Sodium channelopathies and pain

Pflugers Archiv European Journal of Physiology

Volumn 460, Issue 2, 2010, Pages 249-263

  Lampert, Angelika ^a   O'Reilly, Andrias O ^b   Reeh, Peter ^a   Leffler, Andreas ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Mutation; Nav1.7; Pain; Patch clamp; Sodium channel; Three dimensional computer modeling

Indexed keywords

CARBAMAZEPINE; GABAPENTIN; LIDOCAINE; MEXILETINE; PHENYLALANINE; POTASSIUM CHANNEL; SODIUM CHANNEL BLOCKING AGENT; SODIUM CHANNEL NAV1.1; SODIUM CHANNEL NAV1.2; SODIUM CHANNEL NAV1.3; SODIUM CHANNEL NAV1.4; SODIUM CHANNEL NAV1.5; SODIUM CHANNEL NAV1.6; SODIUM CHANNEL NAV1.7; SODIUM CHANNEL NAV1.8; SODIUM CHANNEL NAV1.9; SPIDER VENOM; TYROSINE; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; AMINO ACID SUBSTITUTION; ANALGESIA; CENTRAL NERVOUS SYSTEM; CHANNEL GATING; CHRONIC PAIN; CONGENITAL ANALGESIA; DISEASE ASSOCIATION; DISEASE SEVERITY; ERYTHROMELALGIA; FAMILIAL HEMIPLEGIC MIGRAINE; GENE MUTATION; HERITABILITY; HUMAN; INFLAMMATION; NOCICEPTION; NOCICEPTIVE RECEPTOR; NONHUMAN; PAROXYSMAL EXTREME PAIN DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SODIUM CHANNELOPATHY; TISSUE INJURY;

ANIMALS; CHANNELOPATHIES; ERYTHROMELALGIA; HUMANS; MIGRAINE WITH AURA; NERVE TISSUE PROTEINS; NOCICEPTORS; PAIN; PAIN INSENSITIVITY, CONGENITAL; PHENOTYPE; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS;

EID: 77955567717     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-009-0779-3     Document Type: Review

References (122)

1. Ahmad S, Dahllund L, Eriksson AB, Hellgren D, Karlsson U, Lund P-E, Meijer IA, Meury L, Mills T, Moody A, Morinville A, Morten J, O'Donnell D, Raynoschek C, Salter H, Rouleau GA, Krupp JJ (2007) A stop codon mutation in SCN9A causes lack of pain sensation. Hum Mol Genet 16:2114-2121
2. Akopian AN, Sivilotti L, Wood JN (1996) A tetrodotoxinresistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257-262
3. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, Smith A, Kerr BJ, McMahon SB, Boyce S, Hill R, Stanfa LC, Dickenson AH, Wood JN (1999) The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 2:541-548
4. Amir R, Argoff CE, Bennett GJ, Cummins TR, Durieux ME, Gerner P, Gold MS, Porreca F, Strichartz GR (2006) The role of sodium channels in chronic inflammatory and neuropathic pain. J Pain 7: S1-S29
5. Attwell D, Cohen I, Eisner D, Ohba M, Ojeda C (1979) The steady state TTX-sensitive ("window") sodium current in cardiac Purkinje fibres. Pflugers Arch 379:137-142
6. Beckstein O, Sansom MS (2006) A hydrophobic gate in an ion channel: the closed state of the nicotinic acetylcholine receptor. Phys Biol 3:147-159
7. Bjornsson A, Gudmundsson G, Gudfinnsson E, Hrafnsdottir M, Benedikz J, Skuladottir S, Kristjansson K, Frigge ML, Kong A, Stefansson K, Gulcher JR (2003) Localization of a gene for migraine without aura to chromosome 4q 1. Am J Hum Genet 73:986-993 (Pubitemid 37414215)
8. Black JA, Liu S, Tanaka M, Cummins TR, Waxman SG (2004) Changes in the expression of tetrodotoxin-sensitive sodium channels within dorsal root ganglia neurons in inflammatory pain. Pain 108:237-247
9. Black JA, Nikolajsen L, Kroner K, Jensen TS, Waxman SG (2008) Multiple sodium channel isoforms and mitogen-activated protein kinases are present in painful human neuromas. Ann Neurol 64:644-653
10. Blair NT, Bean BP (2002) Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTX-resistant Na+ current, and Ca2+ current in the action potentials of nociceptive sensory neurons. Josci Neur 22:10277-10290
11. Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB (2000) Potent analgesic effects of GDNF in neuropathic pain states. Science 290:124-127
12. Castro MJ, Stam AH, Lemos C, de Vries B, Vanmolkot KR, Barros J, Terwindt GM, Frants RR, Sequeiros J, Ferrari MD, Pereira-Monteiro JM, van den Maagdenberg AM (2009) First mutation in the voltage-gated Nav1.1 subunit gene SCN1A with co-occurring familial hemiplegic migraine and epilepsy. Cephalalgia 29:308-313
13. Catterall WA (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26:13-25
14. 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
15. Cestele S, Yarov-Yarovoy V, Qu Y, Sampieri F, Scheuer T, Catterall WA (2006) Structure and function of the voltage sensor of sodium channels probed by a beta-scorpion toxin. J Biol Chem 281:21332-21344
16. Cestele S, Scalmani P, Rusconi R, Terragni B, Franceschetti S, Mantegazza M (2008) Self-limited hyperexcitability: functional effect of a familial hemiplegic migraine mutation of the Nav1.1 (SCN1A) Na+ channel. J Neurosci 28:7273-7283
17. Chatelier A, Dahllund L, Eriksson A, Krupp J, Chahine M (2008) Biophysical properties of human Nav1.7 splice variants and their regulation by protein kinase A. J Neurophysiol 99:2241-2250
18. 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
19. Choi J-S, Zhang L, Dib-Hajj SD, Han C, Tyrrell L, Lin Z, Wang X, Yang Y, Waxman SG (2009) Mexiletine-responsive erythromelalgia due to a new Nav1.7 mutation showing use-dependent current falloff. Exp Neurol 216:383
20. Choi JS, Dib-Hajj SD, Waxman SG (2006) Inherited erythermalgia: limb pain from an S4 charge-neutral Na channelopathy. Neurology 67:1563-1567
21. Claes LR, Deprez L, Suls A, Baets J, Smets K, Van Dyck T, Deconinck T, Jordanova A, De Jonghe P (2009) The SCN1A variant database: a novel research and diagnostic tool. Hum Mutat 30: E904-E920
22. Colbert CM, Magee JC, Hoffman DA, Johnston D (1997) Slow recovery from inactivation of Na+ channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J Neurosci 17:6512-6521
23. Coward K, Plumpton C, Facer P, Birch R, Carlstedt T, Tate S, Bountra C, Anand P (2000) Immunolocalization of SNS/PN3 and NaN/SNS2 sodium channels in human pain states. Pain 85:41-50
24. Cox JJ, Reimann F, Nicholas AK, Thornton G, Roberts E, Springell K, Karbani G, Jafri H, Mannan J, Raashid Y, Al-Gazali L, Hamamy H, Valente EM, Gorman S, Williams R, McHale DP, Wood JN, Gribble FM, Woods CG (2006) An SCN9A channelopathy causes congenital inability to experience pain. Nature 444:894-898
25. Crill WE (1996) Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58:349-362
26. Cummins TR, Waxman SG (1997) Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury. J Neurosci 17:3503-3514
27. Cummins TR, Dib-Hajj SD, Waxman SG (2004) Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy. J Neurosci 24:8232-8236
28. Cummins TR, Rush AM (2007) Voltage-gated sodium channel blockers for the treatment of neuropathic pain. Expert Rev Neurother 7:1597-1612
29. de Vries B, Frants RR, Ferrari MD, van den Maagdenberg AM (2009) Molecular genetics of migraine. Hum Genet 126:115-132
30. Dib-Hajj S, Black JA, Felts P, Waxman SG (1996) Downregulation of transcripts for Na channel alpha-SNS in spinal sensory neurons following axotomy. Proc Natl Acad Sci USA 93:14950-14954
31. Dib-Hajj SD, Rush AM, Cummins TR, Hisama FM, Novella S, Tyrrell L, Marshall L, Waxman SG (2005) Gain-of-function mutation in Nav1.7 in familial erythromelalgia induces bursting of sensory neurons. Brain 128:1847-1854
32. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG (2007) From genes to pain: Nav1.7 and human pain disorders. Trends Neurosci 30:555-563
33. Dib-Hajj SD, Estacion M, Jarecki B, Tyrrell L, Fischer T, Lawden M, Cummins TR, Waxman SG (2008) Paroxysmal extreme pain disorder M1627K mutation in human Nav1.7 renders DRG neurons hyperexcitable. Molecular Pain 4:37
34. Dib-Hajj SD, Yang Y, Waxman SG (2008) Genetics and molecular pathophysiology of Na (v) 1.7-related pain syndromes. Adv Genet 63:85-110
35. Dib-Hajj SD, Binshtok AM, Cummins TR, Jarvis MF, Samad T, Zimmermann K (2009) Voltage-gated sodium channels in pain states: role in pathophysiology and targets for treatment. Brain Res Rev 60:65-83
36. Dichgans M, Freilinger T, Eckstein G, Babini E, Lorenz-Depiereux B, Biskup S, Ferrari MD, Herzog J, van den Maagdenberg AM, Pusch M, Strom TM (2005) Mutation in the neuronal voltage-gated sodium channel SCN1A in familial hemiplegic migraine. Lancet 366:371-377
37. Drenth JP, Finley WH, Breedveld GJ, Testers L, Michiels JJ, Guillet G, Taieb A, Kirby RL, Heutink P (2001) The primary erythermalgia-susceptibility gene is located on chromosome 2q31-32. Am J Hum Genet 68:1277-1282
38. 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 124:1333-1338
39. Drenth JP, Waxman SG (2007) Mutations in sodium-channel gene SCN9A cause a spectrum of human genetic pain disorders. J Clin Invest 117:3603-3609
40. Edgerton GB, Blumenthal KM, Hanck DA (2008) Evidence for multiple effects of ProTxII on activation gating in NaV1.5. Toxicon 52:489
41. Ekberg J, Jayamanne A, Vaughan CW, Aslan S, Thomas L, Mould J, Drinkwater R, Baker MD, Abrahamsen B, Wood JN, Adams DJ, Christie MJ, Lewis RJ (2006) muO-conotoxin MrVIB selectively blocks Nav1.8 sensory neuron specific sodium channels and chronic pain behavior without motor deficits. Proc Natl Acad Sci USA 103:17030-17035
42. Escayg A, Heils A, MacDonald BT, Haug K, Sander T, Meisler MH (2001) A novel SCN1A mutation associated with generalized epilepsy with febrile seizures plus-and prevalence of variants in patients with epilepsy. Am J Hum Genet 68:866-873
43. Estacion M, Dib-Hajj SD, Benke PJ, te Morsche RHM, Eastman EM, Macala LJ, Drenth JPH, Waxman SG (2008) NaV1.7 gain-offunction 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 28:11079-11088
44. Fertleman CR, Baker MD, Parker KA, Moffatt S, Elmslie FV, Abrahamsen B, Ostman J, Klugbauer N, Wood JN, Gardiner RM, Rees M (2006) SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 52:767-774
45. Fertleman CR, Ferrie CD (2006) What's in a name-familial rectal pain syndrome becomes paroxysmal extreme pain disorder. J Neurol Neurosurg Psychiatry 77:1294-1295
46. Fertleman CR, Ferrie CD, Aicardi J, Bednarek NA, Eeg-Olofsson O, Elmslie FV, Griesemer DA, Goutieres F, Kirkpatrick M, Malmros IN, Pollitzer M, Rossiter M, Roulet-Perez E, Schubert R, Smith VV, Testard H, Wong V, Stephenson JB (2007) Paroxysmal extreme pain disorder (previously familial rectal pain syndrome). Neurology 69:586-595
47. Fischer TZ, Gilmore ES, Estacion M, Eastman E, Taylor S, Melanson M, Dib-Hajj SD, Waxman SG (2009) A novel Nav1.7 mutation producing carbamazepine-responsive erythromelalgia. Ann Neurol 65:733-741
48. Fleidervish IA, Friedman A, Gutnick MJ (1996) Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol 493 (Pt 1):83-97
49. Foulkes T, Wood JN (2008) Pain genes. PLoS Genet 4: e1000086
50. Gargus JJ, Tournay A (2007) Novel mutation confirms seizure locus SCN1A is also familial hemiplegic migraine locus FHM3. Pediatr Neurol 37:407-410
51. Gecz J, Baker E, Donnelly A, Ming JE, McDonald-McGinn DM, Spinner NB, Zackai EH, Sutherland GR, Mulley JC (1999) Fibroblast growth factor homologous factor 2 (FHF2): gene structure, expression and mapping to the Börjeson-Forssman-Lehmann syndrome region in Xq26 delineated by a duplication breakpoint in a BFLS-like patient. Hum Gen 104:56-63
52. Gold MS, Reichling DB, Shuster MJ, Levine JD (1996) Hyperalgesic agents increase a tetrodotoxin-resistant Na+ current in nociceptors. Proc Natl Acad Sci USA 93:1108-1112
53. Gold MS, Levine JD, Correa AM (1998) Modulation of TTX-R INa by PKC and PKA and their role in PGE2-induced sensitization of rat sensory neurons in vitro. J Neurosci 18:10345-10355
54. Gold MS, Weinreich D, Kim CS, Wang R, Treanor J, Porreca F, Lai J (2003) Redistribution of Na (V) 1.8 in uninjured axons enables neuropathic pain. J Neurosci 23:158-166
55. Goldberg YP, MacFarlane J, MacDonald ML, Thompson J, Dube MP, Mattice M, Fraser R, Young C, Hossain S, Pape T, Payne B, Radomski C, Donaldson G, Ives E, Cox J, Younghusband HB, Green R, Duff A, Boltshauser E, Grinspan GA, Dimon JH, Sibley BG, Andria G, Toscano E, Kerdraon J, Bowsher D, Pimstone SN, Samuels ME, Sherrington R, Hayden MR (2007) Loss-of-function mutations in the Nav1.7 gene underlie congenital indifference to pain in multiple human populations. Clin Genet 71:311-319
56. Goldfarb M (2005) Fibroblast growth factor homologous factors: evolution, structure, and function. Cytokine Growth Factor Rev 16:215-220
57. Han C, Rush AM, Dib-Hajj SD, Li S, Xu Z, Wang Y, Tyrrell L, Wang X, Yang Y, Waxman SG (2006) Sporadic onset of erythermalgia: a gain-of-function mutation in Nav1. Ann Neurol 59:553-558
58. Han C, Dib-Hajj SD, Lin Z, Li Y, Eastman EM, Tyrrell L, Cao X, Yang Y, Waxman SG (2009) Early-and late-onset inherited erythromelalgia: genotype-phenotype correlation. Brain 132 (Pt 7):1711-1722
59. Harty TP, Dib-Hajj SD, Tyrrell L, Blackman R, Hisama FM, Rose JB, Waxman SG (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 26:12566-12575
60. Hillsley K, Lin JH, Stanisz A, Grundy D, Aerssens J, Peeters PJ, Moechars D, Coulie B, Stead RH (2006) Dissecting the role of sodium currents in visceral sensory neurons in a model of chronic hyperexcitability using Nav1.8 and Nav1.9 null mice. J Physiol 576:257-267
61. Iqbal J, Bhat MI, Charoo BA, Syed WA, Sheikh MA, Bhat IN (2009) Experience with oral mexiletine in primary erythromelalgia in children. Ann Saudi Med 29:316-318
62. 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 586:4137-4153. doi:10.1113/jphysiol.2008.154906
63. Jarecki BW, Sheets PL, Xiao Y, Jackson JO 2nd, Cummins TR (2009) Alternative splicing of Na (V) 1.7 exon 5 increases the impact of the painful PEPD mutant channel I1461T. Channels (Austin) 3:259-267
64. Jarvis MF, Honore P, Shieh CC, Chapman M, Joshi S, Zhang XF, Kort M, Carroll W, Marron B, Atkinson R, Thomas J, Liu D, Krambis M, Liu Y, McGaraughty S, Chu K, Roeloffs R, Zhong C, Mikusa JP, Hernandez G, Gauvin D, Wade C, Zhu C, Pai M, Scanio M, Shi L, Drizin I, Gregg R, Matulenko M, Hakeem A, Gross M, Johnson M, Marsh K, Wagoner PK, Sullivan JP, Faltynek CR, Krafte DS (2007) A-803467, a potent and selective Nav1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat. Proc Natl Acad Sci USA 104:8520-8525
65. John VH, Main MJ, Powell AJ, Gladwell ZM, Hick C, Sidhu HS, Clare JJ, Tate S, Trezise DJ (2004) 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 46:425-438
66. Julius D, Basbaum AI (2001) Molecular mechanisms of nociception. Nature 413:203-210
67. Jung HY, Mickus T, Spruston N (1997) Prolonged sodium channel inactivation contributes to dendritic action potential attenuation in hippocampal pyramidal neurons. J Neurosci 17:6639-6646
68. Kahlig KM, Rhodes TH, Pusch M, Freilinger T, Pereira-Monteiro JM, Ferrari MD, van den Maagdenberg AM, Dichgans M, George AL Jr (2008) Divergent sodium channel defects in familial hemiplegic migraine. Proc Natl Acad Sci USA 105:9799-9804
69. Kerr BJ, Souslova V, McMahon SB, Wood JN (2001) A role for the TTX-resistant sodium channel Nav 1.8 in NGF-induced hyperalgesia, but not neuropathic pain. Neuro Report 12:3077-3080
70. Kiernan MC, Krishnan AV, Lin CS, Burke D, Berkovic SF (2005) Mutation in the Na+ channel subunit SCN1B produces paradoxical changes in peripheral nerve excitability. Brain 128:1841-1846
71. Koltzenburg M, Scadding J (2001) Neuropathic pain. Curr Opin Neurol 14:641-647
72. Kort ME, Drizin I, Gregg RJ, Scanio MJ, Shi L, Gross MF, Atkinson RN, Johnson MS, Pacofsky GJ, Thomas JB, Carroll WA, Krambis MJ, Liu D, Shieh CC, Zhang X, Hernandez G, Mikusa JP, Zhong C, Joshi S, Honore P, Roeloffs R, Marsh KC, Murray BP, Liu J, Werness S, Faltynek CR, Krafte DS, Jarvis MF, Chapman ML, Marron BE (2008) Discovery and biological evaluation of 5-aryl-2-furfuramides, potent and selective blockers of the Nav1.8 sodium channel with efficacy in models of neuropathic and inflammatory pain. J Med Chem 51:407-416
73. Kuhnert SM, Phillips WJ, Davis MD (1999) Lidocaine and mexiletine therapy for erythromelalgia. Arch Dermatol 135:1447-1449
74. Kuo A, Gulbis JM, Antcliff JF, Rahman T, Lowe ED, Zimmer J, Cuthbertson J, Ashcroft FM, Ezaki T, Doyle DA (2003) Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 300:1922-1926
75. Lai J, Gold MS, Kim CS, Bian D, Ossipov MH, Hunter JC, Porreca F (2002) Inhibition of neuropathic pain by decreased expression of the tetrodotoxin-resistant sodium channel, NaV1.8. Pain 95:143-152
76. Lai J, Hunter JC, Porreca F (2003) The role of voltage-gated sodium channels in neuropathic pain. Curr Opin Neurobiol 13:291-297
77. Laird JM, Souslova V, Wood JN, Cervero F (2002) Deficits in visceral pain and referred hyperalgesia in Nav1.8 (SNS/PN3) - null mice. J Neurosci 22:8352-8356
78. Lampert A, Dib-Hajj S, Tyrrell L, Waxman S (2006) Size matters: erythromelalgia mutation S241T in Nav1.7 alters channel gating. J Biol Chem 281:36029-36035
79. 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 283:24118-24127
80. Lampert A, Dib-Hajj SD, Eastman EM, Tyrrell L, Lin Z, Yang Y, Waxman SG (2009) Erythromelalgia mutation L823R shifts activation and inactivation of threshold sodium channel Nav1.7 to hyperpolarized potentials. Biochem Biophys Res Commun 390:319-324
81. 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
82. Leffler A, Reiprich A, Mohapatra DP, Nau C (2007) Usedependent block by lidocaine but not amitriptyline is more pronounced in tetrodotoxin (TTX)-resistant Nav1.8 than in TTXsensitive Na+ channels. J Pharmacol Exp Ther 320:354-364
83. Long SB, Campbell EB, Mackinnon R (2005) Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309:903-908
84. Meisler MH, Kearney J, Ottman R, Escayg A (2001) Identification of epilepsy genes in human and mouse. Annu Rev Genet 35:567-588
85. 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. Arch Neurol 62:1587-1590
86. Mickus T, Jung H, Spruston N (1999) Properties of slow, cumulative sodium channel inactivation in rat hippocampal CA1 pyramidal neurons. Biophys J 76:846-860
87. Middleton RE, Warren VA, Kraus RL, Hwang JC, Liu CJ, Dai G, Brochu RM, Kohler MG, Gao Y-D, Garsky VM, Bogusky MJ, Mehl JT, Cohen CJ, Smith MM (2002) Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry 41:14734-14747
88. Miyazawa A, Fujiyoshi Y, Unwin N (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 423:949-955
89. Nassar MA, Stirling LC, Forlani G, Baker MD, Matthews EA, Dickenson AH, Wood JN (2004) Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci USA 101:12706-12711
90. Nathan A, Rose JB, Guite JW, Hehir D, Milovcich K (2005) Primary erythromelalgia in a child responding to intravenous lidocaine and oral mexiletine treatment. Pediatrics 115: e504-e507
91. Natkunarajah J, Atherton D, Elmslie F, Mansour S, Mortimer P (2009) Treatment with carbamazepine and gabapentin of a patient with primary erythermalgia (erythromelalgia) identified to have a mutation in the SCN9A gene, encoding a voltage-gated sodium channel. Clin Exp Dermatol 34: e640-e642
92. Nilsen KB, Nicholas AK, Woods CG, Mellgren SI, Nebuchennykh M, Aasly J (2009) Two novel SCN9A mutations causing insensitivity to pain. Pain 143:155-158
93. O'Reilly AO, Khambay BP, Williamson MS, Field LM, Wallace BA, Davies TG (2006) Modelling insecticide-binding sites in the voltage-gated sodium channel. Biochem J 396:255-263
94. Ong BH, Tomaselli GF, Balser JR (2000) A structural rearrangement in the sodium channel pore linked to slow inactivation and use dependence. J Gen Physiol 116:653-662
95. Priest BT, Blumenthal KM, Smith JJ, Warren VA, Smith MM (2007) ProTx-I and ProTx-II: gating modifiers of voltage-gated sodium channels. Toxicon 49:194
96. Raymond CK, Castle J, Garrett-Engele P, Armour CD, Kan Z, Tsinoremas N, Johnson JM (2004) Expression of alternatively spliced sodium channel alpha-subnit genes: unique splicing patterns are observed in dorsal root ganglia. J Biol Chem 279:46234-46241. doi:10.1074/jbc. M406387200
97. Renganathan M, Cummins TR, Waxman SG (2001) Contribution of Na (v) 1.8 sodium channels to action potential electrogenesis in DRG neurons. J Neurophysiol 86:629-640
98. Roza C, Laird JM, Souslova V, Wood JN, Cervero F (2003) The tetrodotoxin-resistant Na+ channel Nav1.8 is essential for the expression of spontaneous activity in damaged sensory axons of mice. J Physiol 550:921-926
99. Rush AM, Elliott JR (1997) Phenytoin and carbamazepine: differential inhibition of sodium currents in small cells from adult rat dorsal root ganglia. Neurosci Lett 226:95-98
100. Rush AM, Dib-Hajj SD, Liu S, Cummins TR, Black JA, Waxman SG (2006) A single sodium channel mutation produces hyper-or hypoexcitability in different types of neurons. Proc Natl Acad Sci USA 103:8245-8250
101. Rush AM, Cummins TR, Waxman SG (2007) Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J Physiol 579:1-14
102. Sangameswaran L, Delgado SG, Fish LM, Koch BD, Jakeman LB, Stewart GR, Sze P, Hunter JC, Eglen RM, Herman RC (1996) Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J Biol Chem 271:5953-5956
103. Scheib H, McLay I, Guex N, Clare JJ, Blaney FE, Dale TJ, Tate SN, Robertson GM (2006) Modeling the pore structure of voltage-gated sodium channels in closed, open, and fastinactivated conformation reveals details of site 1 toxin and local anesthetic binding. J Mol Model 12:813-822
104. Schmalhofer W, Calhoun J, Burrows R, Bailey T, Kohler MG, Weinglass AB, Kaczorowski GJ, Garcia ML, Koltzenburg M, Priest BT (2008) ProTx-II, a selective inhibitor of NaV1.7 sodium channels, blocks action potential propagation in nociceptors. Mol Pharmacol 74:1476-1484. doi:10.1124/mol.108.047670
105. Scholz J, Woolf CJ (2002) Can we conquer pain? Nat Neurosci 5 (Suppl): 1062-1067
106. 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 581:1019-1031
107. Sheets PL, Heers C, Stoehr T, Cummins TR (2008) Differential block of sensory neuronal voltage-gated sodium channels by lacosamide [(2R)-2-(acetylamino)-N-benzyl-3-methoxypropanamide], lidocaine, and carbamazepine. J Pharmacol Exp Ther 326:89-99
108. Singh NA, Pappas C, Dahle EJ, Claes LRF, Pruess TH, De Jonghe P, Thompson J, Dixon M, Gurnett C, Peiffer A, White HS, Filloux F, Leppert MF (2009) A role of SCN9A in human epilepsies. As a cause of febrile seizures and as a potential modifier of Dravet syndrome. PLoS Genet 5: e1000649
109. Smith JJ, Cummins TR, Alphy S, Blumenthal KM (2007) Molecular interactions of the gating modifier toxin ProTx-II with Nav1.5: implied existence of a novel toxin binding site coupled to activation. J Biol Chem 282:12687-12697
110. Song JH, Nagata K, Huang CS, Yeh JZ, Narahashi T (1996) Differential block of two types of sodium channels by anticonvulsants. NeuroReport 7:3031-3036
111. Takahashi K, Saitoh M, Hoshino H, Mimaki M, Yokoyama Y, Takamizawa M, Mizuguchi M, Lin ZM, Yang Y, Igarashi T (2007) A case of primary erythermalgia. Wintry hypothermia and encephalopathy. Neuropediatrics 38:157
112. Tanaka M, Cummins TR, Ishikawa K, Dib-Hajj SD, Black JA, Waxman SG (1998) SNS Na+ channel expression increases in dorsal root ganglion neurons in the carrageenan inflammatory pain model. NeuroReport 9:967-972
113. Toib A, Lyakhov V, Marom S (1998) Interaction between duration of activity and time course of recovery from slow inactivation in mammalian brain Na+ channels. J Neurosci 18:1893-1903
114. Unwin N (1995) Acetylcholine receptor channel imaged in the open state. Nature 373:37-43
115. Vahedi K, Depienne C, Le Fort D, Riant F, Chaine P, Trouillard O, Gaudric A, Morris MA, Leguern E, Tournier-Lasserve E, Bousser MG (2009) Elicited repetitive daily blindness: a new phenotype associated with hemiplegic migraine and SCN1A mutations. Neurology 72:1178-1183
116. Vanmolkot KR, Babini E, de Vries B, Stam AH, Freilinger T, Terwindt GM, Norris L, Haan J, Frants RR, Ramadan NM, Ferrari MD, Pusch M, van den Maagdenberg AM, Dichgans M (2007) The novel p. L1649Q mutation in the SCN1A epilepsy gene is associated with familial hemiplegic migraine: genetic and functional studies. Mutation in brief # 957. Online. Hum Mutat 28:522
117. Wang CG, Gilles N, Hamon A, Le Gall F, Stankiewicz M, Pelhate M, Xiong YM, Wang DC, Chi CW (2003) Exploration of the functional site of a scorpion alpha-like toxin by sitedirected mutagenesis. Biochemistry 42:4699-4708
118. Wang S-Y, Wang GK (2003) Voltage-gated sodium channels as primary targets of diverse lipid-soluble neurotoxins. Cell Signal 15:151
119. Woolf CJ, Ma Q (2007) Nociceptors-noxious stimulus detectors. Neuron 55:353-364
120. Xiao Y, Bingham J-P, Zhu W, Moczydlowski E, Liang S, Cummins TR (2008) Tarantula huwentoxin-IV inhibits neuronal sodium channels by binding to receptor site 4 and trapping the domain II voltage sensor in the closed configuration. J Biol Chem 283:27300-27313
121. Yang Y, Wang Y, Li S, Xu Z, Li H, Ma L, Fan J, Bu D, Liu B, Fan Z, Wu G, Jin J, Ding B, Zhu X, Shen Y (2004) Mutations in SCN9A, encoding a sodium channel alpha subunit, in patients with primary erythermalgia. J Med Genet 41:171-174
122. Zimmermann K, Leffler A, Babes A, Cendan CM, Carr RW, Kobayashi J, Nau C, Wood JN, Reeh PW (2007) Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 447:855-858 (Pubitemid 46920141)