LRRK2 activation controls the repair of damaged endomembranes in macrophages

EMBO J. 2020 Sep 15;39(18):e104494. doi: 10.15252/embj.2020104494. Epub 2020 Jul 9.

Abstract

Cells respond to endolysosome damage by either repairing the damage or targeting damaged endolysosomes for degradation via lysophagy. However, the signals regulating the decision for repair or lysophagy are poorly characterised. Here, we show that the Parkinson's disease (PD)-related kinase LRRK2 is activated in macrophages by pathogen- or sterile-induced endomembrane damage. LRRK2 recruits the Rab GTPase Rab8A to damaged endolysosomes as well as the ESCRT-III component CHMP4B, thereby favouring ESCRT-mediated repair. Conversely, in the absence of LRRK2 and Rab8A, damaged endolysosomes are targeted to lysophagy. These observations are recapitulated in macrophages from PD patients where pathogenic LRRK2 gain-of-function mutations result in the accumulation of endolysosomes which are positive for the membrane damage marker Galectin-3. Altogether, this work indicates that LRRK2 regulates endolysosomal homeostasis by controlling the balance between membrane repair and organelle replacement, uncovering an unexpected function for LRRK2, and providing a new link between membrane damage and PD.

Keywords: LRRK2; Parkinson's disease; endolysosomal damage; lysosomes; tuberculosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Endosomal Sorting Complexes Required for Transport / genetics
  • Endosomal Sorting Complexes Required for Transport / metabolism
  • Endosomes / genetics
  • Endosomes / metabolism
  • Enzyme Activation / genetics
  • Humans
  • Intracellular Membranes / metabolism*
  • Leucine-Rich Repeat Serine-Threonine Protein Kinase-2 / genetics
  • Leucine-Rich Repeat Serine-Threonine Protein Kinase-2 / metabolism*
  • Lysosomes / genetics
  • Lysosomes / metabolism
  • Macrophages / metabolism*
  • Mice
  • Parkinson Disease / genetics
  • Parkinson Disease / metabolism
  • RAW 264.7 Cells
  • rab GTP-Binding Proteins / genetics
  • rab GTP-Binding Proteins / metabolism

Substances

  • Endosomal Sorting Complexes Required for Transport
  • Rab8a protein, mouse
  • LRRK2 protein, human
  • Leucine-Rich Repeat Serine-Threonine Protein Kinase-2
  • Lrrk2 protein, mouse
  • RAB8A protein, human
  • rab GTP-Binding Proteins