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Abnormal TDP-43 function impairs activity-dependent BDNF secretion, synaptic plasticity, and cognitive behavior

Jason Y Tann1,2, Lik-Wei Wong1,2, Sreedharan Sajikumar1,2

  • 1Department of Physiology, National University of Singapore, Singapore City, Singapore.

The EMBO Journal
|January 30, 2019
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Summary

Aberrant TDP-43 protein function impairs brain-derived neurotrophic factor (BDNF) secretion, a key factor in neurodegenerative diseases. Restoring BDNF function or Sortilin splicing alleviates memory and synaptic defects in mouse models.

Keywords:
LTPbrain‐derived neurotrophic factordendritic spineshippocampusprotein sorting

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Area of Science:

  • Neuroscience
  • Molecular Biology
  • Genetics

Background:

  • TDP-43 protein dysfunction is implicated in various neurodegenerative diseases.
  • The precise mechanisms linking TDP-43 malfunction to disease phenotypes remain incompletely understood.
  • TDP-43 regulates numerous cellular processes, complicating the identification of critical disease pathways.

Purpose of the Study:

  • To investigate the impact of TDP-43 dysfunction on neurotrophin secretion.
  • To elucidate the role of TDP-43 in the regulation of brain-derived neurotrophic factor (BDNF) trafficking and secretion.
  • To explore therapeutic strategies targeting TDP-43-mediated neurodegeneration.

Main Methods:

  • TDP-43 knockdown, aggregation, and mutation were induced in cellular and animal models.
  • Splicing of the Sortilin receptor was analyzed in relation to TDP-43 function.
  • Intracellular sorting and activity-dependent secretion of BDNF were measured.
  • Memory and synaptic plasticity were assessed in adult mice with conditional TDP-43 deficiency.
  • Human induced pluripotent stem cell (iPSC)-derived neurons from patients with mutated TDP-43 were utilized.

Main Results:

  • TDP-43 dysfunction impairs intracellular sorting and activity-dependent secretion of BDNF.
  • Altered splicing of the Sortilin receptor mediates the effect of TDP-43 on BDNF secretion.
  • Mice lacking TDP-43 in hippocampal CA1 neurons exhibit memory deficits and synaptic plasticity impairments.
  • These deficits in mice were ameliorated by restoring Sortilin splicing or BDNF levels.
  • Human neurons with mutated TDP-43 showed impaired BDNF secretion, which was reversible upon mutation correction.

Conclusions:

  • Aberrant TDP-43 function disrupts BDNF secretion via Sortilin splicing alterations.
  • TDP-43-mediated neurodegeneration may stem from the malfunction of critical proteins like BDNF.
  • Targeting Sortilin splicing or BDNF pathways offers potential therapeutic avenues for TDP-43 proteinopathies.