Oligosaccharides from agar inhibit murine intestinal inflammation through the induction of heme oxygenase-1 expression

J Gastroenterol. 2013 Aug;48(8):897-909. doi: 10.1007/s00535-012-0719-4. Epub 2012 Nov 28.

Abstract

Background: Agarose is hydrolyzed easily to yield oligosaccharides, designated as agaro-oligosaccharides (AGOs). Recently, it has been demonstrated that AGOs induce heme oxygenase-1 (HO-1) expression in macrophages and that they might lead to anti-inflammatory property. Nevertheless, the molecular mechanism of AGO-mediated HO-1 induction remains unknown, as does AGOs' ability to elicit anti-inflammatory activity in vivo. This study was undertaken to uncover the mechanism of AGO-mediated HO-1 induction and to investigate the therapeutic effect of AGOs on intestinal inflammation.

Methods: Mice were treated with 2,4,6-trinitrobenzene sulfonic acid (TNBS) to induce colitis. The respective degrees of mucosal injury of mice that had received AGO and control mice were compared. We investigated HO-1 expression using Western blotting, quantitative real-time PCR (qRT-PCR), and immunohistochemistry. The expression of tumor necrosis factor-α (TNF-α) was measured using qRT-PCR and enzyme-linked immunosorbent assay.

Results: AGO administration induced HO-1 expression in colonic mucosa. The induction was observed mainly in F4/80 positive macrophages. Increased colonic damage and myeloperoxidase activity after TNBS treatment were inhibited by AGO administration. TNBS treatment induced TNF-α expression, and AGO administration suppressed induction. However, HO inhibitor canceled AGO-mediated amelioration of colitis. In RAW264 cells, AGOs enhanced HO-1 expression time-dependently and concentration-dependently and suppressed lipopolysaccharide-induced TNF-α expression. Furthermore, agarotetraose-mediated HO-1 induction required NF-E2-related factor 2 function and phosphorylation of c-jun N-terminal kinase.

Conclusions: We infer that AGO administration inhibits TNBS-induced colitis in mice through HO-1 induction in macrophages. Consequently, oral administration of AGOs might be an important therapeutic strategy for inflammatory bowel disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / administration & dosage
  • Anti-Inflammatory Agents / chemistry
  • Anti-Inflammatory Agents / pharmacology
  • Blotting, Western
  • Cell Line
  • Colitis / physiopathology
  • Colitis / prevention & control*
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Enzyme-Linked Immunosorbent Assay
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism*
  • Inflammation / physiopathology
  • Inflammation / prevention & control*
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Oligosaccharides / administration & dosage
  • Oligosaccharides / chemistry
  • Oligosaccharides / pharmacology*
  • Real-Time Polymerase Chain Reaction
  • Sepharose / metabolism
  • Time Factors
  • Trinitrobenzenesulfonic Acid / toxicity

Substances

  • Anti-Inflammatory Agents
  • Oligosaccharides
  • Trinitrobenzenesulfonic Acid
  • Sepharose
  • Heme Oxygenase-1