Synergistic effect between proteasome and autophagosome in the clearance of polyubiquitinated TDP-43

J Neurosci Res. 2010 Mar;88(4):784-97. doi: 10.1002/jnr.22243.

Abstract

Cytoplasmic aggregates of ubiquitinated TAR DNA-binding protein 43 (TDP-43) are a pathological hallmark of amyotrophic lateral sclerosis (ALS). However, the mechanism of TDP-43 polyubiquitination remains elusive. We investigated the effect of nuclear exclusion of TDP-43 on aggregate formation and fragmentation, using TDP-43 expression constructs for WT or mutant TDP-43 with a modified nuclear localizing signal (LQ-NLS). Overexpression of the LQ-NLS mutant alone induced no detectable cytoplasmic aggregates during a 72-hr period. Polyubiquitination of both WT TDP-43 and the LQ-NLS mutant was similar in total cell lysates exposed to the proteasome inhibitor lactacystin. However, analysis of subcellular fractions demonstrated a higher concentration of polyubiquitinated TDP-43 in the nuclear fraction than in the cytosol for WT, and vice versa for the LQ-NLS mutant. Polyubiquitin-charged WT and mutant TDP-43 were highly concentrated in the membrane/microsome fraction, which was also positive for the autophagosome marker LC3. In addition, the autophagy inhibitor 3-methyladenine (3MA) blocked degradation of both TDP-43 types, whereas lactacystin was minimally restorative. Furthermore, lactacystin plus 3MA induced prominent cytoplasmic aggregates. We also demonstrated mediation of TDP-43 polyubiquitination by lysine 48 of ubiquitin, indicating a degradation signal in both TDP-43 types. This is the first report delineating the distribution of polyubiquitinated TDP-43 and the degradation pathway of TDP-43 and clarifying the crucial role of autophagosomes in TDP-43 clearance. We also demonstrate that nuclear exclusion itself is not an immediate trigger for ALS pathology. Further clarification of the mechanism of polyubiquitination of TDP-43 and the role of autophagosomes may help in understanding and treating ALS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcysteine / analogs & derivatives
  • Acetylcysteine / pharmacology
  • Adenine / analogs & derivatives
  • Adenine / pharmacology
  • Analysis of Variance
  • Autophagy / physiology*
  • Cell Line, Tumor
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism
  • Cysteine Proteinase Inhibitors / pharmacology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Dose-Response Relationship, Drug
  • Drug Synergism
  • Green Fluorescent Proteins / genetics
  • Humans
  • Mutation / genetics
  • Neuroblastoma / pathology
  • Proteasome Endopeptidase Complex / genetics
  • Proteasome Endopeptidase Complex / metabolism*
  • Protein Transport / drug effects
  • Protein Transport / genetics
  • Subcellular Fractions / metabolism
  • Transfection / methods
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination / physiology*

Substances

  • Cysteine Proteinase Inhibitors
  • DNA-Binding Proteins
  • enhanced green fluorescent protein
  • lactacystin
  • Green Fluorescent Proteins
  • 3-methyladenine
  • Ubiquitin-Protein Ligases
  • Proteasome Endopeptidase Complex
  • Adenine
  • Acetylcysteine