KMT2D regulates activation, localization, and integrin expression by T-cells

Front Immunol. 2024 May 3:15:1341745. doi: 10.3389/fimmu.2024.1341745. eCollection 2024.

Abstract

Individuals with Kabuki syndrome present with immunodeficiency; however, how pathogenic variants in the gene encoding the histone-modifying enzyme lysine methyltransferase 2D (KMT2D) lead to immune alterations remain poorly understood. Following up on our prior report of KMT2D-altered integrin expression in B-cells, we performed targeted analyses of KMT2D's influence on integrin expression in T-cells throughout development (thymocytes through peripheral T-cells) in murine cells with constitutive- and conditional-targeted Kmt2d deletion. Using high-throughput RNA-sequencing and flow cytometry, we reveal decreased expression (both at the transcriptional and translational levels) of a cluster of leukocyte-specific integrins, which perturb aspects of T-cell activation, maturation, adhesion/localization, and effector function. H3K4me3 ChIP-PCR suggests that these evolutionary similar integrins are under direct control of KMT2D. KMT2D loss also alters multiple downstream programming/signaling pathways, including integrin-based localization, which can influence T-cell populations. We further demonstrated that KMT2D deficiency is associated with the accumulation of murine CD8+ single-positive (SP) thymocytes and shifts in both human and murine peripheral T-cell populations, including the reduction of the CD4+ recent thymic emigrant (RTE) population. Together, these data show that the targeted loss of Kmt2d in the T-cell lineage recapitulates several distinct features of Kabuki syndrome-associated immune deficiency and implicates epigenetic mechanisms in the regulation of integrin signaling.

Keywords: Itgal; Itgb7; KS1-associated immune deficiency (KSAID); Kabuki syndrome (KS); integrin switching; recent thymic emigrant (RTE); thymocyte.

MeSH terms

  • Abnormalities, Multiple
  • Animals
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Face / abnormalities
  • Gene Expression Regulation* / genetics
  • Hematologic Diseases
  • Histone-Lysine N-Methyltransferase* / genetics
  • Histone-Lysine N-Methyltransferase* / metabolism
  • Humans
  • Integrins* / genetics
  • Integrins* / metabolism
  • Lymphocyte Activation / genetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myeloid-Lymphoid Leukemia Protein*
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / immunology
  • Neoplasm Proteins / metabolism
  • Signal Transduction
  • T-Lymphocytes* / immunology
  • T-Lymphocytes* / metabolism
  • Vestibular Diseases / genetics
  • Vestibular Diseases / immunology
  • Vestibular Diseases / metabolism

Substances

  • DNA-Binding Proteins
  • Histone-Lysine N-Methyltransferase
  • Integrins
  • Kmt2d protein, mouse
  • Myeloid-Lymphoid Leukemia Protein
  • Neoplasm Proteins

Supplementary concepts

  • Kabuki syndrome