Reduced central tolerance in Omenn syndrome leads to immature self-reactive oligoclonal T cells

J Allergy Clin Immunol. 2009 Oct;124(4):793-800. doi: 10.1016/j.jaci.2009.06.048. Epub 2009 Sep 19.

Abstract

Background: Omenn syndrome (OS) is characterized by a peculiar severe T-cell immune deficiency associated with autoimmunelike manifestations. Dysregulations of the central and peripheral immune tolerance, mediated by the protein autoimmune regulator (AIRE) and regulatory T cells, respectively, were proposed as possible mechanisms of this aberrant inflammatory process.

Objective: We studied mechanisms of central and peripheral tolerance in patients with OS and also examined the gene expression profile associated with OS features.

Methods: T-cell receptor diversity, DNA rearrangement, and the expression of AIRE and forkhead box P3 mRNA as well as the expression of regulatory T cells in cells obtained from patients with OS were studied. Characterization of gene expression in these cells was carried out by using the TaqMan Low-Density Array.

Results: Transcript expression of peripheral blood AIRE but not forkhead box P3 was reduced in patients with OS. The expression of natural killer T and regulatory T cells was normal, although the latter showed an abnormal CD4-negative population. Patients with OS have oligoclonal T cells with limited DNA recombination activity, including the presence of early but not late T-cell maturation events, regardless of the genetic defect underlying the syndrome. The transcriptional profile associated with OS features reveals significant changes in 25.5% of the tested genes compared with normal control.

Conclusion: Our findings suggest that T-cell oligoclonal expansion in OS emanates from an incomplete block before the maturation stage of negative selection, which may explain escape of autoreactive T cells from the thymus. Dysregulated genes in patients with OS are closely involved with self-tolerance and autoimmunity.

MeSH terms

  • AIRE Protein
  • Autoimmunity* / genetics
  • Autoimmunity* / immunology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • Clone Cells / immunology
  • Clone Cells / metabolism
  • Cytokines / immunology
  • Cytokines / metabolism
  • Down-Regulation / genetics
  • Down-Regulation / immunology
  • Female
  • Forkhead Transcription Factors / immunology
  • Forkhead Transcription Factors / metabolism
  • Gene Expression
  • Gene Rearrangement, T-Lymphocyte
  • Humans
  • Immune Tolerance*
  • Male
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Receptors, Antigen, T-Cell / metabolism
  • Severe Combined Immunodeficiency / genetics
  • Severe Combined Immunodeficiency / immunology*
  • Severe Combined Immunodeficiency / metabolism
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • Transcription Factors / immunology
  • Transcription Factors / metabolism
  • Up-Regulation / genetics
  • Up-Regulation / immunology

Substances

  • Cytokines
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Receptors, Antigen, T-Cell
  • Transcription Factors