Widely distributedDrosophila G-protein-coupled receptor (CG7887) is activated by endogenous tachykinin-related peptides

Birse, Ryan T.; Johnson, Erik C.; Taghert, Paul H.; Nässel, Dick R.

doi:10.1002/neu.20189

Cited by 89 publications

(99 citation statements)

References 38 publications

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“…We used immunocytochemistry with an antiserum to DTKR (see ref. 24 and SI Text ) to confirm that the construct was able to produce ectopic expression of the receptor in flies bearing the UAS-dtkr-GFP construct and Or83b-Gal4 (Fig. S1 A and B).…”

Section: Methodsmentioning

confidence: 80%

“…To ectopically express the DTKR receptor we designed a UASdtkr-GFP fusion construct according to Birse et al (24). This dtkr fusion construct has been shown to be functional when expressed in HEK-296 cells (24). A Bglll/Notl fragment containing the dtkr (CG7887) sequence and the GFP fusion was excised from the pEGFP1 vector.…”

Section: Methodsmentioning

confidence: 99%

“…Immunocytochemistry using an antiserum to the tachykinin receptor DTKR (24) showed that expression in the antennae is localized to cell bodies of ORNs (Fig. 2B).…”

Section: Distribution Of Dtk Peptide and Its Receptor Dtkr In The Olfmentioning

confidence: 99%

“…S3A). The GFP-tagged DTKR has been shown to be functional when expressed in HEK-296 cells (24). Odor-guided behavior was measured by a trap assay with free walking flies that were given a choice between a specific odor and water in a small arena (33,34).…”

Section: The Tachykinin Receptor Dtkr Mediates Presynaptic Inhibition Inmentioning

confidence: 99%

“…The DTKs are expressed in Ϸ150 neurons in the Drosophila brain, and in the antennal lobe glomeruli, there are extensive DTK-immunoreactive arborizations derived from a subset of antennal lobe LNs (21). Two DTK receptors, DTKR and NKD, have been identified in Drosophila (22,23) and 1 of these, DTKR, is strongly expressed in antennal lobe glomeruli (24). Behavioral evidence for a role of DTKs in olfaction was obtained from analysis of flies where dtk expression was knocked down globally using RNA interference (RNAi); these flies displayed diminished odor sensitivity (19).…”

mentioning

confidence: 99%

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Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Ignell

Root

Birse

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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The role of classical neurotransmitters in the transfer and processing of olfactory information is well established in many organisms. Neuropeptide action, however, is largely unexplored in any peripheral olfactory system. A subpopulation of local interneurons (LNs) in the Drosophila antannal lobe is peptidergic, expressing Drosophila tachykinins (DTKs). We show here that olfactory receptor neurons (ORNs) express the DTK receptor (DTKR). Using twophoton microscopy, we found that DTK applied to the antennal lobe suppresses presynaptic calcium and synaptic transmission in the ORNs. Furthermore, reduction of DTKR expression in ORNs by targeted RNA interference eliminates presynaptic suppression and alters olfactory behaviors. We detect opposite behavioral phenotypes after reduction and over expression of DTKR in ORNs. Our findings suggest a presynaptic inhibitory feedback to ORNs from peptidergic LNs in the antennal lobe.olfactory behavior ͉ presynaptic inhibition ͉ tachykinin ͉ two-photon imaging I n Drosophila, odor detection begins when odor molecules activate olfactory receptor neurons (ORNs) in the antennae and maxillary palps. Each of the ORNs expresses only 1 or a few members of a large family of odorant receptor genes (1-4). These ORNs propagate activity to neurons with dendrites in the glomerular compartments of the antennal lobe; each glomerulus receives inputs from ORNs that express the same odorant receptor (1, 3, 5, 6). In the glomeruli, the activity is read by second-order neurons, designated projection neurons (PNs), which relay information to higher olfactory centers in the brain (7).Inhibitory circuits in the glomeruli, mediated by local interneurons (LNs), play a key role in modulating glomerular signal activity. Presynaptic GABAergic inhibition of the ORNs has been shown in both Drosophila (8, 9) and in mammals (10-12). Conversely, cholinergic LNs in the Drosophila antennal lobe have been suggested to increase and redistribute odor-evoked activity at low odor concentrations (13,14).In addition to GABA and acetylcholine it is likely that certain neuropeptides are used as neuromodulators in the antennal lobe circuitry of insects (15, 16), as also suggested in the olfactory bulb in mammals (17,18). One neuropeptide gene that has been implicated in olfactory processing is dtk (19), a gene encoding 5 tachykinin-related peptides, DTKs (20). The DTKs are expressed in Ϸ150 neurons in the Drosophila brain, and in the antennal lobe glomeruli, there are extensive DTK-immunoreactive arborizations derived from a subset of antennal lobe LNs (21). Two DTK receptors, DTKR and NKD, have been identified in Drosophila (22, 23) and 1 of these, DTKR, is strongly expressed in antennal lobe glomeruli (24). Behavioral evidence for a role of DTKs in olfaction was obtained from analysis of flies where dtk expression was knocked down globally using RNA interference (RNAi); these flies displayed diminished odor sensitivity (19).To gain insight into the neuromodulation provided by the DTK signaling system in the antennal lob...

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Section: Methodsmentioning

confidence: 80%

Section: Methodsmentioning

confidence: 99%

“…Immunocytochemistry using an antiserum to the tachykinin receptor DTKR (24) showed that expression in the antennae is localized to cell bodies of ORNs (Fig. 2B).…”

Section: Distribution Of Dtk Peptide and Its Receptor Dtkr In The Olfmentioning

confidence: 99%

Section: The Tachykinin Receptor Dtkr Mediates Presynaptic Inhibition Inmentioning

confidence: 99%

mentioning

confidence: 99%

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Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Ignell

Root

Birse

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

161

197

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Colocalization of allatotropin and tachykinin‐related peptides with classical transmitters in physiologically distinct subtypes of olfactory local interneurons in the cockroach (Periplaneta americana)

Fusca

Schachtner

Kloppenburg

2015

J of Comparative Neurology

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In the insect antennal lobe different types of local interneurons mediate complex excitatory and inhibitory interactions between the glomerular pathways to structure the spatiotemporal representation of odors. Mass spectrometric and immunohistochemical studies have shown that in local interneurons classical neurotransmitters are likely to colocalize with a variety of substances that can potentially act as cotransmitters or neuromodulators. In the antennal lobe of the cockroach Periplaneta americana, gamma-aminobutyric acid (GABA) has been identified as the potential inhibitory transmitter of spiking type I local interneurons, whereas acetylcholine is most likely the excitatory transmitter of nonspiking type IIa1 local interneurons. This study used whole-cell patch clamp recordings combined with single-cell labeling and immunohistochemistry to test if the GABAergic type I local interneurons and the cholinergic type IIa1 local interneurons express allatotropin and tachykinin-related neuropeptides (TKRPs). These are two of the most abundant types of peptides in the insect antennal lobe. GABA-like and choline acetyltransferase (ChAT)-like immunoreactivity were used as markers for GABAergic and cholinergic neurons, respectively. About 50% of the GABA-like immunoreactive (-lir) spiking type I local interneurons were allatotropin-lir, and ∼ 40% of these neurons were TKRP-lir. About 20% of nonspiking ChAT-lir type IIa1 local interneurons were TKRP-lir. Our results suggest that in subpopulations of GABAergic and cholinergic local interneurons, allatotropin and TKRPs might act as cotransmitters or neuromodulators. To unequivocally assign neurotransmitters, cotransmitters, and neuromodulators to identified classes of antennal lobe neurons is an important step to deepen our understanding of information processing in the insect olfactory system.

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Presynaptic modulation of early olfactory processing in Drosophila

Wang

2011

Developmental Neurobiology

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Most animals are endowed with an olfactory system that is essential for finding foods, avoiding predators, and locating mating partners. The olfactory system must encode the identity and intensity of behaviorally relevant stimuli in a dynamic environmental landscape. How is olfactory information represented? How is a large dynamic range of odor concentrations represented in the olfactory system? How is this representation modulated to meet the demands of different internal physiological states? Recent studies have found that sensory terminals are important targets for neuromodulation. The emerging evidence suggests that presynaptic inhibition scales with sensory input and thus, provides a mechanism to increase dynamic range of odor representation. In addition, presynaptic facilitation could be a mechanism to alter behavioral responses in hungry animals. This review will focus on the GABAB receptor-mediated presynaptic inhibition, and neuropeptide-mediated presynaptic modulation in Drosophila.

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Widely distributedDrosophila G-protein-coupled receptor (CG7887) is activated by endogenous tachykinin-related peptides

Cited by 89 publications

References 38 publications

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Colocalization of allatotropin and tachykinin‐related peptides with classical transmitters in physiologically distinct subtypes of olfactory local interneurons in the cockroach (Periplaneta americana)

Presynaptic modulation of early olfactory processing in Drosophila

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