Opposite effects of the S4-S5 linker and PIP2 on voltage-gated channel function: KCNQ1/KCNE1 and other channels

Frontiers in Pharmacology

Volumn 3 JUL, Issue , 2012, Pages

  Choveau, Frank S ^a,b,c,d   Abderemane Ali, Fayal ^a,b,c   Coyan, Fabien C ^a,b,c   Es Salah Lamoureux, Zeineb ^a,b,c   Baró, Isabelle ^a,b,c   Loussouarn, Gildas ^a,b,c  

^a INSERM   (France)

^b CNRS   (France)

^c L INSTITUT DU THORAX   (France)

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

Author keywords

Channelopathies; Patch clamp; Phosphatidylinositol 4,5 bisphosphate; S4 S5 linker; Voltage gated potassium channels

Indexed keywords

ADENYLATE CYCLASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; POTASSIUM CHANNEL; POTASSIUM CHANNEL HERG; POTASSIUM CHANNEL KCNE1; POTASSIUM CHANNEL KCNQ1; POTASSIUM CHANNEL KCNQ2; POTASSIUM CHANNEL KCNQ3; POTASSIUM CHANNEL KCNQ4; POTASSIUM CHANNEL KCNQ5; POTASSIUM CHANNEL KV4.2; PROTEIN KINASE C; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOSENSOR; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HYPERPOLARIZATION; ION CURRENT; LIGAND BINDING; LIPID BILAYER; LONG QT SYNDROME; MEMBRANE DEPOLARIZATION; MUTAGENESIS; NONHUMAN; POINT MUTATION; POTASSIUM CHANNELOPATHY; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

EID: 84866180957     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00125     Document Type: Article

References (155)

1. Adams, P. J., and Snutch, T. P. (2007). Calcium channelopathies: voltage-gated calcium channels. Subcell Biochem. 45, 215-251.
2. Alonso-Ron, C., de la Peña, P., Miranda, P., Domínguez, P., and Barros, F. (2008). Thermodynamic and kinetic properties of amino-terminal and S4-S5 loop HERG channel mutants under steady-state conditions. Bio-phys.J. 94, 3893-3911.
3. Armstrong, C.M. (1981). Sodium channels and gating currents. Physiol. Rev. 61, 644-683.
4. Arnestad, M., Crotti, L., Rognum, T. O., Insolia, R., Pedrazzini, M., Ferrandi, C., Vege, A., Wang, D. W., Rhodes, T. E., George, A. L. Jr., Schwartz, P. J. (2007). Prevalence of long-QT syndrome gene variants in sudden infant death syndrome. Circulation 115, 361-367.
5. Bähring, R. (2012). Voltage sensor inactivation in potassium channels. Front. Pharmacol. 3:100. doi:10.3389/fphar.2012.00100
6. Barghaan, J., and Bähring, R. (2009). Dynamic coupling of voltage sensor and gate involved in closed-state inactivation of kv4.2 channels. J. Gen. Physiol. 133, 205-224.
7. Barhanin, J., Lesage, F., Guillemare, E., Fink, M., Lazdunski, M., and Romey, G. (1996). K(V)LQT1 and lsK (minK) proteins associate to form the I(Ks) cardiac potassium current. Nature 384, 78-80.
8. Barros, F., Domínguez, P., and de la Peña, P. (2012). Cytoplas-mic domains and voltage-dependent potassium channel gating. Front. Pharmacol. 3:49. doi:10.3389/fphar.2012.00049
9. + channels. J. Biol. Chem. 285, 14005-14019.
10. Bender, K., Wellner-Kienitz, M.-C., and Pott, L. (2002). Transfection of a phosphatidyl-4-phosphate 5-kinase gene into rat atrial myocytes removes inhibition of GIRK current by endothelin and alpha-adrenergic agonists. FEBS Lett. 529, 356-360.
11. Berridge, M. J. (1981). Phosphatidyli-nositol hydrolysis: a multifunctional transducing mechanism. Mol. Cell. Endocrinol. 24, 115-140.
12. + channels: II. The components of gating currents and a model of channel activation. Biophys.J. 66, 1011-1021.
13. Bian, J., Cui, J., and McDonald, T. V. (2001). HERG K(+) channel activity is regulated by changes in phos-phatidyl inositol 4,5-bisphosphate. Circ. Res. 89, 1168-1176.
14. Bian, J.-S., Kagan, A., and McDonald, T. V. (2004). Molecular analysis of PIP2 regulation of HERG and IKr. Am. J. Physiol. Heart Circ. Physiol. 287,H2154-H2163.
15. Bofill-Cardona, E., Vartian, N., Nanoff, C., Freissmuth, M., and Boehm, S. (2000). Two different signaling mechanisms involved in the excitation of rat sympathetic neurons by uridine nucleotides. Mol. Pharmacol. 57, 1165-1172.
16. Börjesson, S. I., and Elinder, F. (2008). Structure, function, and modification of the voltage sensor in voltage-gated ion channels. Cell Biochem. Biophys. 52, 149-174.
17. Boulet, I. R., Labro, A. J., Raes, A. L., and Snyders, D. J. (2007). Role of the S6 C-terminus in KCNQ1 channel gating. J. Physiol. (Lond.) 585, 325-337.
18. Broomand, A., Männikkö, R., Larsson, H. P., and Elinder, F. (2003). Molecular movement of the voltage sensor in a K channel. J. Gen. Physiol. 122, 741-748.
19. Catterall, W. A. (1986). Voltage-dependent gating of sodium channels: correlating structure and function. Trends Neurosci. 9, 7-10.
20. Cha, A., Snyder, G. E., Selvin, P. R., and Bezanilla, F. (1999). Atomicscale movement of the voltage-sensing region in a potassium channel measured via spectroscopy. Nature 402, 809-813.
21. Chan da, B., Asamoah, O. K., Blunck, R., Roux, B., and Bezanilla, F. (2005). Gating charge displacement in voltage-gated ion channels involves limited transmembrane movement. Nature 436, 852-856.
22. Chen, J., Mitcheson, J. S., Tristani-Firouzi, M., Lin, M., and Sanguinetti, M. C. (2001). The S4-S5 linker couples voltage sensing and activation of pacemaker channels. Proc. Natl. Acad. Sci. U.S.A. 98, 11277-11282.
23. Chen, J., Zou, A., Splawski, I., Keating, M. T., and Sanguinetti, M. C. (1999). Long QT syndrome-associated mutations in the Per-Arnt-Sim (PAS) domain of HERG potassium channels accelerate channel deactivation. J. Biol. Chem. 274, 10113-10118.
24. Chen, Y.-H., Xu, S.-J., Bendahhou, S., Wang, X.-L., Wang, Y., Xu, W.-Y., Jin, H.-W., Sun, H., Su, X.-Y., Zhuang, Q.-N., Yang, Y. Q., Li, Y. B., Liu, Y., Xu, H. J., Li, X. F., Ma, N., Mou, C. P., Chen, Z., Barhanin, J., and Huang, W. (2003). KCNQ1 gain-of-function mutation in familial atrial fibrillation. Science 299, 251-254.
25. Cheng, Y. M., and Claydon, T. W. (2012). Voltage-dependent gating of HERG potassium channels. Front. Pharmacol. 3:83. doi:10.3389/fphar.2012.0008
26. Choveau, F. S., Rodriguez, N., Abderemane-Ali, F., Labro, A. J., Rose, T., Dahimène, S., Boudin, H., Le Hénaff, C., Escande, D., Snyders, D. J., Charpentier, F., Mérot, J., Baró, I., and Loussouarn, G. (2011). KCNQ1 channels voltage dependence through a voltage-dependent binding of the S4-S5 linker to the pore domain. J. Biol. Chem. 286, 707-716.
27. Cooper, E. C., Harrington, E., Jan, Y. N., and Jan, L. Y. (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.
28. 2+ stores in rat sympathetic neurons. Proc. Natl. Acad. Sci. U.S.A. 95, 7151-7156.
29. Curran, M. E., Splawski, I., Timothy, K. W., Vincent, G. M., Green, E. D., and Keating, M. T. (1995). A molecular basis for cardiac arrhythmia: HERG mutations cause long QT syndrome. Cell 80, 795-803.
30. de la Peña, P., Alonso-Ron, C., Machín, A., Fernández-Trillo, J., Carretero, L., Domínguez, P., and Barros, F. (2011). Demonstration of physical proximity between the N terminus and the S4-S5 linker of the human ether-a-go-go-related gene (hERG) potassium channel. J. Biol. Chem. 286, 19065-19075.
31. Delemotte, L., Tarek, M., Klein, M. L., Amaral, C., and Treptow, W. (2011). Intermediate states of the Kv1.2 voltage sensor from atomistic molecular dynamics simulations. Proc. Natl. Acad. Sci. U.S.A. 108, 6109-6114.
32. Delmas, P., and Brown, D. A. (2005). Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat. Rev. Neurosci. 6, 850-862.
33. Delmas, P., Wanaverbecq, N., Abogadie, E 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.
34. DiFrancesco, D. (1981). A new interpretation of the pace-maker current in calf Purkinje fibres. J. Physiol. (Lond.) 314,359-376.
35. DiFrancesco, D. (1993). Pacemaker mechanisms in cardiac tissue. Annu. Rev. Physiol. 55,455-472.
36. DiFrancesco, D., Noma, A., and Trautwein, W. (1979). Kinetics and magnitude of the time-dependent potassium current in the rabbit sinoatrial node: effect of external potassium. Pflugers Arch. 381, 271-279.
37. Ding, W.-G., Toyoda, F., and Mat-suura, H. (2004). Regulation of cardiac IKs potassium current by membrane phosphatidylinositol 4,5-bisphosphate.J. Biol. Chem. 279, 50726-50734.
38. Dougherty, K., De Santiago-Castillo, J. A., and Covarrubias, M. (2008). Gating charge immobilization in Kv4.2 channels: the basis of closed-state inactivation. J. Gen. Physiol. 131, 257-273.
39. Durell, S. R., and Guy, H. R. (1992). Atomic scale structure and functional models of voltage-gated potassium channels. Biophys. J. 62, 238-247; discussion 247-250.
40. Enkvetchakul, D., Loussouarn, G., Makhina, E., Shyng, S. L., and Nichols, C. G. (2000). The kinetic and physical basis of K(ATP) channel gating: toward a unified molecular understanding. Biophys. J. 78, 2334-2348.
41. + channel. J. Biol. Chem. 281, 12858-12864.
42. Flynn, G. E., and Zagotta, W. N. (2011). Molecular mechanism underlying phosphatidylinositol 4,5-bisphosphate-induced inhibition of SpIH channels. J. Biol. Chem. 286, 15535-15542.
43. 2+/calmodulin. Mol. Biol. Cell 16, 3538-3551.
44. + channels. J. Gen. Physiol. 122, 17-31.
45. Gamper, N., and Shapiro, M. S. (2007). Regulation of ion transport proteins by membrane phosphoinosi-tides. Nat. Rev. Neurosci. 8, 921-934.
46. Gandhi, C. S., Clark, E., Loots, E., Pralle, A., and Isacoff, E. Y. (2003). The orientation and molecular movement of a k(+) channel voltage-sensing domain. Neuron 40, 515-525.
47. Gauss, R., Seifert, R., and Kaupp, U. B. (1998). Molecular identification of a hyperpolarization-activated channel in sea urchin sperm. Nature 393, 583-587.
48. Grabe, M., Lai, H. C., Jain, M., Jan, Y. N., and Jan, L. Y. (2007). Structure prediction for the down state of a potassium channel voltage sensor. Nature 445, 550-553.
49. Guy, H. R., and Seetharamulu, P. (1986). Molecular model of the action potential sodium channel. Proc. Natl. Acad. Sci. U.S.A. 83, 508-512.
50. + channels is caused by energetic coupling to the pore domain. J. Gen. Physiol. 137, 455-472.
51. + channel Kir2.2. Nature 477, 495-498.
52. Hedley, P.L., Jørgensen, P., Schlamowitz, S., Wangari, R., Moolman-Smook, J., Brink, P. A., Kanters, J. K., Corfield, V. A., and Christiansen, M. (2009). The genetic basis of long QT and short QT syndromes: a mutation update. Hum. Mutat. 30, 1486-1511.
53. + channels. J. Gen. Physiol. 132,361-381.
54. Hirdes, W., Horowitz, L. F., and Hille, B. (2004). Muscarinic modulation of erg potassium current. J. Physiol. (Lond.) 559, 67-84.
55. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869-875.
56. Hoshi,T.,Zagotta,W.N.,andAldrich,R. W. (1994). Shaker potassium channel gating. I: transitions near the open state. J. Gen. Physiol. 103, 249-278.
57. + channels. Proc. Natl. Acad. Sci. U.S.A. 100, 10488-10493.
58. Huang, C. L., Feng, S., and Hilgemann, D. W. (1998). Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature 391, 803-806.
59. Jensen, M. Ø., Jogini, V., Borhani, D. W., Leffler, A. E., Dror, R. O., and Shaw, D. E. (2012). Mechanism of voltage gating in potassium channels. Science 336, 229-233.
60. Jerng, H. H., Pfaffinger, P. J., and Covarrubias, M. (2004). Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol. Cell. Neurosci. 27, 343-369.
61. + channel. Nature 423, 33-41.
62. 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.
63. Kang, C., Tian, C, Sonnichsen, F. D., Smith, J. A., Meiler, J., George, A. L. Jr, Vanoye, C. G., Kim, H. J., and Sanders, C. R. (2008). Structure of KCNE1 and implications for how it modulates the KCNQ1 potassium channel. Biochemistry 47, 7999-8006.
64. Kapplinger, J. D., Tester, D. J., Salisbury, B. A., Carr, J. L., Harris-Kerr, C., Pollevick, G. D., Wilde, A. A. M., and Ackerman, M. J. (2009). Spectrum and prevalence of mutations from the first 2,500 consecutive unrelated patients referred for the FAMILION long QT syndrome genetic test. Heart Rhythm 6, 1297-1303.
65. Kubisch, C., Schroeder, B. C., Friedrich, T., Lütjohann, 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.
66. Kwon, Y., Hofmann, T., and Mon-tell, C. (2007). Integration of phosphoinositide- and calmodulin-mediated regulation of TRPC6. Mol. Cell 25, 491-503.
67. Labro, A. J., Boulet, I. R., Choveau, E S., Mayeur, E., Bruyns, T., Loussouarn, G., Raes, A. L., and Snyders, D. J. (2011). The S4-S5 linker of KCNQ 1 channels forms a structural scaffold with the S6 segment controlling gate closure.J. Biol. Chem. 286, 717-725.
68. Lai, L.-P., Su, Y.-N., Hsieh, F.-J., Chiang, F.-T.,Juang,J.-M., Liu, Y.-B., Ho, Y.-L., Chen, W.-J., Yeh, S.-J., Wang, C.-C., Ko, Y. L., Wu, T. J., Ueng, K. C., Lei, M. H., Tsao, H. M., Chen, S. A., Lin, T. K., Wu, M. H., Lo, H. M., Huang, S. K., and Lin, J. L. (2005). Denaturing high-performance liquid chromatography screening of the long QT syndrome-related cardiac sodium and potassium channel genes and identification of novel mutations and single nucleotide polymorphisms. J. Hum. Genet. 50, 490-496.
69. + channel S4. Neuron 16, 387-397.
70. Ledwell, J.L.,and Aldrich,R.W. (1999). Mutations in the S4 region isolate the final voltage-dependent cooperative step in potassium channel activation.J. Gen. Physiol. 113, 389-414.
71. Lee, S.-Y., Banerjee, A., and MacKinnon, R. (2009). Two separate interfaces between the voltage sensor and pore are required for the function of voltage-dependent K(+) channels. PLoS Biol. 7, e47. doi:10.1371/journal.pbio.1000047
72. + channel and its dependence on the lipid membrane. Proc. Natl. Acad. Sci. U.S.A. 102, 15441-15446.
73. Lehmann-Horn, F., and Jurkat-Rott, K. (1999). Voltage-gated ion channels and hereditary disease. Physiol. Rev. 79, 1317-1372.
74. 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,apotassium channel subunit that may contribute to neu-ronal M-current diversity. J. Biol. Chem. 275, 22395-22400.
75. + channel of known structure. J. Gen. Physiol. 131, 549-561.
76. + channel open probability by phosphatidyli-nositol 4,5-bisphosphate. J. Neu-rosci. 25, 9825-9835.
77. Li, Y., Zaydman, M. A., Wu, D., Shi, J., Guan, M., Virgin-Downey, B., and Cui, J. (2011). KCNE1 enhances phosphatidylinositol 4,5-bisphosphate (PIP2) sensitivity of IKs to modulate channel activity. Proc. Natl. Acad. Sci. U.S.A. 108, 9095-9100.
78. Lindner, M., Leitner, M. G., Halaszovich, C. R., Hammond, G. R. V., and Oliver, D. (2011). Probing the regulation of TASK potassium channels by PI4,5P with switchable phospho-inositide phosphatases. J. Physiol. (Lond.) 589, 3149-3162.
79. Logothetis, D. E., Petrou, V. I., Adney, S. K., and Mahajan, R. (2010). Chan-nelopathies linked to plasma membrane phosphoinositides. Pflugers Arch. 460,321-341.
80. + channel. Science 309, 897-903.
81. + channel in a lipid membrane-like environment. Nature 450, 376-382.
82. + channels. Channels (Austin) 1, 124-134.
83. Lopes, C. M. B., Zhang, H., Rohacs, T., Jin, T., Yang, J., and Logothetis, D. E. (2002). Alterations in conserved Kir channel-PIP2 interactions underlie channelopathies. Neuron 34, 933-944.
84. + channels. EMBOJ. 22, 5412-5421.
85. Lu, Z., Klem, A. M., and Ramu, Y. (2001). Ion conduction pore is conserved among potassium channels. Nature 413, 809-813.
86. + channels. J. Gen. Physiol. 120, 663-676.
87. Marx, S. O., Kurokawa, J., Reiken, S., Motoike, H., D'Armiento, J., Marks, A. R., and Kass, R. S. (2002). Requirement of a macromolecular signaling complex for beta adrenergic receptor modulation of the KCNQ1-KCNE1 potassium channel. Science 295,496-499.
88. Matavel, A., and Lopes, C. M. B. (2009). PKC activation and PIP(2) depletion underlie biphasic regulation of IKs by Gq-coupled receptors. J. Mol. Cell. Cardiol. 46, 704-712.
89. Matavel, A., Medei, E., and Lopes, C. M. B. (2010). PKA and PKC partially rescue long QT type 1 phenotype by restoring channel-PIP2 interactions. Channels (Austin) 4, 3-11.
90. McCusker, E. C., D'Avanzo, N., Nichols, C. G., and Wallace, B. A. (2011). Simplified bacterial "pore" channel provides insight into the assembly, stability, and structure of sodium channels. J. Biol .Chem. 286, 16386-16391.
91. Miceli, F., Vargas, E., Bezanilla, F., and Taglialatela, M. (2012). Gating currents from Kv7 channels carrying neuronal hyperexcitabil-ity mutations in the voltage-sensing domain. Biophys. J. 102, 1372-1382.
92. Milescu, M., Bosmans, F., Lee, S., Alabi, A. A., Kim, J. I., and Swartz, K. J. (2009). Interactions between lipids and voltage sensor paddles detected with tarantula toxins. Nat. Struct. Mol. Biol. 16,1080-1085.
93. + channel by three amino acid substitutions. Neuron 16, 853-858.
94. Moroni, A., Gazzarrini, S., Cerana, R., Colombo, R., Sutter, J. U., DiFrancesco, D., Gradmann, D., and Thiel, G. (2000). Mutation in pore domain uncovers cation- and voltage-sensitive recovery from inac-tivation in KAT1 channel. Biophys. J. 78, 1862-1871.
95. Napolitano, C., Priori, S. G., Schwartz, P. J., Bloise, R., Ronchetti, E., Nas-toli, J., Bottelli, G., Cerrone, M., and Leonardi, S. (2005). Genetic testing in the long QT syndrome: development and validation of an efficient approach to genotyping in clinical practice. JAMA 294, 2975-2980.
96. Neyroud, N., Tesson, F., Denjoy, I., Lei-bovici, M., Donger, C., Barhanin, J., Fauré, S., Gary, F., Coumel, P., Petit, C., Schwartz, K., and Guicheney, P. (1997). A novel mutation in the potassium channel gene KVLQT1 causes the Jervell and Lange-Nielsen cardioauditory syndrome. Nat. Genet. 15, 186-189.
97. + channels by membrane lipids. Science 304, 265-270.
98. Pape, H. C. (1996). Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu. Rev. Physiol. 58, 299-327.
99. Park, K.-H., Piron, J., Dahimene, S., Mérot, J., Baró, I., Escande, D., and Loussouarn, G. (2005). Impaired KCNQ1-KCNE1 and phosphatidylinositol-4,5-bisphosphate interaction underlies the long QT syndrome. Circ. Res. 96, 730-739.
100. Payandeh, J., Scheuer, T., Zheng, N., and Catterall, W. A. (2011). The crystal structure of a voltage-gated sodium channel. Nature 475, 353-358.
101. Pian, P., Bucchi, A., Robinson, R. B., and Siegelbaum, S. A. (2006). Regulation of gating and rundown of HCN hyperpolarization-activated channels by exogenous and endogenous PIP2. J. Gen. Physiol. 128, 593-604.
102. Pietrobon, D. (2007). Familial hemi-plegic migraine. Neurotherapeutics 4, 274-284.
103. Prole,D. L., andYellen, G. (2006). Reversal of HCN channel voltage dependence via bridging of the S4-S5 linker and Post-S6. J. Gen. Physiol. 128, 273-282.
104. Restier, L., Cheng, L., and Sanguinetti, M. C. (2008). Mechanisms by which atrial fibrillation-associated mutations in the S1 domain of KCNQ1 slow deactivation of IKs channels. J. Physiol. (Lond.) 586, 4179-4191.
105. + channels. Br. J. Pharmacol. 137, 1173-1186.
106. Rodriguez, N., Amarouch, M. Y., Montnach, J., Piron, J., Labro, A. J., Charpentier, F., Mérot, J., Baró, I., and Loussouarn, G. (2010). Phosphatidylinositol-4,5-bisphosphate (PIP(2)) stabilizes the open pore conformation of the Kv11.1 (hERG) channel. Biophys. J. 99, 1110-1118.
107. Rohács, T., Lopes, C., Mirshahi, T., Jin, T., Zhang, H., and Logothetis, D. E. (2002). Assaying phosphatidylinositol bisphosphate regulation of potassium channels. Meth. Enzymol. 345, 71-92.
108. Rosenhouse-Dantsker, A., and Logothetis, D. E. (2007). Molecular characteristics of phosphoinositide binding. Pflugers Arch. 455,45-53.
109. + channel. Cell 123, 463-475.
110. Sanguinetti, M. C., Curran, M. E., Zou, A., Shen, J., Spector, P. S., Atkinson, D. L., and Keating, M. T. (1996). Coassembly of K(V)LQT1 and minK (IsK) proteins to form cardiac I(Ks) potassium channel. Nature 384, 80-83.
111. Sanguinetti, M. C., Jiang, C., Curran, M. E., and Keating, M. T. (1995). A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell 81, 299-307.
112. Sanguinetti, M. C., and Tristani-Firouzi, M. (2006). hERG potassium channels and cardiac arrhythmia. Nature 440,463-469.
113. Sanguinetti,M. C.,andXu,Q.P. (1999). Mutations of the S4-S5 linker alter activation properties of HERG potassium channels expressed in Xenopus oocytes. J. Physiol. (Lond.) 514(Pt 3), 667-675.
114. Sarria, I., Ling, J., Zhu, M. X., and Gu, J. G. (2011). TRPM8 acute desen-sitization is mediated by calmod-ulin and requires PIP(2): distinction from tachyphylaxis. J. Neurophysiol. 106, 3056-3066.
115. Schmidt, D., Jiang, Q.-X., and MacKinnon, R. (2006). Phospholipids and the origin of cationic gating charges in voltage sensors. Nature 444, 775-779.
116. 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.
117. Shah, M. M., Mistry, M., Marsh, S. J., Brown, D.A., and Delmas, P. (2002). Molecular correlates of the M-current in cultured rat hippocam-pal neurons. J. Physiol. (Lond.) 544, 29-37.
118. Shapiro, M. S., Roche, J. P., Kaftan, E. J., Cruzblanca, H., Mackie, K., and Hille, B. (2000). Reconstitu-tion of muscarinic modulation of the KCNQ2/KCNQ3 K(+) channels that underlie the neuronal M current.J. Neurosci. 20, 1710-1721.
119. Shaya, D., Kreir, M., Robbins, R. A., Wong, S., Hammon, J., Brüggemann, A., and Minor, D. L. Jr. (2011). Voltage-gated sodium channel (NaV) protein dissection creates a set of functional pore-only proteins. Proc. Natl. Acad. Sci. U.S.A. 108, 12313-12318.
120. Smith, J. A., Vanoye, C. G., George, A. L. Jr., Meiler, J., and Sanders, C. R. (2007). Structural models for the KCNQ1 voltage-gated potassium channel. Biochemistry 46, 14141-14152.
121. Smith, P. L., Baukrowitz, T., and Yellen, G. (1996). The inward rectification mechanism of the HERG cardiac potassium channel. Nature 379, 833-836.
122. + channels: I. Ionic and gating currents. Biophys. J. 66, 996-1010.
123. Suh, B.-C., and Hille, B. (2002). Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 35, 507-520.
124. Suh, B.-C., and Hille, B. (2007). Regulation of KCNQ channels by manipulation of phosphoinositides. J. Physiol. (Lond.) 582,911-916.
125. Suh, B.-C., and Hille, B. (2008). PIP2 is a necessary cofactor for ion channel function: how and why? Annu. Rev. Biophys. 37, 175-195.
126. Suh, B.-C., Inoue, T., Meyer, T., and Hille, B. (2006). Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science 314, 1454-1457.
127. 2+ channels. Proc. Natl. Acad. Sci. U.S.A. 109,3161-3166.
128. Telezhkin, V., Reilly, J. M., Thomas, A. M., Tinker, A., and Brown, D. A. (2012). Structural requirements of membrane phospholipids for M-type potassium channel activation and binding. J. Biol. Chem. 287, 10001-10012.
129. Tempel, B. L., Papazian, D. M., Schwarz, T. L., Jan, Y. N., and Jan, L. Y. (1987). Sequence of a probable potassium channel component encoded at shaker locus of Drosophila. Science 237, 770-775.
130. Tester, D. J., Will, M. L., Haglund, C. M., and Ackerman, M. J. (2005). Compendium of cardiac channel mutations in 541 consecutive unrelated patients referred for long QT syndrome genetic testing. Heart Rhythm 2,507-517.
131. Thomas, A. M., Harmer, S. C., Khambra, T., and Tinker, A. (2011). Characterization of a binding site for anionic phospholipids on KCNQ1. J. Biol. Chem. 286,2088-2100.
132. Tombola, F., Pathak, M. M., and Isacoff, E. Y. (2006). How does voltage open an ion channel? Annu. Rev. Cell Dev. Biol. 22,23-52.
133. + channels.J. Biol. Chem. 277,18994-19000.
134. Trudeau, M. C., Warmke, J. W., Ganet-zky, B., and Robertson, G. A. (1995). HERG, a human inward rectifier in the voltage-gated potassium channel family. Science 269, 92-95.
135. Wall-Lacelle, S., Hossain, M. I., Sauvé, R., Blunck, R., and Parent, L. (2011). Double mutant cycle analysis identified a critical leucine residue in the IIS4S5 linker for the activation of the Ca(V)2.3 calcium channel. J. Biol. Chem. 286,27197-27205.
136. Walsh,K. B.,andKass,R.S. (1988). Regulation of a heart potassium channel by protein kinase A and C. Science 242,67-69.
137. Wang, J., Trudeau, M. C., Zappia, A. M., and Robertson, G. A. (1998). Regulation of deactivation by an amino terminal domain in human ether-à-go-go-related gene potassium channels. J. Gen. Physiol. 112, 637-647.
138. Wang, W., Xia, J., and Kass, R.S. (1998). MinK-KvLQT1 fusion proteins, evidence for multiple stoichiometries of the assembled IsK channel. J. Biol. Chem. 273, 34069-34074.
139. Warmke, J. W., and Ganetzky,B. (1994). A family of potassium channel genes related to eag in Drosophila and mammals. Proc. Natl. Acad. Sci. U.S.A. 91,3438-3442.
140. Wen, H., and Levitan, I. B. (2002). Calmodulin is an auxiliary subunit of KCNQ2/3 potassium channels. J. Neurosci. 22,7991-8001.
141. Whorton, M. R., and Mackinnon, R. (2011). Crystal structure of the mammalian GIRK2 K(+) channel and gating regulation by G proteins, PIP(2), and sodium. Cell 147, 199-208.
142. Winks, J. S., Hughes, S., Filippov, A. K., Tatulian, L., Abogadie, F. C., Brown, D. A., and Marsh, S. J. (2005). Relationship between membrane phosphatidylinositol-4,5-bisphosphate and receptor-mediated inhibition of native neuronal M channels. J. Neurosci. 25, 3400-3413.
143. Wu, L., Bauer, C. S., Zhen, X., Xie, C., and Yang, J. (2002). Dual regulation of voltage-gated calcium channels by PtdIns(4,5)P2. Nature 419, 947-952.
144. + channels. Nature 451,826-829.
145. Yang, N., and Horn, R. (1995). Evidence for voltage-dependent S4 movement in sodium channels. Neuron 15, 213-218.
146. Yarov-Yarovoy, V., Baker, D., and Cat-terall, W A. (2006). Voltage sensor conformations in the open and closed states in ROSETTA structural models of K(+) channels. Proc. Natl. Acad. Sci. U.S.A. 103, 7292-7297.
147. Yarov-Yarovoy, V., DeCaen, P. G., West-enbroek, R. E., Pan, C.-Y., Scheuer, T., Baker, D., and Catterall, W A. (2012). Structural basis for gating charge movement in the voltage sensor of a sodium channel. Proc. Natl. Acad. Sci. U.S.A. 109, E93-E102.
148. Zagotta, W N., Hoshi, T., and Aldrich, R. W (1994). Shaker potassium channel gating. III: Evaluation of kinetic models for activation.J. Gen. Physiol. 103, 321-362.
149. Zagotta, W N., Hoshi, T., Dittman, J., and Aldrich, R. W (1994). Shaker potassium channel gating. II: Transitions in the activation pathway. J. Gen. Physiol. 103, 279-319.
150. + channels. J. Physiol. (Lond.) 575, 49-67.
151. 2+ signals direct purinergic P2Y receptor regulation of neuronal ion channels. J. Neurosci. 27, 8914-8926.
152. 2+ channels. J. Biol. Chem. 286, 830-841.
153. Zhang, H., Craciun, L. C., Mirshahi, T., Rohács, T., Lopes, C. M. B., Jin, T., and Logothetis, D. E. (2003). PIP(2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37, 963-975.
154. Zhang, X., Chen, X., Jia, C., Geng, X., Du,X., and Zhang, H. (2010). Depolarization increases phosphatidylinositol (PI) 4,5-bisphosphate level and KCNQ currents through PI 4-kinase mechanisms. J. Biol. Chem. 285, 9402-9409.
155. Zheng, H., Liu, W., Anderson, L. Y., and Jiang, Q.-X. (2011). Lipid-dependent gating of a voltage-gated potassium channel. Nat. Commun. 2, 250.