Hyperoxia-triggered aversion behavior in drosophila foraging larvae is mediated by sensory detection of hydrogen peroxide

Myung Jun Kim, Joshua A. Ainsley, Justin W. Carder, Wayne A. Johnson

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

Reactive oxygen species (ROS) in excess have been implicated in numerous chronic illnesses, including asthma, diabetes, aging, cardiovascular disease, and neurodegenerative illness. However, at lower concentrations, ROS can also serve essential routine functions as part of cellular signal transduction pathways. As products of atmospheric oxygen, ROS-mediated signals can function to coordinate external environmental conditions with growth and development. A central challenge has been a mechanistic distinction between the toxic effects of oxidative stress and endogenous ROS functions occurring at much lower concentrations. Drosophila larval aerotactic behavioral assays revealed strong developmentally regulated aversion to mild hyperoxia mediated by H2O2-dependent activation of class IV multidendritic (mdIV) sensory neurons expressing the Degenerin/epithelial Na+ channel subunit, Pickpocket1 (PPK1). Electrophysiological recordings in foraging-stage larvae (78-84 h after egg laying [AEL]) demonstrated PPK1-dependent activation of mdIV neurons by nanomolar levels of H2O2 well below levels normally associated with oxidative stress. Acute sensitivity was reduced > 100-fold during the larval developmental transition to wandering stage (> 96 h AEL), corresponding to a loss of hyperoxia aversion behavior during the same period. Degradation of endogenous H2O2 by transgenic overexpression of catalase in larval epidermis caused a suppression of hyperoxia aversion behavior. Conversely, disruption of endogenous catalase activity using a UAS-CatRNAi transposon resulted in an enhanced hyperoxia-aversive response. These results demonstrate an essential role for low-level endogenous H2O2 as an environment-derived signal coordinating developmental behavioral transitions.

Original languageEnglish (US)
Pages (from-to)151-162
Number of pages12
JournalJournal of Neurogenetics
Volume27
Issue number4
DOIs
StatePublished - Dec 2013

Bibliographical note

Funding Information:
This work was supported by a grant from the National Institutes of Health to W.A.J. (NS066287) and a predoctoral fellowship from the American Heart Association to J.A.A. (0610138Z). We would like to thank the Bloomington Drosophila Stock Center for its service in providing fly stocks to the research community and acknowledge their support from NIH and NSF.

Keywords

  • DEG/ENaC
  • Reactive oxygen species
  • Somatosensation
  • TRP

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