Distinct Fcα receptor N-glycans modulate the binding affinity to immunoglobulin A (IgA) antibodies

J Biol Chem. 2019 Sep 20;294(38):13995-14008. doi: 10.1074/jbc.RA119.009954. Epub 2019 Jul 30.

Abstract

Human immunoglobulin A (IgA) is the most prevalent antibody class at mucosal sites with an important role in mucosal defense. Little is known about the impact of N-glycan modifications of IgA1 and IgA2 on binding to the Fcα receptor (FcαRI), which is also heavily glycosylated at its extracellular domain. Here, we transiently expressed human epidermal growth factor receptor 2 (HER2)-binding monomeric IgA1, IgA2m(1), and IgA2m(2) variants in Nicotiana benthamiana ΔXT/FT plants lacking the enzymes responsible for generating nonhuman N-glycan structures. By coinfiltrating IgA with the respective glycan-modifying enzymes, we generated IgA carrying distinct homogenous N-glycans. We demonstrate that distinctly different N-glycan profiles did not influence antigen binding or the overall structure and integrity of the IgA antibodies but did affect their thermal stability. Using size-exclusion chromatography, differential scanning and isothermal titration calorimetry, surface plasmon resonance spectroscopy, and molecular modeling, we probed distinct IgA1 and IgA2 glycoforms for binding to four different FcαRI glycoforms and investigated the thermodynamics and kinetics of complex formation. Our results suggest that different N-glycans on the receptor significantly contribute to binding affinities for its cognate ligand. We also noted that full-length IgA and FcαRI form a mixture of 1:1 and 1:2 complexes tending toward a 1:1 stoichiometry due to different IgA tailpiece conformations that make it less likely that both binding sites are simultaneously occupied. In conclusion, N-glycans of human IgA do not affect its structure and integrity but its thermal stability, and FcαRI N-glycans significantly modulate binding affinity to IgA.

Keywords: Fc receptor; adaptive immunity; antibody; glycobiology; glycoprotein structure; glycosylation; immunoglobulin A (IgA); molecular modeling; posttranslational modifications; recombinant protein expression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Glycosylation
  • HEK293 Cells
  • Humans
  • Immunoglobulin A / chemistry
  • Immunoglobulin A / metabolism*
  • Kinetics
  • Molecular Dynamics Simulation
  • Nicotiana / metabolism
  • Polysaccharides / chemistry*
  • Protein Stability
  • Protein Structure, Quaternary
  • Receptors, Fc / chemistry
  • Receptors, Fc / genetics
  • Receptors, Fc / metabolism*
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / isolation & purification
  • Thermodynamics

Substances

  • Immunoglobulin A
  • Polysaccharides
  • Receptors, Fc
  • Recombinant Proteins

Associated data

  • PDB/1ow0