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NPAS3-Regulated Astrocyte Mitochondrial Bioenergetics is Required for Cognition

  • Kateryna Murlanova
  • , Ksenia Novototskaya-Vlasova
  • , Shovgi Huseynov
  • , Olga Pletnikova
  • , Rebecca Howell
  • , Yan Jouroukhin
  • , Dong Won Kim
  • , Adrian Eddy-Sulaiman Jenson
  • , Juhyun Lee
  • , Qin Cheng
  • , Stephen Thompson
  • , Vikyath Saraf
  • , Michael Morales
  • , Eduardo Cortes Gomez
  • , Russell Margolis
  • , Frederick Nucifora
  • , Spencer Rosario
  • , Andrew Pieper
  • , Henry Withers
  • , Samir Haj-Dahmane
  • Kim Juhyun, Mikhail Pletnikov
  • SUNY Buffalo
  • Aarhus University
  • Johns Hopkins University
  • Korea Brain Research Institute
  • Kyungpook National University
  • Roswell Park Cancer Institute
  • Case Western Reserve University
  • Louis Stokes Cleveland VA Medical Center

Research output: Contribution to journalArticlepeer-review

Abstract

The basic helix-loop-helix transcription factor neuronal PAS (Per, Arnt, Sim) domain protein 3 (NPAS3) provides transcriptional regulation of metabolic pathways and is highly expressed in astrocytes. NPAS3 variants have been associated with cognitive dysfunction under several neuropsychiatric conditions, but the underlying brain cell type–specific mechanisms remain obscure. Here, we report that NPAS3 is a key regulator of mitochondrial bioenergetics in astrocytes in the mouse brain. Selective deletion of Npas3 in mature astrocytes decreases expression of mitochondrial glutamate carrier 2 involved in glutamate oxidation, leading to reduced oxidative phosphorylation and lactate production in astrocytes. This deficit reduces intrinsic excitability, dendritic spine density, and excitatory synaptic transmission of medial prefrontal cortex (mPFC) pyramidal neurons. Mice with Npas3-deficient mPFC astrocytes exhibit impaired trace fear conditioning, which is rescued by lactate treatment. Thus, the present study demonstrates a mechanistic link between NPAS3-dependent astrocyte mitochondrial bioenergetics and cognitive function and provides insights for glia-targeting treatment of cognitive dysfunction in neuropsychiatric disease.

Original languageEnglish
Article numbereadt2527
JournalScience Advances
Volume12
Issue number25
DOIs
StatePublished - 2026

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