Genetic polymorphisms in IL-2, IL-10 and FOXP3 are associated with autoimmune neutropenia in early childhood and autoantibody specificity in a Danish cohort

Scand J Immunol. 2024 Aug;100(2):e13374. doi: 10.1111/sji.13374. Epub 2024 May 15.

Abstract

Autoimmune neutropenia (AIN) in early childhood is characterized by chronic neutropenia and positivity for human neutrophil antibodies (HNA), resulting in the excessive destruction of neutrophils. The association between regulatory T cells (Tregs) and AIN has been described, and in this study, we investigated three Treg-associated genes, IL-2, IL-10 and FOXP3. The frequencies of three single nucleotide polymorphisms (SNPs) in IL-2 -330T>G (rs2069762), +114G>T (rs2069763) and IVS3-116 A>G (rs2069772), four SNPs in IL-10 -3575T>A (rs1800890), -1082G>A (rs1800896), -819 C>T (rs1800871) and -592 C>A (rs1800872) and three SNPs in FOXP3 -3499 A>G (rs3761547), -3279 C>A (rs3761548) and -924 A>G (rs2232365) were compared between 166 Danish AIN patients and 358 healthy controls. Disease association was observed for IL-2 IVS3-116 GG (p = 0.0081, OR = 0.35 [0.15-0.80]), IL-10 -3575 TT (p = 0.0078, OR = 1.71 [1.16-2.54]) and IL-10 -1082 AA (p = 0.014, OR = 1.76 [1.14-2.72]) in all patients and FOXP3 -924 (p = 0.0005, A OR = 0.41 [0.25-0.68] and G OR = 2.42 [1.46-4.01]) in male patients. None of the associations were linked to antibody specificity. Disease-associated haplotypes were observed in IL-2 and FOXP3. IL-2 -330T/+114 T/IVS3-116A was associated with anti-FcγRIIIb-positive patients (p = 0.012, OR = 2.07 [1.18-3.62]). FOXP3 -3499A/-3279C/-924A was associated with anti-HNA-1a-positive male patients (p = 0.016, OR = 0.41 [0.20-0.83]), and ACG was associated with female patients, both in the combined group (p = 0.006, OR = NA) and the anti-FcγRIIIb-positive group (p = 0.002, OR = NA). We conclude that our findings reveal a correlation between SNP in Treg-associated genes and AIN, indicating that AIN could be driven by dysfunction of immune homeostatic-evolving Tregs.

Keywords: FOXP3; IL‐10; IL‐2; autoantibody; autoimmune neutropenia; genetic; regulatory T cells.

MeSH terms

  • Adolescent
  • Autoantibodies* / immunology
  • Autoimmune Diseases* / genetics
  • Autoimmune Diseases* / immunology
  • Child
  • Child, Preschool
  • Cohort Studies
  • Denmark
  • Female
  • Forkhead Transcription Factors* / genetics
  • Gene Frequency
  • Genetic Predisposition to Disease
  • Humans
  • Infant
  • Interleukin-10* / genetics
  • Interleukin-2* / genetics
  • Interleukin-2* / immunology
  • Male
  • Neutropenia* / genetics
  • Neutropenia* / immunology
  • Neutrophils / immunology
  • Polymorphism, Single Nucleotide*
  • T-Lymphocytes, Regulatory* / immunology

Substances

  • Forkhead Transcription Factors
  • Interleukin-10
  • Interleukin-2
  • FOXP3 protein, human
  • Autoantibodies
  • IL10 protein, human
  • IL2 protein, human