Cytoskeletal and synaptic polarity of LWamide-like+ ganglion neurons in the sea anemone Nematostella vectensis

Abstract

The centralized nervous systems of bilaterian animals rely on directional signaling facilitated by polarized neurons with specialized axons and dendrites. It is not known whether axo-dendritic polarity is exclusive to bilaterians or was already present in early metazoans. We therefore examined neurite polarity in the starlet sea anemone Nematostella vectensis (Cnidaria). Cnidarians form a sister clade to bilaterians and share many neuronal building blocks characteristic of bilaterians including channels, receptors and synaptic proteins, but their nervous systems comprise a comparatively simple net distributed throughout the body. We developed a tool kit of fluorescent polarity markers for live imaging analysis of polarity in an identified neuron type, large ganglion cells of the body column nerve net that express the LWamide-like neuropeptide. Microtubule polarity differs in bilaterian axons and dendrites, and this in part underlies polarized distribution of cargo to the two types of processes. However, in LWamide-like+ neurons, all neurites had axon-like microtubule polarity suggesting that they may have similar contents. Indeed, presynaptic and postsynaptic markers trafficked to all neurites and accumulated at varicosities where neurites from different neurons often crossed, suggesting the presence of bidirectional synaptic contacts. Furthermore, we could not identify a diffusion barrier in the plasma membrane of any of the neurites like the axon initial segment barrier that separates the axonal and somatodendritic compartments in bilaterian neurons. We conclude that at least one type of neuron in Nematostella vectensis lacks the axo-dendritic polarity characteristic of bilaterian neurons.

Evolution of synapses and neurotransmitter systems: The divide-and-conquer model for early neural cell-type evolution

“…In addition, dense-core vesicles at two-way interneuronal synapses and at neuromuscular synapses have been labelled with antibodies against the neuropeptides RFamide and RWamide indicating the involvement of neuropeptides in synaptic signalling. Consistent with bidirectional signalling, at least one neuron type in Nematostella lacks segregated axo-dendritic compartments as suggested by the live imaging of vesicle transport [68]. Both cnidarian and ctenophore inter-neuronal and neuromuscular synapses lack recognizable postsynaptic specializations in electron micrographs (although in the cnidarian Chrysaora postsynaptic cisternae in the muscle have been described [64](Figure 3B).…”

“…Both cnidarian and ctenophore inter-neuronal and neuromuscular synapses lack recognizable postsynaptic specializations in electron micrographs (although in the cnidarian Chrysaora postsynaptic cisternae in the muscle have been described [64](Figure 3B). However, fluorescently tagged Homer and synaptobrevin (putative markers for post and presynapses) showed contact sites between neurites in Nematostella [68]. Consistent with the role of Homer in postsynaptic sites, another study found Homer puncta in transgenic Nematostella at tentacle-retractor and mesentery-retractor muscles and Homer co-expressed with Shank and iGluRs in muscle-cell transcriptomes [69].…”

Neuropeptide repertoire and 3D anatomy of the ctenophore nervous system

“…35 homologs of voltage-gated potassium channels, 40 two voltage-gated sodium channels, 41 and the voltage-gated calcium channel MleCav2, 42 as well as several homologs of ionotropic glutamate receptors 15,39 and other ion channels, Na/Ca exchanger, a sodium/potassium transporting ATPase, and two innexins are either overexpressed or detectable in the C33 metacell (Table 1; Data S2D). The C33 metacell also expressed structural components defining neuron morphology: [43][44][45] three enriched tubulin genes; the F-actin binding protein dematin; the actin cytoskeleton organizer ABLIM3; contactin 5 and contactin protein-like 2; as well as genes described by ''actin binding'' and ''tubulin binding'' Gene Ontology (GO) terms (Data S2E and S2F). Thus, the expression of multiple genes important for neuronal functions further confirmed that C33 is a neuronal metacell.…”

The chemical brain hypothesis for the origin of nervous systems

“…We will need to learn more about synapses and transmitters in cnidarians. New transgenic approaches [ 137 , 138 ] and serial EM could help to address this.…”