Neuropeptidergic Signaling and Active Feeding State Inhibit Nociception in Caenorhabditis elegans

J Neurosci. 2016 Mar 16;36(11):3157-69. doi: 10.1523/JNEUROSCI.1128-15.2016.

Abstract

Food availability and nutritional status are important cues affecting behavioral states. Here we report that, in Caenorhabditis elegans, a cascade of dopamine and neuropeptide signaling acts to inhibit nociception in food-poor environments. In the absence of food, animals show decreased sensitivity and increased adaptation to soluble repellents sensed by the polymodal ASH nociceptors. The effects of food on adaptation are affected by dopamine and neuropeptide signaling; dopamine acts via the DOP-1 receptor to decrease adaptation on food, whereas the neuropeptide receptors NPR-1 and NPR-2 act to increase adaptation off food. NPR-1 and NPR-2 function cell autonomously in the ASH neurons to increase adaptation off food, whereas the DOP-1 receptor controls neuropeptide release from interneurons that modulate ASH activity indirectly. These results indicate that feeding state modulates nociception through the interaction of monoamine and neuropeptide signaling pathways.

Keywords: C. elegans; chemosensation; dopamine; neuromodulation; neuropeptide.

Publication types

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

MeSH terms

  • Adaptation, Physiological / drug effects
  • Adaptation, Physiological / genetics
  • Adaptation, Physiological / physiology*
  • Animals
  • Animals, Genetically Modified
  • CHO Cells
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism
  • Cationic Amino Acid Transporter 2 / genetics
  • Cationic Amino Acid Transporter 2 / metabolism
  • Copper / pharmacology
  • Cricetulus
  • Dopamine / genetics
  • Dopamine / metabolism
  • Fasting
  • Feeding Behavior / physiology*
  • Neuropeptides / metabolism*
  • Nociception / drug effects
  • Nociception / physiology*
  • Promoter Regions, Genetic / genetics
  • Receptors, Dopamine D1 / genetics
  • Receptors, Dopamine D1 / metabolism
  • Receptors, Neuropeptide Y / genetics
  • Receptors, Neuropeptide Y / metabolism
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Signal Transduction / physiology*

Substances

  • Caenorhabditis elegans Proteins
  • Calcium-Binding Proteins
  • Cationic Amino Acid Transporter 2
  • Dop-1 protein, C elegans
  • NPR-1 protein, C elegans
  • Neuropeptides
  • Receptors, Dopamine D1
  • Receptors, Neuropeptide Y
  • UNC-31 protein, C elegans
  • Copper
  • cupric chloride
  • Dopamine