Limited CD4 T-cell diversity associated with colitis in T-cell receptor alpha mutant mice requires a T helper 2 environment

Gastroenterology. 2000 Oct;119(4):983-95. doi: 10.1053/gast.2000.18153.

Abstract

Background & aims: T-cell receptor alpha mutant (TCRalpha(-/-)) mice spontaneously develop chronic colitis mediated by CD4(+) TCRalpha(-)beta(+) T cells. The aim of this study was to analyze the mechanisms of expansion of these cells by characterization of the TCRbeta repertoire.

Methods: TCRbeta repertoire was analyzed by reverse-transcription polymerase chain reaction/Southern blot and DNA sequencing. Clonality of T cells was examined in the lymphoid tissues and colons of TCRalpha(-/-) mice and interleukin 4-deficient TCRalpha(-/-) mice. In addition, an in vitro culture system using syngeneic colonic epithelial cells as antigens was used.

Results: The clonal expansion of a restricted subset of Vbeta8.2(+) T cells was characterized by conservation of a single negatively charged amino acid residue in the second position of the complementarity-determining region 3 (CDR3). These T cells were observed in the diseased colon and appendix (cecal patch) of TCRalpha(-/-) mice, but not germfree TCRalpha(-/-) mice. Culture of polyclonal T cells from young TCRalpha(-/-) mice with colonic epithelial cells under T helper 2 conditions resulted in the survival of Vbeta8.2(+) T cells characterized by the same CDR3 pattern. In addition, the transfer of the cultivated T cells induced mild colitis in recombination-activating gene 1 mutant mice.

Conclusions: In the TCRalpha(-/-) mice, the development of colitis is associated with the presence of a restricted diversity of Vbeta8. 2(+) T-cell subsets characterized by a specific TCR motif. The limited diversity of lamina propria T cells that are derived from naive T cells expanded by reacting with luminal bacterial antigens is likely caused by the survival of these T cells after stimulation with self-antigens in the presence of a T helper 2 environment.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Antibody Diversity
  • CD4-Positive T-Lymphocytes / immunology*
  • Colitis / genetics*
  • Colitis / immunology*
  • Colon / immunology
  • Genes, T-Cell Receptor alpha*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / immunology
  • Interleukin-4 / deficiency
  • Interleukin-4 / genetics
  • Interleukin-4 / immunology
  • Intestinal Mucosa / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Sequence Data
  • Receptor-CD3 Complex, Antigen, T-Cell / deficiency
  • Receptor-CD3 Complex, Antigen, T-Cell / genetics
  • Receptor-CD3 Complex, Antigen, T-Cell / immunology*
  • Receptors, Antigen, T-Cell, alpha-beta / deficiency
  • Receptors, Antigen, T-Cell, alpha-beta / genetics
  • Receptors, Antigen, T-Cell, alpha-beta / immunology*

Substances

  • Homeodomain Proteins
  • Receptor-CD3 Complex, Antigen, T-Cell
  • Receptors, Antigen, T-Cell, alpha-beta
  • RAG-1 protein
  • Interleukin-4