Systematic morphological and morphometric analysis of identified olfactory receptor neurons in Drosophila melanogaster

Gonzales, Cesar Nava; McKaughan, Quintyn; Bushong, Eric A.; Cauwenberghs, Kalyani; Ng, Renny; Madany, Matthew; Ellisman, Mark H.; Su, Chih‐Ying

doi:10.7554/elife.69896

Cited by 31 publications

(48 citation statements)

References 41 publications

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“…Olfactory sensory neurons are housed in two olfactory organs in D. melanogaster (and other insects), the antenna and maxillary palp ( Figure 1B ). Each OSN extends a ciliated dendrite, where receptor proteins localize, into porous cuticular hairs on the organ surface ( Schmidt and Benton, 2020 ; Gonzales et al, 2021 ). OSN axons project to the antennal lobe in the brain ( Figure 1B ).…”

Section: Insect Olfactory System Basicsmentioning

confidence: 99%

Olfactory Receptor Gene Regulation in Insects: Multiple Mechanisms for Singular Expression

Mika

Benton

2021

Front. Neurosci.

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The singular expression of insect olfactory receptors in specific populations of olfactory sensory neurons is fundamental to the encoding of odors in patterns of neuronal activity in the brain. How a receptor gene is selected, from among a large repertoire in the genome, to be expressed in a particular neuron is an outstanding question. Focusing on Drosophila melanogaster, where most investigations have been performed, but incorporating recent insights from other insect species, we review the multilevel regulatory mechanisms of olfactory receptor expression. We discuss how cis-regulatory elements, trans-acting factors, chromatin modifications, and feedback pathways collaborate to activate and maintain expression of the chosen receptor (and to suppress others), highlighting similarities and differences with the mechanisms underlying singular receptor expression in mammals. We also consider the plasticity of receptor regulation in response to environmental cues and internal state during the lifetime of an individual, as well as the evolution of novel expression patterns over longer timescales. Finally, we describe the mechanisms and potential significance of examples of receptor co-expression.

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Section: Insect Olfactory System Basicsmentioning

confidence: 99%

Olfactory Receptor Gene Regulation in Insects: Multiple Mechanisms for Singular Expression

Mika

Benton

2021

Front. Neurosci.

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“…Given that tormogen cells are also present in sensilla equipped with OSNs that do not express Orco, such as those broadly found in coeloconic sensilla which instead express ionotropic receptors (IRs) sensitive to carboxylic acids and amines, we repeated the experiment with balsamic vinegar, which has been shown to elicit responses in IR-positive, Orco-negative OSNs (Jain et al, 2021). Moreover, we were prompted to test balsamic vinegar due to the fact that tormogen cells also occur in duplets in Drosophila coeloconic sensilla (Shanbhag et al, 2000;Nava Gonzales et al, 2021). Here we found no significant intracellular Ca 2+ responses to vinegar as compared to VUAA1 stimulations (Figure 2C).…”

Section: Evaluation Of Drosophila Support Cell Markers For the Third Antennal Segmentmentioning

confidence: 99%

“…By the same token, do support cells found within larval olfactory systems (Hartenstein, 1988) share similar principles with those of the imago? What are the functions of the numerous extracellular vesicles observed in Drosophila sensilla, suggested to arise from olfactory support cells (Nava Gonzales et al, 2021)? Are various support cell functions conserved across sensory modalities, in other structures such as chordotonal organs, and in sensillum classes that serve gustation and hygro-or thermo-sensing?…”

Section: Future Perspectivesmentioning

confidence: 99%

“…Moreover, auxiliary cells form numerous seals and contacts around the sensory neuron by virtue of septate junctions, as well as maintain closed compartments such as the sensillum lymph and perineuronal lumen between neuron and thecogen cell (Steinbrecht, 1980;Keil andSteinbrecht, 1983, 1987;De Kramer, 1985;Shanbhag et al, 2000). Lastly, auxiliary cells display clear morphological specializations, such as the rich presence of microvilli, proteasomes, mitochondria and vesicles (Shanbhag et al, 2000;Nava Gonzales et al, 2021), suggesting that auxiliary cells function and retain continuous metabolic activity throughout insect adulthood.…”

Section: Introductionmentioning

confidence: 99%

“…Atypically to the general rule of one support cell type per sensillum, Drosophila coeloconic sensilla are populated with two tormogen cells (Shanbhag et al, 2000). A mature tormogen cell is distinct from the trichogen cell in that it extends a characteristically long, stalk-like protrusion that terminates below the level of the OSN soma, at least in Drosophila (Nava Gonzales et al, 2021). Though the validity of the marking is somewhat unclear, tormogen cells have been historically tagged using a promoter found upstream of the Suppressor of Hairless gene (Su(H)) termed ASE5 (Barolo et al, 2000), a DNA-binding protein component of the Notch signaling pathway (Bray and Furriols, 2001) which reportedly contributes to the terminal differentiation of the tormogen socket and trichogen shaft cells Posakony, 1992, 1994;Gho et al, 1996).…”

Section: Introductionmentioning

confidence: 99%

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Functional interaction between Drosophila olfactory sensory neurons and their support cells

Prelic

Mahadevan

Venkateswaran

et al. 2021

Preprint

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Insects detect volatile chemicals using antennae, which house a vast variety of olfactory sensory neurons (OSNs) that innervate hair-like structures called sensilla where odor detection takes place. In addition to OSNs, the antenna also hosts various support cell types. These include the triad of trichogen, tormogen and thecogen support cells that lie adjacent to their respective OSNs. The arrangement of OSN supporting cells occurs stereotypically for all sensilla and is widely conserved in evolution. While insect chemosensory neurons have received considerable attention, little is known about the functional significance of the cells that support them. For instance, it remains unknown whether support cells play an active role in odor detection, or only passively contribute to homeostasis, e.g. by maintaining sensillum lymph composition. To investigate the functional interaction between OSNs and support cells, we used optical and electrophysiological approaches in Drosophila. First, we characterized the distribution of various supporting cells using genetic markers. By means of an ex vivo antennal preparation and genetically-encoded Ca2+ and K+ indicators, we then studied the activation of these auxiliary cells during odor presentation in adult flies. We observed acute responses and distinct differences in Ca2+ and K+ fluxes between support cell types. Finally, we observed alterations in OSN responses upon thecogen cell ablation in mature adults. Upon inducible ablation of thecogen cells, we notice a gain in mechanical responsiveness to mechanical stimulations during single-sensillum recording, but a lack of change to neuronal resting activity. Taken together, these results demonstrate that support cells play a more active and responsive role during odor processing than previously thought. Our observations thus reveal that support cells functionally interact with OSNs and may be important for the extraordinary ability of insect olfactory systems to dynamically and sensitively discriminate between odors in the turbulent sensory landscape of insect flight.

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Innexin expression and localization in the Drosophila antenna indicate gap junction or hemichannel involvement in antennal chemosensory sensilla

Prelic,

Keesey,

Lavista-Llanos

et al. 2024

Cell Tissue Res

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Odor detection in insects is largely mediated by structures on antennae called sensilla, which feature a strongly conserved architecture and repertoire of olfactory sensory neurons (OSNs) and various support cell types. In Drosophila, OSNs are tightly apposed to supporting cells, whose connection with neurons and functional roles in odor detection remain unclear. Coupling mechanisms between these neuronal and non-neuronal cell types have been suggested based on morphological observations, concomitant physiological activity during odor stimulation, and known interactions that occur in other chemosensory systems. For instance, it is not known whether cell–cell coupling via gap junctions between OSNs and neighboring cells exists, or whether hemichannels interconnect cellular and extracellular sensillum compartments. Here, we show that innexins, which form hemichannels and gap junctions in invertebrates, are abundantly expressed in adult drosophilid antennae. By surveying antennal transcriptomes and performing various immunohistochemical stainings in antennal tissues, we discover innexin-specific patterns of expression and localization, with a majority of innexins strongly localizing to glial and non-neuronal cells, likely support and epithelial cells. Finally, by injecting gap junction-permeable dye into a pre-identified sensillum, we observe no dye coupling between neuronal and non-neuronal cells. Together with evidence of non-neuronal innexin localization, we conclude that innexins likely do not conjoin neurons to support cells, but that junctions and hemichannels may instead couple support cells among each other or to their shared sensillum lymph to achieve synchronous activity. We discuss how coupling of sensillum microenvironments or compartments may potentially contribute to facilitate chemosensory functions of odor sensing and sensillum homeostasis.

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Systematic morphological and morphometric analysis of identified olfactory receptor neurons in Drosophila melanogaster

Cited by 31 publications

References 41 publications

Olfactory Receptor Gene Regulation in Insects: Multiple Mechanisms for Singular Expression

Olfactory Receptor Gene Regulation in Insects: Multiple Mechanisms for Singular Expression

Functional interaction between Drosophila olfactory sensory neurons and their support cells

Innexin expression and localization in the Drosophila antenna indicate gap junction or hemichannel involvement in antennal chemosensory sensilla

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