Defects of B-cell terminal differentiation in patients with type-1 Kabuki syndrome

J Allergy Clin Immunol. 2016 Jan;137(1):179-187.e10. doi: 10.1016/j.jaci.2015.06.002. Epub 2015 Jul 17.

Abstract

Background: Kabuki syndrome (KS) is a complex multisystem developmental disorder associated with mutation of genes encoding histone-modifying proteins. In addition to craniofacial, intellectual, and cardiac defects, KS is also characterized by humoral immune deficiency and autoimmune disease, yet no detailed molecular characterization of the KS-associated immune phenotype has been reported.

Objective: We sought to characterize the humoral immune defects found in patients with KS with lysine methyltransferase 2D (KMT2D) mutations.

Methods: We comprehensively characterized B-cell function in a cohort (n = 13) of patients with KS (age, 4 months to 27 years).

Results: Three quarters (77%) of the cohort had a detectable heterozygous KMT2D mutation (50% nonsense, 20% splice site, and 30% missense mutations), and 70% of the reported mutations are novel. Among the patients with KMT2D mutations (KMT2D(Mut/+)), hypogammaglobulinemia was detected in all but 1 patient, with IgA deficiency affecting 90% of patients and a deficiency in at least 1 other isoform seen in 40% of patients. Numbers of total memory (CD27(+)) and class-switched memory B cells (IgM(-)) were significantly reduced in patients with KMT2D(Mut/+) mutations compared with numbers in control subjects (P < .001). Patients with KMT2D(Mut/+) mutations also had significantly reduced rates of somatic hypermutation in IgG (P = .003) but not IgA or IgM heavy chain sequences. Impaired terminal differentiation was noted in primary B cells from patients with KMT2D(Mut/+) mutations. Autoimmune pathology was observed in patients with missense mutations affecting the SET domain and its adjacent domains.

Conclusions: In patients with KS, autosomal dominant KMT2D mutations are associated with dysregulation of terminal B-cell differentiation, leading to humoral immune deficiency and, in some cases, autoimmunity. All patients with KS should undergo serial clinical immune evaluations.

Keywords: AICDA; AID; CD21(lo) B cells; KDM6A; KMT2D; Kabuki syndrome; PTIP; class-switch recombination; hypogammaglobulinemia; memory B cells; polymerase eta; somatic hypermutation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abnormalities, Multiple / genetics*
  • Abnormalities, Multiple / immunology*
  • Adolescent
  • Adult
  • Agammaglobulinemia / genetics
  • Agammaglobulinemia / immunology
  • B-Lymphocytes / cytology*
  • B-Lymphocytes / immunology
  • Cell Differentiation
  • Child
  • Child, Preschool
  • DNA-Binding Proteins / genetics*
  • Face / abnormalities*
  • Hematologic Diseases / genetics*
  • Hematologic Diseases / immunology*
  • Humans
  • Infant
  • Mutation
  • Neoplasm Proteins / genetics*
  • Vestibular Diseases / genetics*
  • Vestibular Diseases / immunology*
  • Young Adult

Substances

  • DNA-Binding Proteins
  • KMT2D protein, human
  • Neoplasm Proteins

Supplementary concepts

  • Kabuki syndrome