Key aromatic/hydrophobic amino acids controlling a cross-amyloid peptide interaction versus amyloid self-assembly

J Biol Chem. 2017 Sep 1;292(35):14587-14602. doi: 10.1074/jbc.M117.774893. Epub 2017 Jul 6.

Abstract

The interaction of the intrinsically disordered polypeptide islet amyloid polypeptide (IAPP), which is associated with type 2 diabetes (T2D), with the Alzheimer's disease amyloid-β (Aβ) peptide modulates their self-assembly into amyloid fibrils and may link the pathogeneses of these two cell-degenerative diseases. However, the molecular determinants of this interaction remain elusive. Using a systematic alanine scan approach, fluorescence spectroscopy, and other biophysical methods, including heterocomplex pulldown assays, far-UV CD spectroscopy, the thioflavin T binding assay, transmission EM, and molecular dynamics simulations, here we identified single aromatic/hydrophobic residues within the amyloid core IAPP region as hot spots or key residues of its cross-interaction with Aβ40(42) peptide. Importantly, we also find that none of these residues in isolation plays a key role in IAPP self-assembly, whereas simultaneous substitution of four aromatic/hydrophobic residues with Ala dramatically impairs both IAPP self-assembly and hetero-assembly with Aβ40(42). Furthermore, our experiments yielded several novel IAPP analogs, whose sequences are highly similar to that of IAPP but have distinct amyloid self- or cross-interaction potentials. The identified similarities and major differences controlling IAPP cross-peptide interaction with Aβ40(42) versus its amyloid self-assembly offer a molecular basis for understanding the underlying mechanisms. We propose that these insights will aid in designing intervention strategies and novel IAPP analogs for the management of type 2 diabetes, Alzheimer's disease, or other diseases related to IAPP dysfunction or cross-amyloid interactions.

Keywords: Alzheimer disease; amyloid; amyloid-beta (AB); diabetes; islet amyloid polypeptide; peptide conformation; peptide interaction; protein aggregation; protein misfolding; protein-protein interaction.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Amino Acids / chemistry
  • Amino Acids / metabolism*
  • Amino Acids, Aromatic
  • Amyloid beta-Peptides / chemical synthesis
  • Amyloid beta-Peptides / chemistry
  • Amyloid beta-Peptides / metabolism*
  • Circular Dichroism
  • Humans
  • Hydrophobic and Hydrophilic Interactions
  • Islet Amyloid Polypeptide / chemical synthesis
  • Islet Amyloid Polypeptide / chemistry
  • Islet Amyloid Polypeptide / metabolism*
  • Kinetics
  • Methylation
  • Microscopy, Electron, Transmission
  • Models, Molecular*
  • Molecular Dynamics Simulation
  • Peptide Fragments / chemical synthesis
  • Peptide Fragments / chemistry
  • Peptide Fragments / metabolism*
  • Protein Aggregation, Pathological / metabolism*
  • Protein Stability
  • Protein Structure, Secondary
  • Solid-Phase Synthesis Techniques
  • Solubility
  • Spectrometry, Fluorescence

Substances

  • Amino Acids
  • Amino Acids, Aromatic
  • Amyloid beta-Peptides
  • Islet Amyloid Polypeptide
  • Peptide Fragments
  • amyloid beta-protein (1-40)
  • amyloid beta-protein (1-42)