Heparin binding confers prion stability and impairs its aggregation

FASEB J. 2014 Jun;28(6):2667-76. doi: 10.1096/fj.13-246777. Epub 2014 Mar 19.

Abstract

The conversion of the prion protein (PrP) into scrapie PrP (PrP(Sc)) is a central event in prion diseases. Several molecules work as cofactors in the conversion process, including glycosaminoglycans (GAGs). GAGs exhibit a paradoxical effect, as they convert PrP into protease-resistant PrP (PrP-res) but also exert protective activity. We compared the stability and aggregation propensity of PrP and the heparin-PrP complex through the application of different in vitro aggregation approaches, including real-time quaking-induced conversion (RT-QuIC). Transmissible spongiform encephalopathy-associated forms from mouse and hamster brain homogenates were used to seed RT-QuIC-induced fibrillization. In our study, interaction between heparin and cellular PrP (PrP(C)) increased thermal PrP stability, leading to an 8-fold decrease in temperature-induced aggregation. The interaction of low-molecular-weight heparin (LMWHep) with the PrP N- or C-terminal domain affected not only the extent of PrP fibrillization but also its kinetics, lowering the reaction rate constant from 1.04 to 0.29 s(-1) and increasing the lag phase from 12 to 19 h in RT-QuIC experiments. Our findings explain the protective effect of heparin in different models of prion and prion-like neurodegenerative diseases and establish the groundwork for the development of therapeutic strategies based on GAGs.

Keywords: glycosaminoglycan; neurodegeneration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid / biosynthesis
  • Animals
  • Cricetinae
  • Heparin
  • Heparin, Low-Molecular-Weight / metabolism*
  • Kinetics
  • Mice
  • PrPC Proteins / metabolism*
  • PrPSc Proteins / chemistry*
  • Prion Diseases / metabolism
  • Prions / metabolism*
  • Protein Binding
  • Protein Multimerization / drug effects*
  • Protein Stability / drug effects

Substances

  • Amyloid
  • Heparin, Low-Molecular-Weight
  • PrPC Proteins
  • PrPSc Proteins
  • Prions
  • Heparin