Stress-Induced Low Complexity RNA Activates Physiological Amyloidogenesis

Cell Rep. 2018 Aug 14;24(7):1713-1721.e4. doi: 10.1016/j.celrep.2018.07.040.

Abstract

Amyloid bodies (A-bodies) are inducible membrane-less nuclear compartments composed of heterogeneous proteins that adopt an amyloid-like state. A-bodies are seeded by noncoding RNA derived from stimuli-specific loci of the rDNA intergenic spacer (rIGSRNA). This raises the question of how rIGSRNA recruits a large population of diverse proteins to confer A-body identity. Here, we show that long low-complexity dinucleotide repeats operate as the architectural determinants of rIGSRNA. On stimulus, clusters of rIGSRNA with simple cytosine/uracil (CU) or adenosine/guanine (AG) repeats spanning hundreds of nucleotides accumulate in the nucleolar area. The low-complexity sequences facilitate charge-based interactions with short cationic peptides to produce multiple nucleolar liquid-like foci. Local concentration of proteins with fibrillation propensity in these nucleolar foci induces the formation of an amyloidogenic liquid phase that seeds A-bodies. These results demonstrate the physiological importance of low-complexity RNA and repetitive regions of the genome often dismissed as "junk" DNA.

Keywords: amyloidogenesis; architectural RNA; beta-amyloid; complex coacervation; junk DNA; liquid-to-solid phase transition; lncRNA; nucleolus; phase separation; rDNA intergenic spacer.

Publication types

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

MeSH terms

  • Amyloid / chemistry
  • Amyloid / genetics
  • Amyloid / metabolism
  • Amyloidogenic Proteins / chemistry*
  • Amyloidogenic Proteins / genetics
  • Amyloidogenic Proteins / metabolism
  • Animals
  • Base Sequence
  • Cell Hypoxia
  • Cell Nucleolus / genetics*
  • Cell Nucleolus / metabolism
  • Cell Nucleolus / ultrastructure
  • DNA, Intergenic / chemistry*
  • DNA, Intergenic / genetics
  • DNA, Intergenic / metabolism
  • DNA, Ribosomal / chemistry*
  • DNA, Ribosomal / genetics
  • DNA, Ribosomal / metabolism
  • Dinucleotide Repeats
  • Gene Expression
  • Heat-Shock Response
  • Humans
  • Hydrogen-Ion Concentration
  • MCF-7 Cells
  • Mice
  • Phase Transition
  • RNA, Ribosomal / chemistry*
  • RNA, Ribosomal / genetics
  • RNA, Ribosomal / metabolism
  • RNA, Untranslated / chemistry*
  • RNA, Untranslated / genetics
  • RNA, Untranslated / metabolism
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Static Electricity
  • Stress, Physiological
  • Time-Lapse Imaging

Substances

  • Amyloid
  • Amyloidogenic Proteins
  • DNA, Intergenic
  • DNA, Ribosomal
  • RNA, Ribosomal
  • RNA, Untranslated
  • Recombinant Fusion Proteins