The Domain II S4-S5 Linker in Nav1.9: A Missense Mutation Enhances Activation, Impairs Fast Inactivation, and Produces Human Painful Neuropathy

NeuroMolecular Medicine

Volumn 17, Issue 2, 2015, Pages 158-169

  Han, Chongyang ^a,b   Yang, Yang ^a,b   de Greef, Bianca T A ^c   Hoeijmakers, Janneke G J ^c   Gerrits, Monique M ^c   Verhamme, Camiel ^d   Qu, Jian ^a,b   Lauria, Giuseppe ^e   Merkies, Ingemar S J ^c,f   Faber, Catharina G ^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 MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e IRCCS   (Italy)

^f Department of Orthopaedic Surgery   (Netherlands)

Author keywords

DRG; Nav1.9; Pain; Sodium channel

Indexed keywords

HYBRID PROTEIN; SCN11A PROTEIN, HUMAN; SODIUM CHANNEL NAV1.9;

ACTION POTENTIAL; AGED; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL; CELL CULTURE; CHANNEL GATING; CHEMISTRY; CYTOLOGY; ERYTHROMELALGIA; GENETIC TRANSFECTION; GENETICS; HUMAN; MALE; MEMBRANE POTENTIAL; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; POINT MUTATION; PROTEIN TERTIARY STRUCTURE; RAT; SENSORY NERVE CELL; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SPINAL GANGLION; SPRAGUE DAWLEY RAT; SUPERIOR CERVICAL GANGLION;

ACTION POTENTIALS; AGED; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELLS, CULTURED; ERYTHROMELALGIA; GANGLIA, SPINAL; HUMANS; ION CHANNEL GATING; MALE; MEMBRANE POTENTIALS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NAV1.9 VOLTAGE-GATED SODIUM CHANNEL; PATCH-CLAMP TECHNIQUES; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; SENSORY RECEPTOR CELLS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SUPERIOR CERVICAL GANGLION; TRANSFECTION;

EID: 84939775748     PISSN: 15351084     EISSN: 15591174     Source Type: Journal    
DOI: 10.1007/s12017-015-8347-9     Document Type: Article

References (46)

1. Allen, A. S., Berkovic, S. F., Cossette, P., Delanty, N., Dlugos, D., Eichler, E. E., et al. (2013). De novo mutations in epileptic encephalopathies. Nature,501(7466), 217–221. doi:10.1038/Nature12439.
2. Amaya, F., Wang, H., Costigan, M., Allchorne, A. J., Hatcher, J. P., Egerton, J., et al. (2006). The voltage-gated sodium channel Na(v)1.9 is an effector of peripheral inflammatory pain hypersensitivity. Journal of Neuroscience,26(50), 12852–12860. doi:10.1523/JNEUROSCI.4015-06.2006.
3. Bendahhou, S., Cummins, T. R., Kula, R. W., Fu, Y. H., & Ptacek, L. J. (2002). Impairment of slow inactivation as a common mechanism for periodic paralysis in DIIS4-S5. Neurology,58(8), 1266–1272.
4. Cannon, S. C. (2002). An expanding view for the molecular basis of familial periodic paralysis. Neuromuscular Disorders,12(6), 533–543. doi:10.1016/S0960-8966(02)00007-X.
5. Cummins, T. R., Dib-Hajj, S. D., Black, J. A., Akopian, A. N., Wood, J. N., & Waxman, S. G. (1999). A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. Journal of neuroscience, 19(24).
6. Cummins, T. R., Dib-Hajj, S. D., & Waxman, S. G. (2004). Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy. Journal of Neuroscience,24(38), 8232–8236. doi:10.1523/JNEUROSCI.2695-04.2004.
7. Dib-Hajj, S., Black, J. A., Cummins, T. R., & Waxman, S. G. (2002). NaN/Nav1.9: a sodium channel with unique properties. Trends in Neurosciences,25(5), 253–259.
8. Dib-Hajj, S. D., Choi, J. S., Macala, L. J., Tyrrell, L., Black, J. A., Cummins, T. R., et al. (2009). Transfection of rat or mouse neurons by biolistics or electroporation. Nature Protocols,4(8), 1118–1126. doi:10.1038/nprot.2009.90.
9. Dib-Hajj, S. D., Tyrrell, L., Black, J. A., & Waxman, S. G. (1998). NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proceedings of the National Academy of Sciences of the United States of America,95(15), 8963–8968.
10. Dib-Hajj, S. D., Tyrrell, L., Cummins, T. R., Black, J. A., Wood, P. M., & Waxman, S. G. (1999a). Two tetrodotoxin-resistant sodium channels in human dorsal root ganglion neurons. FEBS Letters,462(1–2), 117–120.
11. Dib-Hajj, S. D., Tyrrell, L., Escayg, A., Wood, P. M., Meisler, M. H., & Waxman, S. G. (1999b). Coding sequence, genomic organization, and conserved chromosomal localization of the mouse gene Scn11a encoding the sodium channel NaN. Genomics,59(3), 309–318. doi:10.1006/geno.1999.5890.
12. Dib-Hajj, S. D., Yang, Y., Black, J. A., & Waxman, S. G. (2013). The Na(V)1.7 sodium channel: from molecule to man. Nature Reviews Neuroscience,14(1), 49–62. doi:10.1038/nrn3404.
13. Drenth, J. P., & Waxman, S. G. (2007). Mutations in sodium-channel gene SCN9A cause a spectrum of human genetic pain disorders. The Journal of Clinical Investigation,117(12), 3603–3609. doi:10.1172/JCI33297.
14. Estacion, M., & Waxman, S. G. (2013). The response of Na(V)1.3 sodium channels to ramp stimuli: multiple components and mechanisms. Journal of Neurophysiology,109(2), 306–314. doi:10.1152/jn.00438.2012.
15. Faber, C. G., Hoeijmakers, J. G. J., Ahn, H. S., Cheng, X. Y., Han, C. Y., Choi, J. S., et al. (2012a). Gain of function NaV1.7 mutations in idiopathic small fiber neuropathy. Annals of Neurology,71(1), 26–39. doi:10.1002/Ana.22485.
16. Faber, C. G., Lauria, G., Merkies, I. S. J., Cheng, X. Y., Han, C. Y., Ahn, H. S., et al. (2012b). Gain-of-function Na(v)1.8 mutations in painful neuropathy. Proceedings of the National Academy of Sciences of the United States of America,109(47), 19444–19449. doi:10.1073/pnas.1216080109.
17. Fjell, J., Hjelmstrom, P., Hormuzdiar, W., Milenkovic, M., Aglieco, F., Tyrrell, L., et al. (2000). Localization of the tetrodotoxin-resistant sodium channel NaN in nociceptors. NeuroReport,11(1), 199–202. doi:10.1097/00001756-200001170-00039.
18. Han, C., Hoeijmakers, J. G., Ahn, H. S., Zhao, P., Shah, P., Lauria, G., et al. (2012). Nav1.7-related small fiber neuropathy: impaired slow-inactivation and DRG neuron hyperexcitability. Neurology,78(21), 1635–1643. doi:10.1212/WNL.0b013e3182574f12.
19. Han, C., Rush, A. M., Dib-Hajj, S. D., Li, S., Xu, Z., Wang, Y., et al. (2006). Sporadic onset of erythermalgia: a gain-of-function mutation in Nav1.7. Annals of Neurology,59(3), 553–558. doi:10.1002/ana.20776.
20. Han, C., Vasylyev, D., Macala, L. J., Gerrits, M. M., Hoeijmakers, J. G., Bekelaar, K. J., et al. (2014). The G1662S NaV1.8 mutation in small fibre neuropathy: impaired inactivation underlying DRG neuron hyperexcitability. Journal of Neurology, Neurosurgery and Psychiatry,85(5), 499–505. doi:10.1136/jnnp-2013-306095.
21. Hockley, J. R., Boundouki, G., Cibert-Goton, V., McGuire, C., Yip, P. K., Chan, C., et al. (2014). Multiple roles for NaV1.9 in the activation of visceral afferents by noxious inflammatory, mechanical, and human disease-derived stimuli. Pain, 155(10), 1962–1975, doi:10.1016/j.pain.2014.06.015.
22. Hoeijmakers, J. G., Faber, C. G., Lauria, G., Merkies, I. S., & Waxman, S. G. (2012a). Small-fibre neuropathies-advances in diagnosis, pathophysiology and management. Nature Reviews Neurology,8(7), 369–379. doi:10.1038/nrneurol.2012.97.
23. Hoeijmakers, J. G., Han, C., Merkies, I. S., Macala, L. J., Lauria, G., Gerrits, M. M., et al. (2012b) 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, doi:10.1093/brain/awr349
24. Huang, J., Han, C., Estacion, M., Vasylyev, D., Hoeijmakers, J. G., Gerrits, M. M., et al. (2014). Gain-of-function mutations in sodium channel Na(V)1.9 in painful neuropathy. Brain,137, 1627–1642. doi:10.1093/Brain/Awu079.
25. Huang, J., Yang, Y., Zhao, P., Gerrits, M. M., Hoeijmakers, J. G., Bekelaar, K., et al. (2013). Small-fiber neuropathy Nav1.8 mutation shifts activation to hyperpolarized potentials and increases excitability of dorsal root ganglion neurons. Journal of Neuroscience,33(35), 14087–14097. doi:10.1523/JNEUROSCI.2710-13.2013.
26. Lauria, G., Merkies, I. S., & Faber, C. G. (2012). Small fibre neuropathy. Current Opinion in Neurology,25(5), 542–549. doi:10.1097/WCO.0b013e32835804c5.
27. Leipold, E., Liebmann, L., Korenke, G. C., Heinrich, T., Giesselmann, S., Baets, J., et al. (2013). A de novo gain-of-function mutation in SCN11A causes loss of pain perception. Nature Genetics,45(11), 1399–1404. doi:10.1038/ng.2767.
28. Lerche, H., Peter, W., Fleischha, R., Pika-Hartlaub, U., Malina, T., Mitrovic, N., et al. (1997). Role in fast inactivation of the IV/S4-S5 loop of the human muscle Na+ channel probed by cysteine mutagenesis. Journal of Physiology,505(2), 345–352.
29. Lolignier, S., Amsalem, M., Maingret, F., Padilla, F., Gabriac, M., Chapuy, E., et al. (2011). Nav1.9 channel contributes to mechanical and heat pain hypersensitivity induced by subacute and chronic inflammation. PLoS ONE,6(8), e23083. doi:10.1371/journal.pone.0023083.
30. McPhee, J. C., Ragsdale, D. S., Scheuer, T., & Catterall, W. A. (1998). A critical role for the S4-S5 intracellular loop in domain IV of the sodium channel alpha-subunit in fast inactivation. The Journal of biological chemistry,273(2), 1121–1129.
31. Niimura, H., Matsunaga, A., Kumagai, K., Ohwaki, K., Ogawa, M., Noguchi, H., et al. (2004). Genetic analysis of Brugada syndrome in western Japan - Two novel mutations. Circulation Journal,68(8), 740–746. doi:10.1253/Circj.68.740.
32. Ostman, J. A., Nassar, M. A., Wood, J. N., & Baker, M. D. (2008). GTP up-regulated persistent Na+ current and enhanced nociceptor excitability require NaV1.9. Journal of Physiology,586(4), 1077–1087. doi:10.1113/jphysiol.2007.147942.
33. Payandeh, J., El-Din, T. M. G., Scheuer, T., Zheng, N., & Catterall, W. A. (2012). Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature,486(7401), 135–139. doi:10.1038/Nature11077.
34. Payandeh, J., Scheuer, T., Zheng, N., & Catterall, W. A. (2011). The crystal structure of a voltage-gated sodium channel. Nature,475(7356), 353–358. doi:10.1038/Nature10238.
35. Persson, A. K., Black, J. A., Gasser, A., Cheng, X. Y., Fischer, T. Z., & Waxman, S. G. (2010). Sodium-calcium exchanger and multiple sodium channel isoforms in intra-epidermal nerve terminals. Molecular Pain, 6, doi:10.1186/1744-8069-6-84
36. Plassart-Schiess, E., Lhuillier, L., George, A. L., Fontaine, B., & Tabti, N. (1998). Functional expression of the Ile693Thr Na+ channel mutation associated with paramyotonia congenita in a human cell line. Journal of Physiology,507(3), 721–727. doi:10.1111/j.1469-7793.1998.721bs.x.
37. Priest, B. T., Murphy, B. A., Lindia, J. A., Diaz, C., Abbadie, C., Ritter, A. M., et al. (2005). Contribution of the tetrodotoxin-resistant voltage-gated sodium channel NaV1.9 to sensory transmission and nociceptive behavior. Proceedings of the National Academy of Sciences of the United States of America,102(26), 9382–9387. doi:10.1073/pnas.0501549102.
38. Qiu, F., Jiang, Y., Zhang, H., Liu, Y., & Mi, W. (2012). Increased expression of tetrodotoxin-resistant sodium channels Nav1.8 and Nav1.9 within dorsal root ganglia in a rat model of bone cancer pain. Neuroscience Letters,512(2), 61–66. doi:10.1016/j.neulet.2012.01.069.
39. Rugiero, F., Mistry, M., Sage, D., Black, J. A., Waxman, S. G., Crest, M., et al. (2003). Selective expression of a persistent tetrodotoxin-resistant Na+ current and NaV1.9 subunit in myenteric sensory neurons. Journal of Neuroscience,23(7), 2715–2725.
40. Rush, A. M., Dib-Hajj, S. D., Liu, S., Cummins, T. R., Black, J. A., & Waxman, S. G. (2006). A single sodium channel mutation produces hyper- or hypoexcitability in different types of neurons. Proceedings of the National Academy of Sciences of the United States of America,103(21), 8245–8250. doi:10.1073/pnas.0602813103.
41. Smith, M. R., & Goldin, A. L. (1997). Interaction between the sodium channel inactivation linker and domain III S4-S5. Biophysical Journal,73(4), 1885–1895.
42. Waxman, S. G., & Zamponi, G. W. (2014). Regulating excitability of peripheral afferents: emerging ion channel targets. Nature Neuroscience,17(2), 153–163. doi:10.1038/nn.3602.
43. 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. Journal of Medical Genetics,41(3), 171–174. doi:10.1136/jmg.2003.012153.
44. Zhang, X., Ren, W. L., DeCaen, P., Yan, C. Y., Tao, X., Tang, L., et al. (2012). Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature,486(7401), 130–134. doi:10.1038/Nature11054.
45. Zhang, X. Y., Wen, J., Yang, W., Wang, C., Gao, L., Zheng, L. H., et al. (2013). Gain-of-function mutations in SCN11A cause familial episodic pain. American Journal of Human Genetics,93(5), 957–966. doi:10.1016/j.ajhg.2013.09.016.
46. Zuberi, S. M., Brunklaus, A., Birch, R., Reavey, E., Duncan, J., & Forbes, G. H. (2011). Genotype-phenotype associations in SCN1A-related epilepsies. Neurology,76(7), 594–600. doi:10.1212/Wnl.0b013e31820c309b.