A Hyper-IgM Syndrome Mutation in Activation-Induced Cytidine Deaminase Disrupts G-Quadruplex Binding and Genome-wide Chromatin Localization

Immunity. 2020 Nov 17;53(5):952-970.e11. doi: 10.1016/j.immuni.2020.10.003. Epub 2020 Oct 23.

Abstract

Precise targeting of activation-induced cytidine deaminase (AID) to immunoglobulin (Ig) loci promotes antibody class switch recombination (CSR) and somatic hypermutation (SHM), whereas AID targeting of non-Ig loci can generate oncogenic DNA lesions. Here, we examined the contribution of G-quadruplex (G4) nucleic acid structures to AID targeting in vivo. Mice bearing a mutation in Aicda (AIDG133V) that disrupts AID-G4 binding modeled the pathology of hyper-IgM syndrome patients with an orthologous mutation, lacked CSR and SHM, and had broad defects in genome-wide AIDG133V chromatin localization. Genome-wide analyses also revealed that wild-type AID localized to MHCII genes, and AID expression correlated with decreased MHCII expression in germinal center B cells and diffuse large B cell lymphoma. Our findings indicate a crucial role for G4 binding in AID targeting and suggest that AID activity may extend beyond Ig loci to regulate the expression of genes relevant to the physiology and pathology of activated B cells.

Keywords: AID; CSR; DLBCL; G-quadruplex; G4; HIGM; MHC class II; MHCII; SHM; activation-induced cytidine deaminase; class switch recombination; diffuse large B cell lymphoma; germinal center B cells; hyper-IgM syndrome; somatic hypermutation.

Publication types

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

MeSH terms

  • Animals
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • Chromatin / genetics*
  • Chromatin / metabolism*
  • Computational Biology / methods
  • Cytidine Deaminase / genetics*
  • Cytidine Deaminase / metabolism*
  • Disease Models, Animal
  • Disease Susceptibility
  • Enzyme Activation
  • Fluorescent Antibody Technique
  • G-Quadruplexes*
  • Gene Expression Profiling
  • Genome-Wide Association Study
  • Germinal Center / immunology
  • Germinal Center / metabolism
  • HLA Antigens / genetics
  • HLA Antigens / immunology
  • Humans
  • Hyper-IgM Immunodeficiency Syndrome / diagnosis
  • Hyper-IgM Immunodeficiency Syndrome / etiology*
  • Hyper-IgM Immunodeficiency Syndrome / metabolism*
  • Immunoglobulin Class Switching / genetics
  • Immunoglobulin Class Switching / immunology
  • Immunophenotyping
  • Lymphocyte Activation / genetics
  • Lymphoma, Large B-Cell, Diffuse / etiology
  • Lymphoma, Large B-Cell, Diffuse / metabolism
  • Lymphoma, Large B-Cell, Diffuse / pathology
  • Mice
  • Mice, Transgenic
  • Mutation*

Substances

  • Chromatin
  • HLA Antigens
  • Cytidine Deaminase