Traumatic injury compromises nucleocytoplasmic transport and leads to TDP-43 pathology

Elife. 2021 May 26:10:e67587. doi: 10.7554/eLife.67587.

Abstract

Traumatic brain injury (TBI) is a predisposing factor for many neurodegenerative diseases, including amyotrophic lateral sclerosis (ALS), Alzheimer's disease (AD), Parkinson's disease (PD), and chronic traumatic encephalopathy (CTE). Although defects in nucleocytoplasmic transport (NCT) is reported ALS and other neurodegenerative diseases, whether defects in NCT occur in TBI remains unknown. We performed proteomic analysis on Drosophila exposed to repeated TBI and identified resultant alterations in several novel molecular pathways. TBI upregulated nuclear pore complex (NPC) and nucleocytoplasmic transport (NCT) proteins as well as alter nucleoporin stability. Traumatic injury disrupted RanGAP1 and NPC protein distribution in flies and a rat model and led to coaggregation of NPC components and TDP-43. In addition, trauma-mediated NCT defects and lethality are rescued by nuclear export inhibitors. Importantly, genetic upregulation of nucleoporins in vivo and in vitro triggered TDP-43 cytoplasmic mislocalization, aggregation, and altered solubility and reduced motor function and lifespan of animals. We also found NUP62 pathology and elevated NUP62 concentrations in postmortem brain tissues of patients with mild or severe CTE as well as co-localization of NUP62 and TDP-43 in CTE. These findings indicate that TBI leads to NCT defects, which potentially mediate the TDP-43 pathology in CTE.

Keywords: D. melanogaster; TDP-43; amyotrophic lateral sclerosis; chronic traumatic encephalopathy; genetics; genomics; human; neurodegeneration; neuroscience; rat.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus*
  • Animals
  • Animals, Genetically Modified
  • Brain / metabolism*
  • Brain / pathology
  • Brain Injuries, Traumatic / genetics
  • Brain Injuries, Traumatic / metabolism*
  • Brain Injuries, Traumatic / pathology
  • Case-Control Studies
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Disease Models, Animal
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • GTPase-Activating Proteins / genetics
  • GTPase-Activating Proteins / metabolism
  • HEK293 Cells
  • Humans
  • Longevity
  • Male
  • Membrane Glycoproteins / metabolism
  • Motor Activity
  • Nuclear Pore / genetics
  • Nuclear Pore / metabolism*
  • Nuclear Pore / pathology
  • Nuclear Pore Complex Proteins / metabolism
  • Protein Aggregates
  • Protein Aggregation, Pathological
  • Rats
  • Rats, Sprague-Dawley
  • TDP-43 Proteinopathies / genetics
  • TDP-43 Proteinopathies / metabolism*
  • TDP-43 Proteinopathies / pathology

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • GTPase-Activating Proteins
  • Membrane Glycoproteins
  • Nuclear Pore Complex Proteins
  • Nup214 protein, Drosophila
  • Protein Aggregates
  • RanGAP protein, Drosophila
  • TARDBP protein, human
  • TBPH protein, Drosophila
  • Tardbp protein, rat
  • nuclear pore protein p62