Deletion mutation of sodium channel NaV1.7 in inherited erythromelalgia: Enhanced slow inactivation modulates dorsal root ganglion neuron hyperexcitability

Brain

Volumn 134, Issue 7, 2011, Pages 1972-1986

  Cheng, Xiaoyang ^a,b   Dib Hajj, Sulayman D ^a,b   Tyrrell, Lynda ^a,b   Te Morsche, Rene H ^c   Drenth, Joost P H ^c   Waxman, Stephen G ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

channelopathy; erythromelalgia; pain; SCN9A; voltage gated sodium channel

Indexed keywords

SODIUM CHANNEL NAV1.7;

ADULT; ARTICLE; CASE REPORT; ERYTHROMELALGIA; EXON; FEMALE; GENE DELETION; GENE EXPRESSION; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; MUTATIONAL ANALYSIS; NERVE CELL HYPEREXCITABILITY; NERVE EXCITABILITY; NERVE POTENTIAL; PHENOTYPE; PRIORITY JOURNAL; SPINAL GANGLION; STEADY STATE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICAL PHENOMENA; BIOPHYSICS; CELLS, CULTURED; ELECTRIC STIMULATION; ERYTHROMELALGIA; EXONS; FEMALE; GANGLIA, SPINAL; HUMANS; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; SEQUENCE DELETION; SODIUM CHANNELS; TRANSFECTION; YOUNG ADULT;

EID: 79959728800     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr143     Document Type: Article

References (34)

1. Beyreuther B, Callizot N, Stöhr T. Antinociceptive efficacy of lacosamide in a rat model for painful diabetic neuropathy. Eur J Pharmacol 2006; 539: 64-70. (Pubitemid 43783512)
2. Beyreuther BK, Freitag J, Heers C, Krebsfanger N, Scharfenecker U, Stohr T. Lacosamide: a review of preclinical properties. CNS Drug Rev 2007; 13: 21-42. (Pubitemid 46697839)
3. Catterall WA, Goldin AL, Waxman SG. International Union of PharmacologyXLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 2005; 57: 397-409. (Pubitemid 43036431)
4. Chen Y, Yu FH, Surmeier DJ, Scheuer T, Catterall WA. Neuromodulation of Na+ channel slow inactivation via cAMP-dependent protein kinase and protein kinase C. Neuron 2006; 49: 409-20. (Pubitemid 43152242)
5. Cheng X, Dib-Hajj SD, Tyrrell L, Waxman SG. Mutation I136V alters electrophysiological properties of the NaV1.7 channel in a family with onset of erythromelalgia in the second decade. Mol Pain 2008; 4: 1.
6. Choi JS, Cheng X, Foster E, Leffler A, Tyrrell L, Te Morsche RH, et al. Alternative splicing may contribute to time-dependent manifestation of inherited erythromelalgia. Brain 2010; 133: 1823-35.
7. Cummins TR, Waxman SG. 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 1997; 17: 3503-14. (Pubitemid 27200579)
8. Dib-Hajj SD, Choi JS, Macala LJ, Tyrrell L, Black JA, Cummins TR, et al. Transfection of rat or mouse neurons by biolistics or electroporation. Nat Protoc 2009; 4: 1118-26.
9. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG. From genes to pain: NaV1.7 and human pain disorders. Trends Neurosci 2007; 30: 555-63. (Pubitemid 350051424)
10. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG. Sodium channels in normal and pathological pain. Annu Rev Neurosci 2010; 33: 325-47.
11. Drenth JP, te Morsche RH, Guillet G, Taieb A, Kirby RL, Jansen JB. SCN9A mutations define primary erythermalgia as a neuropathic disorder of voltage gated sodium channels. J Invest Dermatol 2005; 124: 1333-8. (Pubitemid 40847424)
12. Drenth JP, Waxman SG. Mutations in sodium-channel gene SCN9A cause a spectrum of human genetic pain disorders. J Clin Invest 2007; 117: 3603-9. (Pubitemid 350224065)
13. Errington AC, Stöhr T, Heers C, Lees G. The investigational anti-convulsant lacosamide selectively enhances slow inactivation of voltage-gated sodium channels. Mol Pharmacol 2008; 73: 157-69. (Pubitemid 350294207)
14. Estacion M, Dib-Hajj SD, Benke PJ, Te Morsche RH, Eastman EM, Macala LJ, et al. 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 2008; 28: 11079-88.
15. Fang X, Djouhri L, McMullan S, Berry C, Waxman SG, Okuse K, et al. 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 2006; 26: 7281-92.
16. Goldin AL. Mechanisms of sodium channel inactivation. Curr Opin Neurobiol 2003; 13: 284-90. (Pubitemid 36792240)
17. Han C, Dib-Hajj SD, Lin Z, Li Y, Eastman EM, Tyrrell L, et al. Early- and late-onset inherited erythromelalgia: genotype-phenotype correlation. Brain 2009; 132: 1711-22.
18. Han C, Rush AM, Dib-Hajj SD, Li S, Xu Z, Wang Y, et al. Sporadic onset of erythermalgia: a gain-of-function mutation in NaV1.7. Ann Neurol 2006; 59: 553-8. (Pubitemid 43358077)
19. Harris JA, Murphy JA. Lacosamide: an adjunctive agent for partial-onset seizures and potential therapy for neuropathic pain. Ann Pharmacother 2009; 43: 1809-17.
20. Harty TP, Dib-Hajj SD, Tyrrell L, Blackman R, Hisama FM, Rose JB, et al. NaV1.7 mutant A863P in erythromelalgia: effects of altered activation and steady-state inactivation on excitability of nociceptive dorsal root ganglion neurons. J Neurosci 2006; 26: 12566-12575. (Pubitemid 44864521)
21. Herzog RI, Cummins TR, Ghassemi F, Dib-Hajj SD, Waxman SG. Distinct repriming and closed-state inactivation kinetics of NaV1.6 and NaV1.7 sodium channels in mouse spinal sensory neurons. J Physiol 2003; 551: 741-50. (Pubitemid 37221069)
22. Hildebrand ME, Smith PL, Bladen C, Eduljee C, Xie JY, Chen L, et al. A novel slow-inactivation-specific ion channel modulator attenuates neuropathic pain. Pain 2011; 152: 833-43.
23. Jarecki BW, Sheets PL, Jackson JO 2nd, Cummins TR. Paroxysmal extreme pain disorder mutations within the D3/S4-S5 linker of Nav1.7 cause moderate destabilization of fast inactivation. J physiol 2008; 586: 4137-53.
24. Klugbauer N, Lacinova L, Flockerzi V, Hofmann F. Structure and functional expression of a new member of the tetrodotoxin-sensitive voltage-activated sodium channel family from human neuroendocrine cells. EMBO J 1995; 14: 1084-90.
25. Nau C, Wang SY, Strichartz GR, Wang GK. Point mutations at N434 in D1-S6 of mu1 Na+ channels modulate binding affinity and stereo-selectivity of local anesthetic enantiomers. Mol Pharmacol 1999; 56: 404-13. (Pubitemid 29347618)
26. O'Reilly JP, Wang SY, Wang GK. Residue-specific effects on slow inacti-vation at V787 in D2-S6 of NaV1.4 sodium channels. Biophys J 2001; 81: 2100-11. (Pubitemid 32917159)
27. Raymond CK, Castle J, Garrett-Engele P, Armour CD, Kan Z, Tsinoremas N, et al. Expression of alternatively spliced sodium channel alpha-subunit genes. Unique splicing patterns are observed in dorsal root ganglia. J Biol Chem 2004; 279: 46234-41.
28. Shafrir Y, Durell SR, Guy HR. Models of the structure and gating mechanisms of the pore domain of the NaChBac ion channel. Biophys J 2008; 95: 3650-62.
29. Sheets PL, Heers C, Stoehr T, Cummins TR. 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 2008; 326: 89-99. (Pubitemid 351872141)
30. Sheets PL, Jackson JO 2nd, Waxman SG, Dib-Hajj SD, Cummins TR. A NaV1.7 channel mutation associated with hereditary erythromelalgia contributes to neuronal hyperexcitability and displays reduced lidocaine sensitivity. J Physiol 2007; 581: 1019-31. (Pubitemid 46887978)
31. Wang SY, Russell C, Wang GK. Tryptophan substitution of a putative D4S6 gating hinge alters slow inactivation in cardiac sodium channels. Biophys J 2005; 88: 3991-9. (Pubitemid 40991111)
32. Wang SY, Wang GK. A mutation in segment I-S6 alters slow inactivation of sodium channels. Biophys J 1997; 72: 1633-40. (Pubitemid 27133102)
33. Zhao Y, Scheuer T, Catterall WA. Reversed voltage-dependent gating of a bacterial sodium channel with proline substitutions in the S6 transmembrane segment. Proc Natl Acad Sci USA 2004a; 101: 17873-8. (Pubitemid 40051979)
34. Zhao Y, Yarov-Yarovoy V, Scheuer T, Catterall WA. A gating hinge in Na+ channels; a molecular switch for electrical signaling. Neuron 2004b; 41: 859-65. (Pubitemid 38429730)