A new model of chronic colitis in SCID mice induced by adoptive transfer of CD62L+ CD4+ T cells: insights into the regulatory role of interleukin-6 on apoptosis

Pathobiology. 2002;70(3):170-6. doi: 10.1159/000068150.

Abstract

Objective: The proinflammatory cytokine interleukin (IL)-6 is involved in various chronic inflammatory processes. IL-6 is a predominant cytokine produced by lamina propria T cells in Crohn's disease and experimental colitis. This study was designed to examine the effect of a neutralizing IL-6-receptor (IL-6R) antibody on the programmed cell death of mucosal T cells in the CD62L+ CD4+ SCID transfer model of chronic experimental colitis in mice and to gain more insight into the pathogenesis of this transfer colitis model.

Methods: For adoptive transfer, we isolated CD62L+ CD4+ double-positive T cells from wild-type BALB/c mice followed by intraperitoneal application of 1 million cells in CB17 SCID mice. The purity of the transferred T-cell population was tested by FACS analysis. Cytokine secretion was measured by ELISA. Western blot analysis was performed to detect phospho-STAT-3 in protein extracts of splenic cells. Cryo- and paraffin colon cross-sections were used to perform immunochemical or fluorescence TUNEL stainings.

Results: We isolated CD62L+ CD4+ and CD62L- CD4+ T cells. In vitro studies showed an increased production of IL-4 by CD62L- CD4+ T cells compared to CD62L+ T cells. 8-10 weeks after transfer of CD62L+ CD4+ T cells in SCID mice, reconstituted mice developed wasting disease, anal prolapse and diarrhea, whereas mice reconstituted with CD62L- CD4+ did not, similar to anti-IL-6R-treated CD62L+ CD4+-reconstituted SCID mice. Anti-IL-6R-treated reconstituted SCID mice showed decreased levels of activated STAT-3. The previously described efficacy of anti-IL-6R antibody treatment on colitis activity appeared to be due to the induction of apoptosis, as many TUNEL-positive cells were detected in the lamina propria.

Conclusions: These results suggest that the activation of the IL-6/STAT-3-signaling pathway plays a pivotal role in the pathogenesis of CD62L+ CD4+ transfer colitis. Moreover, the application of a neutralizing antibody to IL-6R induces apoptosis in transferred T cells. These data implicate the importance of anti-apoptotic pathways in chronic disease and might contribute to future therapies.

MeSH terms

  • Adoptive Transfer*
  • Animals
  • Antibodies, Blocking / pharmacology
  • Antibodies, Blocking / therapeutic use
  • Apoptosis / drug effects
  • Apoptosis / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / pathology
  • CD4-Positive T-Lymphocytes / transplantation*
  • Cell Transplantation
  • Colitis, Ulcerative / drug therapy
  • Colitis, Ulcerative / immunology*
  • Colitis, Ulcerative / pathology
  • Colon / drug effects
  • Colon / metabolism
  • Colon / pathology
  • DNA-Binding Proteins / biosynthesis
  • Disease Models, Animal*
  • Flow Cytometry
  • In Situ Nick-End Labeling
  • Interleukin-6 / immunology*
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / pathology
  • L-Selectin / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, SCID*
  • Receptors, Interleukin-6 / immunology
  • STAT3 Transcription Factor
  • Severe Combined Immunodeficiency / genetics
  • Severe Combined Immunodeficiency / immunology
  • Spleen / metabolism
  • Spleen / pathology
  • Trans-Activators / biosynthesis

Substances

  • Antibodies, Blocking
  • DNA-Binding Proteins
  • Interleukin-6
  • Receptors, Interleukin-6
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • Trans-Activators
  • L-Selectin