S3-s4 linker length modulates the relaxed state of a Voltage-gated potassium channel

Biophysical Journal

Volumn 105, Issue 10, 2013, Pages 2312-2322

  Priest, Michael F ^a   Lacroix, Jérôme J ^a   Villalba Galea, Carlos A ^b   Bezanilla, Francisco ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SHAKER POTASSIUM CHANNEL;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL MEMBRANE; CHANNEL GATING; CHEMISTRY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN STABILITY;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; ION CHANNEL GATING; KINETICS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STABILITY; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS;

EID: 84887930044     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.09.053     Document Type: Article

References (49)

1. R. Olcese, and R. Latorre E. Stefani Correlation between charge movement and ionic current during slow inactivation in Shaker K+ channels J. Gen. Physiol. 110 1997 579 589
2. C.A. Villalba-Galea, and W. Sandtner F. Bezanilla S4-based voltage sensors have three major conformations Proc. Natl. Acad. Sci. USA 105 2008 17600 17607
3. A.J. Labro, and J.J. Lacroix F. Bezanilla Molecular mechanism for depolarization-induced modulation of Kv channel closure J. Gen. Physiol. 140 2012 481 493
4. J.J. Lacroix, A.J. Labro, and F. Bezanilla Properties of deactivation gating currents in Shaker channels Biophys. J. 100 2011 L28 L30
5. P.S. Tan, and M.D. Perry A.P. Hill Voltage-sensing domain mode shift is coupled to the activation gate by the N-terminal tail of hERG channels J. Gen. Physiol. 140 2012 293 306
6. S.A. Seoh, and D. Sigg F. Bezanilla Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel Neuron 16 1996 1159 1167
7. S.K. Aggarwal, and R. MacKinnon Contribution of the S4 segment to gating charge in the Shaker K+ channel Neuron 16 1996 1169 1177
8. Y. Xu, Y. Ramu, and Z. Lu A Shaker K+ channel with a miniature engineered voltage sensor Cell 142 2010 580 589
9. Y. Xu, and Y. Ramu Z. Lu Energetic role of the paddle motif in voltage gating of Shaker K(+) channels Nat. Struct. Mol. Biol. 20 2013 574 581
10. R. Sand, N. Sharmin, C. Morgan, and W.J. Gallin Fine-tuning of voltage sensitivity of the Kv1.2 potassium channel by inter-helix loop dynamics J Biol Chem. 288 2013 9686 9695
11. C. Gonzalez, and E. Rosenman R. Latorre Modulation of the Shaker K(+) channel gating kinetics by the S3-S4 linker J. Gen. Physiol. 115 2000 193 208
12. C. Gonzalez, and E. Rosenman R. Latorre Periodic perturbations in Shaker K+ channel gating kinetics by deletions in the S3-S4 linker Proc. Natl. Acad. Sci. USA 98 2001 9617 9623
13. J.B. Sørensen, and A. Cha F. Bezanilla Deletion of the S3-S4 linker in the Shaker potassium channel reveals two quenching groups near the outside of S4 J. Gen. Physiol. 115 2000 209 222
14. S.Y. Tsang, H. Lesso, and R.A. Li Dissecting the structural and functional roles of the S3-S4 linker of pacemaker (hyperpolarization-activated cyclic nucleotide-modulated) channels by systematic length alterations J. Biol. Chem. 279 2004 43752 43759
15. R. Mathur, and J. Zheng F.J. Sigworth Role of the S3-S4 linker in Shaker potassium channel activation J. Gen. Physiol. 109 1997 191 199
16. E. Perozo, and R. MacKinnon E. Stefani Gating currents from a nonconducting mutant reveal open-closed conformations in Shaker K+ channels Neuron 11 1993 353 358
17. T. Hoshi, W.N. Zagotta, and R.W. Aldrich Biophysical and molecular mechanisms of Shaker potassium channel inactivation Science 250 1990 533 538
18. S.B. Long, and X. Tao R. MacKinnon Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment Nature 450 2007 376 382
19. X. Chen, and Q. Wang J. Ma Structure of the full-length Shaker potassium channel Kv1.2 by normal-mode-based X-ray crystallographic refinement Proc. Natl. Acad. Sci. USA 107 2010 11352 11357
20. E. Vargas, F. Bezanilla, and B. Roux In search of a consensus model of the resting state of a voltage-sensing domain Neuron 72 2011 713 720
21. E. Stefani, and F. Bezanilla Cut-open oocyte voltage-clamp technique Methods Enzymol. 293 1998 300 318
22. R. Shirokov What's in gating currents? Going beyond the voltage sensor movement Biophys. J. 101 2011 512 514 discussion 515-516
23. G.A. Haddad, and R. Blunck Mode shift of the voltage sensors in Shaker K+ channels is caused by energetic coupling to the pore domain J. Gen. Physiol. 137 2011 455 472
24. A.L. Hodgkin, and A.F. Huxley The dual effect of membrane potential on sodium conductance in the giant axon of Loligo J. Physiol. 116 1952 497 506
25. Y. Yang, Y. Yan, and F.J. Sigworth How does the W434F mutation block current in Shaker potassium channels? J. Gen. Physiol. 109 1997 779 789
26. T.M. Gamal El-Din, and G.Q. Martinez W.A. Catterall A gating charge interaction required for late slow inactivation of the bacterial sodium channel NavAb J. Gen. Physiol. 142 2013 181 190
27. Naranjo, D., L. Kolmakova-Partensky, and C. Miller. 1997. Expression of split Shaker K channels in Xenopus oocytes. 1997 Biophysical Society Meeting Abstracts. Biophysical Journal, Supplement, A11, Abstract, M-AM-G4.
28. A. Broomand, and R. Männikkö F. Elinder Molecular movement of the voltage sensor in a K channel J. Gen. Physiol. 122 2003 741 748
29. U. Henrion, and J. Renhorn F. Elinder Tracking a complete voltage-sensor cycle with metal-ion bridges Proc. Natl. Acad. Sci. USA 109 2012 8552 8557
30. T.M. Gamal El-Din, and H. Heldstab N.G. Greeff Double gaps along Shaker S4 demonstrate omega currents at three different closed states Channels (Austin) 4 2010 93 100
31. D.J. Posson, and P.R. Selvin Extent of voltage sensor movement during gating of Shaker K+ channels Neuron 59 2008 98 109
32. D. Sigg, and F. Bezanilla Total charge movement per channel. The relation between gating charge displacement and the voltage sensitivity of activation J. Gen. Physiol. 109 1997 27 39
33. M.O. Jensen, and V. Jogini D.E. Shaw Mechanism of voltage gating in potassium channels Science 336 2012 229 233
34. V. Tiriveedhi, and M. Miller M. Li Autonomous transmembrane segment S4 of the voltage sensor domain partitions into the lipid membrane Biochim. Biophys. Acta 1818 2012 1698 1705
35. L. Tu, and J. Wang C. Deutsch Transmembrane biogenesis of Kv1.3 Biochemistry 39 2000 824 836
36. Y. Sato, and M. Sakaguchi N. Uozumi Integration of Shaker-type K+ channel, KAT1, into the endoplasmic reticulum membrane: synergistic insertion of voltage-sensing segments, S3-S4, and independent insertion of pore-forming segments, S5-P-S6 Proc. Natl. Acad. Sci. USA 99 2002 60 65
37. L.W. Tu, and C. Deutsch A folding zone in the ribosomal exit tunnel for Kv1.3 helix formation J. Mol. Biol. 396 2010 1346 1360
38. D.R. Piper, and A. Varghese M. Tristani-Firouzi Gating currents associated with intramembrane charge displacement in HERG potassium channels Proc. Natl. Acad. Sci. USA 100 2003 10534 10539
39. K. Dougherty, and M. Covarrubias A dipeptidyl aminopeptidase-like protein remodels gating charge dynamics in Kv4.2 channels J. Gen. Physiol. 128 2006 745 753
40. K. Dougherty, and L. Tu M. Covarrubias The dipeptidyl-aminopeptidase-like protein 6 is an integral voltage sensor-interacting beta-subunit of neuronal K(V)4.2 channels Channels (Austin) 3 2009 122 128
41. S. Zhang, S.J. Kehl, and D. Fedida Modulation of Kv1.5 potassium channel gating by extracellular zinc Biophys. J. 81 2001 125 136
42. M. Taglialatela, and E. Stefani Gating currents of the cloned delayed-rectifier K+ channel DRK1 Proc. Natl. Acad. Sci. USA 90 1993 4758 4762
43. C.C. Shieh, K.G. Klemic, and G.E. Kirsch Role of transmembrane segment S5 on gating of voltage-dependent K+ channels J. Gen. Physiol. 109 1997 767 778
44. A. Kuzmenkin, F. Bezanilla, and A.M. Correa Gating of the bacterial sodium channel, NaChBac: voltage-dependent charge movement and gating currents J. Gen. Physiol. 124 2004 349 356
45. F. Bezanilla, R.E. Taylor, and J.M. Fernández Distribution and kinetics of membrane dielectric polarization. 1. Long-term inactivation of gating currents J. Gen. Physiol. 79 1982 21 40
46. R. Shirokov, and R. Levis E. Ríos Two classes of gating current from L-type Ca channels in guinea pig ventricular myocytes J. Gen. Physiol. 99 1992 863 895
47. S.J. Goodchild, and H. Xu D. Fedida Basis for allosteric open-state stabilization of voltage-gated potassium channels by intracellular cations J. Gen. Physiol. 140 2012 495 511
48. F. Abderemane-Ali, and Z. Es-Salah-Lamoureux G. Loussouarn Dual effect of phosphatidylinositol (4,5)-bisphosphate PIP(2) on Shaker K(+) channels J. Biol. Chem. 287 2012 36158 36167
49. A.A. Rodriguez-Menchaca, and S.K. Adney D.E. Logothetis PIP2 controls voltage-sensor movement and pore opening of Kv channels through the S4-S5 linker Proc. Natl. Acad. Sci. USA 109 2012 E2399 E2408