AID Recognizes Structured DNA for Class Switch Recombination

Mol Cell. 2017 Aug 3;67(3):361-373.e4. doi: 10.1016/j.molcel.2017.06.034. Epub 2017 Jul 27.

Abstract

Activation-induced cytidine deaminase (AID) initiates both class switch recombination (CSR) and somatic hypermutation (SHM) in antibody diversification. Mechanisms of AID targeting and catalysis remain elusive despite its critical immunological roles and off-target effects in tumorigenesis. Here, we produced active human AID and revealed its preferred recognition and deamination of structured substrates. G-quadruplex (G4)-containing substrates mimicking the mammalian immunoglobulin switch regions are particularly good AID substrates in vitro. By solving crystal structures of maltose binding protein (MBP)-fused AID alone and in complex with deoxycytidine monophosphate, we surprisingly identify a bifurcated substrate-binding surface that explains structured substrate recognition by capturing two adjacent single-stranded overhangs simultaneously. Moreover, G4 substrates induce cooperative AID oligomerization. Structure-based mutations that disrupt bifurcated substrate recognition or oligomerization both compromise CSR in splenic B cells. Collectively, our data implicate intrinsic preference of AID for structured substrates and uncover the importance of G4 recognition and oligomerization of AID in CSR.

Keywords: AID; APOBEC; CSR; G-quadruplex; activation-induced cytidine deaminase; class switch recombination; crystal structure.

MeSH terms

  • APOBEC Deaminases / genetics
  • APOBEC Deaminases / metabolism
  • Animals
  • Antibody Diversity
  • B-Lymphocytes / enzymology
  • B-Lymphocytes / immunology
  • Cytidine Deaminase / chemistry
  • Cytidine Deaminase / genetics
  • Cytidine Deaminase / metabolism*
  • DNA / chemistry
  • DNA / genetics
  • DNA / metabolism*
  • Humans
  • Immunoglobulin Class Switching*
  • Immunoglobulin Switch Region*
  • Mice
  • Models, Molecular
  • Mutation
  • Nucleic Acid Conformation
  • Protein Binding
  • Protein Conformation
  • Recombination, Genetic*
  • Spleen / enzymology
  • Spleen / immunology
  • Structure-Activity Relationship
  • Substrate Specificity

Substances

  • DNA
  • AICDA (activation-induced cytidine deaminase)
  • APOBEC Deaminases
  • Cytidine Deaminase