NLS-binding deficient Kapβ2 reduces neurotoxicity via selective interaction with C9orf72-ALS/FTD dipeptide repeats

Commun Biol. 2025 Jan 2;8(1):2. doi: 10.1038/s42003-024-07412-x.

Abstract

Arginine-rich dipeptide repeat proteins (R-DPRs) are highly toxic proteins found in patients with C9orf72-linked amyotrophic lateral sclerosis and frontotemporal dementia (C9-ALS/FTD). R-DPRs can cause toxicity by disrupting the natural phase behavior of RNA-binding proteins (RBPs). Mitigating this abnormal phase behavior is, therefore, crucial to reduce R-DPR-induced toxicity. Here, we use FUS as a model RBP to investigate the mechanism of R-DPR-induced aberrant RBP phase transition. We find that this phase transition can be mitigated by Kapβ2. However, as a nuclear import receptor and phase modifier for PY-NLS-containing RBPs, the function of WT Kapβ2 could lead to undesired interaction with its native substrates when used as therapeutics for C9-ALS/FTD. To address this issue, it is crucial to devise effective strategies that allow Kapβ2 to selectively target its binding to the R-DPRs, instead of the RBPs. We show that NLS-binding deficient Kapβ2W460A:W730A can indeed selectively interact with R-DPRs in FUS assembly without affecting normal FUS phase separation. Importantly, Kapβ2W460A:W730A prevents enrichment of poly(GR) in stress granules and mitigates R-DPR neurotoxicity. Thus, NLS-binding deficient Kapβ2 may be implemented as a potential therapeutic for C9-ALS/FTD.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / genetics
  • Amyotrophic Lateral Sclerosis* / metabolism
  • C9orf72 Protein* / genetics
  • C9orf72 Protein* / metabolism
  • Dipeptides* / metabolism
  • Frontotemporal Dementia* / genetics
  • Frontotemporal Dementia* / metabolism
  • HEK293 Cells
  • Humans
  • Protein Binding
  • RNA-Binding Protein FUS / genetics
  • RNA-Binding Protein FUS / metabolism
  • beta Karyopherins / genetics
  • beta Karyopherins / metabolism

Substances

  • C9orf72 Protein
  • Dipeptides
  • C9orf72 protein, human
  • beta Karyopherins
  • RNA-Binding Protein FUS
  • FUS protein, human