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Calcium Channels

A governance of ion selectivity based on the occupancy of the “beacon” in one- and four-domain calcium and sodium channels

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Article: 2191773 | Received 25 Nov 2022, Accepted 07 Mar 2023, Published online: 19 Apr 2023

References

  • Beneski DA, Catterall WA. Covalent labeling of protein components of the sodium channel with a photoactivable derivative of scorpion toxin. Proc Natl Acad Sci U S A. 1980;77:639–26.
  • Hartshorne RP, Coppersmith J, Catterall WA. Size characteristics of the solubilized saxitoxin receptor of the voltage-sensitive sodium channel from rat brain. J Biol Chem. 1980;255:10572–10575.
  • Agnew WS, Moore AC, Levinson SR, et al. Identification of a large molecular weight peptide associated with a tetrodotoxin binding protein from the electroplax of Electrophorus electricus. Biochem Biophys Res Commun. 1980;92:860–866.
  • Noda M, Shimizu S, Tanabe T, et al. Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature. 1984;312:121–127.
  • Bouza AA, Isom LL. Voltage-Gated Sodium Channel beta Subunits and Their Related Diseases. Handb Exp Pharmacol. 2018;246:423–450.
  • Leung AT, Imagawa T, Campbell KP. Structural characterization of the 1,4-dihydropyridine receptor of the voltage-dependent Ca2+ channel from rabbit skeletal muscle. Evidence for two distinct high molecular weight subunits. J Biol Chem. 1987;262:7943–7946.
  • Tanabe T, Takeshima H, Mikami A, et al. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 1987;328:313–318.
  • Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev. 2005;57:397–409.
  • Catterall WA, Perez-Reyes E, Snutch TP, et al. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev. 2005;57:411–425.
  • Perez-Reyes E, Cribbs LL, Daud A, et al. Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature. 1998;391:896–900.
  • Lee JH, Cribbs LL, Perez-Reyes E. Cloning of a novel four repeat protein related to voltage-gated sodium and calcium channels. FEBS Lett. 1999;445:231–236.
  • Senatore A, Monteil A, van Minnen J, et al. NALCN ion channels have alternative selectivity filters resembling calcium channels or sodium channels. PLoS ONE. 2013;8:e55088.
  • Lenaeus MJ, Gamal El-Din TM, Ing C, et al. Structures of closed and open states of a voltage-gated sodium channel. Proc Natl Acad Sci U S A. 2017;114:E3051–60.
  • Gao S, Valinsky WC, On NC, et al. Employing NaChBac for cryo-EM analysis of toxin action on voltage-gated Na(+) channels in nanodisc. Proc Natl Acad Sci U S A. 2020;117:14187–14193.
  • Taiakina V, Boone AN, Fux J, et al. The calmodulin-binding, short linear motif, NSCaTE is conserved in L-type channel ancestors of vertebrate Cav1.2 and Cav1.3 channels. PLoS ONE. 2013;8:e61765.
  • Huang X, Senatore A, Dawson TF, et al. G-proteins modulate invertebrate synaptic calcium channel (LCav2) differently from the classical voltage-dependent regulation of mammalian Cav2.1 and Cav2.2 channels. J Exp Biol. 2010;213:2094–2103.
  • Senatore A, Spafford JD. Transient and big are key features of an invertebrate T-type channel (LCav3) from the central nervous system of Lymnaea stagnalis. J Biol Chem. 2010;285:7447–7458.
  • Catterall WA. Ion channel voltage sensors: structure, function, and pathophysiology. Neuron. 2010;67:915–928.
  • Oelstrom K, Goldschen-Ohm MP, Holmgren M, et al. Evolutionarily conserved intracellular gate of voltage-dependent sodium channels. Nat Commun. 2014;5:3420.
  • Barros F, Pardo LA, Dominguez P, et al. New Structures and Gating of Voltage-Dependent Potassium (Kv) Channels and Their Relatives: a Multi-Domain and Dynamic Question. Int J Mol Sci. 2019;20:20.
  • Whicher JR, MacKinnon R. Structure of the voltage-gated K(+) channel Eag1 reveals an alternative voltage sensing mechanism. Science. 2016;353:664–669.
  • Li M, Zhou X, Wang S, et al. Structure of a eukaryotic cyclic-nucleotide-gated channel. Nature. 2017;542:60–65.
  • Lee CH, MacKinnon R. Structures of the Human HCN1 Hyperpolarization-Activated Channel. Cell. 2017;168:111–20 e11.
  • Tao X, Hite RK, MacKinnon R. Cryo-EM structure of the open high-conductance Ca(2+)-activated K(+) channel. Nature. 2017;541:46–51.
  • Hite RK, MacKinnon R. Structural Titration of Slo2.2, a Na(+)-Dependent K(+) Channel. Cell. 2017;168:390–9 e11.
  • Singh AK, Saotome K, Sobolevsky AI. Swapping of transmembrane domains in the epithelial calcium channel TRPV6. Sci Rep. 2017;7:10669.
  • Hockerman GH, Peterson BZ, Johnson BD, et al. Molecular determinants of drug binding and action on L-type calcium channels. Annu Rev Pharmacol Toxicol. 1997;37:361–396.
  • Doyle DA, Morais Cabral J, Pfuetzner RA, et al. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science. 1998;280:69–77.
  • Stephens RF, Guan W, Zhorov BS, et al. Selectivity filters and cysteine-rich extracellular loops in voltage-gated sodium, calcium, and NALCN channels. Front Physiol. 2015;6:153.
  • Shen H, Liu D, Wu K, et al. Structures of human Nav1.7 channel in complex with auxiliary subunits and animal toxins. Science. 2019;363:1303–1308.
  • Zhao Y, Huang G, Wu J, et al. Molecular Basis for Ligand Modulation of a Mammalian Voltage-Gated Ca(2+) Channel. Cell. 2019;177:1495–506 e12.
  • He L, Yu Z, Geng Z, et al. Structure, gating, and pharmacology of human Ca(V)3.3 channel. Nat Commun. 2022;13:2084.
  • Kschonsak M, Chua HC, Weidling C, et al. Structural architecture of the human NALCN channelosome. Nature. 2022;603:180–186.
  • Payandeh J, Scheuer T, Zheng N, et al. The crystal structure of a voltage-gated sodium channel. Nature. 2011;475:353–358.
  • Toledo G, Hanifin C, Geffeney S, et al. 3rd. Convergent Evolution of Tetrodotoxin-Resistant Sodium Channels in Predators and Prey. Curr Top Membr. 2016;78:87–113.
  • Dutzler R, Campbell EB, Cadene M, et al. X-ray structure of a ClC chloride channel at 3.0 a reveals the molecular basis of anion selectivity. Nature. 2002;415:287–294.
  • Heinemann SH, Terlau H, Stuhmer W, et al. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature. 1992;356:441–443.
  • Schlief T, Schonherr R, Imoto K, et al. Pore properties of rat brain II sodium channels mutated in the selectivity filter domain. Eur Biophys J. 1996;25:75–91.
  • Spafford JD, Spencer AN, Gallin WJ. A putative voltage-gated sodium channel alpha subunit (PpSCN1) from the hydrozoan jellyfish, Polyorchis penicillatus: structural comparisons and evolutionary considerations. Biochem Biophys Res Commun. 1998;244:772–780.
  • Zhou W, Chung I, Liu Z, et al. A voltage-gated calcium-selective channel encoded by a sodium channel-like gene. Neuron. 2004;42:101–112.
  • Zakon HH. Adaptive evolution of voltage-gated sodium channels: the first 800 million years. Proc Natl Acad Sci U S A. 2012;109 Suppl 1:10619–10625.
  • Zakon HH, Li W, Pillai NE, et al. Voltage-gated sodium channel gene repertoire of lampreys: gene duplications, tissue-specific expression and discovery of a long-lost gene. Proc Biol Sci. 2017;284:284.
  • Ren D, Navarro B, Xu H, et al. A prokaryotic voltage-gated sodium channel. Science. 2001;294:2372–2375.
  • Long SB, Campbell EB, Mackinnon R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 2005;309:897–903.
  • Yue L, Navarro B, Ren D, et al. The cation selectivity filter of the bacterial sodium channel. NaChBac J Gen Physiol. 2002;120:845–853.
  • Senatore A, Boone A, Lam S, et al. Mapping of dihydropyridine binding residues in a less sensitive invertebrate L-type calcium channel (LCa v 1). Channels (Austin). 2011;5:173–187.
  • Tang L, Gamal El-Din TM, Payandeh J, et al. Structural basis for Ca2+ selectivity of a voltage-gated calcium channel. Nature. 2014;505:56–61.
  • Guan W, Orellana KG, Stephens RF, et al. A lysine residue from an extracellular turret switches the ion preference in a Cav3 T-Type channel from calcium to sodium ions. J Biol Chem. 2022;2022:102621.
  • Guan W, Stephens RF, Mourad O, et al. Unique cysteine-enriched, D2L5 and D4L6 extracellular loops in CaV3 T-type channels alter the passage and block of monovalent and divalent ions. Sci Rep. 2020;10:12404.
  • Kschonsak M, Chua HC, Noland CL, et al. Structure of the human sodium leak channel NALCN. Nature. 2020;587:313–318.
  • Xie J, Ke M, Xu L, et al. Structure of the human sodium leak channel NALCN in complex with FAM155A. Nat Commun. 2020;11:5831.
  • Chua HC, Wulf M, Weidling C, et al. The NALCN channel complex is voltage sensitive and directly modulated by extracellular calcium. Sci Adv. 2020;6:eaaz3154.
  • Senatore A, Spafford JD. A uniquely adaptable pore is consistent with NALCN being an ion sensor. Channels (Austin). 2013;7:60–68.
  • Senatore A, Guan W, Boone AN, et al. T-type channels become highly permeable to sodium ions using an alternative extracellular turret region (S5-P) outside the selectivity filter. J Biol Chem. 2014;289:11952–11969.
  • Huang G, Liu D, Wang W, et al. High-resolution structures of human Nav1.7 reveal gating modulation through alpha-pi helical transition of S6IV. Cell Rep. 2022;39:110735.
  • Wu J, Yan Z, Li Z, et al. Structure of the voltage-gated calcium channel Ca(v)1.1 at 3.6 a resolution. Nature. 2016;537:191–196.
  • Shen H, Zhou Q, Pan X, et al. Structure of a eukaryotic voltage-gated sodium channel at near-atomic resolution. Science. 2017;355. DOI:10.1126/science.aal4326
  • Fux JE, Mehta A, Moffat J, et al. Eukaryotic Voltage-Gated Sodium Channels: on Their Origins, Asymmetries, Losses, Diversification and Adaptations. Front Physiol. 2018;9:1406.
  • Zhao Y, Huang G, Wu Q, et al. Cryo-EM structures of apo and antagonist-bound human Cav3.1. Nature. 2019;576:492–497.
  • Wang DW, George AL Jr., Bennett PB. Comparison of heterologously expressed human cardiac and skeletal muscle sodium channels. Biophys J. 1996;70:238–245.
  • Vinogradova I, Cook A, Holden-Dye L. The ionic dependence of voltage-activated inward currents in the pharyngeal muscle of Caenorhabditis elegans. Invert Neurosci. 2006;6:57–68.
  • Franks CJ, Pemberton D, Vinogradova I, et al. Ionic basis of the resting membrane potential and action potential in the pharyngeal muscle of Caenorhabditis elegans. J Neurophysiol. 2002;87:954–961.
  • Hess P, Lansman JB, Tsien RW. Calcium channel selectivity for divalent and monovalent cations. Voltage and concentration dependence of single channel current in ventricular heart cells. J Gen Physiol. 1986;88:293–319.
  • Kostiuk PG, Mironov SL, Shuba Ia M. 2 selective filters in the calcium channel of the somatic membrane of mollusk neurons. Neirofiziologiia. 1983;15:420–427.
  • Almers W, McCleskey EW. Non-selective conductance in calcium channels of frog muscle: calcium selectivity in a single-file pore. J Physiol. 1984;353:585–608.
  • Almers W, McCleskey EW, Palade PT. A non-selective cation conductance in frog muscle membrane blocked by micromolar external calcium ions. J Physiol. 1984;353:565–583.
  • Kuo CC, Hess P. Ion permeation through the L-type Ca2+ channel in rat pheochromocytoma cells: two sets of ion binding sites in the pore. J Physiol. 1993;466:629–655.
  • Berridge MJ. Calcium microdomains: organization and function. Cell Calcium. 2006;40:405–412.
  • Shcheglovitov A, Kostyuk P, Shuba Y. Selectivity signatures of three isoforms of recombinant T-type Ca2+ channels. Biochim Biophys Acta. 2007;1768:1406–1419.
  • Hille B. The permeability of the sodium channel to metal cations in myelinated nerve. J Gen Physiol. 1972;59:637–658.
  • Meves H, Vogel W. Calcium inward currents in internally perfused giant axons of Loligo forbesi. J Physiol. 1972;226:89P–90P.
  • Ben-Johny M, Dick IE, Sang L, et al. Towards a Unified Theory of Calmodulin Regulation (Calmodulation) of Voltage-Gated Calcium and Sodium Channels. Curr Mol Pharmacol. 2015;8:188–205.
  • Hanemaaijer NA, Popovic MA, Wilders X, et al. Ca(2+) entry through NaV channels generates submillisecond axonal Ca(2+) signaling. Elife. 2020;9. DOI:10.7554/eLife.54566
  • Qi H, Moran MM, Navarro B, et al. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci U S A. 2007;104:1219–1223.
  • Shimomura T, Yonekawa Y, Nagura H, et al. A native prokaryotic voltage-dependent calcium channel with a novel selectivity filter sequence. Elife. 2020;9. DOI:10.7554/eLife.52828
  • Helliwell KE, Chrachri A, Koester JA, et al. A Novel Single-Domain Na(+)-Selective Voltage-Gated Channel in Photosynthetic Eukaryotes. Plant Physiol. 2020;184:1674–1683.
  • Helliwell KE, Chrachri A, Koester JA, et al. Alternative Mechanisms for Fast Na(+)/Ca(2+) Signaling in Eukaryotes via a Novel Class of Single-Domain Voltage-Gated Channels. Curr Biol. 2019;29:1503–11 e6.
  • Ren D, Navarro B, Perez G, et al. A sperm ion channel required for sperm motility and male fertility. Nature. 2001;413:603–609.
  • Tikhonov DB, Zhorov BS. Possible roles of exceptionally conserved residues around the selectivity filters of sodium and calcium channels. J Biol Chem. 2011;286:2998–3006.
  • McNulty MM, Edgerton GB, Shah RD, et al. Charge at the lidocaine binding site residue Phe-1759 affects permeation in human cardiac voltage-gated sodium channels. J Physiol. 2007;581:741–755.
  • Cortes DM, Cuello LG, Perozo E. Molecular architecture of full-length KcsA: role of cytoplasmic domains in ion permeation and activation gating. J Gen Physiol. 2001;117:165–180.
  • Pan X, Li Z, Zhou Q, et al. Structure of the human voltage-gated sodium channel Na(v)1.4 in complex with beta1. Science. 2018;362. DOI:10.1126/science.aau2486.
  • Chovancova E, Pavelka A, Benes P, et al. CAVER 3.0: a tool for the analysis of transport pathways in dynamic protein structures. PLoS Comput Biol. 2012;8:e1002708.
  • Smart OS, Neduvelil JG, Wang X, et al. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J Mol Graph. 1996;14:354–360.
  • Berka K, Hanak O, Sehnal D, et al. Moleonline 2.0: interactive web-based analysis of biomacromolecular channels. Nucleic Acids Res. 2012;40:W222–7.
  • Pellegrini-Calace M, Maiwald T, Thornton JM. PoreWalker: a novel tool for the identification and characterization of channels in transmembrane proteins from their three-dimensional structure. PLoS Comput Biol. 2009;5:e1000440.
  • Blasic JR, Worcester DL, Gawrisch K, et al. Pore hydration states of KcsA potassium channels in membranes. J Biol Chem. 2015;290:26765–26775.
  • Chakrabarti N, Ing C, Payandeh J, et al. Catalysis of Na+ permeation in the bacterial sodium channel Na(V)Ab. Proc Natl Acad Sci U S A. 2013;110:11331–11336.
  • Charalambous K, Wallace BA. NaChBac: the long lost sodium channel ancestor. Biochemistry. 2011;50:6742–6752.
  • Cai X, Clapham DE, Schwartz A. Evolutionary Genomics Reveals Lineage-Specific Gene Loss and Rapid Evolution of a Sperm-Specific Ion Channel Complex: CatSpers and CatSperβ. PLoS ONE. 2008;3:e3569.
  • Bonigk W, Loogen A, Seifert R, et al. An atypical CNG channel activated by a single cGMP molecule controls sperm chemotaxis. Sci Signal. 2009;2:ra68.
  • Fechner S, Alvarez L, Bonigk W, et al. A K(+)-selective CNG channel orchestrates Ca(2+) signalling in zebrafish sperm. Elife. 2015;4. DOI:10.7554/eLife.07624.
  • Strong M, Chandy KG, Gutman GA. Molecular evolution of voltage-sensitive ion channel genes: on the origins of electrical excitability. Mol Biol Evol. 1993;10:221–242.
  • Chemin J, Taiakina V, Monteil A, et al. Calmodulin regulates Cav3 T-type channels at their gating brake. J Biol Chem. 2017;292:20010–20031.
  • Lodh S, Yano J, Valentine MS, et al. Voltage-gated calcium channels of Paramecium cilia. J Exp Biol. 2016;219:3028–3038.
  • Fujiu K, Nakayama Y, Yanagisawa A, et al. Chlamydomonas CAV2 encodes a voltage- dependent calcium channel required for the flagellar waveform conversion. Curr Biol. 2009;19:133–139.
  • Yabuki A, Kamikawa R, Ishikawa SA, et al. Palpitomonas bilix represents a basal cryptist lineage: insight into the character evolution in Cryptista. Sci Rep. 2014;4:4641.
  • Cavalier-Smith T, Chao EE, Snell EA, et al. Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa. Mol Phylogenet Evol. 2014;81:71–85.
  • Senatore A, Spafford JD. Voltage-Gated Calcium Channels in Invertebrates. In: GW Z, and Weiss N, editors. Voltage-Gated Calcium Channels 2nd . Berlin/Heidelberg, Germany: Springer; 2022. pp. 115–158.
  • Liebeskind BJ, Hillis DM, Zakon HH. Phylogeny unites animal sodium leak channels with fungal calcium channels in an ancient, voltage-insensitive clade. Mol Biol Evol. 2012;29:3613–3616.