Dysregulation of stress granule dynamics by DCTN1 deficiency exacerbates TDP-43 pathology in Drosophila models of ALS/FTD

Acta Neuropathol Commun. 2024 Feb 4;12(1):20. doi: 10.1186/s40478-024-01729-8.

Abstract

The abnormal aggregation of TDP-43 into cytoplasmic inclusions in affected neurons is a major pathological hallmark of amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD). Although TDP-43 is aberrantly accumulated in the neurons of most patients with sporadic ALS/FTD and other TDP-43 proteinopathies, how TDP-43 forms cytoplasmic aggregates remains unknown. In this study, we show that a deficiency in DCTN1, a subunit of the microtubule-associated motor protein complex dynactin, perturbs the dynamics of stress granules and drives the formation of TDP-43 cytoplasmic aggregation in cultured cells, leading to the exacerbation of TDP-43 pathology and neurodegeneration in vivo. We demonstrated using a Drosophila model of ALS/FTD that genetic knockdown of DCTN1 accelerates the formation of ubiquitin-positive cytoplasmic inclusions of TDP-43. Knockdown of components of other microtubule-associated motor protein complexes, including dynein and kinesin, also increased the formation of TDP-43 inclusions, indicating that intracellular transport along microtubules plays a key role in TDP-43 pathology. Notably, DCTN1 knockdown delayed the disassembly of stress granules in stressed cells, leading to an increase in the formation of pathological cytoplasmic inclusions of TDP-43. Our results indicate that a deficiency in DCTN1, as well as disruption of intracellular transport along microtubules, is a modifier that drives the formation of TDP-43 pathology through the dysregulation of stress granule dynamics.

Keywords: Aggregation; DCTN1; Microtubule-dependent transport; Stress granule; TDP-43.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / pathology
  • Animals
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Drosophila / metabolism
  • Drosophila Proteins* / genetics
  • Dynactin Complex* / genetics
  • Frontotemporal Dementia* / pathology
  • Humans
  • Stress Granules

Substances

  • DNA-Binding Proteins
  • Dynactin Complex
  • TBPH protein, Drosophila
  • Drosophila Proteins