Sensory neuron downregulation of the Kv9.1 potassium channel subunit mediates neuropathic pain following nerve injury

Journal of Neuroscience

Volumn 32, Issue 48, 2012, Pages 17502-17513

  Tsantoulas, Christoforos ^a   Zhu, Lan ^a   Shaifta, Yasin ^b   Grist, John ^a   Ward, Jeremy P T ^b   Raouf, Ramin ^a   Michael, Gregory J ^c   McMahon, Stephen B ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; POTASSIUM; POTASSIUM CHANNEL KV9.1; SHAB POTASSIUM CHANNEL; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

AFFERENT NERVE GROUP 1; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EVOKED RESPONSE; FLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTRACELLULAR RECORDING; MALE; MYELINATED NERVE; NERVE EXCITABILITY; NERVE FIBER C; NERVE FIBER TRANSECTION; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; SPIKE WAVE; SPINAL GANGLION;

ANIMALS; AXOTOMY; BEHAVIOR, ANIMAL; DOWN-REGULATION; HYPERALGESIA; MALE; NERVE FIBERS, MYELINATED; NEURALGIA; PAIN MEASUREMENT; PERIPHERAL NERVE INJURIES; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; RATS, WISTAR; RNA, SMALL INTERFERING; SENSORY RECEPTOR CELLS;

EID: 84870233117     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3561-12.2012     Document Type: Article

References (68)

1. + and K+ channel currents of rat dorsal root ganglion neurons. J Neurophysiol 85:644-658.
2. Amir R, Argoff CE, Bennett GJ, Cummins TR, Durieux ME, Gerner P, Gold MS, Porreca F, Strichartz GR (2006) The role of sodium channels in chronic inflammatory and neuropathic pain. J Pain 7:S1-S29.
3. Baron R (2009) Neuropathic pain: a clinical perspective. Handb Exp Pharmacol 194:3-30.
4. Bennett GJ, Chung JM, Honore M, Seltzer Z (2003) Models of neuropathic pain in the rat. Curr Protoc Neurosci Chapter 9:Unit 9.14.
5. Bocksteins E, Raes AL, van de Vijver G, Bruyns T, Van Bogaert PP, Snyders DJ (2009) Kv2.1 and silent Kv subunits underlie the delayed rectifier K+ current in cultured small mouse DRG neurons. Am J Physiol Cell Physiol 296:C1271-1278.
6. Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB (2000) Potent analgesic effects of GDNF in neuropathic pain states. Science 290:124-127.
7. Calvo M, Zhu N, Tsantoulas C, Ma Z, Grist J, Loeb JA, Bennett DL (2010) Neuregulin-ErbB signaling promotes microglial proliferation and che-motaxis contributing to microgliosis and pain after peripheral nerve injury. J Neurosci 30:5437-5450.
8. Campbell JN, Raja SN, Meyer RA, Mackinnon SE (1988) Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32:89-94.
9. Campero M, Serra J, Marchettini P, Ochoa JL (1998) Ectopic impulse generation and autoexcitation in single myelinated afferent fibers in patients with peripheral neuropathy and positive sensory symptoms. Muscle Nerve 21:1661-1667.
10. Cerda O, Trimmer JS (2011) Activity-dependent phosphorylation of neuronal Kv2.1 potassium channels by CDK5. J Biol Chem 286:28738-28748.
11. Chien LY, Cheng JK, Chu D, Cheng CF, Tsaur ML (2007) Reduced expression of A-type potassium channels in primary sensory neurons induces mechanical hypersensitivity. J Neurosci 27:9855-9865.
12. Costigan M, et al. (2010) Multiple chronic pain states are associated with a common amino acid-changing allele in KCNS1. Brain 133:2519-2527.
13. Cox JJ, Reimann F, Nicholas AK, Thornton G, Roberts E, Springell K, Karbani G, Jafri H, Mannan J, Raashid Y, Al-Gazali L, Hamamy H, Valente EM, Gorman S, Williams R, McHale DP, Wood JN, Gribble FM, Woods CG (2006) An SCN9A channelopathy causes congenital inability to experience pain. Nature 444:894-898.
14. Cregg R, Momin A, Rugiero F, Wood JN, Zhao J (2010) Pain channelopa-thies. J Physiol 588:1897-1904.
15. Devor M, Wall PD (1990) Cross-excitation in dorsal root ganglia of nerve-injured and intact rats. J Neurophysiol 64:1733-1746.
16. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG (2010) Sodium channels in normal and pathological pain. Annu Rev Neurosci 33:325-347.
17. Djouhri L, Lawson SN (2004) 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 46:131-145.
18. Dussor GO, Price TJ, Flores CM (2003) Activating transcription factor 3 mRNA is upregulated in primary cultures of trigeminal ganglion neurons. Brain Res Mol Brain Res 118:156-159.
19. Emery EC, Young GT, Berrocoso EM, Chen L, McNaughton PA (2011) HCN2 ion channels play a central role in inflammatory and neuropathic pain. Science 333:1462-1466.
20. Fantozzi I, Platoshyn O, Wong AH, Zhang S, Remillard CV, Furtado MR, Petrauskene OV, Yuan JX (2006) Bone morphogenetic protein-2 up-regulates expression and function of voltage-gated K+ channels in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 291:L993-1004.
21. Flake NM, Lancaster E, Weinreich D, Gold MS (2004) Absence of an association between axotomy-induced changes in sodium currents and excitability in DRG neurons from the adult rat. Pain 109:471-480.
22. Fricker FR, Zhu N, Tsantoulas C, Abrahamsen B, Nassar MA, Thakur M, Garratt AN, Birchmeier C, McMahon SB, Wood JN, Bennett DL (2009) Sensory axon-derived neuregulin-1 is required for axoglial signaling and normal sensory function but not for long-term axon maintenance. J Neu-rosci 29:7667-7678.
23. Gracely RH, Lynch SA, Bennett GJ (1992) Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 51:175-194.
24. Haanpaä M, Attal N, Backonja M, Baron R, Bennett M, Bouhassira D, Cruccu G, Hansson P, Haythornthwaite JA, Iannetti GD, Jensen TS, Kauppila T, Nurmikko TJ, Rice AS, Rowbotham M, Serra J, Sommer C, Smith BH, Treede RD (2011) NeuPSIG guidelines on neuropathic pain assessment. Pain 152:14-27.
25. Han HC, Lee DH, Chung JM (2000) Characteristics of ectopic discharges in a rat neuropathic pain model. Pain 84:253-261.
26. Ishikawa K, Tanaka M, Black JA, Waxman SG (1999) Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 22:502-507.
27. Kajander KC, Bennett GJ (1992) Onset of a painful peripheral neuropathy in rat: a partial and differential deafferentation and spontaneous discharge in A beta and A delta primary afferent neurons. J Neurophysiol 68:734-744.
28. Kerschensteiner D, Soto F, Stocker M (2005) Fluorescence measurements reveal stoichiometry of K+ channels formed by modulatory and delayed rectifier alpha-subunits. Proc Natl Acad Sci USA 102:6160-6165.
29. Khasar SG, Gold MS, Levine JD (1998) A tetrodotoxin-resistant sodium current mediates inflammatory pain in the rat. Neurosci Lett 256:17-20.
30. Knock GA, Snetkov VA, Shaifta Y, Drndarski S, Ward JP, Aaronson PI (2008a) Role of src-family kinases in hypoxic vasoconstriction of rat pulmonary artery. Cardiovasc Res 80:453-462.
31. Knock GA, Shaifta Y, Snetkov VA, Vowles B, Drndarski S, Ward JP, Aaronson PI (2008b) Interaction between src family kinases and rho-kinase in agonist-induced Ca2 + -sensitization of rat pulmonary artery. Cardiovasc Res 77:570-579.
32. LaCroix-Fralish ML, Austin JS, Zheng FY, Levitin DJ, Mogil JS (2011) Patterns of pain: meta-analysis ofmicroarray studies of pain. Pain 152:1888-1898.
33. Liu CN, Wall PD, Ben-Dor E, Michaelis M, Amir R, Devor M (2000) Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 85:503-521.
34. Luo MC, Zhang DQ, Ma SW, Huang YY, Shuster SJ, Porreca F, Lai J (2005) An efficient intrathecal delivery of small interfering RNA to the spinal cord and peripheral neurons. Mol Pain 1:29.
35. Ma C, Shu Y, Zheng Z, Chen Y, Yao H, Greenquist KW, White FA, LaMotte RH (2003) Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J Neurophysiol 89: 1588-1602.
36. Maratou K, Wallace VC, Hasnie FS, Okuse K, Hosseini R, Jina N, Blackbeard J, Pheby T, Orengo C, Dickenson AH, McMahon SB, Rice AS (2009) Comparison of dorsal root ganglion gene expression in rat models of traumatic and HIV-associated neuropathic pain. Eur J Pain 13:387-398.
37. Marchand F, Tsantoulas C, Singh D, Grist J, Clark AK, Bradbury EJ, McMahon SB (2009) Effects of Etanercept and Minocycline in a rat model of spinal cord injury. Eur J Pain 13:673-681.
38. Michael GJ, Averill S, Nitkunan A, Rattray M, Bennett DL, Yan Q, Priestley JV (1997) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J Neurosci 17: 8476-8490.
39. Michael GJ, Averill S, Shortland PJ, Yan Q, Priestley JV (1999) Axotomy results in major changes in BDNF expression by dorsal root ganglion cells: BDNF expression in large trkB and trkC cells, in pericellular baskets, and in projections to deep dorsal horn and dorsal column nuclei. Eur J Neurosci 11:3539-3551.
40. Michaelis M, Liu X, Janig W (2000) Axotomized and intact muscle afferents but no skin afferents develop ongoing discharges of dorsal root ganglion origin after peripheral nerve lesion. J Neurosci 20:2742-2748.
41. Misonou H, Mohapatra DP, Park EW, Leung V, Zhen D, Misonou K, Anderson AE, Trimmer JS (2004) Regulation of ion channel localization and phosphorylation by neuronal activity. Nat Neurosci 7:711-718.
42. Molander C, Hongpaisan J, Persson JK (1994) Distribution of c-fos expressing dorsal horn neurons after electrical stimulation of low threshold sensory fibers in the chronically injured sciatic nerve. Brain Res 644:74-82.
43. Murakoshi H, Trimmer JS (1999) Identification of the Kv2.1 K+ channel as a major component of the delayed rectifier K+ current in rat hippocam-pal neurons. J Neurosci 19:1728-1735.
44. Nassar MA, Levato A, Stirling LC, Wood JN (2005) Neuropathic pain develops normally in mice lacking both Na(v)1.7 and Na(v)1.8. Mol Pain 1:24.
45. Nassar MA, Baker MD, Levato A, Ingram R, Mallucci G, McMahon SB, Wood JN (2006) Nerve injury induces robust allodynia and ectopic discharges in Nav1.3 null mutant mice. Mol Pain 2:33.
46. Neumann S, Doubell TP, Leslie T, Woolf CJ (1996) Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature 384:360-364.
47. Nicoll RA (1979) Dorsal root potentials and changes in extracellular potassium in the spinal cord of the frog. J Physiol 290:113-127.
48. Noguchi K, Dubner R, De Leon M, Senba E, Ruda MA (1994) Axotomy induces preprotachykinin gene expression in a subpopulation of dorsal root ganglion neurons. J Neurosci Res 37:596-603.
49. O'Connor AB, Dworkin RH (2009) Treatment of neuropathic pain: an overview of recent guidelines. Am J Med 122:S22-S32.
50. Ossipov MH, Bian D, Malan TP Jr, Lai J, Porreca F (1999) Lack of involvement of capsaicin-sensitive primary afferents in nerve-ligation injury induced tactile allodynia in rats. Pain 79:127-133.
51. Pongs O, Schwarz JR (2010) Ancillary subunits associated with voltage-dependent K+ channels. Physiol Rev 90:755-796.
52. Richardson FC, Kaczmarek LK (2000) Modification of delayed rectifier potassium currents by the Kv9.1 potassium channel subunit. Hear Res 147: 21-30.
53. Salinas M, Duprat F, Heurteaux C, Hugnot JP, Lazdunski M (1997) New modulatory alpha subunits for mammalian Shab K+ channels. J Biol Chem 272:24371-24379.
54. Sapunar D, Ljubkovic M, Lirk P, McCallum JB, Hogan QH (2005) Distinct membrane effects of spinal nerve ligation on injured and adjacent dorsal root ganglion neurons in rats. Anesthesiology 103:360-376.
55. Sheen K, Chung JM (1993) Signs of neuropathic pain depend on signals from injured nerve fibers in a rat model. Brain Res 610:62-68.
56. Shortland PJ, Baytug B, Krzyzanowska A, McMahon SB, Priestley JV, Averill S (2006) ATF3 expression in L4 dorsal root ganglion neurons after L5 spinal nerve transection. Eur J Neurosci 23:365-373.
57. Stocker M, Kerschensteiner D (1998) Cloning and tissue distribution of two new potassium channel alpha-subunits from rat brain. Biochem Biophys Res Commun 248:927-934.
58. Sukhotinsky I, Ben-Dor E, Raber P, Devor M (2004) Key role of the dorsal root ganglion in neuropathic tactile hypersensibility. Eur J Pain 8:135-143.
59. Svoboda J, Motin V, Hajek I, Sykov A E (1988) Increase in extracellular potassium level in rat spinal dorsal horn induced by noxious stimulation and peripheral injury. Brain Res 458:97-105.
60. Sykova E, Vyklicky L (1977) Changes of extracellular potassium activity in isolated spinal cord of frog under high Mg(2 +) concentration. Neurosci Lett 4:161-165.
61. Torebjork HE, Lundberg LE, LaMotte RH (1992) Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J Physiol 448:765-780.
62. Utzschneider D, Kocsis J, Devor M (1992) Mutual excitation among dorsal root ganglion neurons in the rat. Neurosci Lett 146:53-56.
63. Vacher H, Yang JW, Cerda O, Autillo-Touati A, Dargent B, Trimmer JS (2011) Cdk-mediated phosphorylation of the Kvbeta2 auxiliary subunit regulates Kv1 channel axonal targeting. J Cell Biol 192:813-824.
64. Walters A (1959) The differentiation of causalgia and hyperpathia. Can Med Assoc J 80:105-109.
65. Wang H, Dai Y, Fukuoka T, Yamanaka H, Obata K, Tokunaga A, Noguchi K (2004) Enhancement of stimulation-induced ERK activation in the spi-nal dorsal horn and gracile nucleus neurons in rats with peripheral nerve injury. Eur J Neurosci 19:884-890.
66. Wong LF, Yip PK, Battaglia A, Grist J, Corcoran J, Maden M, Azzouz M, Kingsman SM, Kingsman AJ, Mazarakis ND, McMahon SB (2006) Reti-noic acid receptor beta2 promotes functional regeneration of sensory axons in the spinal cord. Nat Neurosci 9:243-250.
67. Yoon YW, Na HS, Chung JM (1996) Contributions of injured and intact afferents to neuropathic pain in an experimental rat model. Pain 64:27-36.
68. Ziegler EA, Magerl W, Meyer RA, Treede RD (1999) Secondary hyperalgesia to punctate mechanical stimuli. Central sensitization to A-fibre nocicep-tor input. Brain 122:2245-2257.