Chiral mutagenesis of insulin's hidden receptor-binding surface: structure of an allo-isoleucine(A2) analogue

J Mol Biol. 2002 Feb 22;316(3):435-41. doi: 10.1006/jmbi.2001.5377.

Abstract

The hydrophobic core of vertebrate insulins contains an invariant isoleucine residue at position A2. Lack of variation may reflect this side-chain's dual contribution to structure and function: Ile(A2) is proposed both to stabilize the A1-A8 alpha-helix and to contribute to a "hidden" functional surface exposed on receptor binding. Substitution of Ile(A2) by alanine results in segmental unfolding of the A1-A8 alpha-helix, lower thermodynamic stability and impaired receptor binding. Such a spectrum of perturbations, although of biophysical interest, confounds interpretation of structure-activity relationships. To investigate the specific contribution of Ile(A2) to insulin's functional surface, we have employed non-standard mutagenesis: inversion of side-chain chirality in engineered monomer allo-Ile(A2)-DKP-insulin. Although the analogue retains native structure and stability, its affinity for the insulin receptor is impaired by 50-fold. Thus, whereas insulin's core readily accommodates allo-isoleucine at A2, its activity is exquisitely sensitive to chiral inversion. We propose that the Ile(A2) side-chain inserts within a chiral pocket of the receptor as part of insulin's hidden functional surface.

MeSH terms

  • Binding Sites
  • Circular Dichroism
  • Guanidine / pharmacology
  • Humans
  • Insulin / analogs & derivatives*
  • Insulin / chemistry*
  • Insulin / genetics
  • Insulin / metabolism
  • Isoleucine / metabolism*
  • Models, Molecular
  • Mutagenesis / genetics*
  • Protein Denaturation / drug effects
  • Protein Folding
  • Protein Structure, Secondary / drug effects
  • Receptor, Insulin / chemistry
  • Receptor, Insulin / metabolism*
  • Structure-Activity Relationship

Substances

  • Insulin
  • Isoleucine
  • Receptor, Insulin
  • Guanidine

Associated data

  • PDB/1KMF