PIP2-dependent coupling is prominent in Kv7.1 due to weakened interactions between S4-S5 and S6

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Kasimova, Marina A ^a,b   Zaydman, Mark A ^c   Cui, Jianmin ^c   Tarek, Mounir ^a,d  

^a UNIVERSITÉ DE LORRAINE   (France)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; POTASSIUM CHANNEL KCNQ1;

BINDING SITE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY;

BINDING SITES; HUMANS; KCNQ1 POTASSIUM CHANNEL; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY;

EID: 84945219998     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07474     Document Type: Article

References (42)

1. Lu, Z., Klem, A. M., Ramu, Y. Ion conduction pore is conserved among potassium channels. Nature 413, 809-813 (2001).
2. Lu, Z., Klem, A. M., Ramu, Y. Coupling between voltage sensors and activation gate in voltage-gated K1 channels. J. Gen. Physiol. 120, 663-676 (2002).
3. Long, S. B., Campbell, E. B.,MacKinnon, R. Voltage Sensor of Kv1.2: Structural Basis of Electromechanical Coupling. Science 309, 903-908 (2005).
4. Labro, A. J. et al. Kv Channel Gating Requires a Compatible S4-S5 Linker and Bottom Part of S6, Constrained by Non-interacting Residues. J. Gen. Physiol. 132, 667-680 (2008).
5. Choveau, F. S. et al. KCNQ1 Channels Voltage Dependence through a Voltagedependent Binding of the S4-S5 Linker to the Pore Domain. J. Biol. Chem. 286, 707-716 (2011).
6. Haddad, G. A., Blunck, R. Mode shift of the voltage sensors in Shaker K1 channels is caused by energetic coupling to the pore domain. J. Gen. Physiol. 137, 455-472 (2011).
7. Choveau, F. S. et al. Opposite Effects of the S4-S5 Linker and PIP2 on Voltage-Gated Channel Function: KCNQ1/KCNE1 and Other Channels. Front. Pharmacol. 3 (2012).
8. Schow, E. V., Freites, J. A., Nizkorodov, A.,White, S. H., Tobias, D. J. Coupling between the voltage-sensing and pore domains in a voltage-gated potassium channel. Biochim. Biophys. Acta 1818, 1726-1736 (2012).
9. Zaydman,M. A. et al. Kv7.1 ion channels require a lipid to couple voltage sensing to pore opening. Proc. Natl. Acad. Sci. 110, 13180-13185 (2013).
10. Stephens, L., McGregor, A., Hawkins, P. Phosphoinositide-3-kinases: Regulation by cell surface receptors and function of 3-phosphorylated lipids, Biology of Phosphoinositides [Cockcroft, S. (ed.)] [32-107] (Oxford University Press, 2000).
11. Zhang, H. et al. PIP(2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37, 963-975 (2003).
12. Loussouarn, G. et al. Phosphatidylinositol-4,5-bisphosphate, PIP2, controls KCNQ1/KCNE1 voltage-gated potassium channels: a functional homology between voltage-gated and inward rectifier K1channels. EMBO J. 22, 5412-5421 (2003).
13. Eswar, N. et al. Comparative protein structure modeling using MODELLER. Curr. Protoc. Protein Sci. Chapter 2, Unit 2.9 (2007).
14. Long, S. B., Campbell, E. B., MacKinnon, R. Crystal structure of a mammalian voltage-dependent Shaker family K1 channel. Science 309, 897-903 (2005).
15. Zhang, Q. et al. Dynamic PIP2 interactions with voltage sensor elements contribute to KCNQ2 channel gating. Proc. Natl. Acad. Sci. 110, 20093-20098 (2013).
16. Park, K.-H. et al. Impaired KCNQ1-KCNE1 and Phosphatidylinositol-4,5-Bisphosphate Interaction Underlies the Long QT Syndrome. Circ. Res. 96, 730-739 (2005).
17. Thomas, A. M., Harmer, S. C., Khambra, T., Tinker, A. Characterization of a binding site for anionic phospholipids on KCNQ1. J. Biol. Chem. 286, 2088-2100 (2011).
18. Telezhkin, V., Reilly, J. M., Thomas, A. M., Tinker, A., Brown, D. A. Structural Requirements of Membrane Phospholipids for M-type Potassium Channel Activation and Binding. J. Biol. Chem. 287, 10001-10012 (2012).
19. Delemotte, L., Tarek, M., Klein, M. L., Amaral, C., Treptow, W. Intermediate states of the Kv1.2 voltage sensor from atomistic molecular dynamics simulations. Proc. Natl. Acad. Sci. U. S. A. 108, 6109-6114 (2011).
20. Vargas, E. et al. An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations. J. Gen. Physiol. 140, 587-594 (2012).
21. Boulet, I. R., Labro, A. J., Raes, A. L., Snyders, D. J. Role of the S6 C-terminus in KCNQ1 channel gating. J. Physiol. 585, 325-337 (2007).
22. Murata, Y., Iwasaki, H., Sasaki, M., Inaba, K., Okamura, Y. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435, 1239-1243 (2005).
23. Osteen, J. D. et al. KCNE1 alters the voltage sensor movements necessary to open the KCNQ1 channel gate. Proc. Natl. Acad. Sci. U. S. A. 107, 22710-22715 (2010).
24. Horovitz, A., Fersht, A. R. Strategy for analysing the co-operativity of intramolecular interactions in peptides and proteins. J. Mol. Biol. 214, 613-617 (1990).
25. Hernandez, C. C., Zaika, O., Shapiro, M. S. A Carboxy-terminal Inter-Helix Linker As the Site of Phosphatidylinositol 4,5-Bisphosphate Action on Kv7 (Mtype) K1 Channels. J. Gen. Physiol. 132, 361-381 (2008).
26. Coyan, F. C. et al. A Long QT Mutation Substitutes Cholesterol for Phosphatidylinositol-4,5-Bisphosphate in KCNQ1 Channel Regulation. PLoS ONE 9, e93255 (2014).
27. Eckey, K. et al. Novel Kv7.1-phosphatidylinositol 4,5-bisphosphate (PIP2) interaction sites uncovered by charge neutralization scanning. J. Biol. Chem. 289, 22749-22758 (2014).
28. Abderemane-Ali, F. et al. Dual effect of phosphatidyl (4,5)-bisphosphate PIP2 on Shaker K1 channels. J. Biol. Chem. 287, 36158-36167 (2012).
29. Rodriguez-Menchaca, A. A. et al. PIP2 controls voltage-sensor movement and pore opening of Kv channels through the S4-S5 linker. Proc. Natl. Acad. Sci. U. S. A. 109, E2399-2408 (2012).
30. Kasimova, M. A., Tarek, M., Shaytan, A. K., Shaitan, K. V., Delemotte, L. Voltage-gated ion channel modulation by lipids: Insights from molecular dynamics simulations. Biochim. Biophys. Acta 1838, 1322-1331 (2014).
31. Hackos, D. H., Chang, T.-H., Swartz, K. J. Scanning the Intracellular S6 Activation Gate in the Shaker K1 Channel. J. Gen. Physiol. 119, 521-531 (2002).
32. Miceli, F., Cilio, M. R., Taglialatela, M., Bezanilla, F. Gating currents from neuronal K(V)7.4 channels: general features and correlation with the ionic conductance. Channels Austin Tex 3, 274-283 (2009).
33. Ma, L.-J., Ohmert, I., Vardanyan, V. Allosteric features of KCNQ1 gating revealed by alanine scanning mutagenesis. Biophys. J. 100, 885-894 (2011).
34. Jensen, M. ∅. et al Mechanism of voltage gating in potassium channels. Science 336, 229-233 (2012).
35. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics. 23, 2947-2948 (2007).
36. Peng, D. et al. Purification and Structural Study of the Voltage-Sensor Domain of the Human KCNQ1 Potassium Ion Channel. Biochemistry (Mosc.) 53, 2032-2042 (2014).
37. Laskowski, R. A.,MacArthur, M. W.,Moss, D. S., Thornton, J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993).
38. Mackerell, A. D., Jr, Feig, M., Brooks, C. L., 3rd. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25, 1400-1415 (2004).
39. Klauda, J. B. et al. Update of the CHARMM all-atom additive force field for lipids: Validation on six lipid types. J. Phys. Chem. B 114, 7830-7843 (2010).
40. Lupyan, D., Mezei, M., Logothetis, D. E., Osman, R. A molecular dynamics investigation of lipid bilayer perturbation by PIP2. Biophys. J. 98, 240-247 (2010).
41. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926 (1983).
42. Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005).