Cofactors are essential constituents of stable and seeding-active tau fibrils

Proc Natl Acad Sci U S A. 2018 Dec 26;115(52):13234-13239. doi: 10.1073/pnas.1810058115. Epub 2018 Dec 11.

Abstract

Amyloid fibrils are cross-β-rich aggregates that are exceptionally stable forms of protein assembly. Accumulation of tau amyloid fibrils is involved in many neurodegenerative diseases, including Alzheimer's disease (AD). Heparin-induced aggregates have been widely used and assumed to be a good tau amyloid fibril model for most biophysical studies. Here we show that mature fibrils made of 4R tau variants, prepared with heparin or RNA, spontaneously depolymerize and release monomers when their cofactors are removed. We demonstrate that the cross-β-sheet assembly formed in vitro with polyanion addition is unstable at room temperature. We furthermore demonstrate high seeding capacity with transgenic AD mouse brain-extracted tau fibrils in vitro that, however, is exhausted after one generation, while supplementation with RNA cofactors resulted in sustained seeding over multiple generations. We suggest that tau fibrils formed in brains are supported by unknown cofactors and inhere higher-quality packing, as reflected in a more distinct conformational arrangement in the mouse fibril-seeded, compared with heparin-induced, tau fibrils. Our study suggests that the role of cofactors in tauopathies is a worthy focus of future studies, as they may be viable targets for diagnosis and therapeutics.

Keywords: DEER; aggregate cofactors; amyloid aggregates; seeding; tau.

Publication types

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

MeSH terms

  • Alzheimer Disease / metabolism
  • Alzheimer Disease / pathology*
  • Amyloid / chemistry*
  • Amyloid / metabolism
  • Animals
  • Brain / metabolism
  • Brain / pathology*
  • Heparin / chemistry*
  • Heparin / metabolism
  • Mice
  • Mice, Transgenic
  • Protein Conformation
  • RNA / chemistry*
  • RNA / metabolism
  • Recombinant Proteins / chemistry*
  • Recombinant Proteins / metabolism
  • tau Proteins / chemistry*
  • tau Proteins / metabolism

Substances

  • Amyloid
  • Recombinant Proteins
  • tau Proteins
  • RNA
  • Heparin