An integrative approach combining ion mobility mass spectrometry, X-ray crystallography, and nuclear magnetic resonance spectroscopy to study the conformational dynamics of α1 -antitrypsin upon ligand binding

Protein Sci. 2015 Aug;24(8):1301-12. doi: 10.1002/pro.2706. Epub 2015 Jul 14.

Abstract

Native mass spectrometry (MS) methods permit the study of multiple protein species within solution equilibria, whereas ion mobility (IM)-MS can report on conformational behavior of specific states. We used IM-MS to study a conformationally labile protein (α1 -antitrypsin) that undergoes pathological polymerization in the context of point mutations. The folded, native state of the Z-variant remains highly polymerogenic in physiological conditions despite only minor thermodynamic destabilization relative to the wild-type variant. Various data implicate kinetic instability (conformational lability within a native state ensemble) as the basis of Z α1 -antitrypsin polymerogenicity. We show the ability of IM-MS to track such disease-relevant conformational behavior in detail by studying the effects of peptide binding on α1 -antitrypsin conformation and dynamics. IM-MS is, therefore, an ideal platform for the screening of compounds that result in therapeutically beneficial kinetic stabilization of native α1 -antitrypsin. Our findings are confirmed with high-resolution X-ray crystallographic and nuclear magnetic resonance spectroscopic studies of the same event, which together dissect structural changes from dynamic effects caused by peptide binding at a residue-specific level. IM-MS methods, therefore, have great potential for further study of biologically relevant thermodynamic and kinetic instability of proteins and provide rapid and multidimensional characterization of ligand interactions of therapeutic interest.

Keywords: X-ray crystallography; biomolecular; drug discovery; ion mobility mass spectrometry; mass spectrometry/methods; nuclear magnetic resonance; protein dynamics; protein unfolding; α1-antitrypsin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Crystallography, X-Ray
  • Drug Discovery
  • Humans
  • Ligands
  • Mass Spectrometry
  • Molecular Dynamics Simulation
  • Mutation
  • Nuclear Magnetic Resonance, Biomolecular
  • Peptides / chemistry
  • Peptides / pharmacology
  • Protein Binding
  • Protein Conformation
  • Thermodynamics
  • alpha 1-Antitrypsin / chemistry*
  • alpha 1-Antitrypsin / genetics
  • alpha 1-Antitrypsin / metabolism

Substances

  • Ligands
  • Peptides
  • alpha 1-Antitrypsin

Associated data

  • PDB/4PYW