The unusual conformation of cross-strand disulfide bonds is critical to the stability of β-hairpin peptides

Proteins. 2020 Mar;88(3):485-502. doi: 10.1002/prot.25828. Epub 2019 Oct 16.

Abstract

The cross-strand disulfides (CSDs) found in β-hairpin antimicrobial peptides (β-AMPs) show a unique disulfide geometry that is characterized by unusual torsion angles and a short Cα-Cα distance. While the sequence and disulfide bond connectivity of disulfide-rich peptides is well studied, much less is known about the disulfide geometry found in CSDs and their role in the stability of β-AMPs. To address this, we solved the nuclear magnetic resonance (NMR) structure of the β-AMP gomesin (Gm) at 278, 298, and 310 K, examined the disulfide bond geometry of over 800 disulfide-rich peptides, and carried out extensive molecular dynamics (MD) simulation of the peptides Gm and protegrin. The NMR data suggests Cα-Cα distances characteristic for CSDs are independent of temperature. Analysis of disulfide-rich peptides from the Protein Data Bank revealed that right-handed and left-handed rotamers are equally likely in CSDs. The previously reported preference for right-handed rotamers was likely biased by restricting the analysis to peptides and proteins solved using X-ray crystallography. Furthermore, data from MD simulations showed that the short Cα-Cα distance is critical for the stability of these peptides. The unique disulfide geometry of CSDs poses a challenge to biomolecular force fields and to retain the stability of β-hairpin fold over long simulation times, restraints on the torsion angles might be required.

Keywords: MD simulations; NMR; antimicrobial peptides; cysteine-rich peptides; disulfide bonds; disulfide-rich; peptide conformation; peptides; β-hairpin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / chemistry*
  • Anti-Bacterial Agents / metabolism
  • Antimicrobial Cationic Peptides / chemistry*
  • Antimicrobial Cationic Peptides / metabolism
  • Disulfides / chemistry*
  • Disulfides / metabolism
  • Molecular Dynamics Simulation
  • Nuclear Magnetic Resonance, Biomolecular
  • Protein Conformation, beta-Strand
  • Protein Interaction Domains and Motifs
  • Protein Stability
  • Spiders / chemistry
  • Stereoisomerism
  • Temperature
  • Thermodynamics

Substances

  • Anti-Bacterial Agents
  • Antimicrobial Cationic Peptides
  • Disulfides
  • gomesin
  • protegrin-1