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Proc Natl Acad Sci U S A. 2015 Mar 3;112(9):E1010-9. doi: 10.1073/pnas.1422941112. Epub 2015 Feb 17.

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

Author information

1
Department of Biology and Huck Institutes of the Life Sciences, Penn State University, University Park, PA 16802;
2
Department of Biology and.
3
Department of Biology, University of Maryland, College Park, MD 20742; and.
4
The Whitney Marine Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL 32080.
5
Department of Biology and Huck Institutes of the Life Sciences, Penn State University, University Park, PA 16802; tjj3@psu.edu.

Abstract

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.

KEYWORDS:

KCNQ; Mnemiopsis; Nematostella; Shaker; ctenophore

PMID:
25691740
PMCID:
PMC4352839
DOI:
10.1073/pnas.1422941112
[Indexed for MEDLINE]
Free PMC Article

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