The molecular basis for water taste in Drosophila. Nature

Department of Molecular and Cell Biology and Helen Wills Neuroscience Institute, CA, USA.
Nature (Impact Factor: 41.46). 04/2010; 465(7294):91-5. DOI: 10.1038/nature09011
Source: PubMed


The detection of water and the regulation of water intake are essential for animals to maintain proper osmotic homeostasis. Drosophila and other insects have gustatory sensory neurons that mediate the recognition of external water sources, but little is known about the underlying molecular mechanism for water taste detection. Here we identify a member of the degenerin/epithelial sodium channel family, PPK28, as an osmosensitive ion channel that mediates the cellular and behavioural response to water. We use molecular, cellular, calcium imaging and electrophysiological approaches to show that ppk28 is expressed in water-sensing neurons, and that loss of ppk28 abolishes water sensitivity. Moreover, ectopic expression of ppk28 confers water sensitivity to bitter-sensing gustatory neurons in the fly and sensitivity to hypo-osmotic solutions when expressed in heterologous cells. These studies link an osmosensitive ion channel to water taste detection and drinking behaviour, providing the framework for examining the molecular basis for water detection in other animals.

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    • "Previous studies had revealed excellent correspondence between stimulus-evoked electrophysiological responses in sensory neurons and calcium responses in their cell bodies and axon termini in olfactory and gustatory receptor neurons of fruit flies (de Bruyne et al., 2001; Suh et al., 2004; Pelz et al., 2006; Kwon et al., 2007; Cameron et al., 2010). Although we do not know the correlation between the calcium signals observed in the axons of subgroup-D JO neurons and their action potential responses, the tonic calcium response of subgroup-D JO neurons to vibrations of middle-range frequencies, a pulse song, and the anterior deflection observed in this study strongly suggests these signals would be transmitted to their downstream neural circuits. "
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    ABSTRACT: The fruit fly Drosophila melanogaster responds behaviorally to sound, gravity, and wind. Johnston's organ (JO) at the antennal base serves as a sensory organ in the fruit fly to detect these mechanosensory stimuli. Among the five anatomically defined subgroups of sensory neurons in JO, subgroups A and B detect sound vibrations and subgroups C and E respond to static deflections, such as gravity and wind. The functions of subgroup-D JO neurons, however, remain unknown. In this study, we used molecular-genetic methods to explore the physiologic properties of subgroup-D JO neurons. Both vibrations and static deflection of the antennal receiver activated subgroup-D JO neurons. This finding clearly revealed that zone D in the antennal mechanosensory and motor center (AMMC), the projection target of subgroup-D JO neurons, is a primary center for antennal vibrations and deflection in the fly brain. We anatomically identified two types of interneurons downstream of subgroup-D JO neurons, AMMC local neurons (AMMC LNs), and AMMC D1 neurons. AMMC LNs are local neurons whose projections are confined within the AMMC, connecting zones B and D. On the other hand, AMMC D1 neurons have both local dendritic arborizations within the AMMC and descending projections to the thoracic ganglia, suggesting that AMMC D1 neurons are likely to relay information of the antennal movement detected by subgroup-D JO neurons from the AMMC directly to the thorax. Together, these findings provide a neural basis for how JO and its brain targets encode information of complex movements of the fruit fly antenna.
    Frontiers in Physiology 05/2014; 5:179. DOI:10.3389/fphys.2014.00179 · 3.53 Impact Factor
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    • "Frontiers in Behavioral Neuroscience January 2014 | Volume 8 | Article 6 | 1 BEHAVIORAL NEUROSCIENCE et al., 2004; Al-Anzi et al., 2006; Moon et al., 2006; Dahanukar et al., 2007; Benton et al., 2009; Cameron et al., 2010; Weiss et al., 2011; Miyamoto et al., 2012; Zhang et al., 2013 "
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    ABSTRACT: The sensation of bitter substances can alert an animal that a specific type of food is harmful and should not be consumed. However, not all bitter compounds are equally toxic and some may even be beneficial in certain contexts. Thus, taste systems in general may have a broader range of functions than just in alerting the animal. In this study we investigate bitter sensing and processing in Drosophila larvae using quinine, a substance perceived by humans as bitter. We show that behavioral choice, feeding, survival, and associative olfactory learning are all directly affected by quinine. On the cellular level, we show that 12 gustatory sensory receptor neurons that express both GR66a and GR33a are required for quinine-dependent choice and feeding behavior. Interestingly, these neurons are not necessary for quinine-dependent survival or associative learning. On the molecular receptor gene level, the GR33a receptor, but not GR66a, is required for quinine-dependent choice behavior. A screen for gustatory sensory receptor neurons that trigger quinine-dependent choice behavior revealed that a single GR97a receptor gene expressing neuron located in the peripheral terminal sense organ is partially necessary and sufficient. For the first time, we show that the elementary chemosensory system of the Drosophila larva can serve as a simple model to understand the neuronal basis of taste information processing on the single cell level with respect to different behavioral outputs.
    Frontiers in Behavioral Neuroscience 01/2014; 8:6. DOI:10.3389/fnbeh.2014.00006 · 3.27 Impact Factor
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    • "The gustatory system of Drosophila melanogaster has been studied extensively and gustatory receptors that detect sweet tastants (Dahanukar et al. 2001; Ueno et al. 2001; Slone et al. 2007), bitter tastants (Meunier et al. 2003; Thorne et al. 2004; Lee et al. 2009; Weiss et al. 2011), as well as acid (Charlu et al. 2013), water (Cameron et al. 2010; Chen et al. 2010), carbon dioxide (Fischler et al. 2007), and pheromones (Bray and Amrein 2003; Moon et al. 2009) have been identified. Taste representations for different modalities project to segregated regions of the suboesophageal ganglion (Scott et al. 2001; Wang et al. 2004; Marella et al. 2006). "
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    ABSTRACT: Nutrient intake and avoidance of toxins are essential for survival and controlled by attractive and aversive feeding responses. Drosophila melanogaster presents one of the best characterized systems for studies on chemosensation, which is mediated by multigene families of chemoreceptors, including olfactory receptors, gustatory receptors, and odorant-binding proteins (OBPs). Although the response profiles of gustatory receptors have been well studied, the contribution of OBPs to food intake is largely unknown. As most aversive ("bitter") tastants are hydrophobic, we hypothesized that OBPs may fulfill an essential function in transporting bitter tastants to gustatory receptors to modulate feeding behavior. Here, we used 16 RNAi lines that inhibit expression of individual target Obp genes and show that OBPs modulate sucrose intake in response to a panel of nine bitter compounds. Similar to their function in olfaction, OBPs appear to interact with bitter compounds in a combinatorial and sex-dependent manner. RNAi-mediated reduction in expression of individual Obp genes resulted either in enhanced or reduced intake of sucrose in the presence of bitter compounds, consistent with roles for OBPs in transporting tastants to bitter taste receptors, sequestering them to limit their access to these receptors, or interacting directly with gustatory neurons that respond to sucrose.
    Chemical Senses 12/2013; 39(2). DOI:10.1093/chemse/bjt061 · 3.16 Impact Factor
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