Leptin signaling in the dorsomedial hypothalamus couples breathing and metabolism in obesity

Cell Rep. 2023 Dec 26;42(12):113512. doi: 10.1016/j.celrep.2023.113512. Epub 2023 Nov 30.

Abstract

Mismatch between CO2 production (Vco2) and respiration underlies the pathogenesis of obesity hypoventilation. Leptin-mediated CNS pathways stimulate both metabolism and breathing, but interactions between these functions remain elusive. We hypothesized that LEPRb+ neurons of the dorsomedial hypothalamus (DMH) regulate metabolism and breathing in obesity. In diet-induced obese LeprbCre mice, chemogenetic activation of LEPRb+ DMH neurons increases minute ventilation (Ve) during sleep, the hypercapnic ventilatory response, Vco2, and Ve/Vco2, indicating that breathing is stimulated out of proportion to metabolism. The effects of chemogenetic activation are abolished by a serotonin blocker. Optogenetic stimulation of the LEPRb+ DMH neurons evokes excitatory postsynaptic currents in downstream serotonergic neurons of the dorsal raphe (DR). Administration of retrograde AAV harboring Cre-dependent caspase to the DR deletes LEPRb+ DMH neurons and abolishes metabolic and respiratory responses to leptin. These findings indicate that LEPRb+ DMH neurons match breathing to metabolism through serotonergic pathways to prevent obesity-induced hypoventilation.

Keywords: CP: Metabolism; CP: Neuroscience; designer receptor exclusively activated by designer drugs; dorsal raphe nucleus; hypercapnic ventilatory response; inspiratory flow limitation; intranasal administration; leptin receptor; obesity hypoventilation; obstructive sleep apnea; serotonin; sleep disordered breathing.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Hypothalamus / metabolism
  • Hypoventilation* / metabolism
  • Leptin* / metabolism
  • Mice
  • Obesity / metabolism
  • Receptors, Leptin / metabolism
  • Respiration

Substances

  • Leptin
  • Receptors, Leptin