Dominant-negative IKZF1 mutations cause a T, B, and myeloid cell combined immunodeficiency

J Clin Invest. 2018 Jul 2;128(7):3071-3087. doi: 10.1172/JCI98164. Epub 2018 Jun 11.

Abstract

Ikaros/IKZF1 is an essential transcription factor expressed throughout hematopoiesis. IKZF1 is implicated in lymphocyte and myeloid differentiation and negative regulation of cell proliferation. In humans, somatic mutations in IKZF1 have been linked to the development of B cell acute lymphoblastic leukemia (ALL) in children and adults. Recently, heterozygous germline IKZF1 mutations have been identified in patients with a B cell immune deficiency mimicking common variable immunodeficiency. These mutations demonstrated incomplete penetrance and led to haploinsufficiency. Herein, we report 7 unrelated patients with a novel early-onset combined immunodeficiency associated with de novo germline IKZF1 heterozygous mutations affecting amino acid N159 located in the DNA-binding domain of IKZF1. Different bacterial and viral infections were diagnosed, but Pneumocystis jirovecii pneumonia was reported in all patients. One patient developed a T cell ALL. This immunodeficiency was characterized by innate and adaptive immune defects, including low numbers of B cells, neutrophils, eosinophils, and myeloid dendritic cells, as well as T cell and monocyte dysfunctions. Notably, most T cells exhibited a naive phenotype and were unable to evolve into effector memory cells. Functional studies indicated these mutations act as dominant negative. This defect expands the clinical spectrum of human IKZF1-associated diseases from somatic to germline, from haploinsufficient to dominant negative.

Keywords: Genetics; Immunology; Monocytes; Monogenic diseases; T cells.

Publication types

  • Case Reports
  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Amino Acid Sequence
  • Amino Acid Substitution
  • B-Lymphocytes / immunology
  • Child
  • Child, Preschool
  • Female
  • Genes, Dominant
  • Germ-Line Mutation*
  • Heterozygote
  • Humans
  • Ikaros Transcription Factor / chemistry
  • Ikaros Transcription Factor / genetics*
  • Ikaros Transcription Factor / immunology
  • Immunologic Deficiency Syndromes / genetics*
  • Immunologic Deficiency Syndromes / immunology*
  • Infant
  • Loss of Function Mutation*
  • Male
  • Myeloid Cells / immunology
  • Pedigree
  • Phenotype
  • Protein Domains / genetics
  • Sequence Homology, Amino Acid
  • T-Lymphocytes / immunology
  • Young Adult

Substances

  • IKZF1 protein, human
  • Ikaros Transcription Factor