Skip to main content
SpringerLink
Log in

Evolutionary Analysis of Voltage-Gated Potassium Channels by Bayes Method

  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

Voltage-gated potassium channels (VGPCs) are among the most complex families of ion channels. VGPCs are distributed widely among species but their biological roles remain unclear. In this study, the evolution of VGPCs and the functions of ancestral families are determined according to phylogenetic studies. We downloaded 127 genomic data of alpha subunits and 38 genomic data of beta subunits including those from human, rat, mice, Drosophila and Puccinellia tenuiflora. The genetic neighborhood of subfamily genes was determined by neighbor-joining, minimum evolution, maximum parsimony, and Bayes methods. Data was presented as phylogenetic trees. We also detected positive selection sites by site model. New insights into the evolutionary history of the VGPC family are provided. Our assumptions are as follows: (a) KCNH subfamily is likely the most original subfamily in alpha subunit; (b) VGPCs are related to neural and cardiac systems at the earliest time; (c) KCNA4 and KCNF1 may be as ancestors; (d) abnormality in one gene may cause both cardiac and neural diseases; and (e) abnormalities in KCNH6 and KCNQ7 are more likely to cause cardiac diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alzamora R, Gong F, Rondanino C, Lee JK, Smolak C, Pastor-Soler NM, Hallows KR (2010) AMP-activated protein kinase inhibits KCNQ1 channels through regulation of the ubiquitin ligase Nedd4-2 in renal epithelial cells. Am J Physiol Renal Physiol 299:F1308–F1319

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ansel S, Farrugia ME (2013) The yield from testing voltage-gated potassium channel antibodies in patients with cramp. J Neurol Neurosurg Psychiatry 84:e2

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113

    Article  CAS  Google Scholar 

  • Evseev AI, Semenov I, Archer CR, Medina JL, Dube PH, Shapiro MS, Brenner R (2013) Functional effects of KCNQ K(+) channels in airway smooth muscle. Front Physiol 4:277

    Article  PubMed Central  PubMed  Google Scholar 

  • Fantozzi I, Platoshyn O, Wong AH, Zhang S, Remillard CV, Furtado MR, Petrauskene OV, Yuan JX (2006) Bone morphogenetic protein-2 upregulates expression and function of voltage-gated K+ channels in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 291:L993–L1004

    Article  PubMed  CAS  Google Scholar 

  • Gilling M, Rasmussen HB, Calloe K, Sequeira AF, Baretto M, Oliveira G, Almeida J, Lauritsen MB, Ullmann R, Boonen SE, Brondum-Nielsen K, Kalscheuer VM, Tumer Z, Vicente AM, Schmitt N, Tommerup N (2013) Dysfunction of the heteromeric KV7.3/KV7.5 potassium channel is associated with autism spectrum disorders. Front Genet 4:54

    Article  PubMed Central  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Gutman GA, Chandy KG, Grissmer S, Lazdunski M, McKinnon D, Pardo LA, Robertson GA, Rudy B, Sanguinetti MC, Stuhmer W, Wang X (2005) International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev 57:473–508

    Article  PubMed  CAS  Google Scholar 

  • Haitin Y, Carlson AE, Zagotta WN (2013) The structural mechanism of KCNH-channel regulation by the eag domain. Nature 501:444–448

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Heinemann S, Rettig J, Scott V, Parcej DN, Lorra C, Dolly J, Pongs O (1994) The inactivation behaviour of voltage-gated K-channels may be determined by association of alpha- and beta-subunits. J Physiol Paris 88:173–180

    Article  PubMed  CAS  Google Scholar 

  • Horvath LI, Heimburg T, Kovachev P, Findlay JB, Hideg K, Marsh D (1995) Integration of a K+ channel-associated peptide in a lipid bilayer: conformation, lipid–protein interactions, and rotational diffusion. Biochemistry 34:3893–3898

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Hurlock EC, McMahon A, Joho RH (2008) Purkinje-cell-restricted restoration of Kv3.3 function restores complex spikes and rescues motor coordination in Kcnc3 mutants. J Neurosci 28:4640–4648

    Article  PubMed  CAS  Google Scholar 

  • Jensen MV, Haldeman JM, Zhang H, Lu D, Huising MO, Vale WW, Hohmeier HE, Rosenberg P, Newgard CB (2013) Control of voltage-gated potassium channel Kv2.2 expression by pyruvate–isocitrate cycling regulates glucose-stimulated insulin secretion. J Biol Chem 288:23128–23140

    Article  PubMed  CAS  Google Scholar 

  • Judge SI, Lee JM, Bever CT Jr, Hoffman PM (2006) Voltage-gated potassium channels in multiple sclerosis: overview and new implications for treatment of central nervous system inflammation and degeneration. J Rehabil Res Dev 43:111–122

    Article  PubMed  Google Scholar 

  • Judge SI, Smith PJ, Stewart PE, Bever CT Jr (2007) Potassium channel blockers and openers as CNS neurologic therapeutic agents. Recent Pat CNS Drug Discov 2:200–228

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Le Bouter S, El Harchi A, Marionneau C, Bellocq C, Chambellan A, van Veen T, Boixel C, Gavillet B, Abriel H, Le Quang K, Chevalier JC, Lande G, Leger JJ, Charpentier F, Escande D, Demolombe S (2004) Long-term amiodarone administration remodels expression of ion channel transcripts in the mouse heart. Circulation 110:3028–3035

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Han N, Franchini LF, Xu H, Pisciottano F, Elgoyhen AB, Rajan KE, Zhang S (2012) The voltage-gated potassium channel subfamily KQT member 4 (KCNQ4) displays parallel evolution in echolocating bats. Mol Biol Evol 29:1441–1450

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lv P, Wei D, Yamoah EN (2010) Kv7-type channel currents in spiral ganglion neurons: involvement in sensorineural hearing loss. J Biol Chem 285:34699–34707

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Martel P, Leo D, Fulton S, Berard M, Trudeau LE (2011) Role of Kv1 potassium channels in regulating dopamine release and presynaptic D2 receptor function. PLoS One 6:e20402

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Moore GW, Barnabas J, Goodman M (1973) A method for constructing maximum parsimony ancestral amino acid sequences on a given network. J Theor Biol 38:459–485

    Article  PubMed  CAS  Google Scholar 

  • Olesen MS, Bentzen BH, Nielsen JB, Steffensen AB, David JP, Jabbari J, Jensen HK, Haunso S, Svendsen JH, Schmitt N (2012) Mutations in the potassium channel subunit KCNE1 are associated with early-onset familial atrial fibrillation. BMC Med Genet 13:24

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Olesen MS, Refsgaard L, Holst AG, Larsen AP, Grubb S, Haunso S, Svendsen JH, Olesen SP, Schmitt N, Calloe K (2013) A novel KCND3 gain-of-function mutation associated with early-onset of persistent lone atrial fibrillation. Cardiovasc Res 98:488–495

    Article  PubMed  CAS  Google Scholar 

  • Ozaita A, Petit-Jacques J, Volgyi B, Ho CS, Joho RH, Bloomfield SA, Rudy B (2004) A unique role for Kv3 voltage-gated potassium channels in starburst amacrine cell signaling in mouse retina. J Neurosci 24:7335–7343

    Article  PubMed  CAS  Google Scholar 

  • Posada D Using MODELTEST and PAUP* to select a model of nucleotide substitution. Curr Protoc Bioinformatics. 2003; Chapter 6, Unit 6 5

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rus H, Pardo CA, Hu L, Darrah E, Cudrici C, Niculescu T, Niculescu F, Mullen KM, Allie R, Guo L, Wulff H, Beeton C, Judge SI, Kerr DA, Knaus HG, Chandy KG, Calabresi PA (2005) The voltage-gated potassium channel Kv1.3 is highly expressed on inflammatory infiltrates in multiple sclerosis brain. Proc Natl Acad Sci U S A 102:11094–11099

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Serino D, Specchio N, Pontrelli G, Vigevano F, Fusco L (2013) Video/EEG findings in a KCNQ2 epileptic encephalopathy: a case report and revision of literature data. Epileptic Disord 15:158–165

    PubMed  Google Scholar 

  • Shi L, Bian X, Qu Z, Ma Z, Zhou Y, Wang K, Jiang H, Xie J (2013) Peptide hormone ghrelin enhances neuronal excitability by inhibition of Kv7/KCNQ channels. Nat Commun 4:1435

    Article  PubMed  CAS  Google Scholar 

  • Son MK, Ki CS, Park SJ, Huh J, Kim JS, On YK (2013) Genetic mutation in Korean patients of sudden cardiac arrest as a surrogating marker of idiopathic ventricular arrhythmia. J Korean Med Sci 28:1021–1026

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Swartz KJ, MacKinnon R (1997) Mapping the receptor site for hanatoxin, a gating modifier of voltage-dependent K+channels. Neuron 18:675–682

    Article  PubMed  CAS  Google Scholar 

  • Thompson EA (1973) The method of minimum evolution. Ann Hum Genet 36:333–340

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson SE, Tan SV, Kullmann DM, Griggs RC, Burke D, Hanna MG, Bostock H (2010) Nerve excitability studies characterize Kv1.1 fast potassium channel dysfunction in patients with episodic ataxia type 1. Brain 133:3530–3540

    Article  PubMed Central  PubMed  Google Scholar 

  • Veeramah KR, Johnstone L, Karafet TM, Wolf D, Sprissler R, Salogiannis J, Barth-Maron A, Greenberg ME, Stuhlmann T, Weinert S, Jentsch TJ, Pazzi M, Restifo LL, Talwar D, Erickson RP, Hammer MF (2013) Exome sequencing reveals new causal mutations in children with epileptic encephalopathies. Epilepsia 54:1270–1281

    Article  PubMed  CAS  Google Scholar 

  • Xu Q, Chang A, Tolia A, Minor DL Jr (2013) Structure of a Ca(2+)/CaM:Kv7.4 (KCNQ4) B-helix complex provides insight into M current modulation. J Mol Biol 425:378–394

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Wong WS, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118

    Article  PubMed  CAS  Google Scholar 

  • Zamorano-Leon JJ, Yanez R, Jaime G, Rodriguez-Sierra P, Calatrava-Ledrado L, Alvarez-Granada RR, Mateos-Caceres PJ, Macaya C, Lopez-Farre AJ (2012) KCNH2 gene mutation: a potential link between epilepsy and long QT-2 syndrome. J Neurogenet 26:382–386

    Article  PubMed  CAS  Google Scholar 

  • Zhou P, Yu H, Gu M, Nan FJ, Gao Z, Li M (2013) Phosphatidylinositol 4,5-bisphosphate alters pharmacological selectivity for epilepsy-causing KCNQ potassium channels. Proc Natl Acad Sci U S A 110:8726–8731

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurology, First Affiliated Hospital, Guangxi Medical University, Nanning, Guangxi, China

    Qi Huang, Yuan Wu, Xing Wei, Xixia Liu & Jiemei Ye

  2. Department of Cardiothoracic surgery, First Affiliated Hospital, Guangxi Medical University, Nanning, Guangxi, China

    Wenwu He

Authors
  1. Qi Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xing Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenwu He
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xixia Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiemei Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuan Wu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, Q., Wu, Y., Wei, X. et al. Evolutionary Analysis of Voltage-Gated Potassium Channels by Bayes Method. J Mol Neurosci 53, 41–49 (2014). https://doi.org/10.1007/s12031-013-0192-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12031-013-0192-4

Keyword

Search

Navigation