Acute infection of mice with Clostridium difficile leads to eIF2α phosphorylation and pro-survival signalling as part of the mucosal inflammatory response

Immunology. 2013 Sep;140(1):111-22. doi: 10.1111/imm.12122.

Abstract

The current study sought to delineate the gene expression profile of the host response in the caecum and colon during acute infection with Clostridium difficile in a mouse model of infection, and to investigate the nature of the unfolded protein response in this process. The infected mice displayed a significant up-regulation in the expression of chemokines (Cxcl1, Cxcl2 and Ccl2), numerous pro-inflammatory cytokines (Ifng, Il1b, Il6, and Il17f), as well as Il22 and a number of anti-microbial peptides (Defa1, Defa28, Defb1, Slpi and Reg3g) at the site(s) of infection. This was accompanied by a significant influx of neutrophils, dendritic cells, cells of the monocyte/macrophage lineage and all major subsets of lymphocytes to these site(s). However, CD4 T cells of the untreated and C. difficile-infected mice expressed similar levels of CD69 and CD25. Neither tissue had up-regulated levels of Tbx21, Gata3 or Rorc. The caeca and colons of the infected mice showed a significant increase in eukaryotic initiation factor 2α (eIF2α) phosphorylation, but neither the splicing of Xbp1 nor the up-regulation of endoplasmic reticulum chaperones, casting doubt on the full-fledged induction of the unfolded protein response by C. difficile. They also displayed significantly higher phosphorylation of AKT and signal transducer and activator of transcription 3 (STAT3), an indication of pro-survival signalling. These data underscore the local, innate, pro-inflammatory nature of the response to C. difficile and highlight eIF2α phosphorylation and the interleukin-22-pSTAT3-RegIIIγ axis as two of the pathways that could be used to contain and counteract the damage inflicted on the intestinal epithelium.

Keywords: Clostridium difficile; RegIIIγ; eIF2α; interleukin-22; pSTAT3.

Publication types

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

MeSH terms

  • Acute Disease
  • Animals
  • Antimicrobial Cationic Peptides / genetics
  • Chemokines / genetics
  • Clostridioides difficile / immunology
  • Clostridioides difficile / pathogenicity
  • Cytokines / genetics
  • Enterocolitis, Pseudomembranous / genetics
  • Enterocolitis, Pseudomembranous / immunology*
  • Enterocolitis, Pseudomembranous / metabolism*
  • Eukaryotic Initiation Factor-2 / metabolism*
  • Immunity, Innate
  • Immunity, Mucosal
  • Inflammation Mediators / metabolism
  • Interleukin-22
  • Interleukins / genetics
  • Intestinal Mucosa / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Phosphorylation
  • Signal Transduction
  • Transcriptome
  • Unfolded Protein Response

Substances

  • Antimicrobial Cationic Peptides
  • Chemokines
  • Cytokines
  • Eukaryotic Initiation Factor-2
  • Inflammation Mediators
  • Interleukins