Retigabine reduces the excitability of unmyelinated peripheral human axons

Neuropharmacology

Volumn 54, Issue 8, 2008, Pages 1271-1278

  Lang, P M ^a   Fleckenstein, J ^a   Passmore, G M ^b   Brown, D A ^b   Grafe, P ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Axonal excitability; Electrophysiology; Human C fiber; KCNQ; Kv7; M channel; Neuronal potassium channel activator; Neuropathic pain; Nociception; Retigabine; Threshold tracking

Indexed keywords

10,10 BIS(4 PYRIDINYLMETHYL) 9(10H) ANTHRACENONE; POTASSIUM; RETIGABINE;

ACTION POTENTIAL; ADULT; AGED; ARTICLE; DRUG EFFECT; EXCITABILITY; FEMALE; HUMAN; MALE; MEMBRANE CONDUCTANCE; MEMBRANE DEPOLARIZATION; NERVE FIBER C; NEUROPATHIC PAIN; NONMYELINATED NERVE; PRIORITY JOURNAL;

ACTION POTENTIALS; AGED; AGED, 80 AND OVER; ANTHRACENES; ANTICONVULSANTS; AXONS; CARBAMATES; ELECTROPHYSIOLOGY; FEMALE; HUMANS; MALE; MIDDLE AGED; NERVE FIBERS, UNMYELINATED; PATCH-CLAMP TECHNIQUES; PERIPHERAL NERVES; PHENYLENEDIAMINES; SURAL NERVE; TACHYPHYLAXIS;

EID: 43949085016     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2008.04.006     Document Type: Article

References (51)

1. Ali Z., Ringkamp M., Hartke T.V., Chien H.F., Flavahan N.A., Campbell J.N., and Meyer R.A. Uninjured C-fiber nociceptors develop spontaneous activity and alpha-adrenergic sensitivity following L6 spinal nerve ligation in monkey. J. Neurophysiol. 81 (1999) 455-466
2. Amir R., Kocsis J.D., and Devor M. Multiple interacting sites of ectopic spike electrogenesis in primary sensory neurons. J. Neurosci. 25 (2005) 2576-2585
3. Baker M., Bostock H., Grafe P., and Martius P. Function and distribution of three types of rectifying channels in rat spinal root myelinated axons. J. Physiol. (Lond.) 383 (1987) 45-67
4. Bergmans, J., 1970. The Physiology of Single Human Nerve Fibres. Vander, Louvain.
5. Blackburn-Munro G., Dalby-Brown W., Mirza N.R., Mikkelsen J.D., and Blackburn-Munro R.E. Retigabine: chemical synthesis to clinical application. CNS Drug Rev. 11 (2005) 1-20
6. Blackburn-Munro G., and Jensen B.S. The anticonvulsant retigabine attenuates nociceptive behaviours in rat models of persistent and neuropathic pain. Eur. J. Pharmacol. 460 (2003) 109-116
7. Bostock H., Campero M., Serra J., and Ochoa J. Velocity recovery cycles of C fibres innervating human skin. J. Physiol. (Lond.) 553 (2003) 649-663
8. Bostock H., Cikurel K., and Burke D. Threshold tracking techniques in the study of human peripheral nerve. Muscle Nerve 21 (1998) 137-158
9. Bostock H., and Rothwell J.C. Latent addition in motor and sensory fibres of human peripheral nerve. J. Physiol. (Lond.) 498 (1997) 277-294
10. Campbell J.N., and Meyer R.A. Mechanisms of neuropathic pain. Neuron 52 (2006) 77-92
11. Delmas P., and Brown D.A. Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat. Rev. Neurosci. 6 (2005) 850-862
12. + channel. J. Neurosci. 24 (2004) 1236-1244
13. Devor M. Potassium channels moderate ectopic excitability of nerve-end neuromas in rats. Neurosci. Lett. 40 (1983) 181-186
14. Devor M. Response of nerves to injury in relation to neuropathic pain. In: McMahon S.B., and Koltzenburg M. (Eds). Textbook of Pain (2006), Elsevier 905-927
15. Djouhri L., Koutsikou S., Fang X., McMullan S., and Lawson S.N. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J. Neurosci. 26 (2006) 1281-1292
16. Dost R., Rostock A., and Rundfeldt C. The anti-hyperalgesic activity of retigabine is mediated by KCNQ potassium channel activation. Naunyn Schmiedeberg's Arch. Pharmacol. 369 (2004) 382-390
17. Eschenfelder S., Häbler H.J., and Jänig W. Dorsal root section elicits signs of neuropathic pain rather than reversing them in rats with L5 spinal nerve injury. Pain 87 (2000) 213-219
18. George A., Serra J., Navarro X., and Bostock H. Velocity recovery cycles of single C fibres innervating rat skin. J. Physiol. (Lond.) 578 (2007) 213-232
19. Gutman G.A., Chandy K.G., Grissmer S., Lazdunski M., McKinnon D., Pardo L.A., Robertson G.A., Rudy B., Sanguinetti M.C., Stühmer W., and Wang X. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol. Rev. 57 (2005) 473-508
20. Hirano K., Kuratani K., Fujiyoshi M., Tashiro N., Hayashi E., and Kinoshita M. Kv7.2-7.5 voltage-gated potassium channel (KCNQ2-5) opener, retigabine, reduces capsaicin-induced visceral pain in mice. Neurosci. Lett. 413 (2007) 159-162
21. Hu H., Vervaeke K., and Storm J.F. M-channels (Kv7/KCNQ channels) that regulate synaptic integration, excitability, and spike pattern of CA1 pyramidal cells are located in the perisomatic region. J. Neurosci. 27 (2007) 1853-1867
22. Jentsch T.J. Neuronal KCNQ potassium channels: physiology and role in disease. Nat. Rev. Neurosci. 1 (2000) 21-30
23. Kiernan M.C., and Bostock H. Effects of membrane polarization and ischaemia on the excitability properties of human motor axons. Brain 123 (2000) 2542-2551
24. Lang P.M., Burgstahler R., Sippel W., Irnich D., Schlotter-Weigel B., and Grafe P. Characterization of neuronal nicotinic acetylcholine receptors in the membrane of unmyelinated human C-fiber axons by in vitro studies. J. Neurophysiol. 90 (2003) 3295-3303
25. Lang P.M., Fleckenstein J., Passmore G.M., Brown D.A., and Grafe P. A neuronal potassium channel opener reduces the excitability of unmyelinated peripheral human axons. Acta Physiol. 192 Suppl. 663 (2008) PW03-15
26. Liu X., Eschenfelder S., Blenk K.H., Jänig W., and Häbler H. Spontaneous activity of axotomized afferent neurons after L5 spinal nerve injury in rats. Pain 84 (2000) 309-318
27. Michaelis M., Liu X., and Jänig W. Axotomized and intact muscle afferents but not skin afferents develop ongoing discharges of dorsal root ganglion origin after peripheral nerve lesion. J. Neurosci. 20 (2000) 2742-2748
28. Moalem-Taylor G., Lang P.M., Tracey D.J., and Grafe P. Post-spike excitability indicates changes in membrane potential of isolated C-fibers. Muscle Nerve 36 (2007) 172-182
29. Munro G., and Dalby-Brown W. K(v)7 (KCNQ) channel modulators and neuropathic pain. J. Med. Chem. 50 (2007) 2576-2582
30. Nielsen A.N., Mathiesen C., and Blackburn-Munro G. Pharmacological characterisation of acid-induced muscle allodynia in rats. Eur. J. Pharmacol. 487 (2004) 93-103
31. Ocana M., Cendan C.M., Cobos E.J., Entrena J.M., and Baeyens J.M. Potassium channels and pain: present realities and future opportunities. Eur. J. Pharmacol. 500 (2004) 203-219
32. Ochoa J.L., Campero M., Serra J., and Bostock H. Hyperexcitable polymodal and insensitive nociceptors in painful human neuropathy. Muscle Nerve 32 (2005) 459-472
33. Passmore G.M., and Brown D.A. Effects of M-channel modulators on peripheral excitability in rat hairy skin. Soc. Neurosci. Abstr. 681.8 (2007)
34. Passmore G.M., Selyanko A.A., Mistry M., Al Qatari M., Marsh S.J., Matthews E.A., Dickenson A.H., Brown T.A., Burbidge S.A., Main M., and Brown D.A. KCNQ/M currents in sensory neurons: significance for pain therapy. J. Neurosci. 23 (2003) 7227-7236
35. Priestley T., and Hunter J.C. Voltage-gated sodium channels as molecular targets for neuropathic pain. Drug Dev. Res. 67 (2006) 360-375
36. Rivera-Arconada I., and Lopez-Garcia J.A. Retigabine-induced population primary afferent hyperpolarisation in vitro. Neuropharmacology 51 (2006) 756-763
37. Roza, C., Lopez-Garcia, J.A. Retigabine, the specific KCNQ channel opener, blocks ectopic discharges in axotomized sensory fibres. Pain, doi:10.1016/j.pain.2008.01.031, in press.
38. + channels in neuronal cells. Eur. J. Pharmacol. 336 (1997) 243-249
39. Rundfeldt C., and Netzer R. The novel anticonvulsant retigabine activates M-currents in Chinese hamster ovary-cells transfected with human KCNQ2/3 subunits. Neurosci. Lett. 282 (2000) 73-76
40. + current regulating excitability in the rat node of Ranvier. J. Physiol. (Lond.) 573 (2006) 17-34
41. Surti T.S., and Jan L.Y. A potassium channel, the M-channel, as a therapeutic target. Curr. Opin. Investig. Drugs 6 (2005) 704-711
42. Tatulian L., Delmas P., Abogadie F.C., and Brown D.A. Activation of expressed KCNQ potassium currents and native neuronal M-type potassium currents by the anti-convulsant drug retigabine. J. Neurosci. 21 (2001) 5535-5545
43. Vervaeke K., Gu N., Agdestein C., Hu H., and Storm J.F. Kv7/KCNQ/M-channels in rat glutamatergic hippocampal axons and their role in regulation of excitability and transmitter release. J. Physiol. (Lond.) 576 (2006) 235-256
44. Wang H.S., Pan Z., Shi W., Brown B.S., Wymore R.S., Cohen I.S., Dixon J.E., and McKinnon D. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282 (1998) 1890-1893
45. Weidner C., Schmelz M., Schmidt R., Hammarberg B., Orstavik K., Hilliges M., Torebjork H.E., and Handwerker H.O. Neural signal processing: the underestimated contribution of peripheral human C-fibers. J. Neurosci. 22 (2002) 6704-6712
46. Wickenden A.D., Yu W., Zou A., Jegla T., and Wagoner P.K. Retigabine, a novel anti-convulsant, enhances activation of KCNQ2/Q3 potassium channels. Mol. Pharmacol. 58 (2000) 591-600
47. Wladyka C.L., Feng B., Glazebrook P.A., Schild J.H., and Kunze D.L. The KCNQ/M-current modulates arterial baroreceptor function at the sensory terminal in rats. J. Physiol. (Lond.) (2008) 795-802
48. Wu G., Ringkamp M., Hartke T.V., Murinson B.B., Campbell J.N., Griffin J.W., and Meyer R.A. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J. Neurosci. 21 (2001) RC140
49. Wu G., Ringkamp M., Murinson B.B., Pogatzki E.M., Hartke T.V., Weerahandi H.M., Campbell J.N., Griffin J.W., and Meyer R.A. Degeneration of myelinated efferent fibers induces spontaneous activity in uninjured C-fiber afferents. J. Neurosci. 22 (2002) 7746-7753
50. Xiong Q., Gao Z., Wang W., and Li M. Activation of Kv7 (KCNQ) voltage-gated potassium channels by synthetic compounds. Trends Pharmacol. Sci. 29 (2008) 99-107
51. Zaczek R., Chorvat R.J., Saye J.A., Pierdomenico M.E., Maciag C.M., Logue A.R., Fisher B.N., Rominger D.H., and Earl R.A. Two new potent neurotransmitter release enhancers, 10,10-bis(4-pyridinylmethyl)-9(10H)-anthracenone and 10,10-bis(2-fluoro-4-pyridinylmethyl)-9(10H)-anthracenone: comparison to linopirdine. J. Pharmacol. Exp. Ther. 285 (1998) 724-730