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TET3 epigenetically controls feeding and stress response behaviors via AGRP neurons.

Di Xie1,2, Bernardo Stutz2,3, Feng Li1,2

  • 1Department of Obstetrics, Gynecology and Reproductive Sciences.

The Journal of Clinical Investigation
|October 3, 2022
PubMed
Summary
This summary is machine-generated.

TET3 dioxygenase deficiency in mouse AGRP neurons causes overeating, obesity, and diabetes. This TET3 enzyme regulates feeding and stress behaviors by modifying DNA in AGRP neurons.

Keywords:
DiabetesLeptinMetabolismNeuroendocrine regulationNeuroscience

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Area of Science:

  • Epigenetics
  • Neuroscience
  • Metabolism

Background:

  • TET dioxygenases facilitate DNA demethylation via 5-methylcytosine oxidation to 5-hydroxymethylcytosine (5hmC).
  • Hypothalamic agouti-related peptide-expressing (AGRP) neurons are crucial for feeding regulation and modulate nonfeeding behaviors, producing neuropeptide Y (NPY) and GABA.
  • AGRP, NPY, and GABA signaling influence feeding, energy expenditure, and anxiolytic effects.

Purpose of the Study:

  • To investigate the role of TET3 in the central control of appetite and metabolism.
  • To elucidate the molecular mechanisms by which TET3 regulates AGRP neuron function and associated behaviors.

Main Methods:

  • CRISPR-mediated genetic ablation of Tet3 in adult mouse AGRP neurons.
  • Analysis of feeding behavior, body weight, glucose metabolism, and stress-related behaviors.
  • Assessment of AGRP neuron activity, gene expression (Agrp, Npy, Slc32a1), and leptin signaling.
  • Chromatin immunoprecipitation (ChIP) assays to study TET3 binding and 5hmC modification at the Agrp promoter.

Main Results:

  • Genetic ablation of Tet3 in AGRP neurons led to hyperphagia, obesity, diabetes, and reduced stress-like behaviors.
  • TET3 deficiency activated AGRP neurons, upregulated Agrp, Npy, and Slc32a1 expression, and impaired leptin signaling.
  • TET3 dynamically associates with the Agrp promoter, mediating leptin-induced 5hmC modification and transcriptional inhibition.
  • These regulatory mechanisms were conserved in both mouse models and human cells.

Conclusions:

  • TET3 is a critical central regulator of appetite and energy metabolism.
  • TET3 plays an unexpected dual role in controlling feeding and complex behaviors via AGRP neurons.
  • The findings reveal a novel epigenetic mechanism linking leptin signaling, TET3, and metabolic regulation in AGRP neurons.