Inhibitor of PI3Kγ ameliorates TNBS-induced colitis in mice by affecting the functional activity of CD4+CD25+FoxP3+ regulatory T cells

Br J Pharmacol. 2011 May;163(2):358-74. doi: 10.1111/j.1476-5381.2011.01226.x.

Abstract

Background and purpose: Phosphoinositide 3-kinase-γ (PI3Kγ) is implicated in many pathophysiological conditions, and recent evidence has suggested its involvement in colitis. In the present study, we investigated the effects of AS605240, a relatively selective PI3Kγ inhibitor, in experimental colitis and its underlying mechanisms.

Experimental approach: Acute colitis was induced in mice by treatment with trinitrobenzene sulphonic acid (TNBS), and the effect of AS605240 on colonic injury was assessed. Pro-inflammatory mediators and cytokines were measured by immunohistochemistry, elisa, real time-polymerase chain reaction and flow cytometry.

Key results: Oral administration of AS605240 significantly attenuated TNBS-induced acute colitis and diminished the expression of matrix metalloproteinase-9 and vascular endothelial growth factor. The colonic levels and expression of IL-1β, CXCL-1/KC, MIP-2 and TNF-α were also reduced following therapeutic treatment with AS605240. Moreover, AS605240 reduced MIP-2 levels in a culture of neutrophils stimulated with lipopolysaccharide. The mechanisms underlying these actions of AS605240 are related to nuclear factor-κ (NF-κB) inhibition. Importantly, the PI3Kγ inhibitor also up-regulated IL-10, CD25 and FoxP3 expression. In addition, a significant increase in CD25 and FoxP3 expression was found in isolated lamina propria CD4+ T cells of AS605240-treated mice. The effect of AS605240 on Treg induction was further confirmed by showing that concomitant in vivo blockade of IL-10R significantly attenuated its therapeutic activity.

Conclusions and implications: These results suggest that AS605240 protects mice against TNBS-induced colitis by inhibiting multiple inflammatory components through the NF-κB pathway while simultaneously inducing an increase in the functional activity of CD4+CD25+ Treg. Thus, AS605240 may offer a promising new therapeutic strategy for the treatment of inflammatory bowel diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • CD4 Antigens / metabolism*
  • Cells, Cultured
  • Colitis / chemically induced
  • Colitis / drug therapy*
  • Colitis / immunology
  • Colon / drug effects
  • Colon / immunology
  • Colon / pathology
  • Cytokines / metabolism
  • Forkhead Transcription Factors / metabolism*
  • Interleukin-2 Receptor alpha Subunit / metabolism*
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / pathology
  • Male
  • Matrix Metalloproteinase 9 / biosynthesis
  • Mice
  • NF-kappa B / metabolism
  • Neutrophil Infiltration
  • Neutrophils / drug effects
  • Neutrophils / metabolism
  • Phosphoinositide-3 Kinase Inhibitors*
  • Quinoxalines / pharmacology
  • Quinoxalines / therapeutic use*
  • T-Lymphocytes, Regulatory / metabolism*
  • Thiazolidinediones / pharmacology
  • Thiazolidinediones / therapeutic use*
  • Trinitrobenzenesulfonic Acid*
  • Vascular Endothelial Growth Factor A / biosynthesis

Substances

  • 5-quinoxalin-6-ylmethylenethiazolidine-2,4-dione
  • CD4 Antigens
  • Cytokines
  • Forkhead Transcription Factors
  • Foxp3 protein, rat
  • Interleukin-2 Receptor alpha Subunit
  • NF-kappa B
  • Phosphoinositide-3 Kinase Inhibitors
  • Quinoxalines
  • Thiazolidinediones
  • Vascular Endothelial Growth Factor A
  • Trinitrobenzenesulfonic Acid
  • Matrix Metalloproteinase 9