title: Major diversification of voltage-gated K+ channels occurred in ancestral parahoxozoans.
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.
authors.affiliation: Department of Biology and Huck Institutes of the Life Sciences, Penn State University, University Park, PA 16802;
authors.forename: Xiaofan
authors.initials: X
authors.lastname: Li
authors.affiliation: Department of Biology and.
authors.forename: Hansi
authors.initials: H
authors.lastname: Liu
authors.affiliation: Department of Biology and.
authors.forename: Jose
authors.initials: J
authors.lastname: Chu Luo
authors.affiliation: Department of Biology and.
authors.forename: Sarah A
authors.initials: SA
authors.lastname: Rhodes
authors.affiliation: Department of Biology and.
authors.forename: Liana M
authors.initials: LM
authors.lastname: Trigg
authors.affiliation: Department of Biology and Huck Institutes of the Life Sciences, Penn State University, University Park, PA 16802;
authors.forename: Damian B
authors.initials: DB
authors.lastname: van Rossum
authors.affiliation: Department of Biology, University of Maryland, College Park, MD 20742; and.
authors.forename: Andriy
authors.initials: A
authors.lastname: Anishkin
authors.affiliation: Department of Biology and.
authors.forename: Fortunay H
authors.initials: FH
authors.lastname: Diatta
authors.affiliation: Department of Biology and.
authors.forename: Jessica K
authors.initials: JK
authors.lastname: Sassic
authors.affiliation: The Whitney Marine Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL 32080.
authors.forename: David K
authors.initials: DK
authors.lastname: Simmons
authors.affiliation: Department of Biology and.
authors.forename: Bishoy
authors.initials: B
authors.lastname: Kamel
authors.affiliation: Department of Biology and.
authors.forename: Monica
authors.initials: M
authors.lastname: Medina
authors.affiliation: The Whitney Marine Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL 32080.
authors.forename: Mark Q
authors.initials: MQ
authors.lastname: Martindale
authors.affiliation: Department of Biology and Huck Institutes of the Life Sciences, Penn State University, University Park, PA 16802; tjj3@psu.edu.
authors.forename: Timothy
authors.initials: T
authors.lastname: Jegla
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D037302:Ctenophora / Q000235:genetics* / Q000378:metabolism; D030562:Databases, Protein; D019143:Evolution, Molecular; D006801:Humans; D006829:Hydra / Q000235:genetics* / Q000378:metabolism; D051656:KCNQ Potassium Channels / Q000235:genetics* / Q000378:metabolism; D051379:Mice; D008969:Molecular Sequence Data; D010802:Phylogeny; D051637:Shaker Superfamily of Potassium Channels / Q000235:genetics* / Q000378:metabolism; D014982:Xenopus laevis
chemical_list: D051656:KCNQ Potassium Channels; D051637:Shaker Superfamily of Potassium Channels
keywords: KCNQ; Mnemiopsis; Nematostella; Shaker; ctenophore