Nav1.7-A1632G mutation from a family with inherited erythromelalgia: Enhanced firing of dorsal root ganglia neurons evoked by thermal stimuli

Journal of Neuroscience

Volumn 36, Issue 28, 2016, Pages 7511-7522

  Yang, Yang ^a,b   Huang, Jianying ^a,b   Mis, Malgorzata A ^a,b   Estacion, Mark ^a,b   Macala, Lawrence ^a,b   Shah, Palak ^a,b   Schulman, Betsy R ^a,b   Horton, Daniel B ^c   Dib Hajj, Sulayman D ^a,b   Waxman, Stephen G ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Chronic pain; Man on fire syndrome; Sensory neurons; Temperature responses; Thermosensation; Voltage gated sodium channel

Indexed keywords

SODIUM CHANNEL NAV1.7; ALANINE; GLUTAMINE; SCN9A PROTEIN, HUMAN; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL VIABILITY; CHANNEL GATING; CURRENT CLAMP TECHNIQUE; DEPOLARIZATION; ERYTHROMELALGIA; EXON; FEMALE; FIRING RATE; GAIN OF FUNCTION MUTATION; GENE MUTATION; GENE SEQUENCE; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; HYPERPOLARIZATION; MALE; MEMBRANE STEADY POTENTIAL; MOLECULAR GENETICS; NONHUMAN; PLASMID; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL GANGLION; THERMAL STIMULUS TEST; VOLTAGE CLAMP TECHNIQUE; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; MEMBRANE POTENTIAL; MOLECULAR MODEL; MUTATION; NERVE CELL; PATCH CLAMP TECHNIQUE; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TEMPERATURE;

ALANINE; ANIMALS; CELLS, CULTURED; ERYTHROMELALGIA; FEMALE; GANGLIA, SPINAL; GLUTAMINE; HEK293 CELLS; HUMANS; MALE; MEMBRANE POTENTIALS; MODELS, MOLECULAR; MUTATION; NAV1.7 VOLTAGE-GATED SODIUM CHANNEL; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNEL BLOCKERS; TEMPERATURE; TETRODOTOXIN;

EID: 84978818300     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0462-16.2016     Document Type: Article

References (54)

1. Amaral C, Carnevale V, Klein ML, Treptow W (2012) Exploring conformational states of the bacterial voltage-gated sodium channel NavAb via molecular dynamics simulations. Proc Natl Acad Sci U S A 109:21336-21341. CrossRef Medline
2. Atkins JF, Wills NM, Loughran G, Wu CY, Parsawar K, Ryan MD, Wang CH, Nelson CC (2007) A case for “StopGo”: reprogramming translation to augment codon meaning of GGN by promoting unconventional termination (Stop) after addition of glycine and then allowing continued translation (Go). RNA 13:803-810. CrossRef Medline
3. 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. CrossRef Medline
4. Cesca F, Satapathy A, Ferrea E, Nieus T, Benfenati F, Scholz-Starke J (2015) Functional interaction between the scaffold protein Kidins220/ARMS and neuronal voltage-gated Na channels. J Biol Chem 290:18045-18055. CrossRef Medline
5. Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517-524. CrossRef Medline
6. 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. CrossRef Medline
7. Cummins TR, Waxman SG (1997) Downregulation of tetrodotoxinresistant 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. Medline
8. Cummins TR, Howe JR, Waxman SG (1998) Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/ PN1 sodium channel. J Neurosci 18:9607-9619. Medline
9. 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. CrossRef Medline
10. Dib-Hajj SD, Tyrrell L, Black JA, Waxman SG (1998) NaN, a novel voltagegated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc Natl Acad Sci U S A 95: 8963-8968. CrossRef Medline
11. 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. CrossRef Medline
12. Dib-Hajj SD, Choi JS, Macala LJ, Tyrrell L, Black JA, Cummins TR, Waxman SG (2009) Transfection of rat or mouse neurons by biolistics or electroporation. Nat Protoc 4:1118-1126. CrossRef Medline
13. Dib-Hajj SD, Yang Y, Black JA, Waxman SG (2013) The Na(V)1.7 sodium channel: from molecule to man. Nat Rev Neurosci 14:49-62. CrossRef Medline
14. 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. CrossRef Medline
15. Dudley SC Jr, Chang N, Hall J, Lipkind G, Fozzard HA, French RJ (2000) mu-conotoxin GIIIA interactions with the voltage-gated Na() channel predict a clockwise arrangement of the domains. J Gen Physiol 116: 679-690. CrossRef Medline
16. Eberhardt M, Nakajima J, Klinger AB, Neacsu C, Hühne K, O’Reilly AO, Kist AM, Lampe AK, Fischer K, Gibson J, Nau C, Winterpacht A, Lampert A (2014) Inherited pain: sodium channel Nav1.7 A1632T mutation causes erythromelalgia due to a shift of fast inactivation. J Biol Chem 289:1971-1980. CrossRef Medline
17. Estacion M, Dib-Hajj SD, Benke PJ, Te Morsche RH, Eastman EM, Macala LJ, Drenth JP, Waxman SG (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 28:11079-11088. CrossRef Medline
18. Estacion M, Yang Y, Dib-Hajj SD, Tyrrell L, Lin Z, Yang Y, Waxman SG (2013) A new Nav1.7 mutation in an erythromelalgia patient. Biochem Biophys Res Commun 432:99-104. CrossRef Medline
19. Estacion M, Vohra BP, Liu S, Hoeijmakers J, Faber CG, Merkies IS, Lauria G, Black JA, Waxman SG (2015) Ca2 toxicity due to reverse Na/Ca 2 exchange contributes to degeneration of neurites of DRG neurons induced by a neuropathy-associated Nav1.7 mutation. J Neurophysiol 114: 1554-1564. CrossRef Medline
20. Faber CG, Hoeijmakers JG, Ahn HS, Cheng X, Han C, Choi JS, Estacion M, Lauria G, Vanhoutte EK, Gerrits MM, Dib-Hajj S, Drenth JP, Waxman SG, Merkies IS (2012) Gain of function Nanu1.7 mutations in idiopathic small fiber neuropathy. Ann Neurol 71:26-39. CrossRef Medline
21. 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. CrossRef Medline
22. Graham BA, Brichta AM, Callister RJ (2008) Recording temperature affects the excitability of mouse superficial dorsal horn neurons, in vitro. J Neurophysiol 99:2048-2059. CrossRef Medline
23. Han C, Hoeijmakers JG, Liu S, Gerrits MM, te Morsche RH, Lauria G, Dib-Hajj SD, Drenth JP, Faber CG, Merkies IS, Waxman SG (2012) Functional profiles of SCN9A variants in dorsal root ganglion neurons and superior cervical ganglion neurons correlate with autonomic symptoms in small fibre neuropathy. Brain 135:2613-2628. CrossRef Medline
24. Han C, Yang Y, de Greef BT, Hoeijmakers JG, Gerrits MM, Verhamme C, Qu J, Lauria G, Merkies IS, Faber CG, Dib-Hajj SD, Waxman SG (2015) The domain II S4-S5 linker in Nav1.9: a missense mutation enhances activation, impairs fast inactivation, and produces human painful neuropathy. Neuromolecular Med 17:158-169. CrossRef Medline
25. 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. CrossRef Medline
26. Huang J, Yang Y, Zhao P, Gerrits MM, Hoeijmakers JG, Bekelaar K, Merkies IS, Faber CG, Dib-Hajj SD, Waxman SG (2013) Small-fiber neuropathy Nav1.8 mutation shifts activation to hyperpolarized potentials and increases excitability of dorsal root ganglion neurons. J Neurosci 33:14087-14097. CrossRef Medline
27. Huang J, Yang Y, Dib-Hajj SD, van Es M, Zhao P, Salomon J, Drenth JP, Waxman SG (2014a) Depolarized inactivation overcomes impaired activation to produce DRG neuron hyperexcitability in a Nav1.7 mutation in a patient with distal limb pain. J Neurosci 34:12328-12340. CrossRef Medline
28. Huang J, Han C, Estacion M, Vasylyev D, Hoeijmakers JG, Gerrits MM, Tyrrell L, Lauria G, Faber CG, Dib-Hajj SD, Merkies IS, Waxman SG (2014b) Gain-of-function mutations in sodium channel Na(v)1.9 in painful neuropathy. Brain 137:1627-1642. CrossRef Medline
29. Julius D (2013) TRP channels and pain. Annu Rev Cell Dev Biol 29: 355-384. CrossRef Medline
30. Kang D, Choe C, Kim D (2005) Thermosensitivity of the two-pore domain K channels TREK-2 and TRAAK. J Physiol 564:103-116. CrossRef Medline
31. Klugbauer N, Lacinova L, Flockerzi V, Hofmann F (1995) Structure and functional expression of a new member of the tetrodotoxin-sensitive voltage-activated sodium channel family from human neuroendocrine cells. EMBO J 14:1084-1090. Medline
32. Li RA, Ennis IL, French RJ, Dudley SC Jr, Tomaselli GF, Marbań E (2001) Clockwise domain arrangement of the sodium channel revealed by (mu)-conotoxin (GIIIA) docking orientation. J Biol Chem 276:11072-11077. CrossRef Medline
33. Lossin C, Wang DW, Rhodes TH, Vanoye CG, George AL Jr (2002) Molecular basis of an inherited epilepsy. Neuron 34:877-884. CrossRef Medline
34. Luke GA, de Felipe P, Lukashev A, Kallioinen SE, Bruno EA, Ryan MD (2008) Occurrence, function and evolutionary origins of ‘2A-like’ sequences in virus genomes. J Gen Virol 89:1036-1042. CrossRef Medline
35. McDonnell A, Schulman B, Ali Z, Dib-Hajj SD, Brock F, Cobain S, Mainka T, Vollert J, Tarabar S, Waxman SG (2016) Inherited erythromelalgia due to mutations in SCN9A: natural history, clinical phenotype and somatosensory profile. Brain 139:1052-1065. CrossRef Medline
36. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353-358. CrossRef Medline
37. Persson AK, Liu S, Faber CG, Merkies IS, Black JA, Waxman SG (2013) Neuropathy-associated Nav1.7 variant I228M impairs integrity of dorsal root ganglion neuron axons. Ann Neurol 73:140-145. CrossRef Medline
38. Roy A, Xu D, Poisson J, Zhang Y (2011) A protocol for computer-based protein structure and function prediction. J Vis Exp 57:e3259. CrossRef Medline
39. 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 U S A 103:8245-8250. CrossRef Medline
40. 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. CrossRef Medline
41. Ryan MD, Drew J (1994) Foot-and-mouth disease virus 2A oligopeptide mediated cleavage of an artificial polyprotein. EMBO J 13:928-933. Medline
42. Shields SD, Ahn HS, Yang Y, Han C, Seal RP, Wood JN, Waxman SG, Dib-Hajj SD (2012) Nav1.8 expression is not restricted to nociceptors in mouse peripheral nervous system. Pain 153:2017-2030. CrossRef Medline
43. Spira ME, Hai A (2013) Multi-electrode array technologies for neuroscience and cardiology. Nat Nanotechnol 8:83-94. CrossRef Medline
44. Vasylyev DV, Han C, Zhao P, Dib-Hajj S, Waxman SG (2014) Dynamicclamp analysis of wild-type human Nav1.7 and erythromelalgia mutant channel L858H. J Neurophysiol 111:1429-1443. CrossRef Medline
45. Vriens J, Nilius B, Voets T (2014) Peripheral thermosensation in mammals. Nat Rev Neurosci 15:573-589. CrossRef Medline
46. Wainger BJ, Kiskinis E, Mellin C, Wiskow O, Han SS, Sandoe J, Perez NP, Williams LA, Lee S, Boulting G, Berry JD, Brown RH Jr, Cudkowicz ME, Bean BP, Eggan K, Woolf CJ (2014) Intrinsic membrane hyperexcitability of amyotrophic lateral sclerosis patient-derived motor neurons. Cell Rep 7:1-11. CrossRef Medline
47. Waxman SG (2006) Neurobiology: a channel sets the gain on pain. Nature 444:831-832. CrossRef Medline
48. 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. CrossRef Medline
49. Yang Y, Dib-Hajj SD, Zhang J, Zhang Y, Tyrrell L, Estacion M, Waxman SG (2012) Structural modelling and mutant cycle analysis predict pharmacoresponsiveness of a Na(V)1.7 mutant channel. Nat Commun 3:1186. CrossRef Medline
50. Yang Y, Estacion M, Dib-Hajj SD, Waxman SG (2013a) Molecular architecture of a sodium channel S6 helix: radial tuning of the voltage-gated sodium channel 1.7 activation gate. J Biol Chem 288:13741-13747. CrossRef Medline
51. Yang Y, Vasylyev DV, Dib-Hajj F, Veeramah KR, Hammer MF, Dib-Hajj SD, Waxman SG (2013b) Multistate structural modeling and voltage-clamp analysis of epilepsy/autism mutation Kv10.2-R327H demonstrate the role of this residue in stabilizing the channel closed state. J Neurosci 33:16586-16593. CrossRef Medline
52. Yarov-Yarovoy V, DeCaen PG, Westenbroek RE, Pan CY, Scheuer T, Baker D, Catterall WA (2012) Structural basis for gating charge movement in the voltage sensor of a sodium channel. Proc Natl Acad Sci U S A 109: E93-E102. CrossRef Medline
53. Zhang J, Liang Y, Zhang Y (2011) Atomic-level protein structure refinement using fragment-guided molecular dynamics conformation sampling. Structure 19:1784-1795. CrossRef Medline
54. Zhang J, Yang J, Jang R, Zhang Y (2015) GPCR-I-TASSER: a hybrid approach to G protein-coupled receptor structure modeling and the application to the human genome. Structure 23:1538-1549. CrossRef Medline