RNA-binding deficient TDP-43 drives cognitive decline in a mouse model of TDP-43 proteinopathy

Abstract

TDP-43 proteinopathies including frontotemporal lobar degeneration (FTLD) and amyotrophic lateral sclerosis (ALS) are neurodegenerative disorders characterized by aggregation and mislocalization of the nucleic acid-binding protein TDP-43 and subsequent neuronal dysfunction. Here, we developed endogenous models of sporadic TDP-43 proteinopathy based on the principle that disease-associated TDP-43 acetylation at lysine 145 (K145) alters TDP-43 conformation, impairs RNA-binding capacity, and induces downstream mis-regulation of target genes. Expression of acetylation-mimic TDP-43K145Q resulted in stress-induced nuclear TDP-43 foci and loss of TDP-43 function in primary mouse and human-induced pluripotent stem cell (hiPSC)-derived cortical neurons. Mice harboring the TDP-43K145Q mutation recapitulated key hallmarks of FTLD, including progressive TDP-43 phosphorylation and insolubility, TDP-43 mis-localization, transcriptomic and splicing alterations, and cognitive dysfunction. Our study supports a model in which TDP-43 acetylation drives neuronal dysfunction and cognitive decline through aberrant splicing and transcription of critical genes that regulate synaptic plasticity and stress response signaling. The neurodegenerative cascade initiated by TDP-43 acetylation recapitulates many aspects of human FTLD and provides a new paradigm to further interrogate TDP-43 proteinopathies.

Document Details

Document Type
Pub Defense Publication
Publication Date
Oct 11, 2023
Source ID
10.7554/elife.85921.3

Entities

People

  • Adriana S Beltran
  • Ariana B Marquez
  • Baggio A Evangelista
  • Deepa Ajit
  • Feng-chang Lin
  • Huijun Jiang
  • J Ashley Ezzell
  • Jeremy M Simon
  • Julie Necarsulmer
  • Kathryn M Harper
  • Ping Wang
  • Sara Nafees
  • Sheryl S. Moy
  • Todd J Cohen
  • Viktoriya D. Nikolova
  • Xu Tian
  • Youjun Chen

Organizations

  • Eunice Kennedy Shriver National Institute of Child Health and Human Development
  • Muscular Dystrophy Association
  • National Center for Advancing Translational Sciences
  • National Institute of General Medical Sciences
  • National Institute of Neurological Disorders and Stroke
  • National Institute on Aging
  • United States Department of Defense
  • University of North Carolina at Chapel Hill

Tags

Fields of Study

  • Biology

Readers

  • Molecular and Cellular Biology
  • Traumatic Brain Injury (TBI) and Cognitive Aging in the Guam and Border Populations Affected by Alzheimer's Disease and Tau-Associated Dementias.

Technology Areas

  • Biotechnology