Dual roles for ATP in the regulation of phase separated protein aggregates in Xenopus oocyte nucleoli

Elife. 2018 Jul 17:7:e35224. doi: 10.7554/eLife.35224.

Abstract

For many proteins, aggregation is one part of a structural equilibrium that can occur. Balancing productive aggregation versus pathogenic aggregation that leads to toxicity is critical and known to involve adenosine triphosphate (ATP) dependent action of chaperones and disaggregases. Recently a second activity of ATP was identified, that of a hydrotrope which, independent of hydrolysis, was sufficient to solubilize aggregated proteins in vitro. This novel function of ATP was postulated to help regulate proteostasis in vivo. We tested this hypothesis on aggregates found in Xenopus oocyte nucleoli. Our results indicate that ATP has dual roles in the maintenance of protein solubility. We provide evidence of endogenous hydrotropic action of ATP but show that hydrotropic solubilization of nucleolar aggregates is preceded by a destabilizing event. Destabilization is accomplished through an energy dependent process, reliant upon ATP and one or more soluble nuclear factors, or by disruption of a co-aggregate like RNA.

Keywords: ATP; cell biology; developmental biology; nucleolus; nucleus; oocyte; protein aggregation; xenopus.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Adenylyl Imidodiphosphate / pharmacology
  • Animals
  • Cell Nucleolus / drug effects
  • Cell Nucleolus / metabolism*
  • Diffusion
  • Green Fluorescent Proteins / metabolism
  • Guanosine Triphosphate / pharmacology
  • Hydrolysis
  • Models, Biological
  • Oocytes / drug effects
  • Oocytes / metabolism*
  • Protein Aggregates*
  • Ribonuclease, Pancreatic / metabolism
  • Solubility
  • Xenopus laevis / metabolism*

Substances

  • Protein Aggregates
  • Green Fluorescent Proteins
  • Adenylyl Imidodiphosphate
  • Guanosine Triphosphate
  • Adenosine Triphosphate
  • Ribonuclease, Pancreatic