Casein kinase II induced polymerization of soluble TDP-43 into filaments is inhibited by heat shock proteins

PLoS One. 2014 Mar 4;9(3):e90452. doi: 10.1371/journal.pone.0090452. eCollection 2014.

Abstract

Background: Trans-activation Response DNA-binding Protein-43 (TDP-43) lesions are observed in Amyotrophic Lateral Sclerosis (ALS), Frontotemporal Lobar Degeneration with ubiquitin inclusions (FTLD-TDP) and 25-50% of Alzheimer's Disease (AD) cases. These abnormal protein inclusions are composed of either amorphous TDP-43 aggregates or highly ordered filaments. The filamentous TDP-43 accumulations typically contain clean 10-12 nm filaments though wider 18-20 nm coated filaments may be observed. The TDP-43 present within these lesions is phosphorylated, truncated and ubiquitinated, and these modifications appear to be abnormal as they are linked to both a cellular heat shock response and microglial activation. The mechanisms associated with this abnormal TDP-43 accumulation are believed to result in a loss of TDP-43 function, perhaps due to the post-translational modifications or resulting from physical sequestration of the TDP-43. The formation of TDP-43 inclusions involves cellular translocation and conversion of TDP-43 into fibrillogenic forms, but the ability of these accumulations to sequester normal TDP-43 and propagate this behavior between neurons pathologically is mostly inferred. The lack of methodology to produce soluble full length TDP-43 and recapitulate this polymerization into filaments as observed in disease has limited our understanding of these pathogenic cascades.

Results: The protocols described here generate soluble, full-length and untagged TDP-43 allowing for a direct assessment of the impact of various posttranslational modifications on TDP-43 function. We demonstrate that Casein Kinase II (CKII) promotes the polymerization of this soluble TDP-43 into 10 nm diameter filaments that resemble the most common TDP-43 structures observed in disease. Furthermore, these filaments are recognized as abnormal by Heat Shock Proteins (HSPs) which can inhibit TDP-43 polymerization or directly promote TDP-43 filament depolymerization.

Conclusion: These findings demonstrate CKII induces polymerization of soluble TDP-43 into filaments and Hsp90 promotes TDP-43 filament depolymerization. These findings provide rational for potential therapeutic intervention at these points in TDP-43 proteinopathies.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Casein Kinase II / pharmacology*
  • DNA-Binding Proteins / chemistry*
  • DNA-Binding Proteins / isolation & purification
  • DNA-Binding Proteins / metabolism*
  • Frontotemporal Lobar Degeneration / metabolism
  • Frontotemporal Lobar Degeneration / pathology
  • HSP90 Heat-Shock Proteins / metabolism*
  • Humans
  • Inclusion Bodies / drug effects
  • Inclusion Bodies / metabolism
  • Inclusion Bodies / ultrastructure
  • Mice
  • Phosphorylation / drug effects
  • Polymerization / drug effects*
  • Protein Aggregation, Pathological / metabolism
  • Reproducibility of Results
  • Solubility

Substances

  • DNA-Binding Proteins
  • HSP90 Heat-Shock Proteins
  • Casein Kinase II