Patients with T⁺/low NK⁺ IL-2 receptor γ chain deficiency have differentially-impaired cytokine signaling resulting in severe combined immunodeficiency

Eur J Immunol. 2014 Oct;44(10):3129-40. doi: 10.1002/eji.201444689. Epub 2014 Aug 28.

Abstract

X-linked severe combined immunodeficiency (X-SCID) leads to a T(-) NK(-) B(+) immunophenotype and is caused by mutations in the gene encoding the IL-2 receptor γ-chain (IL2RG). IL2RG(R222C) leads to atypical SCID with a severe early onset phenotype despite largely normal NK- and T-cell numbers. To address this discrepancy, we performed a detailed analysis of T, B, and NK cells, including quantitative STAT phosphorylation and functional responses to the cytokines IL-2, IL-4, IL-15, and IL-21 in a patient with the IL2RG(R222C) mutation. Moreover, we identified nine additional unpublished patients with the same mutations, all with a full SCID phenotype, and confirmed selected immunological observations. T-cell development was variably affected, but led to borderline T-cell receptor excision circle (TREC) levels and a normal repertoire. T cells showed moderately reduced proliferation, failing enhancement by IL-2. While NK-cell development was normal, IL-2 enhancement of NK-cell degranulation and IL-15-induced cytokine production were absent. IL-2 or IL-21 failed to enhance B-cell proliferation and plasmablast differentiation. These functional alterations were reflected by a differential impact of IL2RG(R222C) on cytokine signal transduction, with a gradient IL-4<IL-2/IL-15<IL-21. Thus, IL2RG(R222C) causes a consistently severe clinical phenotype that is not predicted by the variable and moderate impairment of T-cell immunity or TREC analysis.

Keywords: Atypical SCID; Common gamma chain; Cytokine signaling; Leaky SCID; Severe combined immunodeficiency.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • B-Lymphocytes / immunology*
  • Cytokines / immunology*
  • Humans
  • Infant
  • Interleukin Receptor Common gamma Subunit / genetics*
  • Interleukin Receptor Common gamma Subunit / immunology
  • Killer Cells, Natural / immunology*
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology
  • Male
  • Mutation
  • Phenotype
  • Severe Combined Immunodeficiency / immunology*
  • Signal Transduction / immunology
  • T-Lymphocytes / immunology*

Substances

  • Cytokines
  • IL2RG protein, human
  • Interleukin Receptor Common gamma Subunit