Abstract
BackgroundThe complex Drosophila larval peripheral nervous system, capable of monitoring sensory input from the external environment, includes a family of multiple dendritic (md) neurons with extensive dendritic arbors tiling the inner surface of the larval body wall. The class IV multiple dendritic (mdIV) neurons are the most complex with dendritic nerve endings forming direct intimate contacts with epithelial cells of the larval body wall. Functioning as polymodal mechanonociceptors with the ability to respond to both noxious mechanical stimulation and noxious heat, the mdIV neurons are also activated by nanomolar levels of the endogenous reactive oxygen species (ROS), H2O2. Although often associated with tissue damage related to oxidative stress, endogenous ROS have also been shown to function as signaling molecules at lower concentrations. The overall role of ROS in sensory signaling is poorly understood but the acutely sensitive response of mdIV neurons to ROS-mediated activation is consistent with a routine role in the regulation of mdIV neuronal activity. Larvae respond to short wavelength ultraviolet (UVC) light with an immediate and visual system-independent writhing and twisting of the body previously described as a nociceptive response. Molecular and cellular mechanisms mediating this response and potential relationships with ROS generation are not well understood. We have used the UVC-induced writhing response as a model for investigation of the proposed link between endogenous ROS production and mdIV neuron function in the larval body wall.ResultsTransgenic inactivation of mdIV neurons caused a strong suppression of UVC-induced writhing behavior consistent with a key role for the mdIV neurons as mediators of the behavioral response. Direct imaging of ROS-activated fluorescence showed that UVC irradiation caused a significant increase in endogenous ROS levels in the larval body wall and transgenic overexpression of antioxidant enzymes strongly suppressed the UVC-induced writhing response. Direct electrophysiological recordings demonstrated that UVC irradiation also increased neuronal activity of the mdIV neurons.ConclusionsResults obtained using UVC irradiation to induce ROS generation provide evidence that UVC-induced writhing behavior is mediated by endogenous production of ROS capable of activating mdIV mechanonociceptors in the larval body wall.
Highlights
The complex Drosophila larval peripheral nervous system, capable of monitoring sensory input from the external environment, includes a family of multiple dendritic neurons with extensive dendritic arbors tiling the inner surface of the larval body wall
UVC induces mdIV-mediated writhing behavior UVC has been shown to induce an immediate behavioral response from Drosophila larvae consisting of repeated vigorous bending of the body from side to side and referred to as writhing behavior [12]
Tissue-specific expression experiments (Figure 2B) suggested that the epidermal layers of the larval body wall may be a prime source of reactive oxygen species (ROS) in response to ultraviolet radiation (UVR), we examined the effect of antioxidant enzyme overexpression in the mdIV neurons themselves using the mdIV neuron-specific ppk1GAL4 transposon (Figure 2D)
Summary
The complex Drosophila larval peripheral nervous system, capable of monitoring sensory input from the external environment, includes a family of multiple dendritic (md) neurons with extensive dendritic arbors tiling the inner surface of the larval body wall. The class IV multiple dendritic (mdIV) neurons extend complex dendritic arbors to completely tile the inner surface of the body wall [3,5]. These neurons express the Drosophila Degenerin/Epithelial Sodium Channel (DEG/ENaC) subunit. Transgenic disruption of the visual system did not lead to suppression of the writhing behavior and restricted irradiation at any position in the body wall where nociceptors extend extensive dendritic arbors could elicit writhing Based on these observations, the UVC-induced writhing motion has been classified as nociception behavior. Ultraviolet radiation (UVR) appears to elicit distinct behavioral responses from Drosophila larvae depending on the wavelength
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