Inherited pain sodium channel nav1.7 A1632T mutation causes erythromelalgia due to a shift of fast inactivation

Journal of Biological Chemistry

Volumn 289, Issue 4, 2014, Pages 1971-1980

  Eberhardt, Mirjam ^a,b   Nakajima, Julika ^a   Klinger, Alexandra B ^a   Neacsu, Cristian ^a   Hühne, Kathrin ^a   O'Reilly, Andrias O ^a   Kist, Andreas M ^a   Lampe, Anne K ^c   Fischer, Kerstin ^a   Gibson, Jane ^d   Nau, Carla ^a,e   Winterpacht, Andreas ^a   Lampert, Angelika ^a,f  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

^d NHS FIFE   (United Kingdom)

^e UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^f RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

PAIN SYNDROMES; SODIUM CHANNEL; SODIUM CURRENT;

SODIUM;

ALANINE; SODIUM CHANNEL NAV1.7; THREONINE;

ADULT; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CASE REPORT; CHANNEL GATING; DEPOLARIZATION; ERYTHROMELALGIA; FEMALE; GENE ACTIVATION; GENE IDENTIFICATION; GENE INACTIVATION; GENE MUTATION; GENE SEQUENCE; HUMAN; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; SODIUM CHANNEL NAV1.7 GENE; SODIUM CURRENT; SPINAL GANGLION; STEADY STATE; WILD TYPE; YOUNG ADULT;

ERYTHROMELALGIA; HYPEREXCITABILITY; MOSAICISM; NEUROPHYSIOLOGY; PAIN; PATCH CLAMP; SITE-DIRECTED MUTAGENESIS; SODIUM CHANNELS;

AMINO ACID SUBSTITUTION; ERYTHROMELALGIA; FEMALE; GANGLIA, SPINAL; HEK293 CELLS; HUMANS; ION TRANSPORT; MALE; MUTATION, MISSENSE; NAV1.7 VOLTAGE-GATED SODIUM CHANNEL; PAIN; RECTUM; SENSORY RECEPTOR CELLS;

EID: 84893086859     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.502211     Document Type: Article

References (31)

1. Catterall, W. A., Goldin, A. L., and Waxman, S. G. (2003) International Union of Pharmacology. XXXIX. Compendium of Voltage-gated ion channels. Sodium channels. Pharmacol. Rev. 55, 575-578
2. Drenth, J. P., Te Morsche, R. H., Guillet, G., Taieb, A., Kirby, R. L., and Jansen, J. B. (2005) SCN9A mutations define primary erythermalgia as a neuropathic disorder of voltage gated sodium channels. J. Invest. Dermatol. 124, 1333-1338
3. Takahashi, K., Saitoh, M., Hoshino, H., Mimaki, M., Yokoyama, Y., Takamizawa, M., Mizuguchi, M., Lin, Z. M., Yang, Y., and Igarashi, T. (2007) A case of primary erythermalgia, wintry hypothermia and encephalopathy. Neuropediatrics 38, 157-159
4. Wu, M. T., Huang, P. Y., Yen, C. T., Chen, C. C., and Lee, M. J. (2013) A novel SCN9A mutation responsible for primary erythromelalgia and is resistant to the treatment of sodium channel blockers. PLoS ONE 8, e55212
5. Estacion, M., Dib-Hajj, S. D., Benke, P. J., Te Morsche, R. H., Eastman, E. M., Macala, L. J., Drenth, J. P., and Waxman, S. G. (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
6. Fertleman, C. R., Ferrie, C. D., Aicardi, J., Bednarek, N. A., Eeg-Olofsson, O., Elmslie, F. V., Griesemer, D. A., Goutières, F., Kirkpatrick, M., Malmros, I. N., Pollitzer, M., Rossiter, M., Roulet-Perez, E., Schubert, R., Smith, V. V., Testard, H., Wong, V., and Stephenson, J. B. (2007) Paroxysmal extreme pain disorder (previously familial rectal pain syndrome). Neurology 69, 586-595
7. Dib-Hajj, S. D., Yang, Y., Black, J. A., and Waxman, S. G. (2013) The Na(V)1.7 sodium channel. From molecule to man. Nat. Rev. Neurosci. 14, 49-62
8. Choi, J.-S., Cheng, X., Foster, E., Leffler, A., Tyrrell, L., Te Morsche, R. H., Eastman, E. M., Jansen, H. J., Huehne, K., Nau, C., Dib-Hajj, S. D., Drenth, J. P., and Waxman, S. G. (2010) Alternative splicing may contribute to time-dependent manifestation of inherited erythromelalgia. Brain 133, 1823-1835
9. Grieco, T. M., Malhotra, J. D., Chen, C., Isom, L. L., and Raman, I. M. (2005) Open-channel block by the cytoplasmic tail of sodium channel β4 as a mechanism for resurgent sodium current. Neuron 45, 233-244
10. Raman, I. M., and Bean, B. P. (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J. Neurosci. 17, 4517-4526
11. Jarecki, B. W., Piekarz, A. D., Jackson, J. O., 2nd, and Cummins, T. R. (2010) Human voltage-gated sodium channel mutations that cause inherited neuronal and muscle channelopathies increase resurgent sodium currents. J. Clin. Invest. 120, 369-378
12. Jarecki, B. W., Sheets, P. L., Jackson, I. I. J. O., and Cummins, T. R. (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
13. Theile, J. W., Jarecki, B. W., Piekarz, A. D., and Cummins, T. R. (2011) Nav1.7 mutations associated with paroxysmal extreme pain disorder, but not erythromelalgia, enhance Navβ4 peptide-mediated resurgent sodium currents. J. Physiol. 589, 597-608
14. Payandeh, J., Scheuer, T., Zheng, N., and Catterall, W. A. (2011) The crystal structure of a voltage-gated sodium channel. Nature 475, 353-358
15. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680
16. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., and Sali, A. (2007) in Current Protocols in Protein Science (Coligan, J. E., Dunn, B. M., Speicher, D. W., and Wingfield, P. T., eds) pp. 2.9.1-31, John Wiley and Sons, New York
17. Willard, L., Ranjan, A., Zhang, H., Monzavi, H., Boyko, R. F., Sykes, B. D., and Wishart, D. S. (2003) VADAR. A web server for quantitative evaluation of protein structure quality. Nucleic Acids Res. 31, 3316-3319
18. Theile, J. W., and Cummins, T. R. (2011) Inhibition of Navβ4 peptidemediated resurgent sodium currents in Nav1.7 channels by carbamazepine, riluzole, and anandamide. Mol. Pharmacol. 80, 724-734
19. Cummins, T. R., Rush, A. M., Estacion, M., Dib-Hajj, S. D., and Waxman, S. G. (2009) Voltage-clamp and current-clamp recordings from mammalian DRG neurons. Nat. Protoc. 4, 1103-1112
20. Han, C., Rush, A. M., Dib-Hajj, S. D., Li, S., Xu, Z., Wang, Y., Tyrrell, L., Wang, X., Yang, Y., and Waxman, S. G. (2006) Sporadic onset of erythermalgia. A gain-of-function mutation in Nav1.7. Ann. Neurol. 59, 553-558
21. Rush, A. M., Dib-Hajj, S. D., Liu, S., Cummins, T. R., Black, J. A., and Waxman, S. G. (2006) A single sodium channel mutation produces hyperor hypoexcitability in different types of neurons. Proc. Natl. Acad. Sci. U.S.A. 103, 8245-8250
22. Waxman, S. G. (2007) Channel, neuronal and clinical function in sodium channelopathies. From genotype to phenotype. Nat. Neurosci. 10, 405-409
23. Lampert, A., O'Reilly, A. O., Reeh, P., and Leffler, A. (2010) Sodium channelopathies and pain. Pfluegers Arch. Eur. J. Physiol. 460, 249-263
24. Cummins, T. R., Dib-Hajj, S. D., and Waxman, S. G. (2004) Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy. J. Neurosci. 24, 8232-8236
25. Cheng, X., Dib-Hajj, S. D., Tyrrell, L., Te Morsche, R. H., Drenth, J. P., and Waxman, S. G. (2011) Deletion mutation of sodium channel Na(V)1.7 in inherited erythromelalgia. Enhanced slow inactivation modulates dorsal root ganglion neuron hyperexcitability. Brain 134, 1972-1986
26. Hoeijmakers, J. G., Han, C., Merkies, I. S., Macala, L. J., Lauria, G., Gerrits, M. M., Dib-Hajj, S. D., Faber, C. G., and Waxman, S. G. (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, 345-358
27. Ahn, H. S., Dib-Hajj, S. D., Cox, J. J., Tyrrell, L., Elmslie, F. V., Clarke, A. A., Drenth, J. P., Woods, C. G., and Waxman, S. G. (2010) A new Nav1.7 sodium channel mutation I234T in a child with severe pain. Eur. J. Pain 14, 944-950
28. Payandeh, J., Gamal El-Din, T. M., Scheuer, T., Zheng, N., and Catterall, W. A. (2012) Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486, 135-139
29. Long, S. B., Campbell, E. B., and Mackinnon, R. (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309, 897-903
30. Tsai, C.-J., Tani, K., Irie, K., Hiroaki, Y., Shimomura, T., McMillan, D. G., Cook, G. M., Schertler, G. F., Fujiyoshi, Y., and Li, X.-D. (2013) Two alternative conformations of a voltage-gated sodium channel. J. Mol. Biol. 425, 4074-4088
31. Chanda, B., and Bezanilla, F. (2002) Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J. Gen. Physiol. 120, 629-645