RuvBL1/2 reduce toxic dipeptide repeat protein burden in multiple models of C9orf72-ALS/FTD

Life Sci Alliance. 2024 Dec 5;8(2):e202402757. doi: 10.26508/lsa.202402757. Print 2025 Feb.

Abstract

A G4C2 hexanucleotide repeat expansion in C9orf72 is the most common cause of amyotrophic lateral sclerosis and frontotemporal dementia (C9ALS/FTD). Bidirectional transcription and subsequent repeat-associated non-AUG (RAN) translation of sense and antisense transcripts leads to the formation of five dipeptide repeat (DPR) proteins. These DPRs are toxic in a wide range of cell and animal models. Therefore, decreasing RAN-DPRs may be of therapeutic benefit in the context of C9ALS/FTD. In this study, we found that C9ALS/FTD patients have reduced expression of the AAA+ family members RuvBL1 and RuvBL2, which have both been implicated in aggregate clearance. We report that overexpression of RuvBL1, but to a greater extent RuvBL2, reduced C9orf72-associated DPRs in a range of in vitro systems including cell lines, primary neurons from the C9-500 transgenic mouse model, and patient-derived iPSC motor neurons. In vivo, we further demonstrated that RuvBL2 overexpression and consequent DPR reduction in our Drosophila model was sufficient to rescue a number of DPR-related motor phenotypes. Thus, modulating RuvBL levels to reduce DPRs may be of therapeutic potential in C9ALS/FTD.

MeSH terms

  • ATPases Associated with Diverse Cellular Activities* / genetics
  • ATPases Associated with Diverse Cellular Activities* / metabolism
  • Amyotrophic Lateral Sclerosis* / genetics
  • Amyotrophic Lateral Sclerosis* / metabolism
  • Animals
  • C9orf72 Protein* / genetics
  • C9orf72 Protein* / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • DNA Helicases* / genetics
  • DNA Helicases* / metabolism
  • DNA Repeat Expansion / genetics
  • Dipeptides* / metabolism
  • Disease Models, Animal*
  • Frontotemporal Dementia* / genetics
  • Frontotemporal Dementia* / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Male
  • Mice
  • Mice, Transgenic*
  • Motor Neurons / metabolism

Substances

  • C9orf72 Protein
  • Dipeptides
  • ATPases Associated with Diverse Cellular Activities
  • RUVBL2 protein, human
  • DNA Helicases
  • RUVBL1 protein, human
  • Carrier Proteins
  • C9orf72 protein, human