Zinc pyrithione-mediated activation of voltage-gated KCNQ potassium channels rescues epileptogenic mutants

Nature Chemical Biology

Volumn 3, Issue 5, 2007, Pages 287-296

  Xiong, Qiaojie ^a   Sun, Haiyan ^a   Li, Min ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL KCNQ; PYRITHIONE ZINC; RETIGABINE; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BENIGN CHILDHOOD EPILEPSY; CONDUCTANCE; CONTROLLED STUDY; DRUG EFFICACY; DRUG IDENTIFICATION; DRUG POTENTIATION; EMBRYO; EPILEPTIC FOCUS; FEMALE; GENE ACTIVATION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; MUTANT; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; RAT;

EID: 34247202495     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio874     Document Type: Article

References (55)

1. Ashcroft, F.M. From molecule to malady. Nature 440, 440-447 (2006).
2. Jan, L.Y. & Jan, Y.N. Cloned potassium channels from eukaryotes and prokaryotes. Annu. Rev. Neurosci. 20, 91-123 (1997).
3. Tombola, F., Pathak, M.M. & Isacoff, E.Y. How far will you go to sense voltage? Neuron 48, 719-725 (2005).
4. Brown, D.A. & Adams, P.R. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283, 673-676 (1980).
5. Marrion, N.V. Control of M-current. Annu. Rev. Physiol. 59, 483-504 (1997).
6. Cooper, E.C., Harrington, E., Jan, Y.N. & Jan, L.Y. M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J. Neurosci. 21, 9529-9540 (2001).
7. Schroeder, B.C., Kubisch, C., Stein, V. & Jentsch, T.J. Moderate loss of function of cyclic-AMP-modulated KCNQ2/KCNQ3 K+ channels causes epilepsy. Nature 396, 687-690 (1998).
8. Hille, B. Ion Channels of Excitable Membranes 220-238 (Sinauer, Sunderland, Massachusetts, USA, 2001).
9. Jentsch, T.J. Neuronal KCNQ potassium channels: physiology and role in disease. Nat. Rev. Neurosci. 1, 21-30 (2000).
10. Rogawski, M.A. KCNQ2/KCNQ3 K+ channels and the molecular pathogenesis of epilepsy: implications for therapy. Trends Neurosci. 23, 393-398 (2000).
11. Charlier, C. et al. A pore mutation in a novel KQT-like potassium channel gene in an idiopathic epilepsy family. Nat. Genet. 18, 53-55 (1998).
12. Gutman, G.A. et al. International Union of Pharmacology. XLI. Compendium of voltage-gated ion channels: potassium channels. Pharmacol. Rev. 55, 583-586 (2003).
13. Kubisch, C. et al. KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell 96, 437-446 (1999).
14. Schroeder, B.C., Hechenberger, M., Weinreich, F., Kubisch, C. & Jentsch, T.J. KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J. Biol. Chem. 275, 24089-24095 (2000).
15. Singh, N.A. et al. A novel potassium channel gene, KCNQ2, is mutated in an inherited epilepsy of newborns. Nat. Genet. 18, 25-29 (1998).
16. Wang, Q. et al. Positional cloning of a novel potassium channel gene: KVLQT1 mutations cause cardiac arrhythmias. Nat. Genet. 12, 17-23 (1996).
17. Shapiro, M.S. et al. Reconstitution of muscarinic modulation of the KCNQ2/KCNQ3 K(+) channels that underlie the neuronal M current. J. Neurosci. 20, 1710-1721 (2000).
18. Wang, H.S. et al. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282, 1890-1893 (1998).
19. Cooper, E.C. & Jan, L.Y. Ion channel genes and human neurological disease: recent progress, prospects, and challenges. Proc. Natl. Acad. Sci. USA 96, 4759-4766 (1999).
20. Armstrong, C.M. Time course of TEA(+)-induced anomalous rectification in squid giant axons. J. Gen. Physiol. 50, 491-503 (1966).
21. Armstrong, C.M. Inactivation of the potassium conductance and related phenomena caused by quaternary ammonium ion injection in squid axons. J. Gen. Physiol. 54, 553-575 (1969).
22. Armstrong, C.M. Interaction of tetraethylammonium ion derivatives with the potassium channels of giant axons. J. Gen. Physiol. 58, 413-437 (1971).
23. Holmgren, M., Smith, P.L. & Yellen, G. Trapping of organic blockers by closing of voltage-dependent K+ channels: evidence for a trap door mechanism of activation gating. J. Gen. Physiol. 109, 527-535 (1997).
24. Xu, J., Chen, Y. & Li, M. High-throughput technologies for studying potassium channels - progresses and challenges. Targets 3, 32-38 (2004).
25. Sanguinetti, M.C. & Tristani-Firouzi, M. hERG potassium channels and cardiac arrhythmia. Nature 440, 463-469 (2006).
26. Rostock, A. et al. D-23129: a new anticonvulsant with a broad spectrum activity in animal models of epileptic seizures. Epilepsy Res. 23, 211-223 (1996).
27. Tober, C., Rostock, A., Rundfeldt, C. & Bartsch, R. D-23129: a potent anticonvulsant in the amygdala kindling model of complex partial seizures. Eur. J. Pharmacol. 303, 163-169 (1996).
28. Rundfeldt, C. The new anticonvulsant retigabine (D-23129) acts as an opener of K+ channels in neuronal cells. Eur. J. Pharmacol. 336, 243-249 (1997).
29. Tatulian, L., Delmas, P., Abogadie, F.C. & Brown, D.A. Activation of expressed KCNQ potassium currents and native neuronal M-type potassium currents by the anticonvulsant drug retigabine. J. Neurosci. 21, 5535-5545 (2001).
30. Ramu, Y., Xu, Y. & Lu, Z. Enzymatic activation of voltage-gated potassium channels. Nature 442, 696-699 (2006).
31. Sun, H., Shikano, S., Xiong, Q. & Li, M. Function recovery after chemobleaching (FRAC): evidence for activity silent membrane receptors on cell surface. Proc. Natl. Acad. Sci. USA 101, 16964-16969 (2004).
32. Sun, H., Liu, X., Xiong, Q., Shikano, S. & Li, M. Chronic inhibition of cardiac kir2.1 and HERG potassium channels by celastrol with dual effects on both ion conductivity and protein trafficking. J. Biol. Chem. 281, 5877-5884 (2006).
33. Terstappen, G.C. Functional analysis of native and recombinant ion channels using a high-capacity nonradioactive rubidium efflux assay. Anal. Biochem. 272, 149-155 (1999).
34. Wickenden, A.D., Yu, W., Zou, A., Jegla, T. & Wagoner, P.K. Retigabine, a novel anticonvulsant, enhances activation of KCNQ2/Q3 potassium channels. Mol. Pharmacol. 58, 591-600 (2000).
35. Bond, A.D.J. Synthesis and characterization of a novel zinc pyrithione hydrate. Mol. Cryst. Liq. Cryst. Sci. Technol. 356, 305-313 (2001).
36. Wang, D.W. Synthesis of N-oxide-2-mercaptopyridine zinc salt. Riyong Huaxue Gongye 33, 340-342 (2003).
37. 2+-indicators. Sci. STKE 2004, PL7 (2004).
38. Barnett, B.L., Kretschmar, H.C. & Hartman, F.A. Structural characterization of bis(N-oxopyridine-2-thionato)zinc (II). Inorg. Chem. 16, 1834-1838 (1977).
39. Main, M.J. et al. Modulation of KCNQ2/3 potassium channels by the novel anticonvulsant retigabine. Mol. Pharmacol. 58, 253-262 (2000).
40. Schenzer, A. et al. Molecular determinants of KCNQ (Kv7) K+ channel sensitivity to the anticonvulsant retigabine. J. Neurosci. 25, 5051-5060 (2005).
41. Wuttke, T.V., Seebohm, G., Bail, S., Maljevic, S. & Lerche, H. 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 (2005).
42. Long, S.B., Campbell, E.B. & Mackinnon, R. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309, 903-908 (2005).
43. Seebohm, G. et al. Differential roles of S6 domain hinges in the gating of KCNQ potassium channels. Biophys. J. 90, 2235-2244 (2006).
44. Biervert, C. et al. A potassium channel mutation in neonatal human epilepsy. Science 279, 403-406 (1998).
45. Dedek, K. et al. Myokymia and neonatal epilepsy caused by a mutation in the voltage sensor of the KCNQ2 K+ channel. Proc. Natl. Acad. Sci. USA 98, 12272-12277 (2001).
46. Horrigan, F.T. & Aldrich, R.W. Coupling between voltage sensor activation, Ca2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120, 267-305 (2002).
47. Bandell, M. et al. High-throughput random mutagenesis screen reveals TRPM8 residues specifically required for activation by menthol. Nat. Neurosci. 9, 493-500 (2006).
48. Li, Y., Gamper, N. & Shapiro, M.S. Single-channel analysis of KCNQ K+ channels reveals the mechanism of augmentation by a cysteine-modifying reagent. J. Neurosci. 24, 5079-5090 (2004).
49. Huang, C.C., Lesburg, C.A., Kiefer, L.L., Fierke, C.A. & Christianson, D.W. Reversal of the hydrogen bond to zinc ligand histidine-119 dramatically diminishes catalysis and enhances metal equilibration kinetics in carbonic anhydrase II. Biochemistry 35, 3439-3446 (1996).
50. Laine, M. et al. Atomic proximity between S4 segment and pore domain in Shaker potassium channels. Neuron 39, 467-481 (2003).
51. Shealy, R.T., Murphy, A.D., Ramarathnam, R., Jakobsson, E. & Subramaniam, S. Sequence-function analysis of the K+-selective family of ion channels using a comprehensive alignment and the KcsA channel structure. Biophys. J. 84, 2929-2942 (2003).
52. Marks, R., Pearse, A.D. & Walker, A.P. The effects of a shampoo containing zinc pyrithione on the control of dandruff. Br. J. Dermatol. 112, 415-422 (1985).
53. Fliss, H. Zinc ionophores as therapeutic agents. US patent 6,495,538 (2002).
54. Mathie, A., Sutton, G.L., Clarke, C.E. & Veale, E.L. Zinc and copper: pharmacological probes and endogenous modulators of neuronal excitability. Pharmacol. Ther. 111, 567-583 (2006).
55. Guex, N. & Peitsch, M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723 (1997).