Cold-aggravated pain in humans caused by a hyperactive NaV1.9 channel mutant

Nature Communications

Volumn 6, Issue , 2015, Pages

  Leipold, Enrico ^a   Hanson Kahn, Andrea ^b   Frick, Miya ^b   Gong, Ping ^b   Bernstein, Jonathan A ^b   Voigt, Martin ^a   Katona, Istvan ^c   Goral, R Oliver ^a   Altmüller, Janine ^d,e   Nürnberg, Peter ^d,e   Weis, Joachim ^c   Hübner, Christian A ^a   Heinemann, Stefan H ^a   Kurth, Ingo ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; SODIUM CHANNEL NAV1.9; SCN11A PROTEIN, HUMAN; SCN11A PROTEIN, MOUSE;

MODELING; MUTATION; PHYSIOLOGY; SENSORY SYSTEM;

ACTION POTENTIAL AMPLITUDE; ANALGESIA (SENSORY DYSFUNCTION); ANIMAL CELL; ARTICLE; CHILD; COLD; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; GAIN OF FUNCTION MUTATION; GENE MUTATION; GENE SEQUENCE; HALF-INACTIVATION VOLTAGE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERPOLARIZATION; MALE; MEMBRANE STEADY POTENTIAL; MISSENSE MUTATION; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PAIN RECEPTOR; PRESCHOOL CHILD; RAT; SENSORY NERVE CELL; SINGLE NUCLEOTIDE POLYMORPHISM; TEMPERATURE DEPENDENCE; VOLTAGE CLAMP TECHNIQUE; ANIMAL; C57BL MOUSE; GENETICS; METABOLISM; PAIN;

ANIMALS; COLD TEMPERATURE; HUMANS; MICE; MICE, INBRED C57BL; MUTATION, MISSENSE; NAV1.9 VOLTAGE-GATED SODIUM CHANNEL; PAIN;

EID: 84949570886     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10049     Document Type: Article

References (40)

1. Dib-Hajj, S. D., Cummins, T. R., Black, J. A. & Waxman, S. G. Sodium channels in normal and pathological pain. Annu. Rev. Neurosci. 33, 325-347 (2010).
2. Baker, M. D., Chandra, S. Y., Ding, Y., Waxman, S. G. & Wood, J. N. GTP-induced tetrodotoxin-resistant Na+ current regulates excitability in mouse and rat small diameter sensory neurones. J. Physiol. 548, 373-382 (2003).
3. Herzog, R. I., Cummins, T. R. & Waxman, S. G. Persistent TTX-resistant Na+ current affects resting potential and response to depolarization in simulated spinal sensory neurons. J. Neurophysiol. 86, 1351-1364 (2001).
4. Waxman, S. G. & Zamponi, G. W. Regulating excitability of peripheral afferents: emerging ion channel targets. Nat. Neurosci. 17, 153-163 (2014).
5. Bennett, D. L. & Woods, C. G. Painful and painless channelopathies. Lancet Neurol. 13, 587-599 (2014).
6. Cox, J. J. et al. An SCN9A channelopathy causes congenital inability to experience pain. Nature 444, 894-898 (2006).
7. Goldberg, Y. P. et al. Loss-of-function mutations in the Nav1.7 gene underlie congenital indifference to pain in multiple human populations. Clin. Genet. 71, 311-319 (2007).
8. Fertleman, C. R. et al. SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 52, 767-774 (2006).
9. Yang, Y. et al. Mutations in SCN9A, encoding a sodium channel alpha subunit, in patients with primary erythermalgia. J. Med. Genet. 41, 171-174 (2004).
10. Wu, M. T., Huang, P. Y., Yen, C. T., Chen, C. C. & Lee, M. J. A novel SCN9A mutation responsible for primary erythromelalgia and is resistant to the treatment of sodium channel blockers. PLoS ONE 8, e55212 (2013).
11. Han, C. et al. Temperature dependence of erythromelalgia mutation L858F in sodium channel Nav1.7. Mol. Pain 3, 3 (2007).
12. Devigili, G. et al. Paroxysmal itch caused by gain-of-function Nav1.7 mutation. Pain 155, 1702-1707 (2014).
13. Faber, C. G. et al. Gain of function NaV1.7 mutations in idiopathic small fiber neuropathy. Ann. Neurol. 71, 26-39 (2012).
14. Faber, C. G. et al. Gain-of-function Nav1.8 mutations in painful neuropathy. Proc. Natl Acad. Sci. USA 109, 19444-19449 (2012).
15. Leipold, E. et al. A de novo gain-of-function mutation in SCN11A causes loss of pain perception. Nat. Genet. 45, 1399-1404 (2013).
16. Woods, C. G., Babiker, M. O., Horrocks, I., Tolmie, J. & Kurth, I. The phenotype of congenital insensitivity to pain due to the Na1.9 variant p.L811P. Eur. J. Hum. Genet. 23, 561-563 (2015).
17. Han, C. et al. 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 (2015).
18. Huang, J. et al. Gain-of-function mutations in sodium channel Na(v)1.9 in painful neuropathy. Brain 137, 1627-1642 (2014).
19. Zhang, X. Y. et al. Gain-of-function mutations in SCN11A cause familial episodic pain. Am. J. Hum. Genet. 93, 957-966 (2013).
20. Chien, H. F. et al. Quantitative pathology of cutaneous nerve terminal degeneration in the human skin. Acta Neuropathol. 102, 455-461 (2001).
21. Redisch, W., Sheckman, E. & Stelle, J. M. Skin temperature response of normal human subjects to various conditions. Circulation 6, 862-867 (1952).
22. Shusterman, V., Anderson, K. P. & Barnea, O. Spontaneous skin temperature oscillations in normal human subjects. Am. J. Physiol. 273, R1173-R1181 (1997).
23. Rush, A. M. & Waxman, S. G. PGE2 increases the tetrodotoxin-resistant Nav1.9 sodium current in mouse DRG neurons via G-proteins. Brain Res. 1023, 264-271 (2004).
24. Ostman, J. A., Nassar, M. A., Wood, J. N. & Baker, M. D. GTP up-regulated persistent Na+ current and enhanced nociceptor excitability require NaV1.9. J. Physiol. 586, 1077-1087 (2008).
25. Cummins, T. R. et al. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J. Neurosci. 19, RC43 (1999).
26. Sato, C. et al. The voltage-sensitive sodium channel is a bell-shaped molecule with several cavities. Nature 409, 1047-1051 (2001).
27. Jiang, Y. et al. X-ray structure of a voltage-dependent K+ channel. Nature 423, 33-41 (2003).
28. Bezanilla, F. The voltage-sensor structure in a voltage-gated channel. Trends Biochem. Sci. 30, 166-168 (2005).
29. Long, S. B., Campbell, E. B. & Mackinnon, R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309, 897-903 (2005).
30. Ferrer, T., Rupp, J., Piper, D. R. & Tristani-Firouzi, M. The S4-S5 linker directly couples voltage sensor movement to the activation gate in the human ether-a'-go-go-related gene (hERG) K+ channel. J. Biol. Chem. 281, 12858-12864 (2006).
31. Lolignier, S. et al. The Nav1.9 channel is a key determinant of cold pain sensation and cold allodynia. Cell Rep. 11, 1067-1078 (2015).
32. Dib-Hajj, S. D., Tyrrell, L., Black, J. A. & Waxman, S. G. NaN a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc. Natl Acad. Sci. USA 95, 8963-8968 (1998).
33. Dib-Hajj, S., Black, J. A., Cummins, T. R. & Waxman, S. G. NaN/Nav1.9: a sodium channel with unique properties. Trends Neurosci. 25, 253-259 (2002).
34. Persson, A. K. et al. Sodium-calcium exchanger and multiple sodium channel isoforms in intra-epidermal nerve terminals. Mol. Pain 6, 84 (2010).
35. Dib-Hajj, S. D., Yang, Y., Black, J. A. & Waxman, S. G. The Na(V)1.7 sodium channel: from molecule to man. Nat. Rev. Neurosci. 14, 49-62 (2013).
36. Han, C. et al. The domain II S4-S5 linker in Nav1.9: a missense mutation enhances activation, impairs fast inactivation, and produces human painful neuropathy. Neuromolecular Med. 2, 158-169 (2015).
37. Catterall, W. A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26, 13-25 (2000).
38. Weis, J. et al. Small-fiber neuropathy in patients with ALS. Neurology 76, 2024-2029 (2011).
39. Ebenezer, G. J., Hauer, P., Gibbons, C., McArthur, J. C. & Polydefkis, M. Assessment of epidermal nerve fibers: a new diagnostic and predictive tool for peripheral neuropathies. J. Neuropathol. Exp. Neurol. 66, 1059-1073 (2007).
40. Dib-Hajj, S. D. et al. Transfection of rat or mouse neurons by biolistics or electroporation. Nat. Protoc. 4, 1118-1126 (2009).