PARIS undergoes liquid-liquid phase separation and poly(ADP-ribose)-mediated solidification

EMBO Rep. 2023 Nov 6;24(11):e56166. doi: 10.15252/embr.202256166. Epub 2023 Oct 23.

Abstract

ZNF746 was identified as parkin-interacting substrate (PARIS). Investigating its pathophysiological properties, we find that PARIS undergoes liquid-liquid phase separation (LLPS) and amorphous solid formation. The N-terminal low complexity domain 1 (LCD1) of PARIS is required for LLPS, whereas the C-terminal prion-like domain (PrLD) drives the transition from liquid to solid phase. In addition, we observe that poly(ADP-ribose) (PAR) strongly binds to the C-terminus of PARIS near the PrLD, accelerating its LLPS and solidification. N-Methyl-N'-nitro-N-nitrosoguanidine (MNNG)-induced PAR formation leads to PARIS oligomerization in human iPSC-derived dopaminergic neurons that is prevented by the PARP inhibitor, ABT-888. Furthermore, SDS-resistant PARIS species are observed in the substantia nigra (SN) of aged mice overexpressing wild-type PARIS, but not with a PAR binding-deficient PARIS mutant. PARIS solidification is also found in the SN of mice injected with preformed fibrils of α-synuclein (α-syn PFF) and adult mice with a conditional knockout (KO) of parkin, but not if α-syn PFF is injected into mice deficient for PARP1. Herein, we demonstrate that PARIS undergoes LLPS and PAR-mediated solidification in models of Parkinson's disease.

Keywords: liquid-liquid phase separation; low complexity domain; parkin-interacting substrate; poly(ADP-ribose); protein solidification.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Dopaminergic Neurons / metabolism
  • Humans
  • Mice
  • Parkinson Disease* / metabolism
  • Poly Adenosine Diphosphate Ribose* / metabolism
  • Poly(ADP-ribose) Polymerase Inhibitors / pharmacology
  • Repressor Proteins / metabolism
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Poly Adenosine Diphosphate Ribose
  • Poly(ADP-ribose) Polymerase Inhibitors
  • Repressor Proteins
  • Ubiquitin-Protein Ligases
  • ZNF746 protein, human
  • ZNF746 protein, mouse