Probing the structural basis for differential KCNQ1 modulation by KCNE1 and KCNE2

Journal of General Physiology

Volumn 140, Issue 6, 2012, Pages 653-669

  Wang, Yuhong ^a   Zhang, Mei ^a   Xu, Yu ^a   Jiang, Min ^a   Zankov, Dimitar P ^a   Cui, Meng ^a   Tseng, Gea Ny ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; POTASSIUM CHANNEL KCNQ1; VOLTAGE GATED POTASSIUM CHANNEL;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL STRAIN COS1; CERCOPITHECUS; CHANNEL GATING; CHEMICAL STRUCTURE; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MUTAGENESIS; OOCYTE; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; CYSTEINE; ION CHANNEL GATING; KCNQ1 POTASSIUM CHANNEL; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; OOCYTES; POTASSIUM CHANNELS, VOLTAGE-GATED;

EID: 84871025455     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210847     Document Type: Article

References (42)

1. Abbott, G.W., F. Sesti, I. Splawski, M.E. Buck, M.H. Lehmann, K.W. Timothy, M.T. Keating, and S.A.N. Goldstein. 1999. MiRP1 forms IKr potassium channels with HERG and is associated with cardiac arrhythmia. Cell. 97:175-187.http://dx.doi.org/10.1016/S0092-8674(00)80728-X
2. Abraham, R.L., T. Yang, M. Blair, D.M. Roden, and D. Darbar. 2010. Augmented potassium current is a shared phenotype for two genetic defects associated with familial atrial fibrillation. J. Mol. Cell. Cardiol. 48:181-190.http://dx.doi.org/10.1016/j.yjmcc.2009.07.020
3. Bendahhou, S., C. Marionneau, K. Haurogne, M.-M. Larroque, R. Derand, V. Szuts, D. Escande, S. Demolombe, and J. Barhanin. 2005. In vitro molecular interactions and distribution of KCNE family with KCNQ1 in the human heart. Cardiovasc. Res. 67:529-538.http://dx.doi.org/10.1016/j.cardiores.2005.02.014
4. Campos, F.V., B. Chanda, B. Roux, and F. Bezanilla. 2007. Two atomic constraints unambiguously position the S4 segment relative to S1 and S2 segments in the closed state of Shaker K channel. Proc. Natl. Acad. Sci. USA. 104:7904-7909.http://dx.doi.org/10.1073/pnas.0702638104
5. Chan, P.J., J.D. Osteen, D. Xiong, M.S. Bohnen, D. Doshi, K.J. Sampson, S.O. Marx, A. Karlin, and R.S. Kass. 2012. Characterization of KCNQ1 atrial fibrillation mutations reveals distinct dependence on KCNE1. J. Gen. Physiol. 139:135-144.http://dx.doi.org/10.1085/jgp.201110672
6. Chen, H., and S.A.N. Goldstein. 2007. Serial perturbation of MinK in IKs implies an α-helical transmembrane span traversing the channel corpus. Biophys. J. 93:2332-2340.http://dx.doi.org/10.1529/biophysj.107.109702
7. Chen, Y.-H., S.-J. Xu, S. Bendahhou, X.-L. Wang, Y. Wang, W.-Y. Xu, H.-W. Jin, H. Sun, X.-Y. Su, Q.-N. Zhuang, et al. 2003. KCNQ1 gain-of-function mutation in familial atrial fibrillation. Science. 299:251-254.http://dx.doi.org/10.1126/science.1077771
8. Chung, D.Y., P.J. Chan, J.R. Bankston, L. Yang, G. Liu, S.O. Marx, A. Karlin, and R.S. Kass. 2009. 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.http://dx.doi.org/10.1073/pnas.0811897106
9. Gagnon, D.G., and F. Bezanilla. 2010. The contribution of individual subunits to the coupling of the voltage sensor to pore opening in Shaker K channels: effect of ILT mutations in heterotetramers. J. Gen. Physiol. 136:555-568.http://dx.doi.org/10.1085/jgp.201010487
10. Hong, K., D.R. Piper, A. Diaz-Valdecantos, J. Brugada, A. Oliva, E. Burashnikov, J. Santos-de-Soto, J. Grueso-Montero, E. Diaz-Enfante, P. Brugada, et al. 2005. De novo KCNQ1 mutation responsible for atrial fibrillation and short QT syndrome in utero. Cardiovasc. Res. 68:433-440.http://dx.doi.org/10.1016/j.cardiores.2005.06.023
11. Jiang, M., M. Zhang, D.G. Tang, H.F. Clemo, J. Liu, D. Holwitt, V. Kasirajan, A.L. Pond, E. Wettwer, and G.-N. Tseng. 2004. KCNE2 protein is expressed in ventricles of different species, and changes in its expression contribute to electrical remodeling in diseased hearts. Circulation. 109:1783-1788.http://dx.doi.org/10.1161/01.CIR.0000124225.43852.50
12. Jiang, M., M. Zhang, I.V. Maslennikov, J. Liu, D.M. Wu, Y.V. Korolkova, A.S. Arseniev, E.V. Grishin, and G.-N. Tseng. 2005. Dynamic conformational changes of extracellular S5-P linkers in the hERG channel. J. Physiol. 569:75-89.http://dx.doi.org/10.1113/jphysiol.2005.093682
13. Jost, N., L. Virág, M. Bitay, J. Takács, C. Lengyel, P. Biliczki, Z. Nagy, G. Bogáts, D.A. Lathrop, J.G. Papp, and A. Varró. 2005. Restricting excessive cardiac action potential and QT prolongation: a vital role for IKs in human ventricular muscle. Circulation. 112:1392-1399.http://dx.doi.org/10.1161/CIRCULATIONAHA.105.550111
14. Kang, C., C. Tian, F.D. Sönnichsen, J.A. Smith, J. Meiler, A.L. George Jr., C.G. Vanoye, H.J. Kim, and C.R. Sanders. 2008. Structure of KCNE1 and implications for how it modulates the KCNQ1 potassium channel. Biochemistry. 47:7999-8006.http://dx.doi.org/10.1021/bi800875q
15. Liu, Y., and R.H. Joho. 1998. A side chain in S6 influences both open-state stability and ion permeation in a voltage-gated K+ channel. Pflugers Arch. 435:654-661.http://dx.doi.org/10.1007/s004240050566
16. Liu, X.-S., M. Zhang, M. Jiang, D.-M. Wu, and G.-N. Tseng. 2007. Probing the interaction between KCNE2 and KCNQ1 in their transmembrane regions. J. Membr. Biol. 216:117-127.http://dx.doi.org/10.1007/s00232-007-9047-7
17. Long, S.B., X. Tao, E.B. Campbell, and R. MacKinnon. 2007. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature. 450:376-382.http://dx.doi.org/10.1038/nature06265
18. Lvov, A., S.D. Gage, V.M. Berrios, and W.R. Kobertz. 2010. Identification of a protein-protein interaction between KCNE1 and the activation gate machinery of KCNQ1. J. Gen. Physiol. 135: 607-618.http://dx.doi.org/10.1085/jgp.200910386
19. Melman, Y.F., A. Domènech, S. de la Luna, and T.V. McDonald. 2001. Structural determinants of KvLQT1 control by the KCNE family of proteins. J. Biol. Chem. 276:6439-6444.http://dx.doi.org/10.1074/jbc.M010713200
20. Nakajo, K., and Y. Kubo. 2007. KCNE1 and KCNE3 stabilize and/or slow voltage sensing S4 segment of KCNQ1 channel. J. Gen. Physiol. 130:269-281.http://dx.doi.org/10.1085/jgp.200709805
21. Osteen, J.D., C. Gonzalez, K.J. Sampson, V. Iyer, S. Rebolledo, H.P. Larsson, and R.S. Kass. 2010. KCNE1 alters the voltage sensor movements necessary to open the KCNQ1 channel gate. Proc. Natl. Acad. Sci. USA. 107:22710-22715.http://dx.doi.org/10.1073/pnas.1016300108
22. Rocheleau, J.M., and W.R. Kobertz. 2008. KCNE peptides differently affect voltage sensor equilibrium and equilibration rates in KCNQ1 K+ channels. J. Gen. Physiol. 131:59-68.http://dx.doi.org/10.1085/jgp.200709816
23. Sanguinetti, M.C., M.E. Curran, A. Zou, J. Shen, P.S. Spector, D.L. Atkinson, and M.T. Keating. 1996. Coassembly of K(V)LQT1 and minK (IsK) proteins to form cardiac I(Ks) potassium channel. Nature. 384:80-83.http://dx.doi.org/10.1038/384080a0
24. Schreibmayer, W., H.A. Lester, and N. Dascal. 1994. Voltage clamping of Xenopus laevis oocytes utilizing agarose-cushion electrodes. Pflugers Arch. 426:453-458.http://dx.doi.org/10.1007/BF00388310
25. Seebohm, G., M.C. Sanguinetti, and M. Pusch. 2003. Tight coupling of rubidium conductance and inactivation in human KCNQ1 potassium channels. J. Physiol. 552:369-378.http://dx.doi.org/10.1113/jphysiol.2003.046490
26. Seebohm, G., N. Strutz-Seebohm, O.N. Ureche, R. Baltaev, A. Lampert, G. Kornichuk, K. Kamiya, T.V. Wuttke, H. Lerche, M.C. Sanguinetti, and F. Lang. 2006. Differential roles of S6 domain hinges in the gating of KCNQ potassium channels. Biophys. J. 90:2235-2244.http://dx.doi.org/10.1529/biophysj.105.067165
27. + channels. PLoS One. 3:e1943.
28. Splawski, I., J. Shen, K.W. Timothy, M.H. Lehmann, S.G. Priori, J.L. Robinson, A.J. Moss, P.J. Schwartz, J.A. Towbin, G.M. Vincent, and M.T. Keating. 2000. Spectrum of mutations in long-QT syndrome genes. KVLQT1, HERG, SCN5A, KCNE1, and KCNE2. Circulation. 102:1178-1185.http://dx.doi.org/10.1161/01.CIR.102.10.1178
29. Tai, K.K., and S.A.N. Goldstein. 1998. The conduction pore of a cardiac potassium channel. Nature. 391:605-608.http://dx.doi.org/10.1038/35416
30. Tao, X., A. Lee, W. Limapichat, D.A. Dougherty, and R. MacKinnon. 2010. A gating charge transfer center in voltage sensors. Science. 328:67-73.http://dx.doi.org/10.1126/science.1185954
31. Tapper, A.R., and A.L. George Jr. 2000. MinK subdomains that mediate modulation of and association with KvLQT1. J. Gen. Physiol. 116:379-390.http://dx.doi.org/10.1085/jgp.116.3.379
32. Tapper, A.R., and A.L. George Jr. 2001. Location and orientation of minK within the IKs potassium channel complex. J. Biol. Chem. 276:38249-38254.
33. Tinel, N., S. Diochot, M. Borsotto, M. Lazdunski, and J. Barhanin. 2000. KCNE2 confers background current characteristics to the cardiac KCNQ1 potassium channel. EMBO J 19:6326-6330.http://dx.doi.org/10.1093/emboj/19.23.6326
34. + channel (minK) subunits. J. Physiol. 510:37-45.http://dx.doi.org/10.1111/j.1469-7793.1998.037bz.x
35. Wang, K.-W., K.K. Tai, and S.A.N. Goldstein. 1996. MinK residues line a potassium channel pore. Neuron. 16:571-577.http://dx.doi.org/10.1016/S0896-6273(00)80076-8
36. Wang, Y.-H., M. Jiang, X.-L. Xu, K.-L. Hsu, M. Zhang, and G.-N. Tseng. 2011. Gating-related molecular motions in the extracellular domain of the IKs channel: implications for IKs channelopathy. J. Membr. Biol. 239:137-156.http://dx.doi.org/10.1007/s00232-010-9333-7
37. Wu, D.-M., M. Jiang, M. Zhang, X.-S. Liu, Y.V. Korolkova, and G.-N. Tseng. 2006. KCNE2 is colocalized with KCNQ1 and KCNE1 in cardiac myocytes and may function as a negative modulator of IKs current amplitude in the heart. Heart Rhythm. 3:1469-1480.http://dx.doi.org/10.1016/j.hrthm.2006.08.019
38. Wu, D., K. Delaloye, M.A. Zaydman, A. Nekouzadeh, Y. Rudy, and J. Cui. 2010. State-dependent electrostatic interactions of S4 arginines with E1 in S2 during Kv7.1 activation. J. Gen. Physiol. 135:595-606.http://dx.doi.org/10.1085/jgp.201010408
39. Xu, X.-L., M. Jiang, K.-L. Hsu, M. Zhang, and G.-N. Tseng. 2008. KCNQ1 and KCNE1 in the IKs channel complex make statedependent contacts in their extracellular domains. J. Gen. Physiol. 131:589-603.http://dx.doi.org/10.1085/jgp.200809976
40. Yang, Y., M. Xia, Q. Jin, S. Bendahhou, J. Shi, Y. Chen, B. Liang, J. Lin, Y. Liu, B. Liu, et al. 2004. Identification of a KCNE2 gain-offunction mutation in patients with familial atrial fibrillation. Am. J. Hum. Genet. 75:899-905.http://dx.doi.org/10.1086/425342
41. Zhang, M., M. Jiang, and G.-N. Tseng. 2001. minK-related peptide 1 associates with Kv4.2 and modulates its gating function: potential role as β subunit of cardiac transient outward channel? Circ. Res. 88:1012-1019.http://dx.doi.org/10.1161/hh1001.090839
42. Zhang, M., Y.-H. Wang, M. Jiang, D.P. Zankov, S.R. Chowdhury, V. Kasirajan, and G.-N. Tseng. 2012. KCNE2 protein is more abundant in ventricles than in atria and can accelerate hERG protein degradation in a phosphorylation-dependent manner. Am. J. Physiol. Heart Circ. Physiol. 302:H910-H922.http://dx.doi.org/10.1152/ajpheart.00691.2011