The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila

Ni, Lina; Klein, Mason; Svec, Kathryn V.; Budelli, Gonzalo; Chang, Elaine; Ferrer, Anggie; Benton, Richard; Samuel, Aravinthan D. T.; Garrity, Paul

doi:10.7554/elife.13254

Cited by 196 publications

(190 citation statements)

References 26 publications

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“…By contrast, consistent with previous analyses262728, we observed expression of IR25a in multiple sensory neurons in all of the larval chemosensory organs (Fig. 2B and data not shown).…”

Section: Resultssupporting

confidence: 93%

“…Neurons in these organs express transcripts and/or genetic reporters for members of three chemosensory families, Odorant Receptors (ORs), Gustatory Receptors (GRs) and Ionotropic Receptors (IRs). ORs appear to be restricted to the Dorsal Organ (where they detect volatile compounds)2425, while individual GRs and IRs are expressed in small numbers of neurons in one or more of these chemosensory organs2627282930. Remarkably few relationships have been defined between specific gustatory ligands and particular sensory neurons in the larva313233.…”

Section: Resultsmentioning

confidence: 99%

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A molecular and neuronal basis for amino acid sensing in the Drosophila larva

Croset

Schleyer

Arguello

et al. 2016

Sci Rep

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133

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Amino acids are important nutrients for animals, reflected in conserved internal pathways in vertebrates and invertebrates for monitoring cellular levels of these compounds. In mammals, sensory cells and metabotropic glutamate receptor-related taste receptors that detect environmental sources of amino acids in food are also well-characterised. By contrast, it is unclear how insects perceive this class of molecules through peripheral chemosensory mechanisms. Here we investigate amino acid sensing in Drosophila melanogaster larvae, which feed ravenously to support their rapid growth. We show that larvae display diverse behaviours (attraction, aversion, neutral) towards different amino acids, which depend upon stimulus concentration. Some of these behaviours require IR76b, a member of the variant ionotropic glutamate receptor repertoire of invertebrate chemoreceptors. IR76b is broadly expressed in larval taste neurons, suggesting a role as a co-receptor. We identify a subpopulation of these neurons that displays physiological activation by some, but not all, amino acids, and which mediate suppression of feeding by high concentrations of at least a subset of these compounds. Our data reveal the first elements of a sophisticated neuronal and molecular substrate by which these animals detect and behave towards external sources of amino acids.

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“…By contrast, consistent with previous analyses262728, we observed expression of IR25a in multiple sensory neurons in all of the larval chemosensory organs (Fig. 2B and data not shown).…”

Section: Resultssupporting

confidence: 93%

Section: Resultsmentioning

confidence: 99%

A molecular and neuronal basis for amino acid sensing in the Drosophila larva

Croset

Schleyer

Arguello

et al. 2016

Sci Rep

Self Cite

133

127

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“…Alternatively, some pharyngeal GRNs may evaluate characteristics other than palatability, such as temperature or viscosity. Ir25a , which is broadly expressed in all 24 pharyngeal GRNs, is required for cool and temperature sensing (Ni et al, 2016, Chen et al, 2015). It will be worth investigating whether one or more pharyngeal GRNs act to integrate information about temperature and chemical quality of food substrates.…”

Section: Discussionmentioning

confidence: 99%

Molecular and Cellular Organization of Taste Neurons in Adult Drosophila Pharynx

Chen

Dahanukar

2017

Cell Reports

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SUMMARY The Drosophila pharyngeal taste organs are poorly characterized despite their location at important sites for monitoring food quality. Functional analysis of pharyngeal neurons has been hindered by the paucity of molecular tools to manipulate them, as well as their relative inaccessibility for neurophysiological investigations. Here, we generate receptor-to-neuron maps of all three pharyngeal taste organs by performing a comprehensive chemoreceptor-GAL4/LexA expression analysis. The organization of pharyngeal neurons reveals similarities and distinctions in receptor repertoires and neuronal groupings compared to external taste neurons. We validate the mapping results by pinpointing a single pharyngeal neuron required for feeding avoidance of L-canavanine. Inducible activation of pharyngeal taste neurons reveals functional differences between external and internal taste neurons and functional subdivision within pharyngeal sweet neurons. Our results provide road maps of pharyngeal taste organs in an insect model system for probing the role of these understudied neurons in controlling feeding behaviors.

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“…Except for activity measurements of thermosensory neurons in the larval dorsal organ ganglion 32,33 , to our knowledge, no other device has been designed to enable precise and restricted application of stimuli such as chemicals or other cues to the larva or, in the case of tastants, even to the adult fly. Our system goes beyond previous approaches [32][33][34] by allowing for (i) precise chemical stimulation of restrained, semi-intact larvae, (ii) multiple stimulus sweeps interspersed with wash steps and (iii) stimulation of the same animal with different chemicals or combinations of chemicals.…”

Section: Advantages and Limitationsmentioning

confidence: 99%

“…Our system goes beyond previous approaches [32][33][34] by allowing for (i) precise chemical stimulation of restrained, semi-intact larvae, (ii) multiple stimulus sweeps interspersed with wash steps and (iii) stimulation of the same animal with different chemicals or combinations of chemicals.…”

Section: Advantages and Limitationsmentioning

confidence: 99%

A microfluidics-based method for measuring neuronal activity in Drosophila chemosensory neurons

et al. 2016

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Animals possess highly specialized sensory neurons that are capable of perceiving information about a continuously changing environment. Measuring neuronal activity in these cells is an important step toward understanding the basic coding principles, as well as the spatial and temporal dynamics, of sensory systems. The fruit fly Drosophila melanogaster is widely used as a genetic model organism to uncover basic mechanisms of taste coding and odor perception [1][2][3][4][5][6][7] . Recent insights into the molecular and functional mechanisms of sensory perception in Drosophila have been achieved by the use of single-sensillum recordings of adult taste or olfactory sensilla 1,4,[8][9][10][11][12][13] . This method enables sensitive measurements of action potential patterns and shows whether responses are excitatory or inhibitory, but drawing final conclusions about the individual firing neuron is difficult, as each sensillum contains two to four neurons 14 . In the larva, multicellular electrophysiological measurements of the taste system have been performed, but this method is technically challenging and it is not clear how many taste neurons are housed in which sensillum 15 .Microfluidic devices have been used previously to image command interneurons (AVA) and sensory neurons (ASH) in the nematode Caenorhabditis elegans and for studies of axotomy in peripheral sensory neurons of Drosophila larvae [16][17][18] . To implement a similar strategy for Drosophila larval chemosensation, we developed a simple and widely applicable microfluidic chip. We used this custom-made microfluidic device to deliver precise and temporally restricted tastant stimulation in the first published physiological characterization of individual larval gustatory receptor neurons (GRNs) expressing the calcium sensor GCaMP5 (ref. 19). Development of the protocolThe design of the chip is simple. It contains a single channel that is connected to a chamber in which the sample can be mounted to bring it into contact with fluids in the channel. The chamber was originally designed to exactly fit the head of a third-instar Drosophila larva; however, it is also suitable for the proboscis or the leg of an adult fly. The channel for delivering stimulants is relatively broad, designed at a width of 1 mm to reduce flow pressure on the sample. We use a single-channel system in which changes of liquids are performed by the tubing system outside the chip, allowing a relatively slow flow rate inside the chip. Here we provide information required for the design and production of this microfluidic device ( Fig. 1; Supplementary Data), as well as a detailed protocol for live imaging to acquire GCaMP-based calcium imaging (Figs. 2 and 3). By introducing the larval head, or the adult proboscis or leg, into the chamber, neuronal activity can be recorded while chemosensory neurons are in contact with the solution pumped through the channel (Figs. 2 and 3).Overview of the procedure An overview of the workflow involved in implementing the procedure is provided in Figu...

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The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila

Cited by 196 publications

References 26 publications

A molecular and neuronal basis for amino acid sensing in the Drosophila larva

A molecular and neuronal basis for amino acid sensing in the Drosophila larva

Molecular and Cellular Organization of Taste Neurons in Adult Drosophila Pharynx

A microfluidics-based method for measuring neuronal activity in Drosophila chemosensory neurons

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