Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
Proc Natl Acad Sci U S A
2015 Mar 03;1129:E1010-9. doi: 10.1073/pnas.1422941112.
Show Gene links
Show Anatomy links
Major diversification of voltage-gated K+ channels occurred in ancestral parahoxozoans.
Li X, Liu H, Chu Luo J, Rhodes SA, Trigg LM, van Rossum DB, Anishkin A, Diatta FH, Sassic JK, Simmons DK, Kamel B, Medina M, Martindale MQ, Jegla T.
???displayArticle.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.
Altschul,
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
1997, Pubmed
Altschul,
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
1997,
Pubmed Bähring,
Mechanisms of closed-state inactivation in voltage-gated ion channels.
2011,
Pubmed Bouchard,
Cloning and functional expression of voltage-gated ion channel subunits from cnidocytes of the Portuguese Man O'War Physalia physalis.
2006,
Pubmed Brown,
Neural KCNQ (Kv7) channels.
2009,
Pubmed Carrasquillo,
IA channels: diverse regulatory mechanisms.
2014,
Pubmed Chapman,
The dynamic genome of Hydra.
2010,
Pubmed Covarrubias,
Shaker, Shal, Shab, and Shaw express independent K+ current systems.
1991,
Pubmed
,
Xenbase Davis,
A mutation in the C. elegans EXP-2 potassium channel that alters feeding behavior.
1999,
Pubmed Delmas,
Pathways modulating neural KCNQ/M (Kv7) potassium channels.
2005,
Pubmed Du,
Frequency-dependent regulation of rat hippocampal somato-dendritic excitability by the K+ channel subunit Kv2.1.
2000,
Pubmed Dunn,
Broad phylogenomic sampling improves resolution of the animal tree of life.
2008,
Pubmed Fairclough,
Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta.
2013,
Pubmed Fawcett,
Mutant analysis of the Shal (Kv4) voltage-gated fast transient K+ channel in Caenorhabditis elegans.
2006,
Pubmed
,
Xenbase Guan,
Kv2 channels regulate firing rate in pyramidal neurons from rat sensorimotor cortex.
2013,
Pubmed Hernandez,
A carboxy-terminal inter-helix linker as the site of phosphatidylinositol 4,5-bisphosphate action on Kv7 (M-type) K+ channels.
2008,
Pubmed Hodge,
Shaw potassium channel genes in Drosophila.
2005,
Pubmed Howard,
Structural insight into KCNQ (Kv7) channel assembly and channelopathy.
2007,
Pubmed Jegla,
Evolution of the human ion channel set.
2009,
Pubmed Jegla,
Multiple Shaker potassium channels in a primitive metazoan.
1995,
Pubmed
,
Xenbase Jegla,
Molecular evolution of K+ channels in primitive eukaryotes.
1994,
Pubmed Jegla,
Expanded functional diversity of shaker K(+) channels in cnidarians is driven by gene expansion.
2012,
Pubmed Jegla,
A novel subunit for shal K+ channels radically alters activation and inactivation.
1997,
Pubmed Johnstone,
Behavioral defects in C. elegans egl-36 mutants result from potassium channels shifted in voltage-dependence of activation.
1997,
Pubmed
,
Xenbase Ketchum,
A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem.
1995,
Pubmed
,
Xenbase King,
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans.
2008,
Pubmed Kreusch,
Crystal structure of the tetramerization domain of the Shaker potassium channel.
1998,
Pubmed Kubisch,
KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness.
1999,
Pubmed
,
Xenbase Lee,
Structure of the KvAP voltage-dependent K+ channel and its dependence on the lipid membrane.
2005,
Pubmed Lien,
Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons.
2003,
Pubmed Loijens,
The phosphatidylinositol 4-phosphate 5-kinase family.
1996,
Pubmed Martinson,
Functional evolution of Erg potassium channel gating reveals an ancient origin for IKr.
2014,
Pubmed
,
Xenbase Misonou,
Kv2.1: a voltage-gated k+ channel critical to dynamic control of neuronal excitability.
2005,
Pubmed Moran,
The evolution of the four subunits of voltage-gated calcium channels: ancient roots, increasing complexity, and multiple losses.
2014,
Pubmed Moroz,
The ctenophore genome and the evolutionary origins of neural systems.
2014,
Pubmed Murata,
Depolarization activates the phosphoinositide phosphatase Ci-VSP, as detected in Xenopus oocytes coexpressing sensors of PIP2.
2007,
Pubmed
,
Xenbase Ogawa,
Postsynaptic density-93 clusters Kv1 channels at axon initial segments independently of Caspr2.
2008,
Pubmed Ogawa,
ADAM22, a Kv1 channel-interacting protein, recruits membrane-associated guanylate kinases to juxtaparanodes of myelinated axons.
2010,
Pubmed Ottschytsch,
Obligatory heterotetramerization of three previously uncharacterized Kv channel alpha-subunits identified in the human genome.
2002,
Pubmed Peters,
Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior.
2005,
Pubmed
,
Xenbase Post,
Kv2.1 and electrically silent Kv6.1 potassium channel subunits combine and express a novel current.
1996,
Pubmed
,
Xenbase Putnam,
Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.
2007,
Pubmed Quattrocki,
A Shab potassium channel contributes to action potential broadening in peptidergic neurons.
1994,
Pubmed
,
Xenbase Riesgo,
The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges.
2014,
Pubmed Ronquist,
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.
2012,
Pubmed Rosenthal,
Molecular identification of SqKv1A. A candidate for the delayed rectifier K channel in squid giant axon.
1996,
Pubmed
,
Xenbase Ryan,
The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution.
2013,
Pubmed Ryan,
The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa.
2010,
Pubmed Ryan,
Did the ctenophore nervous system evolve independently?
2014,
Pubmed Salkoff,
An essential 'set' of K+ channels conserved in flies, mice and humans.
1992,
Pubmed
,
Xenbase Sand,
jShaw1, a low-threshold, fast-activating K(v)3 from the hydrozoan jellyfish Polyorchis penicillatus.
2011,
Pubmed
,
Xenbase Schwake,
Structural determinants of M-type KCNQ (Kv7) K+ channel assembly.
2006,
Pubmed
,
Xenbase Sentenac,
Cloning and expression in yeast of a plant potassium ion transport system.
1992,
Pubmed Shen,
Molecular recognition and assembly sequences involved in the subfamily-specific assembly of voltage-gated K+ channel subunit proteins.
1995,
Pubmed Shinzato,
Using the Acropora digitifera genome to understand coral responses to environmental change.
2011,
Pubmed Srivastava,
The Trichoplax genome and the nature of placozoans.
2008,
Pubmed Srivastava,
The Amphimedon queenslandica genome and the evolution of animal complexity.
2010,
Pubmed Tamura,
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.
2013,
Pubmed Tang,
Shaker and ether-à-go-go K+ channel subunits fail to coassemble in Xenopus oocytes.
1998,
Pubmed
,
Xenbase Tsunoda,
Genetic analysis of Drosophila neurons: Shal, Shaw, and Shab encode most embryonic potassium currents.
1995,
Pubmed Tsunoda,
The major delayed rectifier in both Drosophila neurons and muscle is encoded by Shab.
1995,
Pubmed Wang,
KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel.
1998,
Pubmed
,
Xenbase Wang,
Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones.
1998,
Pubmed Wang,
Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons.
1993,
Pubmed
,
Xenbase Wei,
K+ current diversity is produced by an extended gene family conserved in Drosophila and mouse.
1990,
Pubmed
,
Xenbase Wei,
KCNQ-like potassium channels in Caenorhabditis elegans. Conserved properties and modulation.
2005,
Pubmed
,
Xenbase Wei,
Eight potassium channel families revealed by the C. elegans genome project.
1996,
Pubmed Wen,
A Drosophila KCNQ channel essential for early embryonic development.
2005,
Pubmed Wickenden,
Characterization of KCNQ5/Q3 potassium channels expressed in mammalian cells.
2001,
Pubmed
,
Xenbase Wimmers,
Erg1, erg2 and erg3 K channel subunits are able to form heteromultimers.
2001,
Pubmed Xu,
Assembly of voltage-gated potassium channels. Conserved hydrophilic motifs determine subfamily-specific interactions between the alpha-subunits.
1995,
Pubmed Yu,
The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis.
2004,
Pubmed Zaydman,
PIP2 regulation of KCNQ channels: biophysical and molecular mechanisms for lipid modulation of voltage-dependent gating.
2014,
Pubmed Zaydman,
Kv7.1 ion channels require a lipid to couple voltage sensing to pore opening.
2013,
Pubmed
,
Xenbase Zhang,
PIP(2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents.
2003,
Pubmed
,
Xenbase Zou,
Distribution and functional properties of human KCNH8 (Elk1) potassium channels.
2003,
Pubmed
,
Xenbase
