An evolutionarily conserved mechanism controls reversible amyloids of pyruvate kinase via pH-sensing regions

Dev Cell. 2024 Jul 22;59(14):1876-1891.e7. doi: 10.1016/j.devcel.2024.04.018. Epub 2024 May 23.

Abstract

Amyloids are known as irreversible aggregates associated with neurodegenerative diseases. However, recent evidence shows that a subset of amyloids can form reversibly and fulfill essential cellular functions. Yet, the molecular mechanisms regulating functional amyloids and distinguishing them from pathological aggregates remain unclear. Here, we investigate the conserved principles of amyloid reversibility by studying the essential metabolic enzyme pyruvate kinase (PK) in yeast and human cells. We demonstrate that yeast PK (Cdc19) and human PK (PKM2) form reversible amyloids through a pH-sensitive amyloid core. Stress-induced cytosolic acidification promotes aggregation via protonation of specific glutamate (yeast) or histidine (human) residues within the amyloid core. Mutations mimicking protonation cause constitutive PK aggregation, while non-protonatable PK mutants remain soluble even upon stress. Physiological PK aggregation is coupled to metabolic rewiring and glycolysis arrest, causing severe growth defects when misregulated. Our work thus identifies an evolutionarily conserved, potentially widespread mechanism regulating functional amyloids during stress.

Keywords: aggregate disassembly; aggregate regulation; amyloid regulation; functional amyloids; isoforms; protein aggregation; pyruvate kinase; reversible amyloids; stress response; stress-induced pH changes.

MeSH terms

  • Amyloid* / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Glycolysis
  • Humans
  • Hydrogen-Ion Concentration
  • Mutation / genetics
  • Pyruvate Kinase* / genetics
  • Pyruvate Kinase* / metabolism
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Saccharomyces cerevisiae* / genetics
  • Saccharomyces cerevisiae* / metabolism

Substances

  • Pyruvate Kinase
  • Amyloid
  • Saccharomyces cerevisiae Proteins
  • Cell Cycle Proteins