Dimerization of the cellular prion protein inhibits propagation of scrapie prions

J Biol Chem. 2018 May 25;293(21):8020-8031. doi: 10.1074/jbc.RA117.000990. Epub 2018 Apr 10.

Abstract

A central step in the pathogenesis of prion diseases is the conformational transition of the cellular prion protein (PrPC) into the scrapie isoform, denoted PrPSc Studies in transgenic mice have indicated that this conversion requires a direct interaction between PrPC and PrPSc; however, insights into the underlying mechanisms are still missing. Interestingly, only a subfraction of PrPC is converted in scrapie-infected cells, suggesting that not all PrPC species are suitable substrates for the conversion. On the basis of the observation that PrPC can form homodimers under physiological conditions with the internal hydrophobic domain (HD) serving as a putative dimerization domain, we wondered whether PrP dimerization is involved in the formation of neurotoxic and/or infectious PrP conformers. Here, we analyzed the possible impact on dimerization of pathogenic mutations in the HD that induce a spontaneous neurodegenerative disease in transgenic mice. Similarly to wildtype (WT) PrPC, the neurotoxic variant PrP(AV3) formed homodimers as well as heterodimers with WTPrPC Notably, forced PrP dimerization via an intermolecular disulfide bond did not interfere with its maturation and intracellular trafficking. Covalently linked PrP dimers were complex glycosylated, GPI-anchored, and sorted to the outer leaflet of the plasma membrane. However, forced PrPC dimerization completely blocked its conversion into PrPSc in chronically scrapie-infected mouse neuroblastoma cells. Moreover, PrPC dimers had a dominant-negative inhibition effect on the conversion of monomeric PrPC Our findings suggest that PrPC monomers are the major substrates for PrPSc propagation and that it may be possible to halt prion formation by stabilizing PrPC dimers.

Keywords: Creutzfeldt-Jakob disease; GPI anchor; PrPC, amyloid plaque; amyloid; dimerization; glycosylphosphatidylinositol; neurodegenerative disease; neurological disease; prion disease; scrapie; trafficking.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • HeLa Cells
  • Humans
  • Mice
  • Mice, Transgenic
  • Neuroblastoma / pathology
  • Neuroblastoma / prevention & control*
  • Prion Proteins / chemistry*
  • Prion Proteins / metabolism*
  • Protein Multimerization*
  • Protein Transport
  • Scrapie / pathology
  • Scrapie / prevention & control*
  • Tumor Cells, Cultured

Substances

  • Prion Proteins