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

Xiaofan Li, Hansi Liu, Jose Chu Luo, Sarah A. Rhodes, Liana M. Trigg, Damian B. Van Rossum, Andriy Anishkin, Fortunay H. Diatta, Jessica K. Sassic, David K. Simmons, Bishoy Kamel, Monica Medina, Mark Q. Martindale, Timothy Jegla

Research output: Contribution to journalArticle

13 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)E1010-E1019
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number9
DOIs
StatePublished - Mar 3 2015

Fingerprint

Ctenophora
Cnidaria
Voltage-Gated Potassium Channels
Prednisolone
Action Potentials
Genes

All Science Journal Classification (ASJC) codes

  • General

Cite this

Li, Xiaofan ; Liu, Hansi ; Luo, Jose Chu ; Rhodes, Sarah A. ; Trigg, Liana M. ; Van Rossum, Damian B. ; Anishkin, Andriy ; Diatta, Fortunay H. ; Sassic, Jessica K. ; Simmons, David K. ; Kamel, Bishoy ; Medina, Monica ; Martindale, Mark Q. ; Jegla, Timothy. / Major diversification of voltage-gated K+ channels occurred in ancestral parahoxozoans. In: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; Vol. 112, No. 9. pp. E1010-E1019.
@article{b879c0eeb6af48b3ac352012a48ff9b4,
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.",
author = "Xiaofan Li and Hansi Liu and Luo, {Jose Chu} and Rhodes, {Sarah A.} and Trigg, {Liana M.} and {Van Rossum}, {Damian B.} and Andriy Anishkin and Diatta, {Fortunay H.} and Sassic, {Jessica K.} and Simmons, {David K.} and Bishoy Kamel and Monica Medina and Martindale, {Mark Q.} and Timothy Jegla",
year = "2015",
month = "3",
day = "3",
doi = "10.1073/pnas.1422941112",
language = "English (US)",
volume = "112",
pages = "E1010--E1019",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "9",

}

Li, X, Liu, H, Luo, JC, Rhodes, SA, Trigg, LM, Van Rossum, DB, Anishkin, A, Diatta, FH, Sassic, JK, Simmons, DK, Kamel, B, Medina, M, Martindale, MQ & Jegla, T 2015, 'Major diversification of voltage-gated K+ channels occurred in ancestral parahoxozoans', Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 9, pp. E1010-E1019. https://doi.org/10.1073/pnas.1422941112

Major diversification of voltage-gated K+ channels occurred in ancestral parahoxozoans. / Li, Xiaofan; Liu, Hansi; Luo, Jose Chu; Rhodes, Sarah A.; Trigg, Liana M.; Van Rossum, Damian B.; Anishkin, Andriy; Diatta, Fortunay H.; Sassic, Jessica K.; Simmons, David K.; Kamel, Bishoy; Medina, Monica; Martindale, Mark Q.; Jegla, Timothy.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 9, 03.03.2015, p. E1010-E1019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Major diversification of voltage-gated K+ channels occurred in ancestral parahoxozoans

AU - Li, Xiaofan

AU - Liu, Hansi

AU - Luo, Jose Chu

AU - Rhodes, Sarah A.

AU - Trigg, Liana M.

AU - Van Rossum, Damian B.

AU - Anishkin, Andriy

AU - Diatta, Fortunay H.

AU - Sassic, Jessica K.

AU - Simmons, David K.

AU - Kamel, Bishoy

AU - Medina, Monica

AU - Martindale, Mark Q.

AU - Jegla, Timothy

PY - 2015/3/3

Y1 - 2015/3/3

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84924192527&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84924192527&partnerID=8YFLogxK

U2 - 10.1073/pnas.1422941112

DO - 10.1073/pnas.1422941112

M3 - Article

C2 - 25691740

AN - SCOPUS:84924192527

VL - 112

SP - E1010-E1019

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 9

ER -