Conformation-dependent epitopes recognized by prion protein antibodies probed using mutational scanning and deep sequencing

J Mol Biol. 2015 Jan 30;427(2):328-40. doi: 10.1016/j.jmb.2014.10.024. Epub 2014 Nov 7.

Abstract

Prion diseases are caused by a structural rearrangement of the cellular prion protein, PrP(C), into a disease-associated conformation, PrP(Sc), which may be distinguished from one another using conformation-specific antibodies. We used mutational scanning by cell-surface display to screen 1341 PrP single point mutants for attenuated interaction with four anti-PrP antibodies, including several with conformational specificity. Single-molecule real-time gene sequencing was used to quantify enrichment of mutants, returning 26,000 high-quality full-length reads for each screened population on average. Relative enrichment of mutants correlated to the magnitude of the change in binding affinity. Mutations that diminished binding of the antibody ICSM18 represented the core of contact residues in the published crystal structure of its complex. A similarly located binding site was identified for D18, comprising discontinuous residues in helix 1 of PrP, brought into close proximity to one another only when the alpha helix is intact. The specificity of these antibodies for the normal form of PrP likely arises from loss of this conformational feature after conversion to the disease-associated form. Intriguingly, 6H4 binding was found to depend on interaction with the same residues, among others, suggesting that its ability to recognize both forms of PrP depends on a structural rearrangement of the antigen. The application of mutational scanning and deep sequencing provides residue-level resolution of positions in the protein-protein interaction interface that are critical for binding, as well as a quantitative measure of the impact of mutations on binding affinity.

Keywords: EP1802Y; SMRT; discontinuous epitope; epitope mapping; yeast surface display.

Publication types

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

MeSH terms

  • Animals
  • Binding Sites
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism
  • DNA, Bacterial / genetics
  • DNA, Fungal / genetics
  • Epitope Mapping
  • Epitopes / genetics*
  • Epitopes / immunology
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gene Rearrangement
  • High-Throughput Nucleotide Sequencing / methods*
  • Mice
  • Mutation
  • Prions / chemistry*
  • Prions / genetics
  • Prions / immunology
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Single-Chain Antibodies / genetics*
  • Single-Chain Antibodies / immunology

Substances

  • AGA2 protein, S cerevisiae
  • Cell Adhesion Molecules
  • DNA, Bacterial
  • DNA, Fungal
  • Epitopes
  • Prions
  • Saccharomyces cerevisiae Proteins
  • Single-Chain Antibodies