Food odors trigger an endocrine response that affects food ingestion and metabolism

Cell Mol Life Sci. 2015 Aug;72(16):3143-55. doi: 10.1007/s00018-015-1884-4. Epub 2015 Mar 18.

Abstract

Food odors stimulate appetite and innate food-seeking behavior in hungry animals. The smell of food also induces salivation and release of gastric acid and insulin. Conversely, sustained odor exposure may induce satiation. We demonstrate novel effects of food odors on food ingestion, metabolism and endocrine signaling in Drosophila melanogaster. Acute exposure to attractive vinegar odor triggers a rapid and transient increase in circulating glucose, and a rapid upregulation of genes encoding the glucagon-like hormone adipokinetic hormone (AKH), four insulin-like peptides (DILPs) and some target genes in peripheral tissues. Sustained exposure to food odors, however, decreases food intake. Hunger-induced strengthening of synaptic signaling from olfactory sensory neurons (OSNs) to brain neurons increases food-seeking behavior, and conversely fed flies display reduced food odor sensitivity and feeding. We show that increasing the strength of OSN signaling chronically by genetic manipulation of local peptide neuromodulation reduces feeding, elevates carbohydrates and diminishes lipids. Furthermore, constitutively strengthened odor sensitivity altered gene transcripts for AKH, DILPs and some of their targets. Thus, we show that food odor can induce a transient anticipatory endocrine response, and that boosted sensitivity to this odor affects food intake, as well as metabolism and hormonal signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetic Acid / chemistry
  • Acetic Acid / pharmacology
  • Analysis of Variance
  • Animals
  • Animals, Genetically Modified
  • Blood Glucose / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / physiology*
  • Endocrine System / physiology*
  • Feeding Behavior / physiology*
  • Fluorescent Antibody Technique
  • Food*
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / physiology
  • Immunohistochemistry
  • Insect Hormones / metabolism
  • Metabolic Networks and Pathways / physiology*
  • Odorants / analysis*
  • Oligopeptides / metabolism
  • Pyrrolidonecarboxylic Acid / analogs & derivatives
  • Pyrrolidonecarboxylic Acid / metabolism
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction / physiology*

Substances

  • Blood Glucose
  • Insect Hormones
  • Oligopeptides
  • adipokinetic hormone
  • Acetic Acid
  • Pyrrolidonecarboxylic Acid