β2-adrenergic Agonists Rescue Lysosome Acidification and Function in PSEN1 Deficiency by Reversing Defective ER-to-lysosome Delivery of ClC-7

J Mol Biol. 2020 Apr 3;432(8):2633-2650. doi: 10.1016/j.jmb.2020.02.021. Epub 2020 Feb 24.

Abstract

Lysosomal dysfunction is considered pathogenic in Alzheimer disease (AD). Loss of presenilin-1 (PSEN1) function causing AD impedes acidification via defective vacuolar ATPase (vATPase) V0a1 subunit delivery to lysosomes. We report that isoproterenol (ISO) and related β2-adrenergic agonists reacidify lysosomes in PSEN1 Knock out (KO) cells and fibroblasts from PSEN1 familial AD patients, which restores lysosomal proteolysis, calcium homeostasis, and normal autophagy flux. We identify a novel rescue mechanism involving Portein Kinase A (PKA)-mediated facilitation of chloride channel-7 (ClC-7) delivery to lysosomes which reverses markedly lowered chloride (Cl-) content in PSEN1 KO lysosomes. Notably, PSEN1 loss of function impedes Endoplasmic Reticulum (ER)-to-lysosome delivery of ClC-7. Transcriptomics of PSEN1-deficient cells reveals strongly downregulated ER-to-lysosome transport pathways and reversibility by ISO, thus accounting for lysosomal Cl- deficits that compound pH elevation due to deficient vATPase and its rescue by β2-adrenergic agonists. Our findings uncover a broadened PSEN1 role in lysosomal ion homeostasis and novel pH modulation of lysosomes through β2-adrenergic regulation of ClC-7, which can potentially be modulated therapeutically.

Keywords: PKA; RNA-seq; acidification; chloride; lysosome.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adrenergic beta-2 Receptor Agonists / pharmacology*
  • Alzheimer Disease / drug therapy
  • Alzheimer Disease / genetics
  • Alzheimer Disease / pathology
  • Animals
  • Calcium / metabolism
  • Chloride Channels / metabolism*
  • Chlorides / metabolism
  • Endoplasmic Reticulum / drug effects*
  • Endoplasmic Reticulum / metabolism
  • Fibroblasts / drug effects*
  • Fibroblasts / metabolism
  • Humans
  • Hydrogen-Ion Concentration
  • Lysosomes / drug effects*
  • Lysosomes / metabolism
  • Mice
  • Mice, Knockout
  • Mutation*
  • Presenilin-1 / genetics
  • Presenilin-1 / physiology*
  • Receptors, Adrenergic, beta-2 / chemistry

Substances

  • Adrenergic beta-2 Receptor Agonists
  • Chloride Channels
  • Chlorides
  • Clcn7 protein, mouse
  • PSEN1 protein, human
  • Presenilin-1
  • Receptors, Adrenergic, beta-2
  • presenilin 1, mouse
  • Calcium