Dept. Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany.
Cell Tissue Res. 2024 Oct;398(1):35-62. doi: 10.1007/s00441-024-03909-3. Epub 2024 Aug 23.
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.
昆虫的气味检测主要由触角上称为感觉器的结构介导,这些结构具有强烈保守的结构和嗅觉感觉神经元(OSN)和各种支持细胞类型的 repertoire。在果蝇中,OSN 与支持细胞紧密相邻,其与神经元的连接及其在气味检测中的功能作用尚不清楚。基于形态学观察、气味刺激期间伴随的生理活性以及在其他化学感觉系统中发生的已知相互作用,提出了这些神经元和非神经元细胞类型之间的耦合机制。例如,尚不清楚 OSN 和邻近细胞之间是否存在通过间隙连接的细胞-细胞耦合,或者半通道是否互连成细胞和细胞外感觉器隔室。在这里,我们表明,在无脊椎动物中形成半通道和间隙连接的连接蛋白在成年果蝇触角中大量表达。通过调查触角转录组并在触角组织中进行各种免疫组织化学染色,我们发现连接蛋白具有特定的表达和定位模式,大多数连接蛋白强烈定位在神经胶质和非神经元细胞上,可能是支持细胞和上皮细胞。最后,通过将间隙连接可渗透的染料注入预先确定的感觉器中,我们观察到神经元和非神经元细胞之间没有染料耦合。结合非神经元连接蛋白定位的证据,我们得出结论,连接蛋白可能不会将神经元与支持细胞连接起来,而是连接蛋白和半通道可能将支持细胞彼此连接或连接到它们共享的感觉器淋巴中,以实现同步活动。我们讨论了感觉器微环境或隔室的耦合如何可能有助于促进气味感知和感觉器稳态的化学感觉功能。