Polyphenol-Binding Amyloid Fibrils Self-Assemble into Reversible Hydrogels with Antibacterial Activity

ACS Nano. 2018 Apr 24;12(4):3385-3396. doi: 10.1021/acsnano.7b08969. Epub 2018 Mar 23.

Abstract

Adaptable hydrogel networks with reversible connectivity have emerged as a promising platform for biomedical applications. Synthetic copolymers and low-molecular-weight gelators (LMWG) have been shown to form reversible hydrogels through self-assembly of the molecules driven by self-complementary hydrophobic interaction and hydrogen bonding. Here, inspired by the adhesive proteins secreted by mussels, we found that simply adding natural polyphenols, such as epigallocatechin gallate (EGCG) to amyloid fibrils present in the nematic phase, successfully drives the formation of hydrogels through self-assembly of the hybrid supramolecules. The hydrogels show birefringence under polarized light, indicating that the nematic orientation is preserved in the gel phase. Gel stiffness enhances with incubation time and with an increase in molecular ratios between polyphenol and fibrils, fibril concentration, and pH. The hydrogels are shear thinning and thermostable from 25 to 90 °C without any phase transition. The integrity of the trihydroxyl groups, the gallate ester moiety in EGCG, and the hydrophobicity of the polyphenols govern the interactions with the amyloid fibrils and thus the properties of the ensuing hydrogels. The EGCG-binding amyloid fibrils, produced from lysozyme and peptidoglycans, retain the main binding functions of the enzyme, inducing bacterial agglomeration and immobilization on both Gram-positive and Gram-negative bacteria. Furthermore, the antibacterial mechanism of the lysozyme amyloid fibril hydrogels is initiated by membrane disintegration. In combination with the lack of cytotoxicity to human colonic epithelial cells demonstrated for these hybrid supramolecules, a potential role in combating multidrug-resistant bacteria in biomedical applications is suggested, such as in targeting diseases related to infection of the small intestine.

Keywords: amyloid fibrils; antibacterial activity; polyphenols; reversible hydrogels; self-assembly.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid / chemistry
  • Amyloid / metabolism*
  • Anti-Bacterial Agents / chemical synthesis
  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / pharmacology*
  • Cell Line
  • Gram-Negative Bacteria / drug effects*
  • Gram-Positive Bacteria / drug effects*
  • Humans
  • Hydrogels / chemical synthesis
  • Hydrogels / chemistry
  • Hydrogels / pharmacology*
  • Microbial Sensitivity Tests
  • Molecular Structure
  • Polyphenols / chemistry
  • Polyphenols / pharmacology*

Substances

  • Amyloid
  • Anti-Bacterial Agents
  • Hydrogels
  • Polyphenols