Drosophila insulin-producing cells are differentially modulated by serotonin and octopamine receptors and affect social behavior

PLoS One. 2014 Jun 12;9(6):e99732. doi: 10.1371/journal.pone.0099732. eCollection 2014.

Abstract

A set of 14 insulin-producing cells (IPCs) in the Drosophila brain produces three insulin-like peptides (DILP2, 3 and 5). Activity in IPCs and release of DILPs is nutrient dependent and controlled by multiple factors such as fat body-derived proteins, neurotransmitters, and neuropeptides. Two monoamine receptors, the octopamine receptor OAMB and the serotonin receptor 5-HT1A, are expressed by the IPCs. These receptors may act antagonistically on adenylate cyclase. Here we investigate the action of the two receptors on activity in and output from the IPCs. Knockdown of OAMB by targeted RNAi led to elevated Dilp3 transcript levels in the brain, whereas 5-HT1A knockdown resulted in increases of Dilp2 and 5. OAMB-RNAi in IPCs leads to extended survival of starved flies and increased food intake, whereas 5-HT1A-RNAi produces the opposite phenotypes. However, knockdown of either OAMB or 5-HT1A in IPCs both lead to increased resistance to oxidative stress. In assays of carbohydrate levels we found that 5-HT1A knockdown in IPCs resulted in elevated hemolymph glucose, body glycogen and body trehalose levels, while no effects were seen after OAMB knockdown. We also found that manipulations of the two receptors in IPCs affected male aggressive behavior in different ways and 5-HT1A-RNAi reduced courtship latency. Our observations suggest that activation of 5-HT1A and OAMB signaling in IPCs generates differential effects on Dilp transcription, fly physiology, metabolism and social interactions. However the findings do not support an antagonistic action of the two monoamines and their receptors in this particular system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Brain / metabolism*
  • Courtship
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila Proteins / physiology*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism
  • Drosophila melanogaster / physiology*
  • Female
  • Inhibitor of Apoptosis Proteins / genetics
  • Inhibitor of Apoptosis Proteins / metabolism
  • Insulin / metabolism*
  • Male
  • Neurons / metabolism
  • Neurons / physiology*
  • Receptor, Serotonin, 5-HT1A / genetics
  • Receptor, Serotonin, 5-HT1A / physiology*
  • Receptors, Neurotransmitter / genetics
  • Receptors, Neurotransmitter / physiology*
  • Sexual Behavior, Animal / physiology
  • Signal Transduction / genetics
  • Social Behavior*

Substances

  • DIAP2 protein, Drosophila
  • Drosophila Proteins
  • Inhibitor of Apoptosis Proteins
  • Insulin
  • OAMB protein, Drosophila
  • Receptors, Neurotransmitter
  • Receptor, Serotonin, 5-HT1A

Grant support

The study was supported by: The Swedish Research Council (D.R.N) and The Carl Trygger Foundation (D.R.N., M.J.W.), Stiftelsen Olle Engkvist Byggmästare and Stiftelsen Lars Hiertas Minne (both to M.J.W.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.