Enhancing M currents: A way out for neuropathic pain?

Frontiers in Molecular Neuroscience

Volumn 2, Issue AUG, 2009, Pages

  Rivera Arconada, Ivan ^a   Roza, Carolina ^a   Lopez Garcia, Jose A ^a  

^a UNIVERSITY OF ALCALÁ   (Spain)

Author keywords

Analgesia; KCNQ; Kv7; Neuropathy; Pain; Pain therapy; Potassium current

Indexed keywords

EID: 77649250073     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.02.010.2009     Document Type: Review

References (148)

1. Adams, P. R., Brown, D. A., and Constanti, A. (1982). Pharmacological inhibition of the M-current. J. Physiol. 332, 223-262.
2. Aiken, S. P., Lampe, B. J., Murphy, P. A., and Brown, B. S. (1995). Reduction of spike frequency adaptation and blockade of M-current in rat CA1 pyramidal neurones by linopirdine (DuP 996), a neurotransmitter release enhancer. Br. J. Pharmacol. 115, 1163-1168.
3. Alaburda, A., Perrier, J. F., and Hounsgaard, J. (2002). An M-like outward current regulates the excitability of spinal motoneurones in the adult turtle. J. Physiol. 540, 875-881.
4. Amir, R., and Devor, M. (2003). Electrical excitability of the soma of sensory neurons is required for spike invasion of the soma, but not for through-conduction. Biophys. J. 84, 2181-2191.
5. Amir, R., Kocsis, J. D., and Devor, M. (2005). Multiple interacting sites of ectopic spike electrogenesis in primary sensory neurons. J. Neurosci. 25, 2576-2585.
6. Andersen, M. L., and Tufik, S. (2003). Sleep patterns over 21-day period in rats with chronic constriction of sciatic nerve. Brain Res. 984, 84-92.
7. Barnes, S. (1994). After transduction: response shaping and control of transmission by ion channels of the photoreceptor inner segments. Neuroscience 58, 447-459.
8. Belmonte, C., and Viana, F. (2008). Molecular and cellular limits to somatosensory specificity. Mol. Pain 4, 14.
9. Bennett, G. J., and Xie, Y. K. (1988). A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33, 87-107.
10. Bialer, M., Johannessen, S. I., Levy, R. H., Perucca, E., Tomson, T., and White, H. S. (2009). Progress report on new antiepileptic drugs: a summary of the Ninth Eilat Conference (EILAT IX). Epilepsy Res. 83, 1-43.
11. Biervert, C., Schroeder, B. C., Kubisch, C., Berkovic, S. F., Propping, P., Jentsch, T. J., and Steinlein, O. K. (1998). A potassium channel mutation in neonatal human epilepsy. Science 279, 403-406.
12. Blackburn-Munro, G., and Erichsen, H. K. (2005). Antiepileptics and the treatment of neuropathic pain: evidence from animal models. Curr. Pharm. Des. 11, 2961-2976.
13. Blackburn-Munro, G., and Jensen, B. S. (2003). The anticonvulsant retigabine attenuates nociceptive behaviours in rat models of persistent and neuropathic pain. Eur. J. Pharmacol. 460, 109-116.
14. Bostock, H., Campero, M., Serra, J., and Ochoa, J. L. (2005). Temperaturedependent double spikes in C-nociceptors of neuropathic pain patients. Brain 128, 2154-2163.
15. Brown, B. S., and Yu, S. P. (2000). Modulation and genetic identification of the M channel. Prog. Biophys. Mol. Biol. 73, 135-166.
16. Brown, D. A., and Adams, P. R. (1980). Muscarinic suppression of a novel voltage-sensitive Kvvcurrent in a vertebrate neurone. Nature 283, 673-676.
17. Brown, D. A., Hughes, S. A., Marsh, S. J., and Tinker, A. (2007). Regulation of M(Kv7.2/7.3) channels in neurons by PIP(2) and products of PIP(2) hydrolysis: significance for receptor-mediated inhibition. J. Physiol. 582, 917-925.
18. Brown, D. A., and Passmore, G. M. (2009). Neural KCNQ (Kv7) channels. Br. J. Pharmacol. 156, 1185-1195.
19. Buniel, M., Glazebrook, P. A., Ramirez-Navarro, A., and Kunze, D. L. (2008). Distribution of voltage-gated potassium and hyperpolarization-activated channels in sensory afferent fibers in the rat carotid body. J. Comp. Neurol. 510, 367-377.
20. Caminos, E., Garcia-Pino, E., Martinez-Galan, J. R., and Juiz, J. M. (2007). The potassium channel KCNQ5/Kv7.5 is localized in synaptic endings of auditory brainstem nuclei of the rat. J. Comp. Neurol. 505, 363-378.
21. Campbell, J. N., and Meyer, R. A. (2006). Mechanisms of neuropathic pain. Neuron 52, 77-92.
22. 2+ current via G alpha o in rat sympathetic neurones. J. Physiol. 477(Pt 3), 415-422.
23. Charpak, S., Gahwiler, B. H., Do, K. Q., and Knopfel, T. (1990). Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature 347, 765-767.
24. Costa, A. M. N., and Brown, B. S. (1997). Inhibition of M-current in cultured rat superior cervical ganglia by linopirdine: mechanism of action studies. Neuropharmacology 36, 1747-1753.
25. Crozier, R. A., Ajit, S. K., Kaftan, E. J., and Pausch, M. H. (2007). MrgD activation inhibits KCNQ/M-currents and contributes to enhanced neuronal excitability. J. Neurosci. 27, 4492-4496.
26. 2+ stores in rat sympathetic neurons. Proc. Natl. Acad. Sci. U.S.A. 95, 7151-7156.
27. Dalby-Brown, W., Hansen, H. H., Korsgaard, M. P., Mirza, N., and Olesen, S. P. (2006). K(v)7 channels: function, pharmacology and channel modulators. Curr. Top. Med. Chem. 6, 999-1023.
28. de Lecea, L., Criado, J. R., Prospero-Garcia, O., Gautvik, K. M., Schweitzer, P., Danielson, P. E., Dunlop, C. L., Siggins, G. R., Henriksen, S. J., and Sutcliffe, J. G. (1996). A cortical neuropeptide with neuronal depressant and sleepmodulating properties. Nature 381, 242-245.
29. Decosterd, I., and Woolf, C. J. (2000). Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87, 149-158.
30. + channel. Proc. Natl. Acad. Sci. U.S.A. 98, 12272-12277.
31. Delmas, P., Wanaverbecq, N., Abogadie, F. C., Mistry, M., and Brown, D. A. (2002). Signaling microdomains define the specificity of receptor-mediated InsP(3) pathways in neurons. Neuron 34, 209-220.
32. Devaux, J. J., Kleopa, K. A., Cooper, E. C., and Scherer, S. S. (2004). KCNQ2 is a nodal Kaachannel. J. Neurosci. 24, 1236-1244.
33. Devor, M. (1983). Potassium channels moderate ectopic excitability of nerveend neuromas in rats. Neurosci. Lett. 40, 181-186.
34. Devor, M. (2006). Sodium channels and mechanisms of neuropathic pain. J. Pain 7, S3-S12.
35. Devor, M., Govrin-Lippmann, R., and Angelides, K. (1993). NaAAchannel immunolocalization in peripheral mammalian axons and changes following nerve injury and neuroma formation. J. Neurosci. 13, 1976-1992.
36. Djouhri, L., Koutsikou, S., Fang, X., McMullan, S., and Lawson, S. N. (2006). Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J. Neurosci. 26, 1281-1292.
37. Dost, R., Rostock, A., and Rundfeldt, C. (2004). The anti-hyperalgesic activity of retigabine is mediated by KCNQ potassium channel activation. Naunyn Schmiedebergs Arch. Pharmacol. 369, 382-390.
38. Dubois, J. M. (1981). Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane. J. Physiol. 318, 297-316.
39. Etxeberria, A., Aivar, P., Rodriguez-Alfaro, J. A., Alaimo, A., Villace, P., Gomez-Posada, J. C., Areso, P., and Villarroel, A. (2008). Calmodulin regulates the trafficking of KCNQ2 potassium channels. FASEB J. 22, 1135-1143.
40. + current in rat hippocampal pyramidal neurons. J. Neurosci. 26, 9340-9348.
41. Gutman, G. A., Chandy, K. G., Adelman, J. P., Aiyar, J., Bayliss, D. A., Clapham, D. E., Covarriubias, M., Desir, G. V., Furuichi, K., Ganetzky, B., Garcia, M. L., Grissmer, S., Jan, L. Y., Karschin, A., Kim, D., Kuperschmidt, S., Kurachi, Y., Lazdunski, M., Lesage, F., Lester, H. A., McKinnon, D., Nichols, C. G., O'Kelly, I., Robbins, J., Robertson, G. A., Rudy, B., Sanguinetti, M., Seino, S., Stuehmer, W., Tamkun, M. M., Vandenberg, C. A., Wei, A., Wulff, H., Wymore, R. S., and International Union of Pharmacology. (2003). International Union of Pharmacology. XLI. Compendium of voltage-gated ion channels: potassium channels. Pharmacol. Rev. 55, 583-586.
42. Hadley, J. K., Noda, M., Selyanko, A. A., Wood, I. C., Abogadie, F. C., and Brown, D. A. (2000). Differential tetraethylammonium sensitivity of KCNQ1-4 potassium channels. Br. J. Pharmacol. 129, 413-415.
43. Herrero, J. F., Laird, J. M., and Lopez-Garcia, J. A. (2000). Wind-up of spinal cord neurones and pain sensation: much ado about something? Prog. Neurobiol. 61, 169-203.
44. Hetka, R., Rundfeldt, C., Heinemann, U., and Schmitz, D. (1999). Retigabine strongly reduces repetitive firing in rat entorhinal cortex. Eur. J. Pharmacol. 386, 165-171.
45. Hoshi, N., Zhang, J. S., Omaki, M., Takeuchi, T., Yokoyama, S., Wanaverbecq, N., Langeberg, L. K., Yoneda, Y., Scott, J. D., Brown, D. A., and Higashida, H. (2003). AKAP150 signaling complex promotes suppression of the M-current by muscarinic agonists. Nat. Neurosci. 6, 564-571.
46. Hu, H. J., Carrasquillo, Y., Karim, F., Jung, W. E., Nerbonne, J. M., Schwarz, T. L., and Gereau, R. W. IV. (2006). The kv4.2 potassium channel subunit is required for pain plasticity. Neuron 50, 89-100.
47. Jacquin, T., Champagnat, J., Madamba, S., Denavit-Saubie, M., and Siggins, G. R. (1988). Somatostatin depresses excitability in neurons of the solitary tract complex through hyperpolarization and augmentation of IM, a non-inactivating voltage-dependent outward current blocked by muscarinic agonists. Proc. Natl. Acad. Sci. U.S.A. 85, 948-952.
48. Jentsch, T. J. (2000). Neuronal KCNQ potassium channels: physiology and role in disease. Nat. Rev. Neurosci. 1, 21-30.
49. Ji, R., Kohno, T., Moore, K. A., and Woolf, C. J. (2003). Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci. 26, 696-705.
50. Jia, Z., Bei, J., Rodat-Despoix, L., Liu, B., Jia, Q., Delmas, P., and Zhang, H. (2008). NGF inhibits M/KCNQ currents and selectively alters neuronal excitability in subsets of sympathetic neurons depending on their M/KCNQ current background. J. Gen. Physiol. 131, 575-587.
51. Jones, S., Brown, D. A., Milligan, G., Willer, E., Buckley, N. J., and Caulfield, M. P. (1995). Bradykinin excites rat sympathetic neurons by inhibition of M current through a mechanism involving B2 receptors and G alpha q/11. Neuron 14, 399-405.
52. Kapetanovic, I. M., Yonekawa, W. D., and Kupferberg, H. J. (1995). The effects of D-23129, a new experimental anticonvulsant drug, on neurotransmitter amino acids in the rat hippocampus in vitro. Epilepsy Res. 22, 167-173.
53. Kim, S. H., and Chung, J. M. (1992). An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50, 355-363.
54. Korsgaard, M. P., Hartz, B. P., Brown, W. D., Ahring, P. K., Strobaek, D., and Mirza, N. R. (2005). Anxiolytic effects of Maxipost (BMS-204352) and retigabine via activation of neuronal Kv7 channels. J. Pharmacol. Exp. Ther. 314, 282-292.
55. Koyama, S., and Appel, S. B. (2006). Characterization of M-current in ventral tegmental area dopamine neurons. J. Neurophysiol. 96, 535-543.
56. Kubisch, C., Schroeder, B. C., Friedrich, T., Lutjohann, B., El-Amraoui, A., Marlin, S., Petit, C., and Jentsch, T. J. (1999). KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell 96, 437-446.
57. Kullmann, D. M. (2002). The neuronal channelopathies. Brain 125, 1177-1195.
58. LaBuda, C. J., and Fuchs, P. N. (2000). A behavioral test paradigm to measure the aversive quality of inflammatory and neuropathic pain in rats. Exp. Neurol. 163, 490-494.
59. Lamas, J. A., Reboreda, A., and Codesido, V. (2002). Ionic basis of the resting membrane potential in cultured rat sympathetic neurons. Neuroreport 13, 585-591.
60. Lamas, J. A., Selyanko, A. A., and Brown, D. A. (1997). Effects of a cognition-enhancer, linopirdine (DuP 996), on M-type potassium currents (IK(M) and some other voltage-and ligand-gated membrane currents in rat sympathetic neurons. Eur. J. Neurosci. 9, 605-616.
61. Lang, P. M., Fleckenstein, J., Passmore, G. M., Brown, D. A., and Grafe, P. (2008). Retigabine reduces the excitability of unmyelinated peripheral human axons. Neuropharmacology 54, 1271-1278.
62. Lange, W., Geissendorfer, J., Schenzer, A., Grotzinger, J., Seebohm, G., Friedrich, T., and Schwake, M. (2009). Refinement of the binding site and mode of action of the anticonvulsant Retigabine on KCNQ KRRchannels. Mol. Pharmacol. 75, 272-280.
63. Lawrence, J. J., Saraga, F., Churchill, J. F., Statland, J. M., Travis, K. E., Skinner, F. K., and McBain, C. J. (2006). Somatodendritic Kv7/KCNQ/M channels control interspike interval in hippocampal interneurons. J. Neurosci. 26, 12325-12338.
64. Lechner, S. G., Mayer, M., and Boehm, S. (2003). Activation of M1 muscarinic receptors triggers transmitter release from rat sympathetic neurons through an inhibition of M-type Kaachannels. J. Physiol. 553, 789-802.
65. Lerche, C., Scherer, C. R., Seebohm, G., Derst, C., Wei, A. D., Busch, A. E., and Steinmeyer, K. (2000). Molecular cloning and functional expression of KCNQ5, a potassium channel subunit that may contribute to neuronal Mcurrent diversity. J. Biol. Chem. 275, 22395-22400.
66. Linley, J. E., Rose, K., Patil, M., Robertson, B., Akopian, A. N., and Gamper, N. (2008). Inhibition of M current in sensory neurons by exogenous proteases: a signaling pathway mediating inflammatory nociception. J. Neurosci. 28, 11240-11249.
67. Lisney, S. J. (1989). Regeneration of unmyelinated axons after injury of mammalian peripheral nerve. Q. J. Exp. Physiol. 74, 757-784.
68. 2+ channels. J. Neurochem. 109, 168-181.
69. Madamba, S. G., Schweitzer, P., and Siggins, G. R. (1999a). Dynorphin selectively augments the M-current in hippocampal CA1 neurons by an opiate receptor mechanism. J. Neurophysiol. 82, 1768-1775.
70. Madamba, S. G., Schweitzer, P., and Siggins, G. R. (1999b). Nociceptin augments K(a) currents in hippocampal CA1 neurons by both ORL-1 and opiate receptor mechanisms. J. Neurophysiol. 82, 1776-1785.
71. Main, M. J., Cryan, J. E., Dupere, J. R., Cox, B., Clare, J. J., and Burbidge, S. A. (2000). Modulation of KCNQ2/3 potassium channels by the novel anticonvulsant retigabine. Mol. Pharmacol. 58, 253-262.
72. Maljevic, S., Wuttke, T. V., and Lerche, H. (2008). Nervous system KV7 disorders: breakdown of a subthreshold brake. J. Physiol. 586, 1791-1801.
73. Marrion, N. V., Smart, T. G., Marsh, S. J., and Brown, D. A. (1989). Muscarinic suppression of the M-current in the rat sympathetic ganglion is mediated by receptors of the M1-subtype. Br. J. Pharmacol. 98, 557-573.
74. Martire, M., Castaldo, P., D'Amico, M., Preziosi, P., Annunziato, L., and Taglialatela, M. (2004). M channels containing KCNQ2 subunits modulate norepinephrine, aspartate, and GABA release from hippocampal nerve terminals. J. Neurosci. 24, 592-597.
75. Martire, M., D'Amico, M., Panza, E., Miceli, F., Viggiano, D., Lavergata, F., Iannotti, F. A., Barrese, V., Preziosi, P., Annunziato, L., and Taglialatela, M. (2007). Involvement of KCNQ2 subunits in [3H]dopamine release triggered by depolarization and presynaptic muscarinic receptor activation from rat striatal synaptosomes. J. Neurochem. 102, 179-193.
76. McCormick, D. A., and Williamson, A. (1989). Convergence and divergence of neurotransmitter action in human cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 86, 8098-8102.
77. Miles, G. B., Dai, Y., and Brownstone, R. M. (2005). Mechanisms underlying the early phase of spike frequency adaptation in mouse spinal motoneurones. J. Physiol. 566, 519-532.
78. Monassi, C. R., Bandler, R., and Keay, K. A. (2003). A subpopulation of rats show social and sleep-waking changes typical of chronic neuropathic pain following peripheral nerve injury. Eur. J. Neurosci. 17, 1907-1920.
79. Moore, S. D., Madamba, S. G., Joels, M., and Siggins, G. R. (1988). Somatostatin augments the M-current in hippocampal neurons. Science 239, 278-280.
80. Moore, S. D., Madamba, S. G., Schweitzer, P., and Siggins, G. R. (1994). Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro. J. Neurosci. 14, 809-820.
81. Munro, G., and Dalby-Brown, W. (2007). Kv7 (KCNQ) channel modulators and neuropathic pain. J. Med. Chem. 50, 2576-2582.
82. Murase, K., Ryu, P. D., and Randic, M. (1986). Substance P augments a persistent slow inward calcium-sensitive current in voltage-clamped spinal dorsal horn neurons of the rat. Brain Res. 365, 369-376.
83. Nielsen, A. N., Mathiesen, C., and Blackburn-Munro, G. (2004). Pharmacological characterisation of acid-induced muscle allodynia in rats. Eur. J. Pharmacol. 487, 93-103.
84. Nowak, L. M., and Macdonald, R. L. (1982). Substance P: ionic basis for depolarizing responses of mouse spinal cord neurons in cell culture. J. Neurosci. 2, 1119-1128.
85. Nowak, L. M., and Macdonald, R. L. (1983a). Ionic mechanism of muscarinic cholinergic depolarization of mouse spinal cord neurons in cell culture. J. Neurophysiol. 49, 792-803.
86. Nowak, L. M., and Macdonald, R. L. (1983b). Muscarine-sensitive voltage-dependent potassium current in cultured murine spinal cord neurons. Neurosci. Lett. 35, 85-91.
87. Ocana, M., Cendan, C. M., Cobos, E. J., Entrena, J. M., and Baeyens, J. M. (2004). Potassium channels and pain: present realities and future opportunities. Eur. J. Pharmacol. 500, 203-219.
88. Ochoa, J. L., Campero, M., Serra, J., and Bostock, H. (2005). Hyperexcitable polymodal and insensitive nociceptors in painful human neuropathy. Muscle Nerve 32, 459-472.
89. Orstavik, K., Weidner, C., Schmidt, R., Schmelz, M., Hilliges, M., Jorum, E., Handwerker, H., and Torebjork, E. (2003). Pathological C-fibres in patients with a chronic painful condition. Brain 126, 567-578.
90. Otto, J. F., Kimball, M. M., and Wilcox, K. S. (2002). Effects of the anticonvulsant retigabine on cultured cortical neurons: changes in electroresponsive properties and synaptic transmission. Mol. Pharmacol. 61, 921-927.
91. Otto, J. F., Yang, Y., Frankel, W. N., White, H. S., and Wilcox, K. S. (2006). A spontaneous mutation involving Kcnq2 (Kv7.2) reduces M-current density and spike frequency adaptation in mouse CA1 neurons. J. Neurosci. 26, 2053-2059.
92. Pan, Z., Kao, T., Horvath, Z., Lemos, J., Sul, J. Y., Cranstoun, S. D., Bennett, V., Scherer, S. S., and Cooper, E. C. (2006). A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 26, 2599-2613.
93. Passmore, G. M., and Brown, D. A. (2007). Effects of M-channel Modulators on Peripheral Excitability in Rat Hairy Skin. Program No. 681.8. 2007 Neuroscience Meeting Planner. San Diego, CA, Society for Neuroscience.
94. 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. (2003). KCNQ/M currents in sensory neurons: signifi-cance for pain therapy. J. Neurosci. 23, 7227-7236.
95. Pedersen, L. H., and Blackburn-Munro, G. (2006). Pharmacological characterisation of place escape/avoidance behaviour in the rat chronic constriction injury model of neuropathic pain. Psychopharmacology (Berl) 185, 208-217.
96. Peretz, A., Degani, N., Nachman, R., Uziyel, Y., Gibor, G., Shabat, D., and Attali, B. (2005). Meclofenamic acid and diclofenac, novel templates of KCNQ2/Q3 potassium channel openers, depress cortical neuron activity and exhibit anticonvulsant properties. Mol. Pharmacol. 67, 1053-1066.
97. Peretz, A., Degani-Katzav, N., Takmon, M., Danieli, E., Gopin, A., Malka, E., Nachman, R., Raz, A. Shabat, D., and Attali, B. (2007). A tale of switched functions: from cyclooxygenase inhibition to M-channels modulation in new diphenylamine derivatives. PLoS One 12, e1132. doi: 10.1371/ journal.pone.0001332.
98. Peters, H. C., Hu, H., Pongs, O., Storm, J. F., and Isbrandt, D. (2005). Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat. Neurosci. 8, 51-60.
99. Poliak, S., and Peles, E. (2003). The local differentiation of myelinated axons at nodes of Ranvier. Nat. Rev. Neurosci. 4, 968-980.
100. Qiu, C., Zeyda, T., Johnson, B., Hochgeschwender, U., de Lecea, L., and Tallent, M. K. (2008). Somatostatin receptor subtype 4 couples to the M-current to regulate seizures. J. Neurosci. 28, 3567-3576.
101. Rasband, M. N., Park, E. W., Vanderah, T. W., Lai, J., Porreca, F., and Trimmer, J. S. (2001). Distinct potassium channels on pain-sensing neurons. Proc. Natl. Acad. Sci. U.S.A. 98, 13373-13378.
102. Rivera-Arconada, I., and Lopez-Garcia, J. A. (2005). Effects of M-current modulators on the excitability of immature rat spinal sensory and motor neurones. Eur. J. Neurosci. 22, 3091-3098.
103. Rivera-Arconada, I., and Lopez-Garcia, J. A. (2006). Retigabineinduced population primary afferent hyperpolarisation in vitro. Neuropharmacology 51, 756-763.
104. Rivera-Arconada, I., Martinez-Gomez, J., and Lopez-Garcia, J. A. (2004). M-current modulators alter rat spinal nociceptive transmission: an electrophysiological study in vitro. Neuropharmacology 46, 598-606.
105. Robbins, J. (2001). KCNQ potassium channels: physiology, pathophysiology, and pharmacology. Pharmacol. Ther. 90, 1-19.
106. Romero, M., Reboreda, A., Sanchez, E., and Lamas, J. A. (2004). Newly developed blockers of the M-current do not reduce spike frequency adaptation in cultured mouse sympathetic neurons. Eur. J. Neurosci. 19, 2693-2702.
107. Rouse, S. T., Hamilton, S. E., Potter, L. T., Nathanson, N. M., and Conn, P. J. (2000). Muscarinic-induced modulation of potassium conductances is unchanged in mouse hippocampal pyramidal cells that lack functional M1 receptors. Neurosci. Lett. 278, 61-64.
108. Roza, C., and Lopez-Garcia, J. A. (2008). Retigabine, the specific KCNQ channel opener, blocks ectopic discharges in axotomized sensory fibres. Pain 138, 537-545.
109. Rundfeldt, C., and Netzer, R. (2000a). Investigations into the mechanism of action of the new anticonvulsant retigabine. Interaction with GABAergic and glutamatergic neurotransmission and with voltage gated ion channels. Arzneimittelforschung 50, 1063-1070.
110. Rundfeldt, C., and Netzer, R. (2000b). The novel anticonvulsant retigabine activates M-currents in Chinese hamster ovary-cells transfected with human KCNQ2/3 subunits. Neurosci. Lett. 282, 73-76.
111. Schenzer, A., Friedrich, T., Pusch, M., Saftig, P., Jentsch, T. J., Grotzinger, J., and Schwake, M. (2005). Molecular determinants of KCNQ (Kv7) Kd channel sensitivity to the anticonvulsant retigabine. J. Neurosci. 25, 5051-5060.
112. Schnee, M. E., and Brown, B. S. (1998). Selectivity of linopirdine (DuP 996), a neurotransmitter release enhancer, in blocking voltage-dependent and calcium-activated potassium currents in hippocampal neurons. J. Pharmacol. Exp. Ther. 286, 709-717.
113. Schroder, R. L., Jespersen, T., Christophersen, P., Strobaek, D., Jensen, B. S., and Olesen, S. P. (2001). KCNQ4 channel activation by BMS-204352 and retigabine. Neuropharmacology 40, 888-898.
114. Schroeder, B. C., Hechenberger, M., Weinreich, F., Kubisch, C., and Jentsch, T. J. (2000). KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J. Biol. Chem. 275, 24089-24095.
115. + channels causes epilepsy. Nature 396, 687-690.
116. Schwarz, J. R., Glassmeier, G., Cooper, E. C., Kao, T. C., Nodera, H., Tabuena, D., Kaji, R., and Bostock, H. (2006). KCNQ channels mediate IKs, a slow Ksscurrent regulating excitability in the rat node of Ranvier. J. Physiol. 573, 17-34.
117. Schweitzer, P. (2000). Cannabinoids decrease the K(d) M-current in hippocampal CA1 neurons. J. Neurosci. 20, 51-58.
118. Schweitzer, P., Madamba, S., and Siggins, G. R. (1990). Arachidonic acid metabolites as mediators of somatostatin-induced increase of neuronal M-current. Nature 346, 464-467.
119. Selyanko, A. A., Hadley, J. K., Wood, I. C., Abogadie, F. C., Jentsch, T. J., and Brown, D. A. (2000). Inhibition of KCNQ1-4 potassium channels expressed in mammalian cells via M1 muscarinic acetylcholine receptors. J. Physiol. 522(Pt 3), 349-355.
120. Shen, W., Hamilton, S. E., Nathanson, N. M., and Surmeier, D. J. (2005). Cholinergic suppression of KCNQ channel currents enhances excitability of striatal medium spiny neurons. J. Neurosci. 25, 7449-7458.
121. Sindrup, S. H., and Jensen, T. S. (1999). Efficacy of pharmacological treatments of neuropathic pain: an update and effect related to mechanism of drug action. Pain 83, 389-400.
122. Smith, J. S., Iannotti, C. A., Dargis, P., Christian, E. P., and Aiyar, J. (2001). Differential expression of kcnq2 splice variants: implications to m current function during neuronal development. J. Neurosci. 21, 1096-1103.
123. Stuart, G., Spruston, N., Sakmann, B., and Hausser, M. (1997). Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20, 125-131.
124. Suh, B. C., and Hille, B. (2005). Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr. Opin. Neurobiol. 15, 370-378.
125. Surti, T. S., Huang, L., Jan, Y. N., Jan, L. Y., and Cooper, E. C. (2005). Identification by mass spectrometry and functional characterization of two phosphorylation sites of KCNQ2/KCNQ3 channels. Proc. Natl. Acad. Sci. U.S.A. 102, 17828-17833.
126. Tam, S. W., and Zaczek, R. (1995). Linopirdine. A depolarization-activated releaser of transmitters for treatment of dementia. Adv. Exp. Med. Biol. 363, 47-56.
127. Tatulian, L., and Brown, D. A. (2003). Effect of the KCNQ potassium channel opener retigabine on single KCNQ2/3 channels expressed in CHO cells. J. Physiol. 549, 57-63.
128. van Rijn, C. M., and Willems-van Bree, E. (2003). Synergy between retigabine and GABA in modulating the convulsant site of the GABAA receptor complex. Eur. J. Pharmacol. 464, 95-100.
129. Wang, H. S., Brown, B. S., McKinnon, D., and Cohen, I. S. (2000). Molecular basis for differential sensitivity of KCNQ and I(Ks) channels to the cognitive enhancer XE991. Mol. Pharmacol. 57, 1218-1223.
130. Wang, H. S., Pan, Z., Shi, W., Brown, B. S., Wymore, R. S., Cohen, I. S., Dixon, J. E., and McKinnon, D. (1998). KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282, 1890-1893.
131. Wickenden, A. D., Roeloffs, R., McNaughton-Smith, G., and Rigdon, G. C. (2004). KCNQ potassium channels: drug targets for the treatment of epilepsy and pain. Expert Opin. Ther. Pat. 14, 457-469.
132. Wickenden, A. D., Ye, F., McNaughton-Smith, G., Roeloffs, R., and Rigdon, G. C. (2002). KCNQ Channel Expression in Rat DRG Following Nerve Ligation. Program No. 454.7. 2002 Neuroscience Meeting Planner. Orlando, FL, Society for Neuroscience.
133. Wickenden, A. D., Yu, W., Zou, A., Jegla, T., and Wagoner, P. K. (2000). Retigabine, a novel anti-convulsant, enhances activation of KCNQ2/Q3 potassium channels. Mol. Pharmacol. 58, 591-600.
134. Willis, W. D. Jr. (1999). Dorsal root potentials and dorsal root reflexes: a double-edged sword. Exp. Brain Res. 124, 395-421.
135. Willis, W. D. Jr., and Coggeshall, R. E. (2004). Sensory mechanisms of the spinal cord. New York, NY, Kluwer Academic/Plenum Publishers.
136. Wladyka, C. L., Feng, B., Glazebrook, P. A., Schild, J. H., and Kunze, D. L. (2008). The KCNQ/M-current modulates arterial baroreceptor function at the sensory terminal in rats. J. Physiol. 586, 795-802.
137. Wladyka, C. L., and Kunze, D. L. (2006). KCNQ/M-currents contribute to the resting membrane potential in rat visceral sensory neurons. J. Physiol. 575, 175-189.
138. Wuttke, T. V., Jurkat-Rott, K., Paulus, W., Garncarek, M., Lehmann-Horn, F., and Lerche, H. (2007). Peripheral nerve hyperexcitability due to dominant-negative KCNQ2 mutations. Neurology 69, 2045-2053.
139. Wuttke, T. V., and Lerche, H. (2006). Novel anticonvulsant drugs targeting voltage-dependent ion channels. Expert Opin. Investig. Drugs 15, 1167-1177.
140. Wuttke, T. V., Seebohm, G., Bail, S., Maljevic, S., and Lerche, H. (2005). The new anticonvulsant retigabine favors voltage-dependent opening of the Kv7.2 (KCNQ2) channel by binding to its activation gate. Mol. Pharmacol. 67, 1009-1017.
141. Xiong, Q., Gao, Z., Wang, W., and Li, M. (2008). Activation of Kv7 (KCNQ) voltage-gated potassium channels by synthetic compounds. Trends Pharmacol. Sci. 29, 99-107.
142. Yang, W. P., Levesque, P. C., Little, W. A., Conder, M. L., Ramakrishnan, P., Neubauer, M. G., and Blanar, M. A. (1998). Functional expression of two KvLQT1-related potassium channels responsible for an inherited idiopathic epilepsy. J. Biol. Chem. 273, 19419-19423.
143. Yue, C., and Yaari, Y. (2004). KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci. 24, 4614-4624.
144. Yus-Najera, E., Munoz, A., Salvador, N., Jensen, B. S., Rasmussen, H. B., Defelipe, J., and Villarroel, A. (2003). Localization of KCNQ5 in the normal and epileptic human temporal neocortex and hippocampal formation. Neuroscience 120, 353-364.
145. Yus-Najera, E., Santana-Castro, I., and Villarroel, A. (2002). The identification and characterization of a noncontinuous calmodulin-binding site in noninactivating voltage-dependent KCNQ potassium channels. J. Biol. Chem. 277, 28545-28553.
146. 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. (1998). Two new potent neurotransmitter release enhancers, 10,10-bis(4-pyridinylmethyl)-9(10H)-anthr a cenone and 10,10-bis(2-fluoro-4-pyridinylmethyl)-9(10H)-anthracenone: comparison to linopirdine. J. Pharmacol. Exp. Ther. 285, 724-730.
147. 2+ signals direct purinergic P2Y receptor regulation of neuronal ion channels. J. Neurosci. 27, 8914-8926.
148. Zimmermann, M. (2001). Pathobiology of neuropathic pain. Eur. J. Pharmacol. 429, 23-37.