Na v 1.9: A sodium channel linked to human pain

Nature Reviews Neuroscience

Volumn 16, Issue 9, 2015, Pages 511-519

  Dib Hajj, Sulayman D ^b   Black, Joel A ^b   Waxman, Stephen G ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHANNEL NAV1.9; SCN11A PROTEIN, HUMAN; SODIUM CHANNEL BLOCKING AGENT;

ARTICLE; CENTRAL NERVOUS SYSTEM; CONFUSION; GENE MUTATION; GENETIC ANALYSIS; GENETIC DISORDER; HUMAN; INFLAMMATORY PAIN; MUTATION; NEUROPATHIC PAIN; PAIN; PAIN RECEPTOR; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN FUNCTION; PSYCHOGENIC PAIN; SEDATION; SENSORY NERVE CELL; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

RODENTIA;

ANIMALS; HUMANS; MUTATION; NAV1.9 VOLTAGE-GATED SODIUM CHANNEL; NOCICEPTORS; PAIN; SENSORY RECEPTOR CELLS; SODIUM CHANNEL BLOCKERS;

EID: 84939773551     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3977     Document Type: Article

References (66)

1. Catterall, W. A., Goldin, A. L. & Waxman, S. G. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol. Rev. 57, 397-409 (2005).
2. V1.7 sodium channel: from molecule to man. Nat. Rev. Neurosci. 14, 49-62 (2013).
3. v1.8 mutations in painful neuropathy. Proc. Natl Acad. Sci. USA 109, 19444-19449 (2012).
4. v1.8 mutation shifts activation to hyperpolarized potentials and increases excitability of dorsal root ganglion neurons. J. Neurosci. 33, 14087-14097 (2013).
5. V1.8 mutation in small fibre neuropathy: impaired inactivation underlying DRG neuron hyperexcitability. J. Neurol. Neurosurg. Psychiatry 85, 499-505 (2014).
6. v1.9 in painful neuropathy. Brain 137, 1627-1642 (2014).
7. Leipold, E. et al. A de novo gain-of-function mutation in SCN11A causes loss of pain perception. Nat. Genet. 45, 1399-1404 (2013).
8. Zhang, X. Y. et al. Gain-of-function mutations in SCN11A cause familial episodic pain. Am. J. Hum. Genet. 93, 957-966 (2013).
9. 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).
10. 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).
11. Dib-Hajj, S. D. et al. Coding sequence, genomic organization, and conserved chromosomal localization of the mouse gene Scn11a encoding the sodium channel NaN. Genomics 59, 309-318 (1999).
12. 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).
13. V1.9 subunit in myenteric sensory neurons. J. Neurosci. 23, 2715-2725 (2003).
14. v1.9 (NaN) in nociceptive primary afferent neurons. J. Neurosci. 22, 7425-7433 (2002).
15. Fang, X. 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. 26, 7281-7292 (2006).
16. v1.9 is an effector of peripheral inflammatory pain hypersensitivity. J. Neurosci. 26, 12852-12860 (2006).
17. + current affects resting potential and response to depolarization in simulated spinal sensory neurons. J. Neurophysiol. 86, 1351-1364 (2001).
18. Braz, J. M., Nassar, M. A., Wood, J. N. & Basbaum, A. I. Parallel "pain" pathways arise from subpopulations of primary afferent nociceptor. Neuron 47, 787-793 (2005).
19. 4-positive and-negative nociceptors are functionally distinct. J. Neurosci. 19, 6497-6505 (1999).
20. V1.9 in the activation of visceral afferents by noxious inflammatory, mechanical, and human disease-derived stimuli. Pain 155, 1962-1975 (2014).
21. Santarelli, V. P., Eastwood, A. L., Dougherty, D. A., Horn, R. & Ahern, C. A. A cation-π interaction discriminates among sodium channels that are either sensitive or resistant to tetrodotoxin block. J. Biol. Chem. 282, 8044-8051 (2007).
22. 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).
23. v1.9, in mouse dorsal root ganglion neurons. Pflugers Arch. 449, 76-87 (2004).
24. V1.9 channels in enteric and spinal sensory neurons. Mol. Cell Neurosci. 26, 123-134 (2004).
25. + currents in rat trigeminal ganglion cells. Neuroscience 222, 205-214 (2012).
26. Dib-Hajj, S. D. et al. Two tetrodotoxin-resistant sodium channels in human dorsal root ganglion neurons. FEBS Lett. 462, 117-120 (1999).
27. V1.9 to sensory transmission and nociceptive behavior. Proc. Natl Acad. Sci. USA 102, 9382-9387 (2005).
28. V1.9. J. Physiol. 586, 1077-1087 (2007).
29. + current regulates excitability in mouse and rat small diameter sensory neurones. J. Physiol. 548, 373-382 (2003).
30. V1.7 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 (2006).
31. V1.7 and erythromelalgia mutant channel L858H. J. Neurophysiol. 111, 1429-1443 (2014).
32. v1.9 current in enteric neurons. J. Physiol. 587, 1461-1479 (2009).
33. Osorio, N., Korogod, S. & Delmas, P. Specialized functions of Nav1.5 and Nav1.9 channels in electrogenesis of myenteric neurons in intact mouse ganglia. J. Neurosci. 34, 5233-5244 (2014).
34. 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).
35. Qiu, F., Jiang, Y., Zhang, H., Liu, Y. & Mi, W. Increased expression of tetrodotoxin-resistant sodium channels Nav1.8 and Nav1.9 within dorsal root ganglia in a rat model of bone cancer pain. Neurosci. Lett. 512, 61-66 (2012).
36. Petho, G. & Reeh, P. W. Sensory and signaling mechanisms of bradykinin, eicosanoids, platelet-activating factor, and nitric oxide in peripheral nociceptors. Physiol. Rev. 92, 1699-1775 (2012).
37. v1.9 sodium current in mouse DRG neurons via G-proteins. Brain Res. 1023, 264-271 (2004).
38. Binshtok, A. M. et al. Nociceptors are interleukin-1β sensors. J. Neurosci. 28, 14062-14073 (2008).
39. Maingret, F. et al. Inflammatory mediators increase Nav1.9 current and excitability in nociceptors through a coincident detection mechanism. J. Gen. Physiol. 131, 211-225 (2008).
40. Mogil, J. S. Animal models of pain: progress and challenges. Nat. Rev. Neurosci. 10, 283-294 (2009).
41. Dib-Hajj, S. D. & Waxman, S. G. Translational pain research: lessons from genetics and genomics. Sci. Transl Med. 6, 249sr244 (2014).
42. Black, J. A. & Waxman, S. G. Molecular identities of two tetrodotoxin-resistant sodium channels in corneal axons. Exp. Eye Res. 75, 193-199 (2002).
43. Padilla, F. et al. Expression and localization of the Nav1.9 sodium channel in enteric neurons and in trigeminal sensory endings: Implication for intestinal reflex function and orofacial pain. Mol. Cell Neurosci. 35, 138-152 (2007).
44. Belmonte, C. & Gallar, J. Cold thermoreceptors, unexpected players in tear production and ocular dryness sensations. Invest. Ophthalmol. Vis. Sci. 52, 3888-3892 (2011).
45. Rosenthal, P. & Borsook, D. The corneal pain system. Part I: the missing piece of the dry eye puzzle. Ocul. Surf. 10, 2-14 (2012).
46. Dib-Hajj, S. D. et al. Transfection of rat or mouse neurons by biolistics or electroporation. Nat. Protoc. 4, 1118-1126 (2009).
47. Waxman, S. G. et al. Sodium channel genes in pain-related disorders: phenotype-genotype associations and recommendations for clinical use. Lancet Neurol. 13, 1152-1160 (2014).
48. V1.7 mutations in idiopathic small fiber neuropathy. Ann. Neurol. 71, 26-39 (2012).
49. Han, C. et al. 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 (2012).
50. Rush, A. M. et al. A single sodium channel mutation produces hyper-or hypoexcitability in different types of neurons. Proc. Natl Acad. Sci. USA 103, 8245-8250 (2006).
51. V1.8 expression is not restricted to nociceptors in mouse peripheral nervous system. Pain 153, 2017-2030 (2012).
52. Waxman, S. G., Black, J. A., Kocsis, J. D. & Ritchie, J. M. Low density of sodium channels supports action potential conduction in axons of neonatal rat optic nerve. Proc. Natl Acad. Sci. USA 86, 1406-1410 (1989).
53. Donnelly, D. F. Spontaneous action potential generation due to persistent sodium channel currents in simulated carotid body afferent fibers. J. Appl. Physiol. 104, 1394-1401 (2008).
54. 2+ exchanger. J. Neurosci. 12, 430-439 (1992).
55. V1.7 variant I228M impairs integrity of dorsal root ganglion neuron axons. Ann. Neurol. 73, 140-145 (2012).
56. Swadlow, H. A. & Waxman, S. G. Observations on impulse conduction along central axons. Proc. Natl Acad. Sci. USA 72, 5156-5159 (1975).
57. Chambers, S. M. et al. Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nat. Biotechnol. 30, 715-720 (2012).
58. Young, G. T. et al. Characterizing human stem cell-derived sensory neurons at the single-cell level reveals their ion channel expression and utility in pain research. Mol. Ther. 22, 1530-1543 (2014).
59. Blanchard, J. W. et al. Selective conversion of fibroblasts into peripheral sensory neurons. Nat. Neurosci. 18, 25-35 (2015).
60. Wainger, B. J. et al. Modeling pain in vitro using nociceptor neurons reprogrammed from fibroblasts. Nat. Neurosci. 18, 17-24 (2015).
61. Baker, M. Gene editing at CRISPR speed. Nat. Biotechnol. 32, 309-312 (2014).
62. McCormack, K. et al. Voltage sensor interaction site for selective small molecule inhibitors of voltage-gated sodium channels. Proc. Natl Acad. Sci. USA 11 0, E2724-E2732 (2013).
63. V1.7 channel voltage sensor for pain and itch relief. Cell 157, 1393-1404 (2014).
64. Black, J. A., Vasylyev, D., Dib-Hajj, S. D. & Waxman, S. G. Nav1.9 expression inmagnocellular neurosecretory cells of supraoptic nucleus. Exp. Neurol. 253, 174-179 (2014).
65. Basbaum, A. I., Bautista, D. M., Scherrer, G. & Julius, D. Cellular and molecular mechanisms of pain. Cell 139, 267-284 (2009).
66. Woolf, C. J. & Ma, Q. Nociceptors - noxious stimulus detectors. Neuron 55, 353-364 (2007).