KCNE1 divides the voltage sensor movement in KCNQ1/KCNE1 channels into two steps

Nature Communications

Volumn 5, Issue , 2014, Pages

  Barro Soria, Rene ^a   Rebolledo, Santiago ^a   Liin, Sara I ^a   Perez, Marta E ^a   Sampson, Kevin J ^b   Kass, Robert S ^b   Larsson, H Peter ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b Department of Pharmacology College of Physicians and Surgeons Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMANOL 293B; CYSTEINE; POTASSIUM CHANNEL KCNE1; POTASSIUM CHANNEL KCNQ1; KCNE1 PROTEIN, HUMAN; KCNQ1 PROTEIN, HUMAN; PROTEIN SUBUNIT; VOLTAGE GATED POTASSIUM CHANNEL;

ABNORMALITY; BIOCHEMISTRY; FUNCTIONAL ROLE; MUTATION; PHYSIOLOGY; PROTEIN; SENSOR;

ARTICLE; CONFORMATIONAL TRANSITION; DEPOLARIZATION; DISSOCIATION; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; FLUORESCENCE; HUMAN; HYPERPOLARIZATION; ION CURRENT; KINETICS; MUTATION; REPOLARIZATION; SENSOR; VOLTAGE CLAMP TECHNIQUE; BIOLOGICAL MODEL; CHANNEL GATING; GENETICS; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN SUBUNIT; SITE DIRECTED MUTAGENESIS;

FLUORESCENCE; HUMANS; ION CHANNEL GATING; KCNQ1 POTASSIUM CHANNEL; KINETICS; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN CONFORMATION; PROTEIN SUBUNITS;

EID: 84899623184     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4750     Document Type: Article

References (34)

1. Hille, B. Ion Channels of Excitable Membranes (Sinauer Associates, Inc., 2001).
2. Sun, X., Zaydman, M. A. & Cui, J. Regulation of voltage-activated K(+) channel gating by transmembrane beta subunits. Front. Pharmacol. 3, 63 (2012).
3. Jespersen, T., Grunnet, M. & Olesen, S. P. The KCNQ1 potassium channel: from gene to physiological function. Physiology (Bethesda) 20, 408-416 (2005). (Pubitemid 41812424)
4. Nerbonne, J. M. & Kass, R. S. Molecular physiology of cardiac repolarization. Physiol. Rev. 85, 1205-1253 (2005). (Pubitemid 41362269)
5. Moss, A. J. & Kass, R. S. Long QT syndrome: from channels to cardiac arrhythmias. J. Clin. Invest. 115, 2018-2024 (2005). (Pubitemid 41134137)
6. Goldman, A. M. et al. Arrhythmia in heart and brain: KCNQ1 mutations link epilepsy and sudden unexplained death. Sci. Transl. Med. 1, 2ra6 (2009).
7. Pusch, M., Magrassi, R., Wollnik, B. & Conti, F. Activation and inactivation of homomeric KvLQT1 potassium channels. Biophys. J. 75, 785-792 (1998). (Pubitemid 28357520)
8. Sanguinetti, M. C. et al. Coassembly of K(V)LQT1 and minK (IsK) proteins to form cardiac I(Ks) potassium channel. Nature 384, 80-83 (1996). (Pubitemid 26374592)
9. Barhanin, J. et al. K(V)LQT1 and lsK (minK) proteins associate to form the I(Ks) cardiac potassium current. Nature 384, 78-80 (1996). (Pubitemid 26374591)
10. Sesti, F. & Goldstein, S. A. Single-channel characteristics of wild-type IKs channels and channels formed with two minK mutants that cause long QT syndrome. J. Gen. Physiol. 112, 651-663 (1998). (Pubitemid 29001777)
11. Nakajo, K. & Kubo, Y. KCNE1 and KCNE3 stabilize and/or slow voltage sensing S4 segment of KCNQ1 channel. J. Gen. Physiol. 130, 269-281 (2007). (Pubitemid 47443289)
12. Ruscic, K. J. et al. IKs channels open slowly because KCNE1 accessory subunits slow the movement of S4 voltage sensors in KCNQ1 pore-forming subunits. Proc. Natl Acad. Sci. USA 110, E559-E566 (2013).
13. Osteen, J. D. et al. KCNE1 alters the voltage sensor movements necessary to open the KCNQ1 channel gate. Proc. Natl Acad. Sci. USA 107, 22710-22715 (2010).
14. Rocheleau, J. M. & Kobertz, W. R. KCNE peptides differently affect voltage sensor equilibrium and equilibration rates in KCNQ1 K+ channels. J. Gen. Physiol. 131, 59-68 (2008).
15. Long, S. B., Campbell, E. B. & Mackinnon, R. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309, 903-908 (2005). (Pubitemid 41099920)
16. Panaghie, G. & Abbott, G. W. The role of S4 charges in voltage-dependent and voltage-independent KCNQ1 potassium channel complexes. J. Gen. Physiol. 129, 121-133 (2007). (Pubitemid 46184870)
17. Chung, D. Y. et al. Location of KCNE1 relative to KCNQ1 in the I(KS) potassium channel by disulfide cross-linking of substituted cysteines. Proc. Natl Acad. Sci. USA 106, 743-748 (2009).
18. Lvov, A., Gage, S. D., Berrios, V. M. & Kobertz, W. R. Identification of a protein-protein interaction between KCNE1 and the activation gate machinery of KCNQ1. J. Gen. Physiol. 135, 607-618 (2010).
19. Xu, X., Jiang, M., Hsu, K. L., Zhang, M. & Tseng, G. N. KCNQ1 and KCNE1 in the IKs channel complex make state-dependent contacts in their extracellular domains. J. Gen. Physiol. 131, 589-603 (2008). (Pubitemid 351749199)
20. Soh, H. & Tzingounis, A. V. The specific slow afterhyperpolarization inhibitor UCL2077 is a subtype-selective blocker of the epilepsy associated KCNQ channels. Mol. Pharmacol. 78, 1088-1095 (2010).
21. Pathak, M., Kurtz, L., Tombola, F. & Isacoff, E. The cooperative voltage sensor motion that gates a potassium channel. J. Gen. Physiol. 125, 57-69 (2005). (Pubitemid 40130098)
22. Lerche, C. et al. Chromanol 293B binding in KCNQ1 (Kv7.1) channels involves electrostatic interactions with a potassium ion in the selectivity filter. Mol. Pharmacol. 71, 1503-1511 (2007). (Pubitemid 47010903)
23. Lai, L. P. et al. 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 (2005).
24. Li, Y. et al. KCNE1 enhances phosphatidylinositol 4, 5-bisphosphate (PIP2) sensitivity of IKs to modulate channel activity. Proc. Natl Acad. Sci. USA 108, 9095-9100 (2011).
25. Werry, D., Eldstrom, J., Wang, Z. & Fedida, D. Single-channel basis for the slow activation of the repolarizing cardiac potassium current, I(Ks). Proc. Natl Acad. Sci. USA 110, E996-1005 (2013).
26. Osteen, J. D. et al. Allosteric gating mechanism underlies the flexible gating of KCNQ1 potassium channels. Proc. Natl Acad. Sci. USA 109, 7103-7108 (2012).
27. Silva, J. & Rudy, Y. Subunit interaction determines IKs participation in cardiac repolarization and repolarization reserve. Circulation 112, 1384-1391 (2005). (Pubitemid 41291762)
28. Silva, J. R. et al. A multiscale model linking ion-channel molecular dynamics and electrostatics to the cardiac action potential. Proc. Natl Acad. Sci. USA 106, 11102-11106 (2009).
29. Schoppa, N. E., McCormack, K., Tanouye, M. A. & Sigworth, F. J. The size of gating charge in wild-type and mutant Shaker potassium channels. Science 255, 1712-1715 (1992).
30. Seoh, S. A., Sigg, D., Papazian, D. M. & Bezanilla, F. Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron 16, 1159-1167 (1996). (Pubitemid 26227237)
31. Aggarwal, S. K. & MacKinnon, R. Contribution of the S4 segment to gating charge in the Shaker K+ channel. Neuron 16, 1169-1177 (1996). (Pubitemid 26227238)
32. Zagotta, W. N., Hoshi, T. & Aldrich, R. W. Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J. Gen. Physiol. 103, 321-362 (1994). (Pubitemid 24068562)
33. Hirschberg, B., Rovner, A., Lieberman, M. & Patlak, J. Transfer of twelve charges is needed to open skeletal muscle Na+ channels. J. Gen. Physiol. 106, 1053-1068 (1995). (Pubitemid 26004351)
34. Stefani, E. & Bezanilla, F. Cut-open oocyte voltage-clamp technique. Methods Enzymol. 293, 300-318 (1998). (Pubitemid 29342494)