Abstract
Every cell within living organisms actively maintains an intracellular Na+ concentration that is 10–12 times lower than the extracellular concentration. The cells then utilize this transmembrane Na+ concentration gradient as a driving force to produce electrical signals, sometimes in the form of action potentials. The protein family comprising voltage-gated sodium channels (NaVs) is essential for such signaling and enables cells to change their status in a regenerative manner and to rapidly communicate with one another. NaVs were first predicted in squid and were later identified through molecular biology in the electric eel. Since then, these proteins have been discovered in organisms ranging from bacteria to humans. Recent research has succeeded in decoding the amino acid sequences of a wide variety of NaV family members, as well as the three-dimensional structures of some. These studies and others have uncovered several of the major steps in the functional and structural transition of NaV proteins that has occurred along the course of the evolutionary history of organisms. Here we present an overview of the molecular evolutionary innovations that established present-day NaV α subunits and discuss their contribution to the evolutionary changes in animal bodies.
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References
Akopian AN, Sivilotti L, Wood JN (1996) A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257–262
Amemiya CT, Alföldi J, Lee AP, Fan S, Philippe H, Maccallum I, Braasch I, Manousaki T, Schneider I, Rohner N, Organ C, Chalopin D, Smith JJ, Robinson M, Dorrington RA, Gerdol M, Aken B, Biscotti MA, Barucca M, Baurain D, Berlin AM, Blatch GL, Buonocore F, Burmester T, Campbell MS, Canapa A, Cannon JP, Christoffels A, De Moro G, Edkins AL, Fan L, Fausto AM, Feiner N, Forconi M, Gamieldien J, Gnerre S, Gnirke A, Goldstone JV, Haerty W, Hahn ME, Hesse U, Hoffmann S, Johnson J, Karchner SI, Kuraku S, Lara M, Levin JZ, Litman GW, Mauceli E, Miyake T, Mueller MG, Nelson DR, Nitsche A, Olmo E, Ota T, Pallavicini A, Panji S, Picone B, Ponting CP, Prohaska SJ, Przybylski D, Saha NR, Ravi V, Ribeiro FJ, Sauka-Spengler T, Scapigliati G, Searle SM, Sharpe T, Simakov O, Stadler PF, Stegeman JJ, Sumiyama K, Tabbaa D, Tafer H, Turner-Maier J, van Heusden P, White S, Williams L, Yandell M, Brinkmann H, Volff JN, Tabin CJ, Shubin N, Schartl M, Jaffe DB, Postlethwait JH, Venkatesh B, Di Palma F, Lander ES, Meyer A, Lindblad-Toh K (2013) The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311–316
Anderson PAV, Holman MA, Greenberg RM (1993) Deduced amino acid sequence of a putative sodium channel from the scyphozoan jellyfish Cyanea capillata. Proc Natl Acad Sci U S A 90:7419–7423
Beneski DA, Catterall WA (1980) Covalent labeling of protein components of the sodium channel with a photoactivable derivative of scorpion toxin. Proc Natl Acad Sci U S A 77:639–643
Bichet D, Haass FA, Jan LY (2003) Merging functional studies with structures of inward-rectifier K+ channels. Nat Rev Neurosci 4:957–967
Braasch I, Gehrke AR, Smith JJ, Kawasaki K, Manousaki T, Pasquier J, Amores A, Desvignes T, Batzel P, Catchen J, Berlin AM, Campbell MS, Barrell D, Martin KJ, Mulley JF, Ravi V, Lee AP, Nakamura T, Chalopin D, Fan S, Wcisel D, Cañestro C, Sydes J, Beaudry FE, Sun Y, Hertel J, Beam MJ, Fasold M, Ishiyama M, Johnson J, Kehr S, Lara M, Letaw JH, Litman GW, Litman RT, Mikami M, Ota T, Saha NR, Williams L, Stadler PF, Wang H, Taylor JS, Fontenot Q, Ferrara A, Searle SM, Aken B, Yandell M, Schneider I, Yoder JA, Volff JN, Meyer A, Amemiya CT, Venkatesh B, Holland PW, Guiguen Y, Bobe J, Shubin NH, Di Palma F, Alföldi J, Lindblad-Toh K, Postlethwait JH (2016) The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat Genet 48:427–437
Brozovic M, Martin C, Dantec C, Dauga D, Mendez M, Simion P, Percher M, Laporte B, Scornavacca C, Di Gregorio A, Fujiwara S, Gineste M, Lowe EK, Piette J, Racioppi C, Ristoratore F, Sasakura Y, Takatori N, Brown TC, Delsuc F, Douzery E, Gissi C, McDougall A, Nishida H, Sawada H, Swalla BJ, Yasuo H, Lemaire P (2016) ANISEED 2015: a digital framework for the comparative developmental biology of ascidians. Nucleic Acids Res 44:D808–D818
Brunet T, Arendt D (2015) From damage response to action potentials: early evolution of neural and contractile modules in stem eukaryotes. Philos Trans R Soc Lond B Biol Sci 371:20150043
Calcraft PJ, Arredouani A, Ruas M, Pan Z, Cheng X, , Hao X, Tang J, Rietdorf K, Teboul L, Chuang K-T, Lin P, Xiao R, Wang C, Zhu Y, Lin Y, Wyatt CN, Parrington J, Ma J, Evans AM, Galione A, Zhu MX (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459:596–600
Catterall WA (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26:13–25
Catterall WA, Zheng N (2015) Deciphering voltage-gated Na+ and Ca2+ channels by studying prokaryotic ancestors. Trends Biochem Sci 40:526–534
Catterall WA, Goldin AL, Waxman SG (2005) International union of pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57:397–409
Cavalier-Smith T (2010) Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett 6:342–345
Conway-Morris S (1986) The community structure of the Middle Cambrian Phyllopod Bed (Burgess Shale). Palaeontology 29:423–467
Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968
Fujiu K, Nakayama Y, Yanagisawa A, Sokabe M, Yoshimura K (2009) Chlamydomonas CAV2 encodes a voltage-dependent calcium channel required for the flagellar waveform conversion. Curr Biol 19:133–139
Fukushima Y (1981) Identification and kinetic properties of the current through a single Na+ channel. Proc Natl Acad Sci U S A 78:1274–1277
Gans C, Northcutt RG (1983) Neural crest and the origin of vertebrates: a new head. Science 220:268–273
Garrido JJ, Giraud P, Carlier E, Fernandes F, Moussif A, Fache MP, Debanne D, Dargent B (2003) A targeting motif involved in sodium channel clustering at the axon initial segment. Science 300:2091–2094
Gellens ME, George AL Jr, Chen L, Chahine M, Horn R (1992) Primary structure and functional expression of the human cardiac tetrodotoxin-insensitive voltage-dependent sodium channel. Proc Natl Acad Sci U S A 89:554–558
Goldin AL (2001) Resurgence of sodium channel research. Annu Rev Physiol 63:871–894
Gosselin-Badaroudine P, Moreau A, Simard L, Cens T, Rousset M, Collet C, Charnet P, Chahine M (2016) Biophysical characterization of the honeybee DSC1 orthologue reveals a novel voltage-dependent Ca2+ channel subfamily: CaV4. J Gen Physiol 148:133–145
Gould SJ (1990) Wonderful life: the Burgess Shale and the nature of history. WW Norton & Co., New York
Gur Barzilai M, Reitzel AM, Kraus JE, Gordon D, Technau U, Gurevitz M, Moran Y (2012) Convergent evolution of sodium ion selectivity in metazoan neuronal signaling. Cell Rep 2:242–248
Hartshorne RP, Catterall WA (1981) Purification of the saxitoxin receptor of the sodium channel from rat brain. Proc Natl Acad Sci U S A 78:4620–4624
Hartshorne RP, Keller BU, Talvenheimo JA, Catterall WA, Montal M (1985) Functional reconstitution of the purified brain sodium channel in planar lipid bilayers. Proc Natl Acad Sci U S A 82:240–244
Heinemann SH, Terlau H, Stühmer W, Imoto K, Numa S (1992) Calcium channel characteristics conferred on the sodium channel by single mutations. Nature 356:441–443
Hill AS, Nishino A, Nakajo K, Zhang G, Fineman JR, Selzer ME, Okamura Y, Cooper EC (2008) Ion channel clustering at the axon initial segment and node of Ranvier evolved sequentially in early chordates. PLoS Genet 4:e1000317
Hirai S, Hotta K, Kubo Y, Nishino A, Okabe S, Okamura Y, Okado H (2017) AMPA glutamate receptors are required for sensory-organ formation and morphogenesis in the basal chordate. Proc Natl Acad Sci U S A 114:3939–3944
Hiyama TY, Noda M (2016) Sodium sensing in the subfornical organ and body-fluid homeostasis. Neurosci Res 113:1–11
Hiyama TY, Watanabe E, Ono K, Inenaga K, Tamkun MM, Yoshida S, Noda M (2002) NaX channel involved in CNS sodium-level sensing. Nat Neurosci 5:511–512
Hiyama TY, Watanabe E, Okado H, Noda M (2004) The subfornical organ is the primary locus of sodium-level sensing by NaX sodium channels for the control of salt-intake behavior. J Neurosci 24:9276–9281
Hodgkin AL, Huxley AF (1945) Resting and action potentials in single nerve fibers. J Physiol 104:176–195
Hodgkin AL, Huxley AF (1952) Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol 116:449–472
Holland ND (2003) Early central nervous system evolution: an era of skin brains? Nat Rev Neurosci 4:617–627
Holland ND (2016) Nervous systems and scenarios for the invertebrate-to-vertebrate transition. Phil Trans R Soc Lond B 371:20150047
Hong CS, Ganetzky B (1994) Spatial and temporal expression patterns of two sodium channel genes in Drosophila. J Neurosci 14:5160–5169
Honoré E (2007) The neuronal background K2P channels: focus on TREK1. Nat Rev Neurosci 8:251–261
Hu W, Tian C, Li T, Yang M, Hou H, Shu Y (2009) Distinct contributions of NaV1.6 and NaV1.2 in action potential initiation and backpropagation. Nat Neurosci 12:996–1002
Hyman LH (1955) The invertebrates: Echinodermata. The coelomic Bilateria. McGraw-Hill, New York
Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, MacKinnon R (2003) X-ray structure of a voltage-dependent K+ channel. Nature 423:33–41
Kole MH, Stuart GJ (2012) Signal processing in the axon initial segment. Neuron 73:235–247
Krebs HA (1975) The August Krogh principle: “For many problems there is an animal on which it can be most conveniently studied”. J Exp Zool 194:221–225
Kulkarni NH, Yamamoto AH, Robinson KO, Mackay TFC, Anholt RR (2002) The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster. Genetics 161:1507–1516
Lai J, Porreca F, Hunter JC, Gold MS (2004) Voltage-gated sodium channels and hyperalgesia. Annu Rev Pharmacol Toxicol 44:371–397
Lamaillet G, Walker B, Lambert S (2003) Identification of a conserved ankyrin-binding motif in the family of sodium channel alpha subunits. J Biol Chem 278:27333–27339
Liebeskind BJ, Hillis DM, Zakon HH (2011) Evolution of sodium channels predates the origin of nervous systems in animals. Proc Natl Acad Sci U S A 108:9154–9159
Liebeskind BJ, Hillis DM, Zakon HH (2012) Phylogeny units animal sodium leak channels with fungal calcium channels in an ancient, voltage-insensitive clade. Mol Biol Evol 29:3613–3616
Liebeskind BJ, Hillis DM, Zakon HH (2013) Independent acquisition of sodium selectivity in bacterial and animal sodium channels. Curr Biol 23:R948–R949
Lorincz A, Nusser Z (2010) Molecular identity of dendritic voltage-gated sodium channels. Science 328:906–909
Loughney K, Kreber R, Ganetzky B (1989) Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58:1143–1154
Lu B, Su Y, Das S, Liu J, Xia J, Ren D (2007) The neuronal channel NALCN contributes resting sodium permeability and is required for normal respiratory rhythm. Cell 129:371–383
Machemer H, Ogura A (1979) Ionic conductances of membranes in ciliated and deciliated Paramecium. J Physiol 296:49–60
Moran Y, Zakon HH (2014) The evolution of the four subunits of voltage-gated calcium channels: ancient roots, increasing complexity, and multiple losses. Genome Biol Evol 6:2210–2217
Moran Y, Liebeskind BJ, Zakon HH (2015) Evolution of voltage-gated ion channels at the emergence of Metazoa. J Exp Biol 218:515–525
Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435:1239–1243
Nagahora H, Okada T, Yahagi N, Chong JA, Mandel G, Okamura Y (2000) Diversity of voltage-gated sodium channels in the ascidian larval nervous system. Biochem Biophys Res Commun 275:558–564
Nishino A, Baba SA, Okamura Y (2011) A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor. Proc Natl Acad Sci U S A 108:2599–2604
Noda M, Shimizu S, Tanabe T, Takai T, Kayano T, Ikeda T, Takahashi H, Nakayama H, Kanaoka Y, Minamino N, Kangawa K, Matsuo H, Raftery MA, Hirose T, Inayama S, Hayashida H, Miyata T, Numa S (1984) Primary structure of electrophorus electricus sodium channel deduced from cDNA sequence. Nature 312:121–127
Noda M, Suzuki H, Numa S, Stühmer W (1989) A single point mutation confers tetrodotoxin and saxitoxin insensitivity on the sodium channel II. FEBS Lett 259:213–216
Nomaksteinsky M, Röttinger E, Dufour HD, Chettouh Z, Lowe CJ, Martindale MQ, Brunet JF (2009) Centralization of the deuterostome nervous system predates chordates. Curr Biol 19:1264–1269
Novak AE, Taylor AD, Pineda RH, Lasda EL, Wright MA, Ribera AB (2006a) Embryonic and larval expression of zebrafish voltage-gated sodium channel α-subunit genes. Dev Dyn 235:1962–1973
Novak AE, Jost MC, Lu Y, Taylor AD, Zakon HH, Ribera AB (2006b) Gene duplications and evolution of vertebrate voltage-gated sodium channels. J Mol Evol 63:208–221
Ohno S (1970) Evolution by gene duplication. Springer, New York
Okada T, Hirano H, Takahashi K, Okamura Y (1997) Distinct neuronal lineages of the ascidian embryo revealed by expression of a sodium channel gene. Dev Biol 190:257–272
Okado H, Takahashi K (1988) A simple “neural induction” model with two interacting cleavage-arrested ascidian blastomeres. Proc Natl Acad Sci U S A 85:6197–6201
Okamoto H, Takahashi K, Yamashita N (1977) One-to-one binding of a purified scorpion toxin to Na channels. Nature 266:465–468
Okamura Y, Shidara M (1987) Kinetic differences between Na channels in the egg and the neutrally differentiated blastomere in the tunicate. Proc Natl Acad Sci U S A 84:8702–8706
Okamura Y, Shidara M (1990a) Changes in sodium channels during neural differentiation in the isolated blastomere of the ascidian embryo. J Physiol 431:39–74
Okamura Y, Shidara M (1990b) Inactivation kinetics of the sodium channel in the egg and the isolated, neutrally differentiated blastomere of the ascidian. J Physiol 431:75–102
Okamura Y, Ono F, Okagaki R, Chong JA, Mandel G (1994) Neural expression of a sodium channel gene requires cell-specific interactions. Neuron 13:937–948
Okamura Y, Nishino A, Murata Y, Nakajo K, Iwasaki H, Ohtsuka Y, Tanaka-Kunishima M, Takahashi N, Hara Y, Yoshida T, Nishida M, Okado H, Watari H, Meinertzhagen IA, Satoh N, Takahashi K, Satou Y, Okada Y, Mori Y (2005) Comprehensive analysis of the ascidian genome reveals novel insights into the molecular evolution of ion channel genes. Physiol Genomics 22:269–282
Pan Z, Kao T, Horvath Z, Lemos J, Sul JY, Cranstoun SD, Bennett V, Scherer SS, Cooper EC (2006) A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci 26:2599–2613
Parker A (2003) In the blink of an eye. Basic Books, New York
Payandeh J, Minor DL Jr (2015) Bacterial voltage-gated sodium channels (BacNaVs) from the soil, sea, and salt lakes enlighten molecular mechanisms of electrical signaling and pharmacology in the brain and heart. J Mol Biol 427:3–30
Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutiérrez EL, Dubchak I, Garcia-Fernàndez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin-I T, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071
Ramaswami M, Tanouye MA (1989) Two sodium-channel genes in Drosophila: implications for channel diversity. Proc Natl Acad Sci U S A 86:2079–2082
Ramsey IS, Moran MM, Chong JA, Clapham DE (2006) A voltage-gated proton-selective channel lacking the pore domain. Nature 440:1213–1216
Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE (2001) A prokaryotic voltage-gated sodium channel. Science 294:2372–2375
Rogart RB, Cribbs LL, Muglia LK, Kephart DD, Kaiser MW (1989) Molecular cloning of a putative tetrodotoxin-resistant rat heart Na+ channel isoform. Proc Natl Acad Sci U S A 86:8170–8174
Roger AJ, Simpson AGB (2008) Evolution: revisiting the root of the eukaryote tree. Curr Biol 19:R165–R167
Rogozin IB, Basu MK, Csürös M, Koonin EV (2009) Analysis of rare genomic changes does not support the unikont-bikont phylogeny and suggests cyanobacterial symbiosis as the point of primary radiation of eukaryotes. Genome Biol Evol 1:99–113
Salkoff L, Butler A, Wei A, Scavarda N, Giffen K, Ifune C, Goodman R, Mandel G (1987) Genomic organization and deduced amino acid sequence of a putative sodium channel gene in Drosophila. Science 237:744–749
Sangameswaran L, Fish LM, Koch BD, Rabert DK, Delgado SG, Ilnicka M, Jakeman LB, Novakovic S, Wong K, Sze P, Tzoumaka E, Stewart GR, Herman RC, Chan H, Eglen RM, Hunter JC (1997) A novel tetrodotoxin-sensitive, voltage-gated sodium channel expressed in rat and human dorsal root ganglia. J Biol Chem 272:14805–14809
Sasaki M, Takagi M, Okamura Y (2006) A voltage sensor-domain protein is a voltage-gated proton channel. Science 312:589–592
Sato C, Matsumoto G (1992) Primary structure of squid sodium channel deduced from the complementary DNA sequence. Biochem Biophys Res Commun 186:61–68
Satou Y, Kawashima T, Kohara Y, Satoh N (2003) Large scale EST analyses in Ciona intestinalis: its application as northern blot analyses. Dev Genes Evol 213:314–318
Schredelseker J, Shrivastav M, Dayal A, Grabner M (2010) Non-Ca2+-conducting Ca2+ channels in fish skeletal muscle excitation-contraction coupling. Proc Natl Acad Sci U S A 107:5658–5663
Shen H, Zhou Q, Pan X, Li Z, Wu J, Yan N (2017) Structure of a eukaryotic voltage-gated sodium channel at near-atomic resolution. Science 355:eaal4326
Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N, Campbell MS, Yandell MD, Manousaki T, Meyer A, Bloom OE, Morgan JR, Buxbaum JD, Sachidanandam R, Sims C, Garruss AS, Cook M, Krumlauf R, Wiedemann LM, Sower SA, Decatur WA, Hall JA, Amemiya CT, Saha NR, Buckley KM, Rast JP, Das S, Hirano M, McCurley N, Guo P, Rohner N, Tabin CJ, Piccinelli P, Elgar G, Ruffier M, Aken BL, Searle SM, Muffato M, Pignatelli M, Herrero J, Jones M, Brown CT, Chung-Davidson YW, Nanlohy KG, Libants SV, Yeh CY, McCauley DW, Langeland JA, Pancer Z, Fritzsch B, de Jong PJ, Zhu B, Fulton LL, Theising B, Flicek P, Bronner ME, Warren WC, Clifton SW, Wilson RK, Li W (2013) Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet 45(415–421):421e1–421e2
Strong M, Chandy KG, Gutman GA (1993) Molecular evolution of voltage-sensitive ion channel genes: on the origins of electrical excitability. Mol Biol Evol 10:221–242
Stühmer W, Conti F, Suzuki H, Wang X, Noda M, Yahagi N, Kubo H, Numa S (1989) Structure parts involved in activation and inactivation of the sodium channel. Nature 339:597–603
Takahashi K, Okamura Y (1998) Ion channels and early development of neural cells. Physiol Rev 78:307–337
Takahashi K, Yoshii M (1981) Development of sodium, calcium and potassium channels in the cleavage-arrested embryo of an ascidian. J Physiol 315:515–529
Tate S, Benn S, Hick C, Trezise D (1998) Two sodium channels contribute to the TTX-R sodium current in primary sensory neurons. Nat Neurosci 1:653–655
Tessmar-Raible K, Raible F, Christodoulou F, Guy K, Rembold M, Hausen H, Arendt D (2007) Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 129:1389–1400
Toledo-Aral JJ, Moss BL, He ZJ, Koszowski AG, Whisenand T, Levinson SR, Wolf JJ, Silos-Santiago I, Halegoua S, Mandel G (1997) Identification of PN1, a predominant voltage-dependent sodium channel expressed principally in peripheral neurons. Proc Natl Acad Sci U S A 94:1527–1532
Tomer R, Denes AS, Tessmar-Raible K, Arendt D (2010) Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 142:800–809
Torruella G, Derelle R, Paps J, Lang BF, Roger AJ, Shalchian-Tabrizi K, Ruiz-Trillo I (2011) Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single copy protein domains. Mol Biol Evol 29:531–544
Vergara HM, Bertucci PY, Hantz P, Tosches MA, Achim K, Vopalensky P, Arendt D (2017) Whole-organism cellular gene-expression atlas reveals conserved cell types in the ventral nerve cord of Platynereis dumerilii. Proc Natl Acad Sci U S A 114:5878–5885
West JW, Patton DE, Scheuer T, Wang Y, Goldin AL, Catterall WA (1992) A cluster of hydrophobic amino acid residues required for fast Na+-channel inactivation. Proc Natl Acad Sci U S A 89:10910–10914
Widmark J, Sundström G, Ocampo Daza D, Larhammar D (2011) Differential evolution of voltage-gated sodium channels in tetrapods and teleost fishes. Mol Biol Evol 28:859–871
Willey A (1894) Amphioxus and the ancestry of the vertebrates. Macmillan, New York
Won Y-J, Ono F, Ikeda SR (2012) Characterization of Na+ and Ca2+ channels in zebrafish dorsal root ganglion neurons. PLoS One 7:e42602
Yan Z, Zhou Q, Wang L, Wu J, Zhao Y, Huang G, Peng W, Shen H, Lei J, Yan N (2017) Structure of the NaV1.4-β1 complex from electric eel. Cell 170:470–482.e11
Yue L, Navarro B, Ren D, Ramos A, Clapham DE (2002) The cation selectivity filter of the bacterial sodium channel, NaChBac. J Gen Physiol 120:845–853
Zakon HH (2012) Adaptive evolution of voltage-gated sodium channels: the first 800 million years. Proc Natl Acad Sci U S A 109(Suppl 1):10619–10625
Zakon HH, Jost MC, Lu Y (2011) Expansion of voltage-dependent Na+ channel gene family in early tetrapods coincided with the emergence of terrestriality and increased brain complexity. Mol Biol Evol 28:1415–1424
Zalc B (2016) The acquisition of myelin: an evolutionary perspective. Brain Res 1641:4–10
Zalc B, Goujet D, Colman D (2008) The origin of the myelination program in vertebrates. Curr Biol 18:R511–R512
Zhang T, Wang Z, Wang L, Luo N, Jiang L, Liu Z, Wu C-F, Dong K (2013) Role of the DSC1 channel in regulating neuronal excitability in Drosophila melanogaster: extending nervous system stability under stress. PLoS Genet 9:e1003327
Zhou W, Chung I, Liu Z, Goldin A, Dong K (2004) A voltage-gated calcium-selective channel encoded by a sodium channel-like gene. Neuron 42:101–112
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Drs. Patrick Lemaire, Hiroki Nishida, and Hitoshi Sawada allowed us to utilize genome datasets from ascidians, Halocynthia roretzi and H. aurantium, before the publication of the data.
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Nishino, A., Okamura, Y. (2017). Evolutionary History of Voltage-Gated Sodium Channels. In: Chahine, M. (eds) Voltage-gated Sodium Channels: Structure, Function and Channelopathies. Handbook of Experimental Pharmacology, vol 246. Springer, Cham. https://doi.org/10.1007/164_2017_70
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