Abnormal Peyer patch development and B-cell gut homing drive IgA deficiency in Kabuki syndrome

J Allergy Clin Immunol. 2020 Mar;145(3):982-992. doi: 10.1016/j.jaci.2019.11.034. Epub 2019 Dec 6.

Abstract

Background: Kabuki syndrome (KS) is commonly caused by mutations in the histone-modifying enzyme lysine methyltransferase 2D (KMT2D). Immune dysfunction is frequently observed in individuals with KS, but the role of KMT2D in immune system function has not been identified.

Objective: We sought to understand the mechanisms driving KS-associated immune deficiency (hypogammaglobulinemia [low IgA], splenomegaly, and diminished immunization responses).

Methods: We performed a comprehensive evaluation of humoral immunity and secondary lymphoid tissues in an established KS (Kmt2d+/βGeo) mouse model and validated select findings in a patient with KS.

Results: Compared with wild-type littermates, Kmt2d+/βGeo mice demonstrated deficiencies in multiple B-cell lineages and reduced serum IgA and elevated IgM levels across multiple ages. The bone marrow, spleen, and intestine of Kmt2d+/βGeo mice contained diminished numbers of IgA-secreting cells, while elevated germinal center B cells were found in the mesenteric lymph node and Peyer patches. Kmt2d+/βGeo mice have decreased size and numbers of Peyer patches, a finding confirmed in human samples. We identified deficiency of Itgb7 RNA and protein expression, a gene encoding an adhesion protein that mediates intestinal homing, and we demonstrated KMT2D-dependent control of ITGB7 expression in a human cell line.

Conclusions: Kmt2d haploinsufficiency has broad deleterious effects on B-cell differentiation, specifically hampering gut lymphocyte homing and IgA+ plasma cell differentiation. Intestinal lymphoid defects caused by ITGB7 deficiency have not previously been recognized in KS, and these results provide new mechanistic insights into the pathogenesis of KS-associated immune deficiency.

Keywords: B-cell maturation; B1 B cells; ITGB7; IgA; KMT2D; epigenetics; gut lymphocyte homing; hypogammaglobulinemia.

Publication types

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

MeSH terms

  • Abnormalities, Multiple / immunology*
  • Abnormalities, Multiple / pathology*
  • Animals
  • B-Lymphocytes / immunology
  • B-Lymphocytes / pathology*
  • Cell Differentiation / immunology
  • Cell Movement / immunology
  • DNA-Binding Proteins / genetics
  • Face / abnormalities*
  • Face / pathology
  • Hematologic Diseases / immunology*
  • Hematologic Diseases / pathology*
  • Histone-Lysine N-Methyltransferase / genetics
  • Humans
  • IgA Deficiency / genetics
  • IgA Deficiency / immunology
  • Integrin beta Chains / metabolism
  • Intestines / immunology
  • Mice
  • Mutation
  • Myeloid-Lymphoid Leukemia Protein / genetics
  • Neoplasm Proteins / genetics
  • Peyer's Patches / immunology
  • Peyer's Patches / pathology*
  • Vestibular Diseases / immunology*
  • Vestibular Diseases / pathology*

Substances

  • DNA-Binding Proteins
  • Integrin beta Chains
  • KMT2D protein, human
  • Neoplasm Proteins
  • integrin beta7
  • Myeloid-Lymphoid Leukemia Protein
  • Histone-Lysine N-Methyltransferase
  • Kmt2b protein, mouse

Supplementary concepts

  • Kabuki syndrome