A gain-of-function voltage-gated sodium channel 1.8 mutation drives intense hyperexcitability of A- and C-fiber neurons

Pain

Volumn 155, Issue 5, 2014, Pages 896-905

  Garrison, Sheldon R ^a   Weyer, Andy D ^a   Barabas, Marie E ^a   Beutler, Bruce A ^b   Stucky, Cheryl L ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Gain of function; Inflammatory pain; Mechanical hyperalgesia; Neuropathic pain; Scn10a; Spontaneous activity

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL; CALCIUM; SCN10A PROTEIN, MOUSE; SODIUM CHANNEL NAV1.8;

ACOUSTIC NERVE FIBER; ANIMAL EXPERIMENT; ARTICLE; EVOKED RESPONSE; GAIN OF FUNCTION MUTATION; MALE; MECHANICAL STIMULATION; MOUSE; NERVE EXCITABILITY; NERVE FIBER; NERVE FIBER C; NONHUMAN; PAIN RECEPTOR; PATCH CLAMP TECHNIQUE; POINT MUTATION; PRIORITY JOURNAL; SENSORY NERVE CELL; ACTION POTENTIAL; ANIMAL; ANIMAL BEHAVIOR; GENETICS; METABOLISM; MYELINATED NERVE; NONMYELINATED NERVE; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSIOLOGY; STIMULATION; TRANSGENIC MOUSE;

ACTION POTENTIALS; ANIMALS; AXONS; BEHAVIOR, ANIMAL; CALCIUM; MICE; MICE, TRANSGENIC; NAV1.8 VOLTAGE-GATED SODIUM CHANNEL; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED; PAIN MEASUREMENT; PAIN THRESHOLD; PATCH-CLAMP TECHNIQUES; PHYSICAL STIMULATION; POINT MUTATION;

EID: 84898597785     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.01.012     Document Type: Article

References (51)

1. A.N. Akopian, V. Souslova, S. England, K. Okuse, N. Ogata, J. Ure, A. Smith, B.J. Kerr, S.B. McMahon, S. Boyce, R. Hill, L.C. Stanfa, A.H. Dickenson, and J.N. Wood The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways Nat Neurosci 2 1999 541 548 (Pubitemid 30491235)
2. F. Amaya, I. Decosterd, T.A. Samad, C. Plumpton, S. Tate, R.J. Mannion, M. Costigan, and C.J. Woolf Diversity of expression of the sensory neuron-specific TTX-resistant voltage-gated sodium ion channels SNS and SNS2 Mol Cell Neurosci 15 2000 331 342 (Pubitemid 30266270)
3. M.E. Barabas, E.A. Kossyreva, and C.L. Stucky TRPA1 is functionally expressed primarily by IB4-binding, non-peptidergic mouse and rat sensory neurons PLoS One 7 2012 e47988
4. J.A. Black, S. Liu, M. Tanaka, T.R. Cummins, and S.G. Waxman Changes in the expression of tetrodotoxin-sensitive sodium channels within dorsal root ganglia neurons in inflammatory pain PAIN® 108 2004 237 247 (Pubitemid 38353046)
5. C. Bladen, and G.W. Zamponi Common mechanisms of drug interactions with sodium and T-type calcium channels Mol Pharmacol 82 2012 481 487
6. N.T. Blair, and B.P. Bean Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTX-resistant Na+ current, and Ca2+ current in the action potentials of nociceptive sensory neurons J Neurosci 22 2002 10277 10290 (Pubitemid 35416866)
7. A.L. Blasius, A.E. Dubin, M.J. Petrus, B.K. Lim, A. Narezkina, J.R. Criado, D.N. Wills, Y. Xia, E.M. Moresco, C. Ehlers, K.U. Knowlton, A. Patapoutian, and B. Beutler Hypermorphic mutation of the voltage-gated sodium channel encoding gene Scn10a causes a dramatic stimulus-dependent neurobehavioral phenotype Proc Natl Acad Sci USA 108 2011 19413 19418
8. S.M. Brierley, J. Castro, A.M. Harrington, P.A. Hughes, A.J. Page, G.Y. Rychkov, and L.A. Blackshaw TRPA1 contributes to specific mechanically activated currents and sensory neuron mechanical hypersensitivity J Physiol 589 2011 3575 3593
9. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, and T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J Neurosci Methods 53 1994 55 63 (Pubitemid 24238751)
10. J.S. Choi, S.D. Dib-Hajj, and S.G. Waxman Differential slow inactivation and use-dependent inhibition of Nav1.8 channels contribute to distinct firing properties in IB4+ and IB4- DRG neurons J Neurophysiol 97 2007 1258 1265 (Pubitemid 46239503)
11. T.R. Cummins, S.D. Dib-Hajj, and S.G. Waxman Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy J Neurosci 24 2004 8232 8236 (Pubitemid 39280802)
12. I. Daou, A.H. Tuttle, G. Longo, J.S. Wieskopf, R.P. Bonin, A.R. Ase, J.N. Wood, Y. De Koninck, A. Ribeiro-da-Silva, J.S. Mogil, and P. Seguela Remote optogenetic activation and sensitization of pain pathways in freely moving mice J Neurosci 33 2013 18631 18640
13. M. De Felice, R. Sanoja, R. Wang, L. Vera-Portocarrero, J. Oyarzo, T. King, M.H. Ossipov, T.W. Vanderah, J. Lai, G.O. Dussor, H.L. Fields, T.J. Price, and F. Porreca Engagement of descending inhibition from the rostral ventromedial medulla protects against chronic neuropathic pain PAIN® 152 2011 2701 2709
14. S.D. Dib-Hajj, A.M. Rush, T.R. Cummins, F.M. Hisama, S. Novella, L. Tyrrell, L. Marshall, and S.G. Waxman Gain-of-function mutation in Nav1.7 in familial erythromelalgia induces bursting of sensory neurons Brain 128 2005 1847 1854 (Pubitemid 41373656)
15. S. Dirajlal, L.E. Pauers, and C.L. Stucky Differential response properties of IB(4)-positive and -negative unmyelinated sensory neurons to protons and capsaicin J Neurophysiol 89 2003 513 524 (Pubitemid 36134040)
16. W.J. Dixon Efficient analysis of experimental observations Annu Rev Pharmacol Toxicol 20 1980 441 462
17. L. Djouhri, X. Fang, K. Okuse, J.N. Wood, C.M. Berry, and S.N. Lawson The TTX-resistant sodium channel Nav1.8 (SNS/PN3): expression and correlation with membrane properties in rat nociceptive primary afferent neurons J Physiol 550 2003 739 752 (Pubitemid 37010060)
18. L. Djouhri, and S.N. Lawson Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals Brain Res Brain Res Rev 46 2004 131 145 (Pubitemid 39298861)
19. C.G. Faber, G. Lauria, I.S. Merkies, X. Cheng, C. Han, H.S. Ahn, A.K. Persson, J.G. Hoeijmakers, M.M. Gerrits, T. Pierro, R. Lombardi, D. Kapetis, S.D. Dib-Hajj, and S.G. Waxman Gain-of-function Nav1.8 mutations in painful neuropathy Proc Natl Acad Sci USA 109 2012 19444 19449
20. C.R. Fertleman, M.D. Baker, K.A. Parker, S. Moffatt, F.V. Elmslie, B. Abrahamsen, J. Ostman, N. Klugbauer, J.N. Wood, R.M. Gardiner, and M. Rees SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes Neuron 52 2006 767 774 (Pubitemid 44828442)
21. T. Fukuoka, K. Kobayashi, H. Yamanaka, K. Obata, Y. Dai, and K. Noguchi Comparative study of the distribution of the alpha-subunits of voltage-gated sodium channels in normal and axotomized rat dorsal root ganglion neurons J Comp Neurol 510 2008 188 206
22. T. Fukuoka, and K. Noguchi Comparative study of voltage-gated sodium channel alpha-subunits in non-overlapping four neuronal populations in the rat dorsal root ganglion Neurosci Res 70 2011 164 171
23. L.S. Gilchrist, D.M. Cain, C. Harding-Rose, A.N. Kov, G. Wendelschafer-Crabb, W.R. Kennedy, and D.A. Simone Re-organization of P2X3 receptor localization on epidermal nerve fibers in a murine model of cancer pain Brain Res 1044 2005 197 205 (Pubitemid 40693452)
24. Q. Hogan, D. Sapunar, K. Modric-Jednacak, and J.B. McCallum Detection of neuropathic pain in a rat model of peripheral nerve injury Anesthesiology 101 2004 476 487 (Pubitemid 38988505)
25. J. Huang, Y. Yang, P. Zhao, M.M. Gerrits, J.G. Hoeijmakers, K. Bekelaar, I.S. Merkies, C.G. Faber, S.D. Dib-Hajj, and S.G. Waxman Small-fiber neuropathy Nav1.8 mutation shifts activation to hyperpolarized potentials and increases excitability of dorsal root ganglion neurons J Neurosci 33 2013 14087 14097
26. A. Iggo, and K.H. Andres Morphology of cutaneous receptors Annu Rev Neurosci 5 1982 1 31
27. M.F. Jarvis, P. Honore, C.C. Shieh, M. Chapman, S. Joshi, X.F. Zhang, M. Kort, W. Carroll, B. Marron, R. Atkinson, J. Thomas, D. Liu, M. Krambis, Y. Liu, S. McGaraughty, K. Chu, R. Roeloffs, C. Zhong, J.P. Mikusa, G. Hernandez, D. Gauvin, C. Wade, C. Zhu, M. Pai, M. Scanio, L. Shi, I. Drizin, R. Gregg, M. Matulenko, A. Hakeem, M. Gross, M. Johnson, K. Marsh, P.K. Wagoner, J.P. Sullivan, C.R. Faltynek, and D.S. Krafte A-803467, a potent and selective Nav1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat Proc Natl Acad Sci USA 104 2007 8520 8525 (Pubitemid 47175520)
28. K.O. Johnson The roles and functions of cutaneous mechanoreceptors Curr Opin Neurobiol 11 2001 455 461 (Pubitemid 32739172)
29. S.E. Jordt, D.M. Bautista, H.H. Chuang, D.D. McKemy, P.M. Zygmunt, E.D. Hogestatt, I.D. Meng, and D. Julius Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1 Nature 427 2004 260 265 (Pubitemid 38112043)
30. S.K. Joshi, J.P. Mikusa, G. Hernandez, S. Baker, C.C. Shieh, T. Neelands, X.F. Zhang, W. Niforatos, K. Kage, P. Han, D. Krafte, C. Faltynek, J.P. Sullivan, M.F. Jarvis, and P. Honore Involvement of the TTX-resistant sodium channel Nav 1.8 in inflammatory and neuropathic, but not post-operative, pain states PAIN® 123 2006 75 82 (Pubitemid 43816759)
31. S. Kelly, and V. Chapman Selective cannabinoid CB1 receptor activation inhibits spinal nociceptive transmission in vivo J Neurophysiol 86 2001 3061 3064 (Pubitemid 33139072)
32. M. Koltzenburg, and G.R. Lewin Receptive properties of embryonic chick sensory neurons innervating skin J Neurophysiol 78 1997 2560 2568 (Pubitemid 27495481)
33. Kral MG, Xiong Z, Study RE Alteration of Na+ currents in dorsal root ganglion neurons from rats with a painful neuropathy PAIN® 81 1999 15 24
34. K.Y. Kwan, J.M. Glazer, D.P. Corey, F.L. Rice, and C.L. Stucky TRPA1 modulates mechanotransduction in cutaneous sensory neurons J Neurosci 29 2009 4808 4819
35. L. Li, M. Rutlin, V.E. Abraira, C. Cassidy, L. Kus, S. Gong, M.P. Jankowski, W. Luo, N. Heintz, H.R. Koerber, C.J. Woodbury, and D.D. Ginty The functional organization of cutaneous low-threshold mechanosensory neurons Cell 147 2011 1615 1627
36. C.N. Liu, M. Devor, S.G. Waxman, and J.D. Kocsis Subthreshold oscillations induced by spinal nerve injury in dissociated muscle and cutaneous afferents of mouse DRG J Neurophysiol 87 2002 2009 2017 (Pubitemid 34670763)
37. M. Liu, and J.N. Wood The roles of sodium channels in nociception: implications for mechanisms of neuropathic pain Pain Med 12 2013 S93 S99
38. S.L. McIlwrath, J.J. Lawson, C.E. Anderson, K.M. Albers, and H.R. Koerber Overexpression of neurotrophin-3 enhances the mechanical response properties of slowly adapting type 1 afferents and myelinated nociceptors Eur J Neurosci 26 2007 1801 1812 (Pubitemid 47493204)
39. D.C. Molliver, D.E. Wright, M.L. Leitner, A.S. Parsadanian, K. Doster, D. Wen, Q. Yan, and W.D. Snider IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life Neuron 19 1997 849 861 (Pubitemid 27471389)
40. B.L. Munger, and C. Ide The structure and function of cutaneous sensory receptors Arch Histol Cytol 51 1988 1 34
41. Ramachandra R, McGrew SY, Baxter JC, Howard JR, Elmslie KS. NaV1.8 channels are expressed in large, as well as small, diameter sensory afferent neurons. Channels (Austin) 2013;7:34-7.
42. P.W. Reeh Sensory receptors in a mammalian skin-nerve in vitro preparation Prog Brain Res 74 1988 271 276
43. M. Renganathan, T.R. Cummins, and S.G. Waxman Contribution of Na(v)1.8 sodium channels to action potential electrogenesis in DRG neurons J Neurophysiol 86 2001 629 640 (Pubitemid 32738555)
44. S.D. Shields, H.S. Ahn, Y. Yang, C. Han, R.P. Seal, J.N. Wood, S.G. Waxman, and S.D. Dib-Hajj Nav1.8 expression is not restricted to nociceptors in mouse peripheral nervous system PAIN® 153 2012 2017 2030
45. S.D. Shields, X. Cheng, A. Gasser, C.Y. Saab, L. Tyrrell, E.M. Eastman, M. Iwata, P.J. Zwinger, J.A. Black, S.D. Dib-Hajj, and S.G. Waxman A channelopathy contributes to cerebellar dysfunction in a model of multiple sclerosis Ann Neurol 71 2012 186 194
46. A.J. Stone, J.S. Kim, K. Yamauchi, V. Ruiz-Velasco, and M.P. Kaufman Attenuation of autonomic reflexes by A803467 may not be solely caused by blockade of NaV 1.8 channels Neurosci Lett 543 2013 177182
47. Study RE, Kral MG Spontaneous action potential activity in isolated dorsal root ganglion neurons from rats with a painful neuropathy PAIN® 65 1996 235 242
48. P.W. Wacnik, L.J. Eikmeier, T.R. Ruggles, M.L. Ramnaraine, B.K. Walcheck, A.J. Beitz, and G.L. Wilcox Functional interactions between tumor and peripheral nerve: morphology, algogen identification, and behavioral characterization of a new murine model of cancer pain J Neurosci 21 2001 9355 9366 (Pubitemid 33096879)
49. Q. Wu, and J.L. Henry Delayed onset of changes in soma action potential genesis in nociceptive A-beta DRG neurons in vivo in a rat model of osteoarthritis Mol Pain 5 2009 57
50. Q. Wu, and J.L. Henry Changes in Abeta non-nociceptive primary sensory neurons in a rat model of osteoarthritis pain Mol Pain 6 2010 37
51. J.M. Zhang, D.F. Donnelly, X.J. Song, and R.H. Lamotte Axotomy increases the excitability of dorsal root ganglion cells with unmyelinated axons J Neurophysiol 78 1997 2790 2794 (Pubitemid 27495502)