Plasticity of the Electrical Connectome of C. elegans

Abstract

The specific patterns and functional properties of electrical synapses of a nervous system are defined by the neuron-specific complement of electrical synapse constituents. We systematically examined the molecular composition of the electrical connectome of the nematode C. elegans through a genomeand nervous-system-wide analysis of the expression patterns of the invertebrate electrical synapse constituents, the innexins. We observe highly complex combinatorial expression patterns throughout the nervous system and found that these patterns change in a strikingly neuron-type-specific manner throughout the nervous system when animals enter an insulin-controlled diapause arrest stage under harsh environmental conditions, the dauer stage. By analyzing several individual synapses, we demonstrate that dauer-specific electrical synapse remodeling is responsible for specific aspects of the altered locomotory and chemosensory behavior of dauers. We describe an intersectional gene regulatory mechanism involving terminal selector and FoxO transcription factors mediating dynamic innexin expression plasticity in a neuron-type-and environment-specific manner.

The Caenorhabditis elegans INX‐4/Innexin is required for the fine‐tuning of temperature orientation in thermotaxis behavior

“…Innexins are wide expressed in nervous system of C. elegans (Altun et al, 2009;Bhattacharya et al, 2019) to form gap junctions (electrical synapses). Some studies to date reported their implication of neuronal innexins in behavior: unc-9 for aggregation of social behavior (Jang et al, 2017), inx-1 for behavioral components of avoidance behavior (Hori, Oda, Suehiro, Iino, & Mitani, 2018), and unc-9 and unc-7 for bias for forward movement (Kawano et al, 2011) and regulation of sleep (Huang et al, 2018).…”

“…The human genome contains 21 connexins and 3 pannexins (Penuela, Harland, Simek, & Laird, ; Söhl & Willecke, ), whereas the Caenorhabditis elegans and Drosophila melanogaster genomes have 25 and 8 innexins, respectively (Phelan & Starich, ; Stebbings et al, ). Although in vivo neuronal expressions of innexins are documented comprehensively in C. elegans (Altun, Chen, Wang, & Hall, ; Bhattacharya, Aghayeva, Berghoff, & Hobert, ), their roles in biological processes are still poorly understood.…”

Gap junctions in theC. elegansnervous system regulate ageing and lifespan

“…2). C. elegans gap junctions have a plethora of functions in all organs, with different groups of innexins being expressed in each of them 18,20 .…”

Diet-responsive Transcriptional Regulation of Insulin in a Single Neuron Controls Systemic Metabolism

“…Neurons are terminally differentiated, yet retain a degree of plasticity to facilitate responses to ephemeral environments and internal metabolic states (Bhattacharya et al, 2019;Cho et al, 2016;Delaney et al, 2017;Gruner et al, 2014;Pocock and Hobert, 2010;Witham et al, 2016). Neuronal plasticity can be mediated through transcriptional changes that alter synapse formation, receptor composition, and signalling molecules (Bayer and Hobert, 2018;Gruner et al, 2016).…”

“…Currently, however, there is a dearth of knowledge about the transcription factors that define and drive neuronal adaption to nutrient availability. And we are only just beginning to appreciate the extent to which the transcription factors that specify neuronal fates are re-purposed, post-mitotically, to drive adaptive changes in neuronal gene expression (Bhattacharya et al, 2019).…”