Voltage-gated Sodium Channels in Sensory Information Processing

Author(s): You Zhou , Ping Pan , Zhi-Yong Tan , Yong-Hua Ji* .

Journal Name: CNS & Neurological Disorders - Drug Targets

Volume 18 , Issue 4 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Objective & Background: Voltage-gated sodium channels (VGSCs) and potassium channels are critical in the generation of action potentials in the nervous system. VGSCs and potassium channels play important roles in the five fundamental senses of vision, audition, olfaction, taste and touch. Dysfunctional VGSCs are associated with clinical sensory symptoms, such as hyperpselaphesia, parosphresia, and so on.

Conclusion: This short review highlights the recent advances in the study of VGSCs in sensory information processing and discusses the potential role of VGSCs to serve as pharmacological targets for the treatment of sensory system diseases.

Keywords: Voltage-gated sodium channel, action potential, information processing, membrane, protein complexes central nervous system, pharmacological.

Catterall WA. From ionic currents to molecular mechanisms: The structure and function of voltage-gated sodium channels. Neuron 2000; 26(1): 13-25.
Patino GA, Isom LL. Electrophysiology and beyond: Multiple roles of Na+ channel beta subunits in development and disease. Neurosci Lett 2010; 486(2): 53-9.
Yu FH, Yarov-Yarovoy V, Gutman GA, Catterall WA. Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacol Rev 2005; 57(4): 387-95.
Andavan GS, Lemmens-Gruber R. Voltage-gated sodium channels: Mutations, channelopathies and targets. Curr Med Chem 2011; 18(3): 377-97.
Weiss J, Pyrski M, Jacobi E, et al. Loss-of-function mutations in sodium channel Nav1.7 cause anosmia. Nature 2011; 472(7342): 186-90.
Litovsky R. Development of the auditory system. Handbook of clinical neurology 2015; 129: 55-72.
Johnson SL, Eckrich T, Kuhn S, et al. Position-dependent patterning of spontaneous action potentials in immature cochlear inner hair cells Nature Neurosci 201; 14(6): 711-7
Sendin G, Bourien J, Rassendren F, Puel JL, Nouvian R. Spatiotemporal pattern of action potential firing in developing inner hair cells of the mouse cochlea. Proc Natl Acad Sci USA 2014; 111(5): 1999-2004.
Marcotti W, Johnson SL, Kros CJ. A transiently expressed SK current sustains and modulates action potential activity in immature mouse inner hair cells. J Physiol 2004; 560(Pt 3): 691-708.
Marcotti W, Johnson SL, Rusch A, Kros CJ. Sodium and calcium currents shape action potentials in immature mouse inner hair cells. J Physiol 2003; 552(Pt 3): 743-61.
Johnson SL, Adelman JP, Marcotti W. Genetic deletion of SK2 channels in mouse inner hair cells prevents the developmental linearization in the Ca2+ dependence of exocytosis. J Physiol 2007; 583(Pt 2): 631-46.
Johnson SL, Kuhn S, Franz C, et al. Presynaptic maturation in auditory hair cells requires a critical period of sensory-independent spiking activity. Proc Natl Acad Sci USA 2013; 110(21): 8720-5.
Eckrich T, Varakina K, Johnson SL, et al. Development and function of the voltage-gated sodium current in immature mammalian cochlear inner hair cells. PLoS One 2012; 7(9)e45732
D OM. Hudspeth AJ. Effects of cochlear loading on the motility of active outer hair cells. Proc Natl Acad Sci USA 2013; 110(14): 5474-9.
Oliver D, Plinkert P, Zenner HP, Ruppersberg JP. Sodium current expression during postnatal development of rat outer hair cells. Pflugers Archiv: Euro J Physiol 1997; 434(6): 772-8.
Housley GD, Marcotti W, Navaratnam D, Yamoah EN. Hair cells--beyond the transducer. J Membr Biol 2006; 209(2-3): 89-118.
Sangameswaran L, Fish LM, Koch BD, et al. A novel tetrodotoxin-sensitive, voltage-gated sodium channel expressed in rat and human dorsal root ganglia. J Biol Chem 1997; 272(23): 14805-9.
Zhou Y, Fang FH, Liu ZR, Ji YH. Dissection of voltage-gated sodium channels in developing cochlear sensory epithelia. Protein Cell 2015; 6(6): 458-62.
Froud KE, Wong AC, Cederholm JM, et al. Type II spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the cochlear amplifier. Nat Commun 2015; 6: 7115.
Fryatt AG, Vial C, Mulheran M, Gunthorpe MJ, Grubb BD. Voltage-gated sodium channel expression in rat spiral ganglion neurons. Mol Cell Neurosci 2009; 42(4): 399-407.
Hossain WA, Antic SD, Yang Y, Rasband MN, Morest DK. Where is the spike generator of the cochlear nerve? Voltage-gated sodium channels in the mouse cochlea. J Neurosci 2005; 25(29): 6857-68.
Liu Y, Li X. Effects of salicylate on voltage-gated sodium channels in rat inferior colliculus neurons. Hear Res 2004; 193(1-2): 68-74.
Liu Y, Zhang H, Li X, et al. Inhibition of voltage-gated channel currents in rat auditory cortex neurons by salicylate. Neuropharmacology 2007; 53(7): 870-80.
Weinmeister KP. Prolonged suppression of tinnitus after peripheral nerve block using bupivacaine and lidocaine. Reg Anesth Pain Med 2000; 25(1): 67-8.
Savastano M. Lidocaine intradermal injection--a new approach in tinnitus therapy: Preliminary report. Adv Ther 2004; 21(1): 13-20.
Trellakis S, Lautermann J, Lehnerdt G. Lidocaine: Neurobiological targets and effects on the auditory system. Prog Brain Res 2007; 166: 303-22.
Kallio H, Niskanen ML, Havia M, Neuvonen PJ, Rosenberg PH, Kentala E. I.V. ropivacaine compared with lidocaine for the treatment of tinnitus. Br J Anaesth 2008; 101(2): 261-5.
Ciodaro F, Mannella VK, Cammaroto G, Bonanno L, Galletti F, Galletti B. Oral gabapentin and intradermal injection of lidocaine: Is there any role in the treatment of moderate/severe tinnitus? Eur Arch Oto-Rhino-L 2015; 272(10): 2825-30.
Elzayat S, El-Sherif H, Hegazy H, Gabr T, El-Tahan AR. Tinnitus: Evaluation of intratympanic injection of combined lidocaine and corticosteroids. Orl J Oto-Rhino-Lary 2016; 78(3): 159-66.
Seabrook TA, Burbridge TJ, Crair MC, Huberman AD. Architecture, function, and assembly of the mouse visual system. Annu Rev Neurosci 2017; 40: 499-538.
Kawai F, Horiguchi M, Suzuki H, Miyachi E. Na(+) action potentials in human photoreceptors. Neuron 2001; 30(2): 451-8.
Ohkuma M, Kawai F, Horiguchi M, Miyachi E. Patch-clamp recording of human retinal photoreceptors and bipolar cells. Photochem Photobiol 2007; 83(2): 317-22.
Zenisek D, Henry D, Studholme K, Yazulla S, Matthews G. Voltage-dependent sodium channels are expressed in nonspiking retinal bipolar neurons. J Neurosci 2001; 21(13): 4543-50.
Cui J, Pan ZH. Two types of cone bipolar cells express voltage-gated Na+ channels in the rat retina. Vis Neurosci 2008; 25(5-6): 635-45.
Smith BJ, Tremblay F, Cote PD. Voltage-gated sodium channels contribute to the b-wave of the rodent electroretinogram by mediating input to rod bipolar cell GABA(c) receptors. Exp Eye Res 2013; 116: 279-90.
Tian M, Jarsky T, Murphy GJ, Rieke F, Singer JH. Voltage-gated Na channels in AII amacrine cells accelerate scotopic light responses mediated by the rod bipolar cell pathway. J Neurosci 2010; 30(13): 4650-9.
Cohen ED. Voltage-gated calcium and sodium currents of starburst amacrine cells in the rabbit retina. Vis Neurosci 2001; 18(5): 799-809.
Fjell J, Dib-Hajj S, Fried K, Black JA, Waxman SG. Differential expression of sodium channel genes in retinal ganglion cells. Brain Res Mol Brain Res 1997; 50(1-2): 197-204.
Kaneda M, Kaneko A. Voltage-gated sodium currents in isolated retinal ganglion cells of the cat: Relation between the inactivation kinetics and the cell type. Neurosci Res 1991; 11(4): 261-75.
Lipton SA, Tauck DL. Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. J Physiol 1987; 385: 361-91.
Schmid S, Guenther E. Alterations in channel density and kinetic properties of the sodium current in retinal ganglion cells of the rat during in vivo differentiation. Neuroscience 1998; 85(1): 249-58.
Smith BJ, Cote PD, Tremblay F. Contribution of Nav1.8 sodium channels to retinal function. Neuroscience 2017; 340: 279-90.
Puthussery T, Venkataramani S, Gayet-Primo J, Smith RG, Taylor WR. NaV1.1 channels in axon initial segments of bipolar cells augment input to magnocellular visual pathways in the primate retina. J Neurosci 2013; 33(41): 16045-59.
Smith BJ, Cote PD. Reduced retinal function in the absence of Na(v)1.6. PLoS One 2012; 7(2)e31476
O’Brien BJ, Caldwell JH, Ehring GR, Bumsted O’Brien KM, Luo S, Levinson SR. Tetrodotoxin-resistant voltage-gated sodium channels Na(v)1.8 and Na(v)1.9 are expressed in the retina. J Comp Neurol 2008; 508(6): 940-51.
Bolz F, Kasper S, Bufe B, Zufall F, Pyrski M. Organization and plasticity of sodium channel expression in the mouse olfactory and vomeronasal epithelia. Front Neuroanat 2017; 11: 28.
Firestein S. How the olfactory system makes sense of scents? Nature 2001; 413(6852): 211-8.
Kaupp UB. Olfactory signalling in vertebrates and insects: Differences and commonalities. Nat Rev Neurosci 2010; 11(3): 188-200.
Chen N, Lucero MT. Transient and persistent tetrodotoxin-sensitive sodium currents in squid olfactory receptor neurons. J Behav Physiol 1999; 184(1): 63-72.
Trombley PQ, Westbrook GL. Voltage-gated currents in identified rat olfactory receptor neurons. J Neurosci 1991; 11(2): 435-44.
Goldberg YP, MacFarlane J, MacDonald ML, et al. Loss-of-function mutations in the Nav1.7 gene underlie congenital indifference to pain in multiple human populations. Clin Genet 2007; 71(4): 311-9.
Zufall F, Pyrski M, Weiss J, Leinders-Zufall T. Link between pain and olfaction in an inherited sodium channelopathy. Arch Neurol-Chicago 2012; 69(9): 1119-23.
Shorer Z, Wajsbrot E, Liran TH, Levy J, Parvari R. A novel mutation in scn9a in a child with congenital insensitivity to pain. Pediatr Neurol 2014; 50(1): 73-6.
Nilsen KB, Nicholas AK, Woods CG, Mellgren SI, Nebuchennykh M, Aasly J. Two novel SCN9A mutations causing insensitivity to pain. Pain 2009; 143(1-2): 155-8.
Heimann D, Lotsch J, Hummel T, Doehring A, Oertel BG. Linkage between increased nociception and olfaction via a SCN9A Haplotype. PLoS One 2013; 8(7): 253-8.
Ahn HS, Black JA, Zhao P, Tyrrell L, Waxman SG, Dib-Hajj SD. Nav1.7 is the predominant sodium channel in rodent olfactory sensory neurons. Mol Pain 2011; 7: 32.
Rupasinghe DB, Knapp O, Blomster LV, et al. Localization of Nav 1.7 in the normal and injured rodent olfactory system indicates a critical role in olfaction, pheromone sensing and immune function. Channels 2012; 6(2): 103-10.
Kis-Toth K, Hajdu P, Bacskai I, et al. Voltage-gated sodium channel Nav1.7 maintains the membrane potential and regulates the activation and chemokine-induced migration of a monocyte-derived dendritic cell subset. J Immunol 2011; 187(3): 1273-80.
Frenz CT, Hansen A, Dupuis ND, et al. NaV1.5 sodium channel window currents contribute to spontaneous firing in olfactory sensory neurons. J Neurophysiol 2014; 112(5): 1091-104.
Schneider ER, Gracheva EO, Bagriantsev SN. Evolutionary specialization of tactile perception in vertebrates. Physiology 2016; 31(3): 193-200.
Bolanowski SJ Jr. Intensity and frequency characteristics of pacinian corpuscles. III. Effects of tetrodotoxin on transduction process. J Neurophysiol 1984; 51(4): 831-9.
Pawson L, Bolanowski SJ. Voltage-gated sodium channels are present on both the neural and capsular structures of Pacinian corpuscles. Somatosens Mot Res 2002; 19(3): 231-7.
Hu J, Lewin GR. Mechanosensitive currents in the neurites of cultured mouse sensory neurones. J Physiol 2006; 577(Pt 3): 815-28.
Low SE, Zhou WB, Choong I, et al. Na(v)1.6a is required for normal activation of motor circuits normally excited by tactile stimulation. Dev Neurobiol 2010; 70(7): 508-22.
Beyder A, Rae JL, Bernard C, Strege PR, Sachs F, Farrugia G. Mechanosensitivity of Nav1.5, a voltage-sensitive sodium channel. J Physiol 2010; 588(Pt 24): 4969-85.
Morris CE, Juranka PF. Nav channel mechanosensitivity: Activation and inactivation accelerate reversibly with stretch. J Biophys 2007; 93(3): 822-33.
Wang JA, Lin W, Morris T, Banderali U, Juranka PF, Morris CE. Membrane trauma and Na+ leak from Nav1.6 channels. Am J Physiol 2009; 297(4): C823-34.
Price MP, Lewin GR, McIlwrath SL, et al. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 2000; 407(6807): 1007-11.
Raouf R, Rugiero F, Kiesewetter H, et al. Sodium channels and mammalian sensory mechanotransduction. Mol Pain 2012; 8: 21.
Liman ER, Zhang YV, Montell C. Peripheral coding of taste. Neuron 2014; 81(5): 984-1000.
Gilbertson TA. The physiology of vertebrate taste reception. Curr Opin Neurobiol 1993; 3(4): 532-9.
Lindemann B. Taste reception. Physiol Rev 1996; Jul 76(3): 718-66.
Roper SD. Signal transduction and information processing in mammalian taste buds. Pflugers Archiv: Eur Physiol 2007; 454(5): 759-76.
Sugita M. Taste perception and coding in the periphery. Cell Mol Sci 2006; 63(17): 2000-15.
Herness MS, Sun XD. Voltage-dependent sodium currents recorded from dissociated rat taste cells. J Membr Biol 1995; 146(1): 73-84.
Takeuchi K, Yoshii K. Effect of superoxide derived from lucifer yellow CH on voltage-gated currents of mouse taste bud cells. Chem Senses 2008; 33(5): 425-32.
Suwabe T, Kitada Y. Voltage-gated inward currents of morphologically identified cells of the frog taste disc. Chem Senses 2004; 29(1): 61-73.
Gao N, Lu M, Echeverri F, et al. Voltage-gated sodium channels in taste bud cells. BMC Neurosci 2009; 10: 20.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Page: [273 - 278]
Pages: 6
DOI: 10.2174/1871527317666180627114849
Price: $58

Article Metrics

PDF: 31