Transcriptional regulation of metabolism in neurons

NIH RePORTER · NIH · R01 · $435,080 · view on reporter.nih.gov ↗

Abstract

Epidemiological, genetic, and biological evidence implicates mitochondrial dysfunction in the pathogenesis of Parkinson Disease (PD). Recent transcriptional studies have identified clusters of genes reduced in dopaminergic neurons of the substantia nigra of patients with subclinical and symptomatic PD, the majority of which are involved in neuronal metabolism and mitochondrial function. These findings raise the possibility that the function of transcriptional regulators of metabolic and mitochondrial genes may be compromised in idiopathic PD and that targeting key transcriptional pathways for gene regulation may be an appropriate strategy for preventing and/or rescuing metabolic deficits and neuronal cell death. Using bioinformatics and transcriptional assays, we have identified a potential transcription factor required for the regulation of metabolic and nuclear-encoded gene transcription in dopaminergic nigral neurons. This protein, estrogen-related receptor γ (ERRγ), drives the expression of nuclear-encoded genes for mitochondrial biogenesis and respiration in peripheral tissues, and it can directly associate with peroxisome proliferator- activated receptor γ coactivator 1α (PGC-1α), a transcriptional coactivator that is reduced in PD and can be neuroprotective when overexpressed in PD models. Our preliminary data indicate that ERRγ is expressed by neurons of the substantia nigra in rodents and that deletion of ERRγ from the mouse midbrain causes a reduction in ERRγ-driven metabolic genes and motor activity. Furthermore, our data indicate that PGC-1α- target genes are enriched in binding sites for ERRγ and that PGC-1α and ERRγ can synergistically drive mitochondrial gene expression. Importantly, the majority of mitochondrial genes of the electron transport chain reduced in PD are ERRγ target genes. The experiments proposed in this application will expand upon these initial findings to test the hypotheses that ERRγ is a central regulator of metabolic and mitochondrial gene expression in nigral neurons (Aim 1), that ERRγ is required for PGC-1α to induce metabolic and mitochondrial genes (Aim 2), and that overexpression of ERRγ can prevent cell dysfunction and death in rodent model of PD (Aim 3). These experiments have the potential to reveal the critical pathways by which nigral neurons maintain metabolic and mitochondrial homeostasis and a novel avenue for improving mitochondrial function in disease. Furthermore, considering that ERRγ can orchestrate a transcriptional program for a number of genes reduced in PD, ERRγ deletion in nigral neurons could serve as a biologically relevant model of idiopathic PD.

Key facts

NIH application ID
9898487
Project number
5R01NS101958-05
Recipient
SOUTHERN RESEARCH INSTITUTE
Principal Investigator
Rita Marie Cowell
Activity code
R01
Funding institute
NIH
Fiscal year
2020
Award amount
$435,080
Award type
5
Project period
2017-05-01 → 2022-04-30