X-linked carriers of chronic granulomatous disease: Illness, lyonization, and stability

J Allergy Clin Immunol. 2018 Jan;141(1):365-371. doi: 10.1016/j.jaci.2017.04.035. Epub 2017 May 18.

Abstract

Background: Chronic granulomatous disease (CGD) is characterized by recurrent life-threatening bacterial and fungal infections and aberrant inflammation. Mutations in CYBB cause X-linked CGD and account for 65% to 70% of cases in Western countries.

Objective: We sought to understand the clinical manifestations associated with the X-linked CGD carrier state.

Methods: We undertook a comprehensive retrospective study of 162 affected female subjects. We examined dihydrorhodamine 123 (DHR) oxidation data for percentage of X-chromosome inactivation. We correlated lyonization (%DHR+) with clinical features. Where possible, we followed %DHR+ values over time.

Results: Clinical data were available for 93 female subjects: %DHR+ values were 46% (mean) and 47% (median; SD, 24). Using the %DHR+ value as the criterion for X inactivation, 78% of patients had levels of inactivation of 20% to 80%, suggesting random inactivation that was independent of age. In contrast, carriers with CGD-type infections had median %DHR+ values of 8% (n = 14; range, 0.06% to 48%), and those with only autoimmune or inflammatory manifestations had median %DHR+ values of 39% (n = 31; range, 7.4% to 74%). Those with both infections and autoimmunity had low %DHR+ values (n = 6; range, 3% to 14%). A %DHR+ value of less than 10% was strongly associated with infections (odds ratio, 99). Strong association persisted when %DHR+ values were less than 20% (odds ratio, 12). Autoimmunity was not associated with %DHR+ values. In 2 sets of identical twins, the %DHR+ populations tracked closely over time. Although the %DHR+ populations were very similar between sisters, those between mothers and daughters were unrelated.

Conclusions: A low %DHR+ value strongly predicts infection risk in X-linked CGD carriers, and the carrier state itself is associated with autoimmunity.

Keywords: Superoxide; X inactivation; autoimmunity; dihydrorhodamine flow cytometry test; lyonization.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Biomarkers
  • Child
  • Child, Preschool
  • Female
  • Genes, X-Linked*
  • Genetic Association Studies*
  • Granulomatous Disease, Chronic / complications
  • Granulomatous Disease, Chronic / diagnosis*
  • Granulomatous Disease, Chronic / genetics*
  • Granulomatous Disease, Chronic / immunology
  • Heterozygote*
  • Humans
  • Immunoglobulin G / immunology
  • Immunoglobulin M / immunology
  • Infant
  • Infections / etiology
  • Middle Aged
  • Mutation
  • Odds Ratio
  • Phenotype*
  • Symptom Assessment
  • X Chromosome Inactivation
  • Young Adult

Substances

  • Biomarkers
  • Immunoglobulin G
  • Immunoglobulin M