Determinants within the turret and pore-loop domains of KCNQ3 K+ channels governing functional activity

Biophysical Journal

Volumn 95, Issue 11, 2008, Pages 5121-5137

  Zaika, Oleg ^a   Hernandez, Ciria C ^a   Bal, Manjot ^a   Tolstykh, Gleb P ^a   Shapiro, Mark S ^a,b  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARIUM; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL KCNQ3; TETRYLAMMONIUM;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BINDING SITE; BIOTINYLATION; CELL MEMBRANE; CHEMISTRY; CHO CELL; CRICETULUS; ELECTRIC CONDUCTIVITY; ENZYME SPECIFICITY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; HAMSTER; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; POROSITY; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BARIUM; BINDING SITES; BIOTINYLATION; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; ELECTRIC CONDUCTIVITY; GENE EXPRESSION REGULATION; HUMANS; KCNQ3 POTASSIUM CHANNEL; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; POROSITY; POTASSIUM CHANNEL BLOCKERS; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TETRAETHYLAMMONIUM;

EID: 58149331215     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.137604     Document Type: Article

References (74)

1. Robbins, J. 2001. KCNQ potassium channels: physiology, pathophysiology, and pharmacology. Pharmacol. Ther. 90:1-19.
2. Delmas, P., and D. A. Brown. 2005. Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat. Rev. Neurosci. 6:850-862.
3. Jespersen, T., M. Grunnet, and S. P. Olesen. 2005. The KCNQ1 potassium channel: from gene to physiological function. Physiology (Bethesda). 20:408-416.
4. Wang, H. S., Z. Pan, W. Shi, B. S. Brown, R. S. Wymore, I. S. Cohen, J. E. Dixon, and D. McKinnon. 1998. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science. 282:1890-1893.
5. Cooper, E. C., E. Harrington, Y. N. Jan, and L. Y. Jan. 2001. 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.
6. + channel. J. Neurosci. 24:1236-1244.
7. Cooper, E. C., K. D. Aldape, A. Abosch, N. M. Barbaro, M. S. Berger, W. S. Peacock, Y. N. Jan, and L. Y. Jan. 2000. Colocalization and coassembly of two human brain M-type potassium channel subunits that are mutated in epilepsy. Proc. Natl. Acad. Sci. USA. 97:4914-4919.
8. Passmore, G. M., A. A. Selyanko, M. Mistry, M. Al-Qatari, S. J. Marsh, E. A. Matthews, A. H. Dickenson, T. A. Brown, S. A. Burbidge, M. Main, and D. A. Brown. 2003. KCNQ/M currents in sensory neurons: significance for pain therapy. J. Neurosci. 23:7227-7236.
9. Lerche, C., C. R. Scherer, G. Seebohm, C. Derst, A. D. Wei, A. E. Busch, and K. Steinmeyer. 2000. Molecular cloning and functional expression of KCNQ5, a potassium channel subunit that may contribute to neuronal M-current diversity. J. Biol. Chem. 275:22395-22400.
10. Schroeder, B. C., M. Hechenberger, F. Weinreich, C. Kubisch, and T. J. Jentsch. 2000. KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J. Biol. Chem. 275:24089-24095.
11. Shah, M. M., M. Mistry, S. J. Marsh, D. A. Brown, and P. Delmas. 2002. Molecular correlates of the M-current in cultured rat hippocampal neurons. J. Physiol. 544:29-37.
12. Yus-Najera, E., A. Munoz, N. Salvador, B. S. Jensen, H. B. Rasmussen, J. Defelipe, and A. Villarroel. 2003. Localization of KCNQ5 in the normal and epileptic human temporal neocortex and hippocampal formation. Neuroscience. 120:353-364.
13. Coucke, P. J., P. V. Hauwe, P. M. Kelley, H. Kunst, I. Schatteman, D. V. Velzen, J. Meyers, R. J. Ensink, M. Verstreken, F. Declau, H. Marres, K. Kastury, S. Bhasin, W. T. McGuirt, R. J. Smith, C. W. Cremers, P. V. Heyning, P. J. Willems, S. D. Smith, and G. V. Camp. 1999. Mutations in the KCNQ4 gene are responsible for autosomal dominant deafness in four DFNA2 families. Hum. Mol. Genet. 8:1321-1328.
14. Kubisch, C., B. C. Schroeder, T. Friedrich, B. Lutjohann, A. El-Amraoui, S. Marlin, C. Petit, and T. J. Jentsch. 1999. KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell. 96:437-446.
15. Etxeberria, A., I. Santana-Castro, M. P. Regalado, P. Aivar, and A. Villarroel. 2004. Three mechanisms underlie KCNQ2/3 heteromeric potassium M-channel potentiation. J. Neurosci. 24:9146-9152.
16. + channels causes epilepsy. Nature. 396:687-690.
17. Yang, W. P., P. C. Levesque, W. A. Little, M. L. Conder, P. Ramakrishnan, M. G. Neubauer, and M. A. Blanar. 1998. Functional expression of two KvLQT1-related potassium channels responsible for an inherited idiopathic epilepsy. J. Biol. Chem. 273:19419-19423.
18. Gamper, N., J. D. Stockand, and M. S. Shapiro. 2003. Subunit-specific modulation of KCNQ potassium channels by Src tyrosine kinase. J. Neurosci. 23:84-95.
19. + channel assembly. J. Neurosci. 26:3757-3766.
20. + channel sensitivity to the anticonvulsant retigabine. J. Neurosci. 25:5051-5060.
21. 2+/calmodulin. Mol. Biol. Cell. 16:3538-3551.
22. + channels reveals the mechanism of augmentation by a cysteine-modifying reagent. J. Neurosci. 24:5079-5090.
23. Selyanko, A. A., J. K. Hadley, and D. A. Brown. 2001. Properties of single M-type KCNQ2/KCNQ3 potassium channels expressed in mammalian cells. J. Physiol. 534:15-24.
24. Pusch, M. 1998. Increase of the single-channel conductance of KvLQT1 potassium channels induced by the association with minK. Pflugers Arch. 437:172-174.
25. + channel open probability by phosphatidylinositol (4,5)-bisphosphate. J. Neurosci. 25:9825-9835.
26. + channel assembly. EMBO Rep. 4:76-81.
27. Howard, R. J., K. A. Clark, J. M. Holton, and D. L. Minor, Jr. 2007. Structural insight into KCNQ (Kv7) channel assembly and channelopathy. Neuron. 53:663-675.
28. Nakajo, K., and Y. Kubo. 2008. Second coiled-coil domain of KCNQ channel controls current expression and subfamily specific heteromultimerization by salt bridge networks. J. Physiol. 586:2827-2840.
29. + channels involved in epilepsy. J. Biol. Chem. 275:13343-13348.
30. Gamper, N., J. D. Stockand, and M. S. Shapiro. 2005. The use of Chinese hamster ovary (CHO) cells in the study of ion channels. J. Pharmacol. Toxicol. Methods. 51:177-185.
31. Axelrod, D. 2003. Total internal reflection fluorescence microscopy in cell biology. Methods Enzymol. 361:1-33.
32. Rae, J., K. Cooper, P. Gates, and M. Watsky. 1991. Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Methods. 37:15-26.
33. + channel. Nature. 423:33-41.
34. Schwede, T., J. Kopp, N. Guex, and M. C. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
35. Axelrod, D., T. P. Burghardt, and N. L. Thompson. 1984. Total internal reflection fluorescence. Annu. Rev. Biophys. Bioeng. 13:247-268.
36. Steyer, J. A., and W. Almers. 2001. A real-time view of life within 100 nm of the plasma membrane. Nat. Rev. Mol. Cell Biol. 2:268-275.
37. + channel by phosphatidylinositol 3,4,5-trisphosphate and phosphatidylinositol 3,4-bisphosphate produced by phosphoinositide 3-OH kinase. J. Biol. Chem. 279:22654-22663.
38. + channels assayed by TIRF/FRET in living cells. J. Physiol. 586:2307-2320.
39. + conduction and selectivity. Science. 280:69-77.
40. MacKinnon, R., and C. Miller. 1989. Mutant potassium channels with altered binding of charybdotoxin, a pore-blocking peptide inhibitor. Science. 245:1382-1385.
41. MacKinnon, R., L. Heginbotham, and T. Abramson. 1990. Mapping the receptor site for charybdotoxin, a pore-blocking potassium channel inhibitor. Neuron. 5:767-771.
42. Yus-Najera, E., I. Santana-Castro, and A. Villarroel. 2002. The identification and characterization of a noncontinuous calmodulin binding site in non-inactivating voltage-dependent KCNQ potassium channels. J. Biol. Chem. 277:28545-28553.
43. Yellen, G. 1998. The moving parts of voltage-gated ion channels. Q. Rev. Biophys. 31:239-295.
44. Lopez-Barneo, J., T. Hoshi, S. H. Heinemann, and R. W. Aldrich. 1993. Effects of external cations and mutations in the pore region on C-type inactivation of Shaker potassium channels. Receptors Channels. 1:61-71.
45. + channels by internally and externally applied barium ions. J. Gen. Physiol. 80:663-682.
46. Robbins, J., J. Trouslard, S. J. Marsh, and D. A. Brown. 1992. Kinetic and pharmacological properties of the M-current in rodent neuroblastoma x glioma hybrid cells. J. Physiol. 451:159-185.
47. Gibor, G., D. Yakubovich, A. Peretz, and B. Attali. 2004. External barium affects the gating of KCNQ1 potassium channels and produces a pore block via two discrete sites. J. Gen. Physiol. 124:83-102.
48. Gibor, G., D. Yakubovich, A. Rosenhouse-Dantsker, A. Peretz, H. Schottelndreier, G. Seebohm, N. Dascal, D. E. Logothetis, Y. Paas, and B. Attali. 2007. An inactivation gate in the selectivity filter of KCNQ1 potassium channels. Biophys. J. 93:4159-4172.
49. + channel. J. Gen. Physiol. 92:569-586.
50. Neyton, J., and C. Miller. 1988. Potassium blocks barium permeation through a calcium-activated potassium channel. J. Gen. Physiol. 92:549-567.
51. Jiang, Y., and R. MacKinnon. 2000. The barium site in a potassium channel by x-ray crystallography. J. Gen. Physiol. 115:269-272.
52. + channel. PLoS Biol. 5:e121.
53. + channel locked in the conductive conformation. Science. 314:1004-1007.
54. Cordero-Morales, J. F., L. G. Cuello, Y. Zhao, V. Jogini, D. M. Cortes, B. Roux, and E. Perozo. 2006. Molecular determinants of gating at the potassium-channel selectivity filter. Nat. Struct. Mol. Biol. 13:311-318.
55. Cordero-Morales, J. F., V. Jogini, A. Lewis, V. Vasquez, D. M. Cortes, B. Roux, and E. Perozo. 2007. Molecular driving forces determining potassium channel slow inactivation. Nat. Struct. Mol. Biol. 14:1062-1069.
56. + selectivity filter: charge balance and coupling of ion binding to a protein conformational change underlie high conduction rates. J. Mol. Biol. 333:965-975.
57. + channel-Fab complex at 2.0 A resolution. Nature. 414:43-48.
58. + channel during gating. Neuron. 16:859-867.
59. + channel allows inactivation to be modulated by metal binding. Biophys. J. 66:1068-1075.
60. Brown, D. A. 2008. Kv7 (KCNQ) potassium channels that are mutated in human diseases. J. Physiol. 586:1781-1783.
61. Yue, C., and Y. Yaari. 2006. Axo-somatic and apical dendritic Kv7/M channels differentially regulate the intrinsic excitability of adult rat CA1 pyramidal cells. J. Neurophysiol. 95:3480-3495.
62. Peretz, A., A. Sheinin, C. Yue, N. Degani-Katzav, G. Gibor, R. Nachman, A. Gopin, E. Tam, D. Shabat, Y. Yaari, and B. Attali. 2007. Pre- and postsynaptic activation of M-channels by a novel opener dampens neuronal firing and transmitter release. J. Neurophysiol. 97:283-295.
63. Maljevic, S., T. V. Wuttke, and H. Lerche. 2008. Nervous system Kv7 disorders: breakdown of a subthreshold brake. J. Physiol. 586:1791-1801.
64. Pan, Z., T. Kao, Z. Horvath, J. Lemos, J. Y. Sul, S. D. Cranstoun, V. Bennett, S. S. Scherer, and E. C. Cooper. 2006. A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 26:2599-2613.
65. Chung, H. J., Y. N. Jan, and L. Y. Jan. 2006. Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains. Proc. Natl. Acad. Sci. USA. 103:8870-8875.
66. + channels in brain. J. Neurosci. 21:4609-4624.
67. + channels. J. Physiol. 548:353-360.
68. +-free media. J. Gen. Physiol. 75:61-78.
69. +-channel activation gating. Science. 285:73-78.
70. + channel. Neuron. 32:649-656.
71. Jiang, Y., A. Lee, J. Chen, M. Cadene, B. T. Chait, and R. MacKinnon. 2002. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:515-522.
72. + channel. Science. 309:897-903.
73. + channel with altered conduction properties and selectivity filter ion distribution. J. Mol. Biol. 338:839-846.
74. Berneche, S., and B. Roux. 2005. A gate in the selectivity filter of potassium channels. Structure. 13:591-600.