A Ubl/ubiquitin switch in the activation of Parkin

EMBO J. 2015 Oct 14;34(20):2492-505. doi: 10.15252/embj.201592237. Epub 2015 Aug 7.

Abstract

Mutations in Parkin and PINK1 cause an inherited early-onset form of Parkinson's disease. The two proteins function together in a mitochondrial quality control pathway whereby PINK1 accumulates on damaged mitochondria and activates Parkin to induce mitophagy. How PINK1 kinase activity releases the auto-inhibited ubiquitin ligase activity of Parkin remains unclear. Here, we identify a binding switch between phospho-ubiquitin (pUb) and the ubiquitin-like domain (Ubl) of Parkin as a key element. By mutagenesis and SAXS, we show that pUb binds to RING1 of Parkin at a site formed by His302 and Arg305. pUb binding promotes disengagement of the Ubl from RING1 and subsequent Parkin phosphorylation. A crystal structure of Parkin Δ86-130 at 2.54 Å resolution allowed the design of mutations that specifically release the Ubl domain from RING1. These mutations mimic pUb binding and promote Parkin phosphorylation. Measurements of the E2 ubiquitin-conjugating enzyme UbcH7 binding to Parkin and Parkin E3 ligase activity suggest that Parkin phosphorylation regulates E3 ligase activity downstream of pUb binding.

Keywords: Parkinson's disease; mitochondria; mitophagy; phosphorylation; ubiquitination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cloning, Molecular
  • Crystallization
  • Enzyme Activation / genetics*
  • Humans
  • Mitochondria / metabolism*
  • Models, Molecular*
  • Mutagenesis
  • Nuclear Magnetic Resonance, Biomolecular
  • Phosphorylation
  • Protein Binding
  • Protein Conformation
  • Protein Kinases / chemistry*
  • Protein Kinases / metabolism*
  • Protein Structure, Tertiary
  • Scattering, Small Angle
  • Ubiquitin / metabolism
  • Ubiquitin-Conjugating Enzymes / metabolism
  • Ubiquitin-Protein Ligases / chemistry*
  • Ubiquitin-Protein Ligases / metabolism*

Substances

  • Ubiquitin
  • UBE2L3 protein, human
  • Ubiquitin-Conjugating Enzymes
  • Ubiquitin-Protein Ligases
  • parkin protein
  • Protein Kinases
  • PTEN-induced putative kinase