Expression mosaic of odorant‐binding proteins in <i>Drosophila</i> olfactory organs

Shanbhag, Shubha R.; Hekmat-Scafe, Daria S.; Kim, M. S.; Park, S. K.; Carlson, John R.; Pikielny, Claudio W.; Smith, Dean P.; Steinbrecht, Rudolf Alexander

doi:10.1002/jemt.1179

Cited by 108 publications

(99 citation statements)

References 44 publications

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“…2D). The localization of CjapNPC2 was similar to that of OBP (25), suggesting that CjapNPC2 is likely to carry hydrophobic compounds in the sensillum cavity in the basiconic sensillum.…”

Section: Cjapnpc2 Accumulates In the Sensillum Cavity In Worker Basicmentioning

confidence: 74%

Niemann–Pick type C2 protein mediating chemical communication in the worker ant

Ishida

Tsuchiya

Fujii

et al. 2014

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

104

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Ants are eusocial insects that are found in most regions of the world. Within its caste, worker ants are responsible for various tasks that are required for colony maintenance. In their chemical communication, α-helical carrier proteins, odorant-binding proteins, and chemosensory proteins, which accumulate in the sensillum lymph in the antennae, play essential roles in transferring hydrophobic semiochemicals to chemosensory receptors. It has been hypothesized that semiochemicals are recognized by α-helical carrier proteins. The number of these proteins, however, is not sufficient to interact with a large number of semiochemicals estimated from chemosensory receptor genes. Here we shed light on this conundrum by identifying a Niemann–Pick type C2 (NPC2) protein from the antenna of the worker Japanese carpenter ant, Camponotus japonicus (CjapNPC2). CjapNPC2 accumulated in the sensillum cavity in the basiconic sensillum. The ligand-binding pocket of CjapNPC2 was composed of a flexible β-structure that allowed it to bind to a wide range of potential semiochemicals. Some of the semiochemicals elicited electrophysiolgical responses in the worker antenna. In vertebrates, NPC2 acts as an essential carrier protein for cholesterol from late endosomes and lysosomes to other cellular organelles. However, the ants have evolved an NPC2 with a malleable ligand-binding pocket as a moderately selective carrier protein in the sensillum cavity of the basiconic sensillum. CjapNPC2 might be able to deliver various hydrophobic semiochemicals to chemosensory receptor neurons and plays crucial roles in chemical communication required to perform the worker ant tasks.

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“…2D). The localization of CjapNPC2 was similar to that of OBP (25), suggesting that CjapNPC2 is likely to carry hydrophobic compounds in the sensillum cavity in the basiconic sensillum.…”

Section: Cjapnpc2 Accumulates In the Sensillum Cavity In Worker Basicmentioning

confidence: 74%

Niemann–Pick type C2 protein mediating chemical communication in the worker ant

Ishida

Tsuchiya

Fujii

et al. 2014

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

104

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“…In D. melanogaster, diverse OBPs are synthesised in the same supporting cells and then secreted to a Insect chemosensory gene family evolution A Sánchez-Gracia et al restricted group of specialised sensilla. Moreover, the same OBPs can be expressed in several types of olfactory hairs and even in non-sensory tissues (Galindo and Smith, 2001;Shanbhag et al, 2001;Hekmat-Scafe et al, 2002). In contrast, olfactory and gustatory receptors are expressed in a much more precise pattern, with each sensory neuron deterministically expressing only a few specific chemoreceptor genes (generally not more than two).…”

Section: Genomic Organisation and Phylogenetic Analysismentioning

confidence: 99%

Molecular evolution of the major chemosensory gene families in insects

2009

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Chemoreception is a crucial biological process that is essential for the survival of animals. In insects, olfaction allows the organism to recognise volatile cues that allow the detection of food, predators and mates, whereas the sense of taste commonly allows the discrimination of soluble stimulants that elicit feeding behaviours and can also initiate innate sexual and reproductive responses. The most important proteins involved in the recognition of chemical cues comprise moderately sized multigene families. These families include odorant-binding proteins (OBPs) and chemosensory proteins (CSPs), which are involved in peripheral olfactory processing, and the chemoreceptor superfamily formed by the olfactory receptor (OR) and gustatory receptor (GR) families. Here, we review some recent evolutionary genomic studies of chemosensory gene families using the data from fully sequenced insect genomes, especially from the 12 newly available Drosophila genomes. Overall, the results clearly support the birth-and-death model as the major mechanism of evolution in these gene families. Namely, new members arise by tandem gene duplication, progressively diverge in sequence and function, and can eventually be lost from the genome by a deletion or pseudogenisation event. Adaptive changes fostered by environmental shifts are also observed in the evolution of chemosensory families in insects and likely involve reproductive, ecological or behavioural traits. Consequently, the current size of these gene families is mainly a result of random gene gain and loss events. This dynamic process may represent a major source of genetic variation, providing opportunities for FUTURE specific adaptations.

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“…In contrast, basiconic sensilla display a dendritic branching pattern, with their dendrites split into as few as 5 to as many as 150 parallel terminal branches (29). As with pheromone-detecting sensilla in moths, which house species-specific pheromone-binding proteins (26), an OBP from D. melanogaster, termed LUSH, is specifically expressed in trichoid sensilla (31) and seems to be essential for pheromone reception (23). In addition, a sensory membrane protein (SNMP), originally isolated from moth antennae (32), seems essential for pheromone detection in the trichoid sensilla of the fruit fly, but it is not involved in odorant reception by basiconic sensilla (33).…”

Section: Responses To Bombykol By Bmoror1 Receptors In the Trichoidmentioning

confidence: 99%

Bombykol receptors in the silkworm moth and the fruit fly

Syed¹,

Kopp

Kimbrell

et al. 2010

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

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Male moths are endowed with odorant receptors (ORs) to detect species-specific sex pheromones with remarkable sensitivity and selectivity. We serendipitously discovered that an endogenous OR in the fruit fly, Drosophila melanogaster, is highly sensitive to the sex pheromone of the silkworm moth, bombykol. Intriguingly, the fruit fly detectors are more sensitive than the receptors of the silkworm moth, although its ecological significance is unknown. By expression in the "empty neuron" system, we identified the fruit fly bombykol-sensitive OR as DmelOR7a (= DmOR7a). The profiles of this receptor in response to bombykol in the native sensilla (ab4) or expressed in the empty neuron system (ab3 sensilla) are indistinguishable. Both WT and transgenic flies responded with high sensitivity, in a dose-dependent manner, and with rapid signal termination. In contrast, the same empty neuron expressing the moth bombykol receptor, BmorOR1, demonstrated low sensitivity and slow signal inactivation. When expressed in the trichoid sensilla T1 of the fruit fly, the neuron housing BmorOR1 responded with sensitivity comparable to that of the native trichoid sensilla in the silkworm moth. By challenging the native bombykol receptor in the fruit fly with high doses of another odorant to which the receptor responds with the highest sensitivity, we demonstrate that slow signal termination is induced by overdose of a stimulus. As opposed to the empty neuron system in the basiconic sensilla, the structural, biochemical, and/or biophysical features of the sensilla make the T1 trichoid system of the fly a better surrogate for the moth receptor.S ince the identification of bombykol (IUPAC name (10E,12Z)-hexadeca-10,12-dien-1-ol) as a sex pheromone for the silkworm moth, Bombyx mori (1), hundreds of sex pheromones have been identified from lepidopteran species (2). In general, femaleproduced sex pheromones in moths are complex mixtures of straight-chain acetates, aldehydes, and alcohols, with 10-12 carbon atoms and up to three unsaturations (3). This fatty acid-derived semiochemistry (4, 5) is unique to chemical communication in moths, although (7Z)-dodec-7-en-1-yl acetate also has been identified as a sex pheromone for the Asian elephant, Elephas maximus (6). Male moths detect these sex pheromones with such high selectivity and sensitivity that minimal structural modifications render them inactive (7), whereas a single molecule of bombykol is estimated to be sufficient to activate olfactory receptor neurons (ORNs) in male antennae of the silkworm moth (8). These species-specific communication channels seem to have evolved under a strong evolutionary pressure into a sophisticated signal receptor system. In contrast, we have serendipitously identified an ORN housed in the ab4 basiconic sensilla in the antennae of the fruit fly, Drosophila melanogaster, which responds to bombykol with high sensitivity (9), although the ecological significance of this bombykol detector in the fruit fly remains enigmatic. The OR housed in the ab4a neuron was pr...

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Expression mosaic of odorant‐binding proteins in Drosophila olfactory organs

Cited by 108 publications

References 44 publications

Niemann–Pick type C2 protein mediating chemical communication in the worker ant

Niemann–Pick type C2 protein mediating chemical communication in the worker ant

Molecular evolution of the major chemosensory gene families in insects

Bombykol receptors in the silkworm moth and the fruit fly

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