Hypusination of Eif5a regulates cytoplasmic TDP-43 aggregation and accumulation in a stress-induced cellular model

Biochim Biophys Acta Mol Basis Dis. 2021 Jan 1;1867(1):165939. doi: 10.1016/j.bbadis.2020.165939. Epub 2020 Aug 31.

Abstract

TAR DNA-binding protein 43 (TDP-43) is a nuclear RNA/DNA binding protein involved in mRNA metabolism. Aberrant mislocalization to the cytoplasm and formation of phosphorylated/aggregated TDP-43 inclusions remains the hallmark pathology in a spectrum of neurodegenerative diseases, including frontotemporal disorders and Alzheimer's disease. Eukaryotic Translation Initiation Factor 5A undergoes a unique post-translation modification of lysine to hypusine (K50), which determines eIF5A binding partners. We used a sodium arsenite-induced cellular stress model to investigate the role of hypusinated eIF5A (eIF5AHypK50) in governing TDP-43 cytoplasmic mislocalization and accumulation in stress granule. Our proteomics and functional data provide evidence that eIF5A interacts with TDP-43 in a hypusine-dependent manner. Additionally, we showed that following stress TDP-43 interactions with eIF5AHypK50 were induced both in the cytoplasm and stress granules. Pharmacological reduction of hypusination or mutations of lysine residues within the hypusine loop decreased phosphorylated and insoluble TDP-43 levels. The proteomic and biochemical analysis also identified nuclear pore complex importins KPNA1/2, KPNB1, and RanGTP as interacting partners of eIF5AHypK50. These findings are the first to provide a novel pathway and potential therapeutic targets that require further investigation in models of TDP-43 proteinopathies.

Keywords: Cytoplasmic accumulation; Hypusination; Nuclear import; Proteinopathy; Stress granule; TDP-43; eIF5A.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / genetics
  • Alzheimer Disease / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Eukaryotic Translation Initiation Factor 5A
  • Frontotemporal Dementia / genetics
  • Frontotemporal Dementia / metabolism
  • HeLa Cells
  • Humans
  • Models, Biological*
  • Peptide Initiation Factors / genetics
  • Peptide Initiation Factors / metabolism*
  • Protein Modification, Translational*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Stress, Physiological*

Substances

  • DNA-Binding Proteins
  • Peptide Initiation Factors
  • RNA-Binding Proteins
  • TARDBP protein, human