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Research Paper

Functional modulation of the human voltage-gated sodium channel NaV1.8 by auxiliary β subunits

, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 79-93 | Received 24 Nov 2020, Accepted 30 Nov 2020, Published online: 29 Dec 2020

References

  • Hartshorne RP, Messner DJ, Coppersmith JC, et al. The saxitoxin receptor of the sodium channel from rat brain. Evidence for two nonidentical β subunits. J Biol Chem. 1982;257(23):13888–13891.
  • Hartshorne RP, Catterall WA. The sodium channel from rat brain. Purification and subunit composition. J Biol Chem. 1984;259(3):1667–1675.
  • Morgan K, Stevens EB, Shah B, et al. β3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proc Natl Acad Sci U S A. 2000;97(5):2308–2313.
  • Yu FH, Westenbroek RE, Silos-Santiago I, et al. Sodium channel β4, a new disulfide-linked auxiliary subunit with similarity to β2. J Neurosci. 2003;23(20):7577–7585.
  • Shah BS, Stevens EB, Gonzalez MI, et al. β3, a novel auxiliary subunit for the voltage-gated sodium channel, is expressed preferentially in sensory neurons and is upregulated in the chronic constriction injury model of neuropathic pain. Eur J Neurosci. 2000;12(11):3985–3990.
  • Isom LL, De Jongh KS, Patton DE, et al. Primary structure and functional expression of the β1 subunit of the rat brain sodium channel. Science. 1992;256(5058):839–842.
  • Isom LL, Ragsdale DS, De Jongh KS, et al. Structure and function of the β2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell. 1995;83(3):433–442.
  • Kraner SD, Tanaka JC, Barchi RL. Purification and functional reconstitution of the voltage-sensitive sodium channel from rabbit T-tubular membranes. J Biol Chem. 1985;260(10):6341–6347.
  • Black JA, Dib-Hajj S, McNabola K, et al. Spinal sensory neurons express multiple sodium channel α-subunit mRNAs. Brain Res Mol Brain Res. 1996;43(1–2)):117–131.
  • Felts PA, Yokoyama S, Dib-Hajj S, et al. Sodium channel α-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Brain Res Mol Brain Res. 1997;45(1):71–82.
  • Dib-Hajj SD, Tyrrell L, Black JA, et al. NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc Natl Acad Sci U S A. 1998;95(15):8963–8968.
  • Djouhri L, Fang X, Okuse K, et al. The TTX-resistant sodium channel Nav1.8 (SNS/PN3): expression and correlation with membrane properties in rat nociceptive primary afferent neurons. J Physiol. 2003;550(Pt 3):739–752.
  • Akopian AN, Sivilotti L, Wood JN. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature. 1996;379(6562):257–262.
  • Sutkowski EM, Catterall WA. β1 subunits of sodium channels. Studies with subunit-specific antibodies. J Biol Chem. 1990;265(21):12393–12399.
  • Akopian AN, Souslova V, England S, et al. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci. 1999;2(6):541–548.
  • Wang J, Ou S-W, Wang Y-J. Distribution and function of voltage-gated sodium channels in the nervous system. Channels. 2017;11(6):534–554.
  • Faber CG, Lauria G, Merkies IS, et al. Gain-of-function Nav1.8 mutations in painful neuropathy. Proc Natl Acad Sci USA. 2012;109(47):19444–19449.
  • Zimmermann K, Leffler A, Babes A, et al. Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature. 2007;447(7146):855–858.
  • Dib-Hajj SD, Binshtok AM, Cummins TR, et al. Voltage-gated sodium channels in pain states: role in pathophysiology and targets for treatment. Brain Res Rev. 2009;60(1):65–83.
  • Porreca F, Lai J, Bian D, et al. A comparison of the potential role of the tetrodotoxin-insensitive sodium channels, PN3/SNS and NaN/SNS2, in rat models of chronic pain. Proc Natl Acad Sci U S A. 1999;96(14):7640–7644.
  • Novakovic SD, Tzoumaka E, McGivern JG, et al. Distribution of the tetrodotoxin-resistant sodium channel PN3 in rat sensory neurons in normal and neuropathic conditions. J Neurosci. 1998;18(6):2174–2187.
  • Okuse K, Chaplan SR, McMahon SB, et al. Regulation of expression of the sensory neuron-specific sodium channel SNS in inflammatory and neuropathic pain. Mol Cell Neurosci. 1997;10(3/4):196–207.
  • Dib-Hajj SD, Fjell J, Cummins TR, et al. Plasticity of sodium channel expression in DRG neurons in the chronic constriction injury model of neuropathic pain. Pain. 1999;83(3):591–600.
  • Dib-Hajj S, Black JA, Felts P, et al. Down-regulation of transcripts for Na channel α-SNS in spinal sensory neurons following axotomy. Proc Natl Acad Sci USA. 1996;93(25):14950–14954.
  • Coward K, Jowett A, Plumpton C, et al. Sodium channel β1 and β2 subunits parallel SNS/PN3 α-subunit changes in injured human sensory neurons. Neuroreport. 2001;12(3):483–488.
  • Meadows LS, Chen YH, Powell AJ, et al. Functional modulation of human brain Nav1.3 sodium channels, expressed in mammalian cells, by auxiliary β1, β2 and β3 subunits. Neuroscience. 2002;114(3):745–753.
  • Blackburn-Munro G, Fleetwood-Walker SM. The sodium channel auxiliary subunits β1 and β2 are differentially expressed in the spinal cord of neuropathic rats. Neuroscience. 1999;90(1):153–164.
  • Casula MA, Facer P, Powell AJ, et al. Expression of the sodium channel β3 subunit in injured human sensory neurons. Neuroreport. 2004;15(10):1629–1632.
  • Takahashi N, Kikuchi S, Dai Y, et al. Expression of auxiliary β subunits of sodium channels in primary afferent neurons and the effect of nerve injury. Neuroscience. 2003;121(2):441–450.
  • Vijayaragavan K, O’Leary ME, Chahine M. Gating properties of Nav1.7 and Nav1.8 peripheral nerve sodium channels. J Neurosci. 2001;21(20):7909–7918.
  • Fitzgerald EM, Okuse K, Wood JN, et al. cAMP-dependent phosphorylation of the tetrodotoxin-resistant voltage-dependent sodium channel SNS. J Physiol. 1999;516(Pt 2):433–446.
  • John VH, Main MJ, Powell AJ, et al. Heterologous expression and functional analysis of rat Nav1.8 (SNS) voltage-gated sodium channels in the dorsal root ganglion neuroblastoma cell line ND7-23. Neuropharmacology. 2004;46(3):425–438.
  • Zhang Z-N, Li Q, Liu C, et al. The voltage-gated Na+ channel Nav1.8 contains an ER-retention/retrieval signal antagonized by the β3 subunit. J Cell Sci. 2008;121:3243–3252.
  • Knapp O, Nevin ST, Yasuda T, et al. Biophysical properties of Nav1.8/Nav1.2 chimeras and inhibition by µO-conotoxin MrVIB. Br J Pharmacol. 2012;166(7):2148–2160.
  • Deuis JR, Dekan Z, Inserra MC, et al. Development of a µO-conotoxin analogue with improved lipid membrane interactions and potency for the analgesic sodium channel Nav1.8. J Biol Chem. 2016;291(22):11829–11842.
  • Browne LE, Clare JJ, Wray D. Functional and pharmacological properties of human and rat Nav1.8 channels. Neuropharmacology. 2009;56(5):905–914.
  • Zhao J, O’Leary ME, Chahine M. Regulation of Nav1.6 and Nav1.8 peripheral nerve Na+ channels by auxiliary β-subunits. J Neurophysiol. 2011;106(2):608–619.
  • Kvist T, Hansen KB, Brauner-Osborne H. The use of Xenopus oocytes in drug screening. Expert Opin Drug Discov. 2011;6(2):141–153.
  • Messner DJ, Catterall WA. The sodium channel from rat brain. Separation and characterization of subunits. J Biol Chem. 1985;260(19):10597–10604.
  • Yan Z, Zhou Q, Wang L, et al. Structure of the Nav1.4-β1 complex from electric eel. Cell. 2017;170(3):470–482e11.
  • Namadurai S, Balasuriya D, Rajappa R, et al. Crystal structure and molecular imaging of the Nav channel β3 subunit indicates a trimeric assembly. J Biol Chem. 2014;289(15):10797–10811.
  • Gloor S, Pongs O, Schmalzing G. A vector for the synthesis of cRNAs encoding Myc epitope-tagged proteins in Xenopus laevis oocytes. Gene. 1995;160(2):213–217.
  • Nicke A, Bäumert HG, Rettinger J, et al. P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. Embo J. 1998;17(11):3016–3028.
  • Smith RD, Goldin AL. Functional analysis of the rat I sodium channel in Xenopus oocytes. J Neurosci. 1998;18(3):811–820.
  • Stevens EB, Cox PJ, Shah BS, et al. Tissue distribution and functional expression of the human voltage-gated sodium channel β3 subunit. Pflugers Arch. 2001;441(4):481–488.
  • Vijayaragavan K, Powell AJ, Kinghorn IJ, et al. Role of auxiliary β1-, β2-, and β3-subunits and their interaction with Nav1.8 voltage-gated sodium channel. Biochem Biophys Res Commun. 2004;319(2):531–540.
  • Wilson MJ, Zhang MM, Azam L, et al. Navβ subunits modulate the inhibition of Nav1.8 by the analgesic gating modifier µO-conotoxin MrVIB. J Pharmacol Exp Ther. 2011;338(2):687–693.
  • Browne LE, Blaney FE, Yusaf SP, et al. Structural determinants of drugs acting on the Nav1.8 channel. J Biol Chem. 2009;284(16):10523–10536.
  • Zhu W, Voelker TL, Varga Z, et al. Mechanisms of noncovalent β subunit regulation of NaV channel gating. J Gen Physiol. 2017;149(8):813–831.
  • Cummins TR, Aglieco F, Renganathan M, et al. Nav1.3 sodium channels: rapid repriming and slow closed-state inactivation display quantitative differences after expression in a mammalian cell line and in spinal sensory neurons. J Neurosci. 2001;21(16):5952–5961.
  • Han C, Estacion M, Huang J, et al. Human Nav1.8: enhanced persistent and ramp currents contribute to distinct firing properties of human DRG neurons. J Neurophysiol. 2015;113(9):3172–3185.
  • Isom LL. Sodium channel β subunits: anything but auxiliary. Neuroscientist. 2001;7(1):42–54.
  • Isom LL. The role of sodium channels in cell adhesion. Front Biosci. 2002;7:12–23.
  • Barchi RL, Casadei JM, Gordon RD, et al. Voltage-sensitive sodium channels: an evolving molecular view. Soc Gen Physiol Ser. 1987;41:125–148.
  • Malik-Hall M, Poon WY, Baker MD, et al. Sensory neuron proteins interact with the intracellular domains of sodium channel NaV1.8. Brain Res Mol Brain Res. 2003;110(2):298–304.
  • Okuse K, Malik-Hall M, Baker MD, et al. Annexin II light chain regulates sensory neuron-specific sodium channel expression. Nature. 2002;417(6889):653–656.
  • Fotia AB, Ekberg J, Adams DJ, et al. Regulation of neuronal voltage-gated sodium channels by the ubiquitin-protein ligases Nedd4 and Nedd4-2. J Biol Chem. 2004;279(28):28930–28935.
  • Dib-Hajj SD, Ishikawa K, Cummins TR, et al. Insertion of a SNS-specific tetrapeptide in S3-S4 linker of D4 accelerates recovery from inactivation of skeletal muscle voltage-gated Na channel µ1 in HEK293 cells. FEBS Lett. 1997;416(1):11–14.
  • Oh Y, Sashihara S, Black JA, et al. Na+ channel β1 subunit mRNA: differential expression in rat spinal sensory neurons. Brain Res Mol Brain Res. 1995;30(2):357–361.
  • Ho C, Zhao J, Malinowski S, et al. Differential expression of sodium channel β subunits in dorsal root ganglion sensory neurons. J Biol Chem. 2012;287(18):15044–15053.
  • Blackburn-Munro G, Fleetwood-Walker SM. The sodium channel β3 subunit in injured human sensory neurons. Neuroreport. 2004;15(1):153–164.
  • Fjell J, Cummins TR, Dib-Hajj SD, et al. Differential role of GDNF and NGF in the maintenance of two TTX-resistant sodium channels in adult DRG neurons. Brain Res Mol Brain Res. 1999;67(2):267–282.
  • Leffler A, Cummins TR, Dib-Hajj SD, et al. GDNF and NGF reverse changes in repriming of TTX-sensitive Na+ currents following axotomy of dorsal root ganglion neurons. J Neurophysiol. 2002;88(2):650–658.
  • Cummins TR, Black JA, Dib-Hajj SD, et al. Glial-derived neurotrophic factor upregulates expression of functional SNS and NaN sodium channels and their currents in axotomized dorsal root ganglion neurons. J Neurosci. 2000;20(23):8754–8761.
  • Dib-Hajj SD, Black JA, Cummins TR, et al. Rescue of α-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo. J Neurophysiol. 1998;79(5):2668–2676.