Amyloid nucleation and hierarchical assembly of Ure2p fibrils. Role of asparagine/glutamine repeat and nonrepeat regions of the prion domains

J Biol Chem. 2004 Jan 30;279(5):3361-9. doi: 10.1074/jbc.M310494200. Epub 2003 Nov 10.

Abstract

The yeast prion protein Ure2 forms amyloid-like filaments in vivo and in vitro. This ability depends on the N-terminal prion domain, which contains Asn/Gln repeats, a motif thought to cause human disease by forming stable protein aggregates. The Asn/Gln region of the Ure2p prion domain extends to residue 89, but residues 15-42 represent an island of "normal" random sequence, which is highly conserved in related species and is relatively hydrophobic. We compare the time course of structural changes monitored by thioflavin T (ThT) binding fluorescence and atomic force microscopy for Ure2 and a series of prion domain mutants under a range of conditions. Atomic force microscopy height images at successive time points during a single growth experiment showed the sequential appearance of at least four fibril types that could be readily differentiated by height (5, 8, 12, or 9 nm), morphology (twisted or smooth), and/or time of appearance (early or late in the plateau phase of ThT binding). The Ure2 dimer (h = 2.6 +/- 0.5 nm) and granular particles corresponding to higher order oligomers (h = 4-12 nm) could also be detected. The mutants 15Ure2 and Delta 15-42Ure2 showed the same time-dependent variation in fibril types but with an increased lag time detected by ThT binding compared with wild-type Ure2. In addition, Delta 15-42Ure2 showed reduced binding to ThT. The results imply a role of the conserved region in both amyloid nucleation and formation of the binding surface recognized by ThT. Further, Ure2 amyloid formation is a multistep process via a series of fibrillar intermediates.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Sequence
  • Amyloid / chemistry*
  • Amyloid / metabolism
  • Asparagine / chemistry
  • Benzothiazoles
  • Dimerization
  • Glutamine / chemistry
  • Glutathione Peroxidase
  • Hydrogen-Ion Concentration
  • Kinetics
  • Microscopy, Atomic Force
  • Molecular Sequence Data
  • Mutation
  • Prions / chemistry*
  • Prions / metabolism
  • Protein Binding
  • Protein Structure, Tertiary
  • Saccharomyces cerevisiae Proteins / chemistry*
  • Saccharomyces cerevisiae Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Thiazoles / chemistry
  • Time Factors

Substances

  • Amyloid
  • Benzothiazoles
  • Prions
  • Saccharomyces cerevisiae Proteins
  • Thiazoles
  • Glutamine
  • thioflavin T
  • Asparagine
  • Glutathione Peroxidase
  • URE2 protein, S cerevisiae