C9orf72 ALS/FTD dipeptide repeat protein levels are reduced by small molecules that inhibit PKA or enhance protein degradation

EMBO J. 2022 Jan 4;41(1):e105026. doi: 10.15252/embj.2020105026. Epub 2021 Nov 18.

Abstract

Intronic GGGGCC (G4C2) hexanucleotide repeat expansion within the human C9orf72 gene represents the most common cause of familial forms of amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD) (C9ALS/FTD). Repeat-associated non-AUG (RAN) translation of repeat-containing C9orf72 RNA results in the production of neurotoxic dipeptide-repeat proteins (DPRs). Here, we developed a high-throughput drug screen for the identification of positive and negative modulators of DPR levels. We found that HSP90 inhibitor geldanamycin and aldosterone antagonist spironolactone reduced DPR levels by promoting protein degradation via the proteasome and autophagy pathways respectively. Surprisingly, cAMP-elevating compounds boosting protein kinase A (PKA) activity increased DPR levels. Inhibition of PKA activity, by both pharmacological and genetic approaches, reduced DPR levels in cells and rescued pathological phenotypes in a Drosophila model of C9ALS/FTD. Moreover, knockdown of PKA-catalytic subunits correlated with reduced translation efficiency of DPRs, while the PKA inhibitor H89 reduced endogenous DPR levels in C9ALS/FTD patient-derived iPSC motor neurons. Together, our results suggest new and druggable pathways modulating DPR levels in C9ALS/FTD.

Keywords: C9orf72; C9ALS/FTD; DPR; PKA; protein clearance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • C9orf72 Protein / metabolism*
  • Cell Line
  • Codon, Initiator / genetics
  • Cyclic AMP-Dependent Protein Kinases / antagonists & inhibitors*
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • DNA Repeat Expansion / genetics
  • Dipeptides / metabolism*
  • Disease Models, Animal
  • Drosophila / drug effects
  • Frontotemporal Dementia / pathology
  • HEK293 Cells
  • High-Throughput Screening Assays
  • Humans
  • Induced Pluripotent Stem Cells / pathology
  • Isoquinolines / pharmacology
  • Longevity / drug effects
  • Motor Neurons / drug effects
  • Motor Neurons / pathology
  • Protein Biosynthesis / drug effects
  • Proteolysis* / drug effects
  • RNA Interference
  • Small Molecule Libraries / pharmacology*
  • Sulfonamides / pharmacology

Substances

  • C9orf72 Protein
  • Codon, Initiator
  • Dipeptides
  • Isoquinolines
  • Small Molecule Libraries
  • Sulfonamides
  • Cyclic AMP-Dependent Protein Kinases
  • N-(2-(4-bromocinnamylamino)ethyl)-5-isoquinolinesulfonamide