Engineered synthetic antibodies as probes to quantify the energetic contributions of ligand binding to conformational changes in proteins

J Biol Chem. 2018 Feb 23;293(8):2815-2828. doi: 10.1074/jbc.RA117.000656. Epub 2018 Jan 10.

Abstract

Conformational changes in proteins due to ligand binding are ubiquitous in biological processes and are integral to many biological systems. However, it is often challenging to link ligand-induced conformational changes to a resulting biological function because it is difficult to distinguish between the energetic components associated with ligand binding and those due to structural rearrangements. Here, we used a unique approach exploiting conformation-specific and regio-specific synthetic antibodies (sABs) to probe the energetic contributions of ligand binding to conformation changes. Using maltose-binding protein (MBP) as a model system, customized phage-display selections were performed to generate sABs that stabilize MBP in different conformational states, modulating ligand-binding affinity in competitive, allosteric, or peristeric manners. We determined that the binding of a closed conformation-specific sAB (sAB-11M) to MBP in the absence of maltose is entropically driven, providing new insight into designing antibody-stabilized protein interactions. Crystal structures of sABs bound to MBP, together with biophysical data, delineate the basis of free energy differences between different conformational states and confirm the use of the sABs as energy probes for dissecting enthalpic and entropic contributions to conformational transitions. Our work provides a foundation for investigating the energetic contributions of distinct conformational dynamics to specific biological outputs. We anticipate that our approach also may be valuable for analyzing the energy landscapes of regulatory proteins controlling biological responses to environmental changes.

Keywords: allostery; antibody engineering; conformation-specific synthetic antibodies; crystal structure; energy probes; epitope mapping; phage display; thermodynamics.

Publication types

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

MeSH terms

  • Amino Acid Substitution
  • Antibodies, Blocking / chemistry
  • Antibodies, Blocking / genetics
  • Antibodies, Blocking / metabolism*
  • Antibody Affinity
  • Apoproteins / chemistry
  • Apoproteins / metabolism
  • Biotinylation
  • Crystallography, X-Ray
  • Escherichia coli K12 / enzymology*
  • Escherichia coli K12 / metabolism
  • Escherichia coli Proteins / chemistry
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism*
  • Ligands
  • Maltose / chemistry
  • Maltose / metabolism*
  • Maltose-Binding Proteins / chemistry
  • Maltose-Binding Proteins / genetics
  • Maltose-Binding Proteins / metabolism*
  • Models, Molecular*
  • Molecular Probes / chemistry
  • Molecular Probes / genetics
  • Molecular Probes / metabolism*
  • Mutation
  • Peptide Library
  • Protein Conformation
  • Protein Engineering
  • Protein Processing, Post-Translational
  • Protein Stability
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Thermodynamics

Substances

  • Antibodies, Blocking
  • Apoproteins
  • Escherichia coli Proteins
  • Ligands
  • Maltose-Binding Proteins
  • Molecular Probes
  • Peptide Library
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • Maltose

Associated data

  • PDB/5BK1
  • PDB/5BJZ
  • PDB/5BK2
  • PDB/3PUZ
  • PDB/1OMP
  • PDB/3PGF