Proinflammatory progranulin antibodies in inflammatory bowel diseases

Dig Dis Sci. 2014 Aug;59(8):1733-42. doi: 10.1007/s10620-014-3089-3. Epub 2014 Mar 4.

Abstract

Background: Recently, we identified neutralizing autoantibodies against progranulin (PGRN) in a wide spectrum of rheumatic diseases including cases with enteropathic spondylarthritis. PGRN is a secreted protein with strong anti-inflammatory effects, believed to be mediated by the direct inhibition of TNF receptors 1&2. Given the central role of TNF-α as proinflammatory cytokine, a neutralizing antibody directed against its physiologic antagonist PGRN might entertain a proinflammatory environment.

Objective: The aim of the present study was to investigate a possible occurrence of PGRN-antibodies (PGRN-Abs) in inflammatory bowel disease (IBD), and to investigate a possible pathogenic effect.

Materials and methods: Sera samples of 141 patients with Crohn's disease (CD) and of 71 patients with ulcerative colitis (UC) were tested for PGRN-Abs by ELISA. PGRN plasma levels were detected by ELISA. Proinflammatory effects of progranulin-antibodies were analyzed by TNF-α-mediated cytotoxicity assays using HT29 cells and by examination of possible effects of PGRN and of PGRN-antibodies on TNF-α-induced downmodulation of FOXP3 expression in CD4(+)CD25(hi) Tregs.

Results: PGRN-Abs were found in sera of 23/141 (16.31%) patients with CD, and 15/71 (21.13%) patients with UC. PGRN-Abs were more frequent than anti-neutrophil cytoplasmic autoantibodies (ANCAs) in UC, but less frequent than anti-Saccharomyces cerevisiae antibodies (ASCAs) in CD. PGRN-Abs belonged mostly to IgG1 (71.1%) and IgA (26.3%). They occurred in relevant titres and had significant neutralizing effects on PGRN plasma levels. Cytotoxicity assays comparing PGRN-antibody-positive sera with negative sera from matched patients with IBD showed a proinflammatory effect of PGRN-Abs on HT29 cells. Moreover, PGRN-antibodies led to an increase of TNF-α-induced downmodulation of FOXP3 in CD4(+)CD25(hi) Tregs.

Conclusion: The results suggest that PGRN-Abs occur frequently in CD and UC, and have a proinflammatory effect.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Antibodies, Antineutrophil Cytoplasmic / biosynthesis
  • Antibodies, Antineutrophil Cytoplasmic / blood
  • Case-Control Studies
  • Colitis, Ulcerative / immunology*
  • Colitis, Ulcerative / pathology*
  • Crohn Disease / immunology*
  • Crohn Disease / pathology*
  • Cytotoxicity Tests, Immunologic
  • Female
  • HEK293 Cells
  • HT29 Cells
  • Humans
  • Intercellular Signaling Peptides and Proteins / immunology*
  • Male
  • Middle Aged
  • Progranulins
  • Saccharomyces cerevisiae / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • Tumor Necrosis Factor-alpha / metabolism
  • Young Adult

Substances

  • Antibodies, Antineutrophil Cytoplasmic
  • GRN protein, human
  • Intercellular Signaling Peptides and Proteins
  • Progranulins
  • Tumor Necrosis Factor-alpha