Feeding state regulates pheromone-mediated avoidance behavior via the insulin signaling pathway in Caenorhabditis elegans

EMBO J. 2018 Aug 1;37(15):e98402. doi: 10.15252/embj.201798402. Epub 2018 Jun 19.

Abstract

Animals change sensory responses and their eventual behaviors, depending on their internal metabolic status and external food availability. However, the mechanisms underlying feeding state-dependent behavioral changes remain undefined. Previous studies have shown that Caenorhabditis elegans hermaphrodite exhibits avoidance behaviors to acute exposure of a pheromone, ascr#3 (asc-ΔC9, C9). Here, we show that the ascr#3 avoidance behavior is modulated by feeding state via the insulin signaling pathway. Starvation increases ascr#3 avoidance behavior, and loss-of-function mutations in daf-2 insulin-like receptor gene dampen this starvation-induced ascr#3 avoidance behavior. DAF-2 and its downstream signaling molecules, including the DAF-16 FOXO transcription factor, act in the ascr#3-sensing ADL neurons to regulate synaptic transmission to downstream target neurons, including the AVA command interneurons. Moreover, we found that starvation decreases the secretion of INS-18 insulin-like peptides from the intestine, which antagonizes DAF-2 function in the ADL neurons. Altogether, this study provides insights about the molecular communication between intestine and sensory neurons delivering hunger message to sensory neurons, which regulates avoidance behavior from pheromones to facilitate survival chance.

Keywords: DAF‐2 insulin receptor; avoidance behavior; feeding state; pheromone; synaptic transmission.

Publication types

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

MeSH terms

  • Animals
  • Avoidance Learning / physiology*
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Forkhead Transcription Factors / genetics
  • Insulin / metabolism*
  • Neurons / metabolism
  • Peptide Hormones / metabolism
  • Pheromones / metabolism
  • Receptor, Insulin / genetics
  • Receptor, Insulin / metabolism*
  • Signal Transduction
  • Starvation / metabolism*
  • Synaptic Transmission / genetics
  • Synaptic Transmission / physiology*

Substances

  • Caenorhabditis elegans Proteins
  • Forkhead Transcription Factors
  • INS-18 protein, C elegans
  • Insulin
  • Peptide Hormones
  • Pheromones
  • daf-16 protein, C elegans
  • DAF-2 protein, C elegans
  • Receptor, Insulin