inflammation. Administration of indomethacin abrogated the anticolitic effect of Taenia. Thus, T. crassiceps infection limits the pathology of ulcerative colitis by suppressing inflammatory responses mechanistically associated with AAMФs and prostaglandins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase
  • Colitis, Ulcerative / chemically induced
  • Colitis, Ulcerative / genetics
  • Colitis, Ulcerative / parasitology*
  • Crohn Disease / chemically induced
  • Crohn Disease / genetics
  • Crohn Disease / parasitology*
  • Dextran Sulfate / toxicity
  • Disease Models, Animal
  • Female
  • Humans
  • Inflammation / chemically induced
  • Inflammation / genetics
  • Inflammation / parasitology*
  • Interleukin-10 / biosynthesis
  • Interleukin-4 / biosynthesis
  • Intestinal Mucosa / parasitology
  • Intestinal Mucosa / pathology
  • Macrophages / metabolism
  • Macrophages / pathology
  • Mice
  • Nitric Oxide Synthase Type II / biosynthesis
  • Prostaglandins / biosynthesis*
  • Prostaglandins / metabolism
  • Taenia / pathogenicity
  • Taeniasis / complications
  • Taeniasis / parasitology

Substances

  • IL10 protein, human
  • Prostaglandins
  • Interleukin-10
  • Interleukin-4
  • Dextran Sulfate
  • NOS2 protein, human
  • Nitric Oxide Synthase Type II
  • ARG1 protein, human
  • Arginase