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      Temperature, Oxygen, and Salt-Sensing Neurons in C. elegans Are Carbon Dioxide Sensors that Control Avoidance Behavior

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          Summary

          Homeostatic control of body fluid CO 2 is essential in animals but is poorly understood. C. elegans relies on diffusion for gas exchange and avoids environments with elevated CO 2. We show that C. elegans temperature, O 2, and salt-sensing neurons are also CO 2 sensors mediating CO 2 avoidance. AFD thermosensors respond to increasing CO 2 by a fall and then rise in Ca 2+ and show a Ca 2+ spike when CO 2 decreases. BAG O 2 sensors and ASE salt sensors are both activated by CO 2 and remain tonically active while high CO 2 persists. CO 2-evoked Ca 2+ responses in AFD and BAG neurons require cGMP-gated ion channels. Atypical soluble guanylate cyclases mediating O 2 responses also contribute to BAG CO 2 responses. AFD and BAG neurons together stimulate turning when CO 2 rises and inhibit turning when CO 2 falls. Our results show that C. elegans senses CO 2 using functionally diverse sensory neurons acting homeostatically to minimize exposure to elevated CO 2.

          Highlights

          ► The major temperature, O 2, and salt-sensing neurons of C. elegans are CO 2 sensors ► AFD, BAG, and ASE neurons have unique CO 2-response properties ► O 2-sensing atypical soluble guanylate cyclases also mediate CO 2 neuronal responses ► CO 2 sensing involves both transient and persistent neuronal responses

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          Most cited references58

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          Molecular architecture of smell and taste in Drosophila.

          The chemical senses-smell and taste-allow animals to evaluate and distinguish valuable food resources from dangerous substances in the environment. The central mechanisms by which the brain recognizes and discriminates attractive and repulsive odorants and tastants, and makes behavioral decisions accordingly, are not well understood in any organism. Recent molecular and neuroanatomical advances in Drosophila have produced a nearly complete picture of the peripheral neuroanatomy and function of smell and taste in this insect. Neurophysiological experiments have begun to provide insight into the mechanisms by which these animals process chemosensory cues. Given the considerable anatomical and functional homology in smell and taste pathways in all higher animals, experimental approaches in Drosophila will likely provide broad insights into the problem of sensory coding. Here we provide a critical review of the recent literature in this field and comment on likely future directions.
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            Two chemosensory receptors together mediate carbon dioxide detection in Drosophila.

            Blood-feeding insects, including the malaria mosquito Anopheles gambiae, use highly specialized and sensitive olfactory systems to locate their hosts. This is accomplished by detecting and following plumes of volatile host emissions, which include carbon dioxide (CO2). CO2 is sensed by a population of olfactory sensory neurons in the maxillary palps of mosquitoes and in the antennae of the more genetically tractable fruitfly, Drosophila melanogaster. The molecular identity of the chemosensory CO2 receptor, however, remains unknown. Here we report that CO2-responsive neurons in Drosophila co-express a pair of chemosensory receptors, Gr21a and Gr63a, at both larval and adult life stages. We identify mosquito homologues of Gr21a and Gr63a, GPRGR22 and GPRGR24, and show that these are co-expressed in A. gambiae maxillary palps. We show that Gr21a and Gr63a together are sufficient for olfactory CO2-chemosensation in Drosophila. Ectopic expression of Gr21a and Gr63a together confers CO2 sensitivity on CO2-insensitive olfactory neurons, but neither gustatory receptor alone has this function. Mutant flies lacking Gr63a lose both electrophysiological and behavioural responses to CO2. Knowledge of the molecular identity of the insect olfactory CO2 receptors may spur the development of novel mosquito control strategies designed to take advantage of this unique and critical olfactory pathway. This in turn could bolster the worldwide fight against malaria and other insect-borne diseases.
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              The molecular basis of CO2 reception in Drosophila.

              CO(2) elicits a response from many insects, including mosquito vectors of diseases such as malaria and yellow fever, but the molecular basis of CO(2) detection is unknown in insects or other higher eukaryotes. Here we show that Gr21a and Gr63a, members of a large family of Drosophila seven-transmembrane-domain chemoreceptor genes, are coexpressed in chemosensory neurons of both the larva and the adult. The two genes confer CO(2) response when coexpressed in an in vivo expression system, the "empty neuron system." The response is highly specific for CO(2) and dependent on CO(2) concentration. The response shows an equivalent dependence on the dose of Gr21a and Gr63a. None of 39 other chemosensory receptors confers a comparable response to CO(2). The identification of these receptors may now allow the identification of agents that block or activate them. Such agents could affect the responses of insect pests to the humans they seek.
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                Author and article information

                Journal
                Neuron
                Neuron
                Neuron
                Cell Press
                0896-6273
                1097-4199
                24 March 2011
                24 March 2011
                : 69
                : 6-4
                : 1099-1113
                Affiliations
                [1 ]MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 0QH, UK
                Author notes
                []Corresponding author debono@ 123456mrc-lmb.cam.ac.uk
                Article
                NEURON10589
                10.1016/j.neuron.2011.02.023
                3115024
                21435556
                c086cce0-8fae-41da-9728-9ee586068a04
                © 2011 ELL & Excerpta Medica.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 23 December 2010
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                Neurosciences
                Neurosciences

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