An invisible ubiquitin conformation is required for efficient phosphorylation by PINK1

EMBO J. 2017 Dec 15;36(24):3555-3572. doi: 10.15252/embj.201797876. Epub 2017 Nov 13.

Abstract

The Ser/Thr protein kinase PINK1 phosphorylates the well-folded, globular protein ubiquitin (Ub) at a relatively protected site, Ser65. We previously showed that Ser65 phosphorylation results in a conformational change in which Ub adopts a dynamic equilibrium between the known, common Ub conformation and a distinct, second conformation wherein the last β-strand is retracted to extend the Ser65 loop and shorten the C-terminal tail. We show using chemical exchange saturation transfer (CEST) nuclear magnetic resonance experiments that a similar, C-terminally retracted (Ub-CR) conformation also exists at low population in wild-type Ub. Point mutations in the moving β5 and neighbouring β-strands shift the Ub/Ub-CR equilibrium. This enabled functional studies of the two states, and we show that while the Ub-CR conformation is defective for conjugation, it demonstrates improved binding to PINK1 through its extended Ser65 loop, and is a superior PINK1 substrate. Together our data suggest that PINK1 utilises a lowly populated yet more suitable Ub-CR conformation of Ub for efficient phosphorylation. Our findings could be relevant for many kinases that phosphorylate residues in folded protein domains.

Keywords: PINK1; Parkin; Parkinson's disease; nuclear magnetic resonance; ubiquitin phosphorylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Crystallization
  • Humans
  • Magnetic Resonance Spectroscopy
  • Models, Molecular
  • Models, Structural
  • Molecular Conformation
  • Phosphorylation
  • Point Mutation
  • Protein Domains
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Protein Stability
  • Substrate Specificity
  • Ubiquitin / chemistry
  • Ubiquitin / genetics
  • Ubiquitin / metabolism*

Substances

  • Ubiquitin
  • Protein Kinases
  • PTEN-induced putative kinase