Human antibody C10 neutralizes by diminishing Zika but enhancing dengue virus dynamics

Cell. 2021 Dec 9;184(25):6067-6080.e13. doi: 10.1016/j.cell.2021.11.009. Epub 2021 Nov 30.

Abstract

The human monoclonal antibody (HmAb) C10 potently cross-neutralizes Zika virus (ZIKV) and dengue virus. Analysis of antibody fragment (Fab) C10 interactions with ZIKV and dengue virus serotype 2 (DENV2) particles by cryoelectron microscopy (cryo-EM) and amide hydrogen/deuterium exchange mass spectrometry (HDXMS) shows that Fab C10 binding decreases overall ZIKV particle dynamics, whereas with DENV2, the same Fab causes increased dynamics. Testing of different Fab C10:DENV2 E protein molar ratios revealed that, at higher Fab ratios, especially at saturated concentrations, the Fab enhanced viral dynamics (detected by HDXMS), and observation under cryo-EM showed increased numbers of distorted particles. Our results suggest that Fab C10 stabilizes ZIKV but that with DENV2 particles, high Fab C10 occupancy promotes E protein dimer conformational changes leading to overall increased particle dynamics and distortion of the viral surface. This is the first instance of a broadly neutralizing antibody eliciting virus-specific increases in whole virus particle dynamics.

Keywords: DENV2; ZIKV; intradimer contacts; non-uniform epitope recognition; viral particle dynamics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Monoclonal / immunology
  • Antibodies, Neutralizing* / immunology
  • Antibodies, Neutralizing* / metabolism
  • Antibodies, Viral / immunology
  • Cross Reactions
  • Dengue Virus* / immunology
  • Dengue Virus* / physiology
  • Dengue* / immunology
  • Dengue* / virology
  • Humans
  • Protein Binding
  • Viral Envelope Proteins* / chemistry
  • Viral Envelope Proteins* / immunology
  • Viral Envelope Proteins* / metabolism
  • Zika Virus Infection* / immunology
  • Zika Virus Infection* / virology
  • Zika Virus* / immunology
  • Zika Virus* / physiology

Substances

  • Antibodies, Monoclonal
  • Antibodies, Neutralizing
  • Antibodies, Viral
  • Viral Envelope Proteins