jShaw1, a low-threshold, fast-activating Kv3 from the hydrozoan jellyfish <i>Polyorchis penicillatus</i>

Sand, Rheanna; Atherton, Donna; Spencer, Andrew N.; Gallin, Warren J.

doi:10.1242/jeb.057000

Cited by 13 publications

(11 citation statements)

References 64 publications

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“…Our results combined with previous studies (15,16,23,29,55) show that the functional and molecular diversification of Shaker and KCNQ families of voltage-gated K + channels was largely complete before the divergence of cnidarians and bilaterians. Furthermore, Erg K + channels, which constitute one of three bilaterian Ether-a-go-go gene subfamilies, are also highly conserved on functional level between cnidarians and vertebrates (70).…”

Section: Discussionsupporting

confidence: 79%

“…3 A and C, and Table 1). NvShaw1 currents are similar to Drosophila Shaw (26) and a Shaw channel from the hydrozoan Polyorchis penicillatus (29). We failed to obtain functional homomeric channels when we expressed two additional Shaw channels from the heart of the Nematostella gene expansion (Fig.…”

Section: Resultsmentioning

confidence: 78%

“…A Caenorhabditis elegans Shaw has slow kinetics but a high activation threshold (28), and a single expressed cnidarian Shaw channel has the opposite: a low activation threshold but relatively fast kinetics (29). Thus, the ancestral properties and function of Shaw channels is not yet understood.…”

Section: Significancementioning

confidence: 99%

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Major diversification of voltage-gated K ⁺ channels occurred in ancestral parahoxozoans

Liu²,

Luo³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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We examined the origins and functional evolution of the Shaker and KCNQ families of voltage-gated K + channels to better understand how neuronal excitability evolved. In bilaterians, the Shaker family consists of four functionally distinct gene families (Shaker, Shab, Shal, and Shaw) that share a subunit structure consisting of a voltage-gated K + channel motif coupled to a cytoplasmic domain that mediates subfamily-exclusive assembly (T1). We traced the origin of this unique Shaker subunit structure to a common ancestor of ctenophores and parahoxozoans (cnidarians, bilaterians, and placozoans). Thus, the Shaker family is metazoan specific but is likely to have evolved in a basal metazoan. Phylogenetic analysis suggested that the Shaker subfamily could predate the divergence of ctenophores and parahoxozoans, but that the Shab, Shal, and Shaw subfamilies are parahoxozoan specific. In support of this, putative ctenophore Shaker subfamily channel subunits coassembled with cnidarian and mouse Shaker subunits, but not with cnidarian Shab, Shal, or Shaw subunits. The KCNQ family, which has a distinct subunit structure, also appears solely within the parahoxozoan lineage. Functional analysis indicated that the characteristic properties of Shaker, Shab, Shal, Shaw, and KCNQ currents evolved before the divergence of cnidarians and bilaterians. These results show that a major diversification of voltage-gated K + channels occurred in ancestral parahoxozoans and imply that many fundamental mechanisms for the regulation of action potential propagation evolved at this time. Our results further suggest that there are likely to be substantial differences in the regulation of neuronal excitability between ctenophores and parahoxozoans.Shaker | KCNQ | Nematostella | ctenophore | Mnemiopsis

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Section: Discussionsupporting

confidence: 79%

Section: Resultsmentioning

confidence: 78%

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Major diversification of voltage-gated K ⁺ channels occurred in ancestral parahoxozoans

Liu²,

Luo³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Electrophysiology-Ionic currents were recorded 24 -48 h post-injection from X. laevis oocytes at room temperature using two-electrode voltage clamp as described previously (35). Traces were filtered at 1 kHz and sampled at 10 kHz with P/4 leak subtraction.…”

Section: Methodsmentioning

confidence: 99%

Fine-tuning of Voltage Sensitivity of the Kv1.2 Potassium Channel by Interhelix Loop Dynamics

Sand

Sharmin

Morgan

et al. 2013

Journal of Biological Chemistry

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Background: Potassium channels change conformation in response to transmembrane voltage. Results: The loop connecting the voltage sensing helix to an adjacent helix affects the voltage sensitivity. Conclusion: Loop length and charge distribution on the interacting surfaces of the voltage sensor and pore domain are responsible for this effect. Significance: Variation in loop length and composition is a factor in determining the voltage sensitivity of voltage-gated channels.

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“…On a molecular level, cnidarians share almost all the major gene families of neuronal signaling proteins with bilaterians (Putnam et al, 2007), including all gene families of voltage-gated ion channels (Nayak et al, 2009). The biophysical properties of the cnidarian channels in these families are highly conserved (Jegla et al, 1995; Jegla and Salkoff, 1997;Sand et al, 2011;Gur Barzilai et al, 2012; Jegla et al, 2012; Martinson et al, 2014), suggesting they play similar physiological roles. Furthermore, Nematostella has key components of the AIS barrier including β-spectrin (Putnam et al, 2007;Bennett and Lorenzo, 2013) and an ankyrin ortholog with a full β-spectrin binding domain (Putnam et al, 2007).…”

Section: So When Did Neuronal Polarity Evolve?mentioning

confidence: 99%

Neuronal polarity: an evolutionary perspective

Rolls

Jegla

2015

Journal of Experimental Biology

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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...

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jShaw1, a low-threshold, fast-activating Kv3 from the hydrozoan jellyfish Polyorchis penicillatus

Cited by 13 publications

References 64 publications

Major diversification of voltage-gated K ⁺ channels occurred in ancestral parahoxozoans

Major diversification of voltage-gated K ⁺ channels occurred in ancestral parahoxozoans

Fine-tuning of Voltage Sensitivity of the Kv1.2 Potassium Channel by Interhelix Loop Dynamics

Neuronal polarity: an evolutionary perspective

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jShaw1, a low-threshold, fast-activating Kv3 from the hydrozoan jellyfish Polyorchis penicillatus

Cited by 13 publications

References 64 publications

Major diversification of voltage-gated K + channels occurred in ancestral parahoxozoans

Major diversification of voltage-gated K + channels occurred in ancestral parahoxozoans

Fine-tuning of Voltage Sensitivity of the Kv1.2 Potassium Channel by Interhelix Loop Dynamics

Neuronal polarity: an evolutionary perspective

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Major diversification of voltage-gated K ⁺ channels occurred in ancestral parahoxozoans

Major diversification of voltage-gated K ⁺ channels occurred in ancestral parahoxozoans