Short-term suppression of A315T mutant human TDP-43 expression improves functional deficits in a novel inducible transgenic mouse model of FTLD-TDP and ALS

Acta Neuropathol. 2015 Nov;130(5):661-78. doi: 10.1007/s00401-015-1486-0. Epub 2015 Oct 5.

Abstract

The nuclear transactive response DNA-binding protein 43 (TDP-43) undergoes relocalization to the cytoplasm with formation of cytoplasmic deposits in neurons in amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD). Pathogenic mutations in the TDP-43-encoding TARDBP gene in familial ALS as well as non-mutant human TDP-43 have been utilized to model FTD/ALS in cell culture and animals, including mice. Here, we report novel A315T mutant TDP-43 transgenic mice, iTDP-43(A315T), with controlled neuronal over-expression. Constitutive expression of human TDP-43(A315T) resulted in pronounced early-onset and progressive neurodegeneration, which was associated with compromised motor performance, spatial memory and disinhibition. Muscle atrophy resulted in reduced grip strength. Cortical degeneration presented with pronounced astrocyte activation. Using differential protein extraction from iTDP-43(A315T) brains, we found cytoplasmic localization, fragmentation, phosphorylation and ubiquitination and insolubility of TDP-43. Surprisingly, suppression of human TDP-43(A315T) expression in mice with overt neurodegeneration for only 1 week was sufficient to significantly improve motor and behavioral deficits, and reduce astrogliosis. Our data suggest that functional deficits in iTDP-43(A315T) mice are at least in part a direct and transient effect of the presence of TDP-43(A315T). Furthermore, it illustrates the compensatory capacity of compromised neurons once transgenic TDP-43 is removed, with implications for future treatments.

Keywords: Amyotrophic lateral sclerosis; Frontotemporal lobar degeneration; Mouse model; Pathogenic mutation; TDP-43.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / pathology
  • Amyotrophic Lateral Sclerosis / physiopathology*
  • Animals
  • Astrocytes / pathology
  • Astrocytes / physiology
  • Brain / pathology
  • Brain / physiopathology
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism*
  • Disease Models, Animal
  • Doxycycline
  • Female
  • Frontotemporal Lobar Degeneration / genetics
  • Frontotemporal Lobar Degeneration / pathology
  • Frontotemporal Lobar Degeneration / physiopathology*
  • Gliosis / pathology
  • Gliosis / physiopathology
  • Hand Strength / physiology
  • Humans
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Motor Activity / physiology
  • Mutation*
  • Neurons / metabolism
  • Neurons / pathology
  • Recovery of Function / physiology*
  • Spatial Memory / physiology

Substances

  • DNA-Binding Proteins
  • TARDBP protein, human
  • Doxycycline