TDP-43 proteinopathy in ALS is triggered by loss of ASRGL1 and associated with HML-2 expression

Nat Commun. 2024 May 16;15(1):4163. doi: 10.1038/s41467-024-48488-7.

Abstract

TAR DNA-binding protein 43 (TDP-43) proteinopathy in brain cells is the hallmark of amyotrophic lateral sclerosis (ALS) but its cause remains elusive. Asparaginase-like-1 protein (ASRGL1) cleaves isoaspartates, which alter protein folding and susceptibility to proteolysis. ASRGL1 gene harbors a copy of the human endogenous retrovirus HML-2, whose overexpression contributes to ALS pathogenesis. Here we show that ASRGL1 expression was diminished in ALS brain samples by RNA sequencing, immunohistochemistry, and western blotting. TDP-43 and ASRGL1 colocalized in neurons but, in the absence of ASRGL1, TDP-43 aggregated in the cytoplasm. TDP-43 was found to be prone to isoaspartate formation and a substrate for ASRGL1. ASRGL1 silencing triggered accumulation of misfolded, fragmented, phosphorylated and mislocalized TDP-43 in cultured neurons and motor cortex of female mice. Overexpression of ASRGL1 restored neuronal viability. Overexpression of HML-2 led to ASRGL1 silencing. Loss of ASRGL1 leading to TDP-43 aggregation may be a critical mechanism in ALS pathophysiology.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / genetics
  • Amyotrophic Lateral Sclerosis* / metabolism
  • Amyotrophic Lateral Sclerosis* / pathology
  • Animals
  • Asparaginase* / genetics
  • Asparaginase* / metabolism
  • Autoantigens / genetics
  • Autoantigens / metabolism
  • Brain / metabolism
  • Brain / pathology
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Endogenous Retroviruses / genetics
  • Endogenous Retroviruses / metabolism
  • Female
  • Humans
  • Male
  • Mice
  • Motor Cortex / metabolism
  • Motor Cortex / pathology
  • Neurons* / metabolism
  • Neurons* / pathology
  • TDP-43 Proteinopathies* / genetics
  • TDP-43 Proteinopathies* / metabolism
  • TDP-43 Proteinopathies* / pathology

Substances

  • Asparaginase
  • ASRGL1 protein, human
  • Autoantigens
  • DNA-Binding Proteins
  • TARDBP protein, human