Altered sodium channel gating as molecular basis for pain: Contribution of activation, inactivation, and resurgent currents

Handbook of Experimental Pharmacology

Volumn 221, Issue , 2014, Pages 91-110

  Lampert, Angelika ^a   Eberhardt, Mirjam ^b   Waxman, Stephen G ^c,d  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VA Neuroscience Research Center ^*  (United States)

Author keywords

Hyperexcitability; Nav1.7; Pain; Resurgent current

Indexed keywords

CARBAMAZEPINE; OXALIPLATIN; SODIUM CHANNEL NAV1.1; SODIUM CHANNEL NAV1.2; SODIUM CHANNEL NAV1.4; SODIUM CHANNEL NAV1.6; SODIUM CHANNEL NAV1.7; VOLTAGE GATED SODIUM CHANNEL BETA 4 SUBUNIT; SODIUM; VOLTAGE GATED SODIUM CHANNEL;

AMINO ACID SUBSTITUTION; ANALGESIA (SENSORY DYSFUNCTION); ARTICLE; CHANNEL GATING; FAST INACTIVATION; GAIN OF FUNCTION MUTATION; GENE DELETION; HUMAN; INHERITED ERYTHROMELALGIA; MEMBRANE BIOLOGY; MEMBRANE POLARIZATION AND DEPOLARIZATION; MEMBRANE POTENTIAL; MOLECULAR PATHOLOGY; MUTATIONAL ANALYSIS; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PAIN RECEPTOR; PAROXYSMAL EXTREME PAIN DISORDER; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PSYCHOGENIC PAIN; RESURGENT CURRENT; S4 S5 LINKER; SCN9A GENE; SLOW INACTIVATION; SMALL FIBER NEUROPATHY; SODIUM CHANNELOPATHY; VOLTAGE SENSING DOMAIN; ANIMAL; CHEMISTRY; GENETICS; KINETICS; METABOLISM; PAIN THRESHOLD; PATHOPHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; SYNDROME;

ANIMALS; HUMANS; ION CHANNEL GATING; KINETICS; MEMBRANE POTENTIALS; NOCICEPTORS; PAIN; PAIN THRESHOLD; SIGNAL TRANSDUCTION; SODIUM; SYNDROME; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84903906262     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/978-3-642-41588-3_5     Document Type: Article

References (75)

1. Ahn HS, Dib-Hajj SD, Cox JJ, Tyrrell L, Elmslie FV, Clarke AA et al (2010) A new Nav1.7 sodium channel mutation I234T in a child with severe pain. Eur J Pain 14(9):944-950
2. Catterall WA (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26(1):13-25
3. Chanda B, Bezanilla F (2002) Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J Gen Physiol 120(5):629-645
4. Chen Y, Yu FH, Surmeier DJ, Scheuer T, Catterall WA (2006) Neuromodulation of Na+ channel slow inactivation via cAMP-dependent protein kinase and protein kinase C. Neuron 49(3):409-420
5. Cheng X, Dib-Hajj S, Tyrrell L, Waxman S (2008) Mutation I136V alters electrophysiological properties of the NaV1.7 channel in a family with onset of erythromelalgia in the second decade. Mol Pain 4(1):1
6. Cheng X, Dib-Hajj SD, Tyrrell L, Wright DA, Fischer TZ, Waxman SG (2010) Mutations at opposite ends of the DIII/S4-S5 linker of sodium channel NaV1.7 produce distinct pain disorders. Mol Pain 6:24
7. Cheng X, Dib-Hajj SD, Tyrrell L, Te Morsche RH, Drenth JP, Waxman SG (2011) Deletion mutation of sodium channel Na(V)1.7 in inherited erythromelalgia: enhanced slow inactivation modulates dorsal root ganglion neuron hyperexcitability. Brain 134(Pt 7):1972-1986
8. Choi JS, Dib-Hajj SD, Waxman SG (2006) Inherited erythermalgia: limb pain from an S4 charge- neutral Na channelopathy. Neurology 67(9):1563-1567
9. Choi J-S, Zhang L, Dib-Hajj SD, Han C, Tyrrell L, Lin Z et al (2009) Mexiletine-responsive erythromelalgia due to a new Nav1.7 mutation showing use-dependent current fall-off. Exp Neurol 216(2):383
10. Choi J-S, Cheng X, Foster E, Leffler A, Tyrrell L, te Morsche RHM et al (2010) Alternative splicing may contribute to time-dependent manifestation of inherited erythromelalgia. Brain 133(6):1823-1835
11. Choi JS, Boralevi F, Brissaud O, Sanchez-Martin J, Te Morsche RH, Dib-Hajj SD et al (2011) Paroxysmal extreme pain disorder: a molecular lesion of peripheral neurons. Nat Rev Neurol 7 (1):51-55
12. Clayton GM, Altieri S, Heginbotham L, Unger VM, Morais-Cabral JH (2008) Structure of the transmembrane regions of a bacterial cyclic nucleotide-regulated channel. Proc Natl Acad Sci 105(5):1511-1515
13. Cruz JS, Silva DF, Ribeiro LA, Araujo IG, Magalhaes N, Medeiros A et al (2011) Resurgent Na+ current: a new avenue to neuronal excitability control. Life Sci 89(15-16):564-569
14. Cummins TR, Dib-Hajj SD, Waxman SG (2004) Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy. J Neurosci 24(38):8232-8236
15. Cummins TR, Dib-Hajj SD, Herzog RI, Waxman SG (2005) Nav1.6 channels generate resurgent sodium currents in spinal sensory neurons. FEBS Lett 579(10):2166
16. Dib-Hajj SD, Rush AM, Cummins TR, Hisama FM, Novella S, Tyrrell L et al (2005) Gain-of- function mutation in Nav1.7 in familial erythromelalgia induces bursting of sensory neurons. Brain 128(Pt 8):1847-1854
17. Dib-Hajj S, Estacion M, Jarecki B, Tyrrell L, Fischer T, Lawden M et al (2008) Paroxysmal extreme pain disorder M1627K mutation in human Nav1.7 renders DRG neurons hyperexcit- able. Mol Pain 4(1):37
18. Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL et al (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280 (5360):69-77
19. Drenth JP, te Morsche RH, Guillet G, Taieb A, Kirby RL, Jansen JB (2005) SCN9A mutations define primary erythermalgia as a neuropathic disorder of voltage gated sodium channels. J Invest Dermatol 124(6):1333-1338
20. Estacion M, Dib-Hajj SD, Benke PJ, te Morsche RHM, Eastman EM, Macala LJ et al (2008) NaV1.7 gain-of-function mutations as a continuum: A1632E displays physiological changes associated with erythromelalgia and paroxysmal extreme pain disorder mutations and produces symptoms of both disorders. J Neurosci 28(43):11079-11088
21. Estacion M, Choi JS, Eastman EM, Lin Z, Li Y, Tyrrell L et al (2010) Can robots patch-clamp as well as humans? Characterization of a novel sodium channel mutation. J Physiol 588(Pt 11): 1915-1927
22. Estacion M, Han C, Choi JS, Hoeijmakers JG, Lauria G, Drenth JP et al (2011) Intra- and interfamily phenotypic diversity in pain syndromes associated with a gain-of-function variant of NaV1.7. Mol Pain 7:92
23. Estacion M, Yang Y, Dib-Hajj SD, Tyrrell L, Lin Z, Yang Y et al (2013) A new Nav1.7 mutation in an erythromelalgia patient. Biochem Biophys Res Commun 432(1):99-104
24. Faber CG, Hoeijmakers JG, Ahn HS, Cheng X, Han C, Choi JS et al (2012) Gain of function NaV1.7 mutations in idiopathic small fiber neuropathy. Ann Neurol 71(1):26-39
25. Fang X, Djouhri L, McMullan S, Berry C, Waxman SG, Okuse K et al (2006) Intense isolectin-B4 binding in rat dorsal root ganglion neurons distinguishes c-fiber nociceptors with broad action potentials and high Nav1.9 expression. J Neurosci 26(27):7281-7292
26. Felts PA, Yokoyama S, Dib-Hajj S, Black JA, Waxman SG (1997) Sodium channel alpha-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Brain Res Mol Brain Res 45(1):71-82
27. Fertleman CR, Baker MD, Parker KA, Moffatt S, Elmslie FV, Abrahamsen B et al (2006) SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 52:767-774
28. Fertleman CR, Ferrie CD, Aicardi J, Bednarek NA, Eeg-Olofsson O, Elmslie FV et al (2007) Paroxysmal extreme pain disorder (previously familial rectal pain syndrome). Neurology 69 (6):586-595
29. Fischer TZ, Gilmore ES, Estacion M, Eastman E, Taylor S, Melanson M et al (2009) A novel Nav1.7 mutation producing carbamazepine-responsive erythromelalgia. Ann Neurol 65(6): 733-741
30. Grieco TM, Raman IM (2004) Production of resurgent current in NaV1.6-null Purkinje neurons by slowing sodium channel inactivation with β-pompilidotoxin. J Neurosci 24(1):35-42
31. Grieco TM, Malhotra JD, Chen C, Isom LL, Raman IM (2005) Open-channel block by the cytoplasmic tail of sodium channel [β]4 as a mechanism for resurgent sodium current. Neuron 45(2):233-244
32. Han C, Rush AM, Dib-Hajj SD, Li S, Xu Z, Wang Y et al (2006) Sporadic onset of erythermalgia: a gain-of-function mutation in Nav1.7. Ann Neurol 59(3):553-558
33. Han C, Dib-Hajj SD, Lin Z, Li Y, Eastman EM, Tyrrell L et al (2009) Early- and late-onset inherited erythromelalgia: genotype-phenotype correlation. Brain 132:awp078
34. Han C, Hoeijmakers JGJ, Ahn H-S, Zhao P, Shah P, Lauria G et al (2012) Nav1.7-related small fiber neuropathy. Neurology 78:1635-43
35. Harper AA, Lawson SN (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol 359:31-46
36. Harty TP, Dib-Hajj SD, Tyrrell L, Blackman R, Hisama FM, Rose JB et al (2006) Na(V)1.7 mutant A863P in erythromelalgia: effects of altered activation and steady-state inactivation on excitability of nociceptive dorsal root ganglion neurons. J Neurosci 26(48):12566-12575
37. Ho C, O‘Leary ME (2011) Single-cell analysis of sodium channel expression in dorsal root ganglion neurons. Mol Cell Neurosci 46(1):159-166
38. Hoeijmakers JG, Han C, Merkies IS, Macala LJ, Lauria G, Gerrits MM et al (2012) Small nerve fibres, small hands and small feet: a new syndrome of pain, dysautonomia and acromesomelia in a kindred with a novel NaV1.7 mutation. Brain 135(Pt 2):345-358
39. Huth T, Rittger A, Saftig P, Alzheimer C (2011) Beta-site APP-cleaving enzyme 1 (BACE1) cleaves cerebellar Na+ channel beta4-subunit and promotes Purkinje cell firing by slowing the decay of resurgent Na+ current. Pflugers Arch 461:355-371
40. Jarecki BW, Sheets PL, Jackson IIJO, Cummins TR (2008) Paroxysmal extreme pain disorder mutations within the D3/S4-S5 linker of Nav1.7 cause moderate destabilization of fast- inactivation. J Physiol 586:4137-53
41. Jarecki BW, Piekarz AD, Jackson JO 2nd, Cummins TR (2010) Human voltage-gated sodium channel mutations that cause inherited neuronal and muscle channelopathies increase resurgent sodium currents. J Clin Invest 120(1):369-378
42. Klinger AB, Eberhardt M, Link AS, Namer B, Schuy ET, Sittl R et al (2012) Sea-anemone toxin ATX-II elicits A-fiber-dependent pain and enhances resurgent and persistent sodium currents in large sensory neurons. Mol Pain 8(1):69
43. Kremeyer B, Lopera F, Cox JJ, Momin A, Rugiero F, Marsh S et al (2010) A gain-of-function mutation in TRPA1 causes familial episodic pain syndrome. Neuron 66(5):671-680
44. Kuo A, Gulbis JM, Antcliff JF, Rahman T, Lowe ED, Zimmer J et al (2003) Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 300(5627):1922-1926
45. Lampert A, Dib-Hajj SD, Tyrrell L, Waxman SG (2006) Size matters: erythromelalgia mutation S241T in Nav1.7 alters channel gating. J Biol Chem 281(47):36029-36035
46. Lampert A, O‘Reilly AO, Dib-Hajj SD, Tyrrell L, Wallace BA, Waxman SG (2008) A pore- blocking hydrophobic motif at the cytoplasmic aperture of the closed-state Nav1.7 channel is disrupted by the erythromelalgia-associated F1449V mutation. J Biol Chem 283(35): 24118-24127
47. Lampert A, Dib-Hajj S, Eastman E, Tyrrell L, Lin Z, Yang Y et al (2009) Erythromelalgia mutation L823R shifts activation and inactivation of threshold sodium channel Nav1.7 to hyperpolarized potentials. Biochem Biophys Res Commun 390(2):319-324
48. Lee MJ, Yu HS, Hsieh ST, Stephenson DA, Lu CJ, Yang CC (2007) Characterization of a familial case with primary erythromelalgia from Taiwan. J Neurol 254:210-214
49. Lewis AH, Raman IM (2011) Cross-species conservation of open-channel block by Na channel β4 peptides reveals structural features required for resurgent Na current. J Neurosci 31(32): 11527-11536
50. Michiels JJ, te Morsche RH, Jansen JB, Drenth JP (2005) Autosomal dominant erythermalgia associated with a novel mutation in the voltage-gated sodium channel alpha subunit Nav1.7. Arch Neurol 62(10):1587-1590
51. Nau C, Wang GK (2004) Interactions of local anesthetics with voltage-gated Na + channels. J Membr Biol 201(1):1-8
52. Oliveira JS, Redaelli E, Zaharenko AJ, Cassulini RR, Konno K, Pimenta DC et al (2004) Binding specificity of sea anemone toxins to Nav 1.1-1.6 sodium channels: unexpected contributions from differences in the IV/S3-S4 outer loop. J Biol Chem 279(32):33323-33335
53. O‘Reilly JP, Wang S-Y, Wang GK (2001) Residue-specific effects on slow inactivation at V787 in D2-S6 of Nav1.4 sodium channels. J Biophys 81(4):2100-2111
54. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475(7356):353-358
55. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17(12):4517-4526
56. Raman IM, Bean BP (2001) Inactivation and recovery of sodium currents in cerebellar purkinje neurons: evidence for two mechanisms. Biophys J 80(2):729-737
57. Raman IM, Sprunger LK, Meisler MH, Bean BP (1997) Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19(4):881-891
58. Rathmayer W (1979) Anemone toxin discriminates between ionic channels for receptor potential and for action potential production in a sensory neuron. Neurosci Lett 13(3):313-318
59. Schiavon E, Sacco T, Cassulini RR, Gurrola G, Tempia F, Possani LD et al (2006) Resurgent current and voltage sensor trapping enhanced activation by a β-scorpion toxin solely in Nav1.6 channel: significance in mice purkinje neurons. J Biol Chem 281(29):20326-20337
60. Schmalhofer W, Calhoun J, Burrows R, Bailey T, Kohler MG, Weinglass AB, et al. (2008). ProTx- II, a selective inhibitor of NaV1.7 sodium channels, blocks action potential propagation in nociceptors. Mol Pharmacol: mol. 108. 047670
61. Sheets MF, Hanck DA (2003) Molecular action of lidocaine on the voltage sensors of sodium channels. J Gen Physiol 121(2):163-175
62. Sheets PL, Jackson JO 2nd, Waxman SG, Dib-Hajj SD, Cummins TR (2007) A Nav1.7 channel mutation associated with hereditary erythromelalgia contributes to neuronal hyperexcitability and displays reduced lidocaine sensitivity. J Physiol 581(Pt 3):1019-1031
63. Sittl R, Lampert A, Huth T, Schuy ET, Link AS, Fleckenstein J et al (2012) Anticancer drug oxaliplatin induces acute cooling-aggravated neuropathy via sodium channel subtype NaV1.6- resurgent and persistent current. Proc Natl Acad Sci 109(17):6704-6709
64. Skeik N, Rooke TW, Davis MD, Davis DM, Kalsi H, Kurth I et al (2012) Severe case and literature review of primary erythromelalgia: novel SCN9A gene mutation. Vascular Med 17(1):44-49
65. Smith MR, Smith RD, Plummer NW, Meisler MH, Goldin AL (1998) Functional analysis of the mouse Scn8a sodium channel. J Neurosci 18(16):6093
66. Takahashi K, Saitoh M, Hoshino H, Mimaki M, Yokoyama Y, Takamizawa M et al (2007) A case of primary erythermalgia, wintry hypothermia and encephalopathy. Neuropediatrics 38(03): 157
67. Theile JW, Cummins TR (2011) Inhibition of Nav{β}4 peptide-mediated resurgent sodium currents in Nav1.7 channels by carbamazepine, riluzole and anandamide. Mol Pharmacol 80 (4):724-34
68. Theile JW, Jarecki BW, Piekarz AD, Cummins TR (2011) Nav1.7 mutations associated with paroxysmal extreme pain disorder, but not erythromelalgia, enhance Navβ4 peptide-mediated resurgent sodium currents. J Physiol 589(Pt 3):597-608
69. Wang GK, Strichartz GR (2012) State-dependent inhibition of sodium channels by local anesthetics: a 40-year evolution. Biochem (Mosc) Suppl Ser A Membr Cell Biol 6(2):120-127
70. Wang GK, Edrich T, Wang SY (2006) Time-dependent block and resurgent tail currents induced by mouse β4(154-167) peptide in cardiac Na+ channels. J Gen Physiol 127(3):277-289
71. Wu MT, Huang PY, Yen CT, Chen CC, Lee MJ (2013) A novel SCN9A mutation responsible for primary erythromelalgia and is resistant to the treatment of sodium channel blockers. PLoS One 8(1):e55212
72. Yang Y, Wang Y, Li S, Xu Z, Li H, Ma L et al (2004) Mutations in SCN9A, encoding a sodium channel alpha subunit, in patients with primary erythermalgia. J Med Genet 41(3):171-174
73. Yang Y, Dib-Hajj SD, Zhang J, Zhang Y, Tyrrell L, Estacion M et al (2012) Structural modeling and mutant cycle analysis predict pharmacoresponsiveness of a Na(v)1.7 mutant channel. Nat Commun 3:1186
74. Yang Y, Estacion M, Dib-Hajj SD, Waxman SG (2013) Molecular architecture of a sodium channel S6 helix: radial tuning of the voltage-gated sodium channel 1.7 activation gate. J Biol Chem 288(19):13741-13747
75. Yu FH, Westenbroek RE, Silos-Santiago I, McCormick KA, Lawson D, Ge P et al (2003) Sodium channel β4, a new disulfide-linked auxiliary subunit with similarity to β2. J Neurosci 23 (20):7577