Convergent Evolution of Sodium Ion Selectivity in Metazoan Neuronal Signaling

Polarized distribution of signaling molecules to axons and dendrites facilitates directional information flow in complex vertebrate nervous systems. The topic we address here is when the key aspects of neuronal polarity evolved. All neurons have a central cell body with thin processes that extend from it to cover long distances, and they also all rely on voltage-gated ion channels to propagate signals along their length. The most familiar neurons, those in vertebrates, have additional cellular features that allow them to send directional signals efficiently. In these neurons, dendrites typically receive signals and axons send signals. It has been suggested that many of the distinct features of axons and dendrites, including the axon initial segment, are found only in vertebrates. However, it is now becoming clear that two key cytoskeletal features that underlie polarized sorting, a specialized region at the base of the axon and polarized microtubules, are found in invertebrate neurons as well. It thus seems likely that all bilaterians generate axons and dendrites in the same way. As a next step, it will be extremely interesting to determine whether the nerve nets of cnidarians and ctenophores also contain polarized neurons with true axons and dendrites, or whether polarity evolved in concert with the more centralized nervous systems found in bilaterians. KEY WORDS: Axon, Dendrite, Axon initial segment, MicrotubuleIntroduction: are vertebrates special because of their neurons?The elaborate behaviors of vertebrates are made possible by the evolution of nervous systems of unparalleled size and complexity. The developmental mechanisms that assemble the vertebrate nervous system and physical mapping of the circuits that underlie behavior are subjects of intense study. But are the neurons of the vertebrate nervous system themselves also unique or special in some way? Do they have vertebrate-only features that facilitate the assembly of large, complex nervous systems? Or is the vertebrate nervous system based on an ancient and highly adaptable neuronal cell type? Understanding the evolutionary history of neurons is critical to understanding how vertebrate nervous systems and behavior came to be. Another very practical reason for asking these questions is that it is helpful to know which features of neurons are shared with and can thus be studied in cheap, efficient invertebrate model systems. Vertebrate-specific neuronal features, in contrast, must be studied in model systems such as zebrafish or mouse, for which time and expense often limit the scientific questions that can be asked.The polarized functional organization of neurons that facilitates assembly of complex circuits might be a good candidate for being associated specifically with vertebrates. Indeed, in a highly cited review on neuronal polarity from 1994, invertebrate neurons are seen as 'sufficiently different' in terms of organization from vertebrate neurons that the polarized sorting mechanisms are suggested to also differ (Craig and Banker, 1994...

Section: So When Did Neuronal Polarity Evolve?mentioning

confidence: 99%

Neuronal polarity: an evolutionary perspective

Rolls

Jegla

2015

“…It is thought that in the common ancestor of vertebrates only one Na V 1 gene was present, which underwent two rounds of duplication in the basal vertebrate and further duplication and diversification in teleosts and tetrapods (Widmark et al, 2011;Zakon et al, 2011). As in the case of K V s discussed before, the finding of such a diversity of sodium channels in a sea anemone was highly unexpected (Gur Barzilai et al, 2012).Heterologous expression of NvNa V 2.5 showed this channel to be sodium selective, similar to Na V 1 channels (Gur Barzilai et al, 2012). Moreover, replacing the selectivity filter of NvNa V 2.5 (DKEA) with that from Na V 1 (DEKA) resulted in the loss of sodium selectivity (Gur Barzilai et al, 2012), while replacing the selectivity filter of Na V 1 with that from NvNa V 2.5 also resulted in the loss of sodium selectivity (Schlief et al, 1996).…”

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confidence: 92%

“…Moreover, as K V s generates the falling phase of the action potential, while Na V s is responsible for its rising phase, there is a clear functional advantage in separating the sodium and potassium ion fluxes and increasing the selectivity of Na V channels to sodium ions. It is therefore likely that the pore regions in both the urbilaterian Na V 1 and the primordial Na V 2.5 cnidarian channel evolved under selective pressure to cease potassium and calcium ion conductance, resulting in sodium-selective channels.Despite the advantages of sodium selectivity, Nematostella Na V 2.5 was shown to be expressed only in a subset of cells, while many other putative neurons express calcium-conducting Na V 2 channels (Gur Barzilai et al, 2012), indicating that cnidarian signaling is heavily based on calcium. Hence, it is likely that when early neuronal networks emerged, their signaling was calcium based, as exemplified by contemporary ctenophores (Hille, 2001;Meech and Mackie, 2007).…”

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confidence: 99%

“…Examination of the selectivity filters of the Monosiga and Thecamonas channels showed they are constituted of the residues DEEA and DEES, respectively (Liebeskind et al, 2011; Cai, 2012). In Trichoplax and Mnemiopsis, all Na V channels were found to have the selectivity filer DEEA (Liebeskind et al, 2011;Gur Barzilai et al, 2012). However, in sponges, no Na V channel homologs are present.…”

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confidence: 99%

See 1 more Smart Citation

Evolution of voltage-gated ion channels at the emergence of Metazoa

Moran

Barzilai

Liebeskind

et al. 2015

Self Cite

122

112

Voltage-gated ion channels are large transmembrane proteins that enable the passage of ions through their pore across the cell membrane. These channels belong to one superfamily and carry pivotal roles such as the propagation of neuronal and muscular action potentials and the promotion of neurotransmitter secretion in synapses. In this review, we describe in detail the current state of knowledge regarding the evolution of these channels with a special emphasis on the metazoan lineage. We highlight the contribution of the genomic revolution to the understanding of ion channel evolution and for revealing that these channels appeared long before the appearance of the first animal. We also explain how the elucidation of channel selectivity properties and function in non-bilaterian animals such as cnidarians (sea anemones, corals, jellyfish and hydroids) can contribute to the study of channel evolution. Finally, we point to open questions and future directions in this field of research. KEY WORDS: Voltage-gated ion channels, Animal evolution, Ion selectivity Introduction: the superfamily of voltage-gated ion channelsThis review aims to cover and clarify the evolution and diversification of metazoan voltage-gated ion channels, particularly at the beginning of multicellularity in the lineage leading to Metazoa and at the emergence of nervous systems. Voltage-gated ion channels are imperative for neuronal signaling, muscle contraction and secretion, and are thought to play a critical role in the evolution of animals (Hille, 2001). Nonetheless, these channels are also found in prokaryotes and viruses, although their roles in these organisms are largely unknown (Martinac et al., 2008;Plugge et al., 2000). The superfamily of voltage-gated ion channels is characterized by the ability to rapidly respond to changes in membrane potential (hence 'voltage-gated'), which results in selective ion conductance. This ion channel superfamily includes voltage-gated potassium channels (K V s), voltage-gated calcium channels (Ca V s) and voltage-gated sodium channels (Na V s). Their α-subunits are composed of four domains (DI-IV), with each domain containing six transmembrane segments (S1-S6; Fig. 1) (Noda et al., 1984;Noda et al., 1986;Guy and Seetharamulu, 1986;Tanabe et al., 1987). Voltage-dependent activation is enabled by conserved positively charged residues at every third position in S4 (voltage sensor) of the four domains, which move outwards upon changes in membrane potential (Noda et al., 1984; Catterall, 1986;Guy and Seetharamulu, 1986), inducing a conformational change that results in opening of the channel pore (Armstrong and Bezanilla, 1974;Stühmer et al., 1989;Papazian et al., 1991;Yang et al., 1996). The pore is formed by the segments S5 and S6, and the selectivity to specific ions is enabled by the selectivity filter, which is composed of conserved residues, specific for the ion conducted by the channel, and these residues are situated at the pore-lining loops (p-loops) connecting S5 to S6 in the four domains ( ...

“…Choanoflagellates do not produce synapses and neurons, but the genome of M. brevicollis encodes synaptic protein homologs, including cation channels similar to voltage-gated sodium channels (Liebeskind et al, 2011;Gur Barzilai et al, 2012) and the postsynaptic density (PSD) proteins Homer, Shank and PSD-95 (Alié and Manuel, 2010;Emes and Grant, 2012;Ryan and Grant, 2009;Sakarya et al, 2007). Moreover, homologs of various types of metazoan plasma membrane Ca 2+ channels including the storeoperated channel, ligand-operated channels, voltage-operated channels, second messenger-operated channels and transient…”

Section: Introductionmentioning

confidence: 99%

The origin and evolution of synaptic proteins – choanoflagellates lead the way

Burkhardt

2015

The origin of neurons was a key event in evolution, allowing metazoans to evolve rapid behavioral responses to environmental cues. Reconstructing the origin of synaptic proteins promises to reveal their ancestral functions and might shed light on the evolution of the first neuron-like cells in metazoans. By analyzing the genomes of diverse metazoans and their closest relatives, the evolutionary history of diverse presynaptic and postsynaptic proteins has been reconstructed. These analyses revealed that choanoflagellates, the closest relatives of metazoans, possess diverse synaptic protein homologs. Recent studies have now begun to investigate their ancestral functions. A primordial neurosecretory apparatus in choanoflagellates was identified and it was found that the mechanism, by which presynaptic proteins required for secretion of neurotransmitters interact, is conserved in choanoflagellates and metazoans. Moreover, studies on the postsynaptic protein homolog Homer revealed unexpected localization patterns in choanoflagellates and new binding partners, both which are conserved in metazoans. These findings demonstrate that the study of choanoflagellates can uncover ancient and previously undescribed functions of synaptic proteins.