Structural investigation of the transmembrane domain of KCNE1 in proteoliposomes

Biochemistry

Volumn 53, Issue 40, 2014, Pages 6392-6401

  Sahu, Indra D ^a   Kroncke, Brett M ^b   Zhang, Rongfu ^a   Dunagan, Megan M ^a   Smith, Hubbell J ^a   Craig, Andrew ^a   McCarrick, Robert M ^a   Sanders, Charles R ^b   Lorigan, Gary A ^a  

^a MIAMI UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOLIPOSOMES; STRUCTURAL INVESTIGATION; TRANS-MEMBRANE DOMAINS;

DETERGENT; NANOPARTICLE; POTASSIUM CHANNEL KCNE1; POTASSIUM CHANNEL KCNQ1; PROTEOLIPOSOME; 1-PALMITOYL-2-OLEOYLGLYCERO-3-PHOSPHOGLYCEROL; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; KCNE1 PROTEIN, HUMAN; LIPID BILAYER; LIPOSOME; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL; VOLTAGE GATED POTASSIUM CHANNEL;

ANALYTIC METHOD; ARTICLE; ARTIFACT; BILAYER MEMBRANE; DOUBLE ELECTRON ELECTRON RESONANCE; GENE OVEREXPRESSION; HYPOTHESIS; MICELLE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SIMULATION; SITE DIRECTED MUTAGENESIS; SPIN LABELING; AMINO ACID SUBSTITUTION; CHEMISTRY; GENETICS; HUMAN; LIPID BILAYER; MOLECULAR DYNAMICS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

AMINO ACID SUBSTITUTION; HUMANS; LIPID BILAYERS; LIPOSOMES; MOLECULAR DYNAMICS SIMULATION; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 84908032225     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500943p     Document Type: Article

References (57)

1. Kang, C., Tian, C., Sonnichsen, F. D., Smith, J. A., Meiler, J., George, A. L. J., 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
2. Tai, K. K. and Goldstein, S. A. N. (1998) The conduction pore of a cardiac potassium channel Nature 391, 605-608
3. Uysal, S., Vasquez, V., Tereshko, V., Esaki, K., Fellouse, F. A., Sidhu, S. S., Koide, S., Perozo, E., and Kossiakoff, A. (2009) Crystal structure of full-length KcsA in its closed conformation Proc. Natl. Acad. Sci. U.S.A. 106, 6644-6649
4. Ketchum, K. A., Joiner, W. J., Sellers, A. J., Kaczmarek, L. K., and Goldstein, S. A. N. (1995) A new family of outwardly rectifying potassium channel proteins with 2 pore domains in tandem Nature 376, 690-695
5. Herlyn, H., Zechner, U., Oswald, F., Pfeufer, A., Zischler, H., and Haaf, T. (2009) Positive selection at codon 38 of the human KCNE1 (minK) gene and sporadic absence of 38Ser-coding mRNAs in Gly38Ser heterozygotes BMC Evol. Biol. 9, 188
6. Vanoye, C. G., Welch, R. C., Tian, C., Sanders, C. R., and George, A. L. J. (2010) KCNQ1/KCNE1 assembly, co-translation not required Channels 4, 108-114
7. Kang, C. B., Vanoye, C. G., Welch, R. C., Van Horn, W. D., and Sanders, C. R. (2010) Functional delivery of a membrane protein into oocyte membranes using bicelles Biochemistry 49, 653-655
8. Huang, F. D., Chen, J., Lin, M., Keating, M. T., and Sanguinetti, M. C. (2001) Long-QT syndrome-associated missense mutations in the pore helix of the HERG potassium channel Circulation 104, 1071-1075
9. Tapper, A. R. and George, A. L. (2000) MinK subdomains that mediate modulation of and association with KvLQT1 J. Gen. Physiol. 116, 379-390
10. Wang, Y., Zhang, M., Xu, Y., Jiang, M., Zankov, D. P., Cui, M., and Tseng, G.-N. (2012) Probing the structural basis for differential KCNQ1 modulation by KCNE1 and KCNE2 J. Gen. Physiol. 140, 653-669
11. Melman, Y. F., Um, S. Y., Krumerman, A., Kagan, A., and McDonald, T. V. (2004) KCNE1 binds to the KCNQ1 pore to regulate potassium channel activity Neuron 42, 927-937
12. Tian, C., Vanoye, C. G., Kang, C., Welch, R. C., Kim, H. J., George, A. L., and Sanders, C. R. (2007) Preparation, functional characterization, and NMR studies of human KCNE1, a voltage-gated potassium channel accessory subunit associated with deafness and long QT syndrome Biochemistry 46, 11459-11472
13. Wang, Z., Fermini, B., and Nattel, S. (1994) Rapid and slow components of delayed rectifi er current in human atrial myocytes Cardiovasc. Res. 28, 1540-1546
14. Harmer, S. C. and Tinker, A. (2007) The role of abnormal trafficking of KCNE1 in long QT syndrome 5 Biochem. Soc. Trans. 35, 1074-1076
15. Gofman, Y., Shats, S., Attali, B., Haliloglu, T., and Ben-Tal, N. (2012) How does KCNE1 regulate the Kv7.1 potassium channel? Model-structure, mutations, and dynamics of the Kv7.1-KCNE1 complex Structure 20, 1343-1352
16. Xu, Y., Wang, Y., Meng, X.-Y., Zhang, M., Jiang, M., Cui, M., and Tseng, G.-N. (2013) Building KCNQ1/KCNE1 channel models and probing their interactions by molecular-dynamics simulations Biophys. J. 105, 2461-2473
17. Nakajo, K. and Kubo, Y. (2014) Steric hindrance between S4 and S5 of the KCNQ1/KCNE1 channel hampers pore opening Nat. Commun. 5, 4100-4100
18. Coey, A. T., Sahu, I. D., Gunasekera, T. S., Troxel, K. R., Hawn, J. M., Swartz, M. S., Wickenheiser, M. R., Reid, R. J., Welch, R. C., Vanoye, C. G., Kang, C. B., Sanders, C. R., and Lorigan, G. A. (2011) Reconstitution of KCNE1 into lipid bilayers: comparing the structural, dynamic, and activity differences in micelle and vesicle environments Biochemistry 50, 10851-10859
19. Barrett, P. J., Song, Y., Van Horn, W. D., Hustedt, E. J., Schafer, J. M., Hadziselimovic, A., Beel, A. J., and Sanders, C. R. (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol Science 336, 1168-1171
20. Sahu, I. D., MaCarrick, R. M., Troxel, K. R., Zhang, R., Smith, J. H., Dunagan, M. M., Swartz, M. S., Rajan, P. V., Kroncke, B. M., Sanders, C. R., and Lorigan, G. A. (2013) DEER EPR measurement for membrane protein structures via bifunctional spin labels and lipodisq nanoparticles Biochemistry 52, 6627-6632
21. Song, Y., Hustedt, E. J., Brandon, S., and Sanders, C. R. (2013) Competition between homodimerization and cholesterol binding to the C99 domain of the amyloid precursor protein Biochemistry 52, 5051-5064
22. Orwick-Rydmark, M., Lovett, J. E., Graziadei, A., Lindholm, L., Hicks, M. R., and Watts, A. (2012) Detergent-free incorporation of a seven-transmembrane receptor protein into nanosized bilayer lipodisq particles for functional and biophysical studies Nano Lett. 12, 4687-4692
23. Orwick, M. C., Judge, P. J., Procek, J., Lindholm, L., Graziadei, A., Engel, A., Grobner, G., and Watts, A. (2012) Detergent-free formation and physicochemical characterization of nanosized lipid-polymer complexes: lipodisq Angew. Chem., Int. Ed. 51, 4653-4657
24. Jeschke, G. (2012) DEER distance measurements on proteins Annu. Rev. Phys. Chem. 419-446
25. Feldmann, E. A., Ni, S., Sahu, I. D., Mishler, C. H., Risser, D. D., Murakami, J. L., Tom, S. K., McCarrick, R. M., Lorigan, G. A., Tolbert, B. S., Callahan, S. M., and Kennedy, M. A. (2011) Evidence for direct binding between HetR from Anabaena sp PCC 7120 and PatS-5 Biochemistry 50, 9212-9224
26. Jeschke, G., Chechik, V., Ionita, P., Godt, A., Zimmermann, H., Banham, J., Timmel, C. R., Hilger, D., and Jung, H. (2006) DeerAnalysis2006-a comprehensive software package for analyzing pulsed ELDOR data Appl. Magn. Reson. 30, 473-498
27. Chiang, Y. W., Borbat, P. P., and Freed, J. H. (2005) The determination of pair distance distributions by pulsed ESR using Tikhonov regularization J. Magn. Reson. 172, 279-295
28. Schwieters, C. D., Kuszewski, J. J., Tjandra, N., and Clore, G. M. (2003) The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160, 65-73
29. Schwieters, C. D., Kuszewski, J. J., and Clore, G. M. (2006) Using Xplor-NIH for NMR molecular structure determination Prog. Nucl. Magn. Reson. Spectrosc. 48, 47-62
30. Mokdad, A., Herrick, D. Z., Kahn, A. K., Andrews, E., Kim, M., and Cafiso, D. S. (2012) Ligand-induced structural changes in the Escherichia coli ferric citrate transporter reveal modes for regulating protein-protein interactions J. Mol. Biol. 423, 818-830
31. Herrick, D. Z., Kuo, W., Huang, H., Schwieters, C. D., Ellena, J. F., and Cafiso, D. S. (2009) Solution and membrane-bound conformations of the tandem C2A and C2B domains of synaptotagmin 1: evidence for bilayer bridging J. Mol. Biol. 390, 913-923
32. Jao, C. C., Hegde, B. G., Chen, J., Haworth, I. S., and Langen, R. (2008) Structure of membrane-bound alpha-synuclein from site-directed spin labeling and computational refinement Proc. Natl. Acad. Sci. U.S.A. 105, 19666-19671
33. Schwieters, C. D. and Clore, G. M. (2001) The VMD-XPLOR visualization package for NMR structure refinement J. Magn. Reson. 149, 239-244
34. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics J. Mol. Graphics 14, 33-38
35. MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102, 3586-3616
36. MacKerell, A. D., Feig, M., and Brooks, C. L. (2004) Improved treatment of the protein backbone in empirical force fields J. Am. Chem. Soc. 126, 698-699
37. Sezer, D., Freed, J. H., and Roux, B. (2008) Parametrization, molecular dynamics simulation, and calculation of electron spin resonance spectra of a nitroxide spin label on a polyalanine alpha-helix J. Phys. Chem. B 112, 5755-5767
38. Jo, S., Kim, T., Iyer, V. G., and Im, W. (2008) Software news and updates-CHARNIM-GUI: a web-based grraphical user interface for CHARMM J. Comput. Chem. 29, 1859-1865
39. Fleissner, M. R., Bridges, M. D., Brooks, E. K., Cascio, D., Kálai, T., Hideg, K., and Hubbell, W. L. (2012) Structure and dynamics of a conformationally constrained nitroxide side chain and applications in EPR spectroscopy Proc. Natl. Acad. Sci. U.S.A. 108, 16241-16246
40. Borbat, P. P., McHaourab, H. S., and Freed, J. H. (2002) Protein structure determination using long-distance constraints from double-quantum coherence ESR: study of T4 lysozyme J. Am. Chem. Soc. 124, 5304-5314
41. Jeschke, G. and Polyhach, Y. (2007) Distance measurements on spin-labelled biomacromolecules by pulsed electron paramagnetic resonance Phys. Chem. Chem. Phys. 9, 1895-1910
42. Sahu, I. D., McCarrick, R. M., and Lorigan, G. A. (2013) Use of electron paramagnetic resonance to solve biochemical problems Biochemistry 52, 5967-5984
43. McHaourab, H. S., Steed, P. R., and Kazmier, K. (2011) Toward the fourth dimension of membrane protein structure: insight into dynamics from spin-labeling EPR spectroscopy Structure 19, 1549-1561
44. Zou, P. and McHaourab, H. S. (2010) Increased sensitivity and extended range of distance measurements in spin-labeled membrane proteins: Q-band double electron-electron resonance and nanoscale bilayers Biophys. J. 98, L18-L20
45. Endeward, B., Butterwick, J. A., MacKinnon, R., and Prisner, T. F. (2009) Pulsed electron-electron double-resonance determination of spin-label distances and orientations on the tetrameric potassium ion channel KcsA J. Am. Chem. Soc. 131, 15246-15250
46. Zou, P., Bortolus, M., and McHaourab, H. S. (2009) Conformational cycle of the ABC transporter MsbA in liposomes: detailed analysis using double electron-electron resonance spectroscopy J. Mol. Biol. 393, 586-597
47. Georgieva, E. R., Ramlall, T. F., Borbat, P. P., Freed, J. H., and Eliezer, D. (2008) Membrane-bound alpha-synuclein forms an extended helix: long-distance pulsed ESR measurements using vesicles, bicelles, and rodlike micelles J. Am. Chem. Soc. 130, 12856-12857
48. Xu, Q., Ellena, J. F., Kim, M., and Cafiso, D. S. (2006) Substrate-dependent unfolding of the energy coupling motif of a membrane transport protein determined by double electron-electron resonance Biochemistry 45, 10847-10854
49. Dastvan, R., Bode, B. E., Karuppiah, M. P. R., Marko, A., Lyubenova, S., Schwalbe, H., and Prisner, T. F. (2010) Optimization of transversal relaxation of nitroxides for pulsed electron-electron double resonance spectroscopy in phospholipid membranes J. Phys. Chem. B 114, 13507-13516
50. Ghimire, H., McCarrick, R. M., Budil, D. E., and Lorigan, G. A. (2009) Significantly improved sensitivity of Q-band PELDOR/DEER experiments relative to X-band is observed in measuring the intercoil distance of a leucine zipper motif peptide (GCN4-LZ) Biochemistry 48, 5782-5784
51. Polyhach, Y., Bordignon, E., Tschaggelar, R., Gandra, S., Godt, A., and Jeschke, G. (2012) High sensitivity and versatility of the DEER experiment on nitroxide radical pairs at Q-band frequencies Phys. Chem. Chem. Phys. 14, 10762-10773
52. Li, Q., Wanderling, S., Sompornpisut, P., and Perozo, E. (2014) Structural basis of lipid-driven conformational transitions in the KvAP voltage-sensing domain Nat. Struct. Mol. Biol. 21, 160-166
53. Kucerka, N., Tristram-Nagle, S., and Nagle, J. F. (2005) Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains J. Membr. Biol. 208, 193-202
54. Tsai, H.-H. G., Lee, J.-B., Huang, J.-M., and Juwita, R. (2013) A Molecular dynamics study of the structural and dynamical properties of putative arsenic substituted lipid bilayers Int. J. Mol. Sci. 14, 7702-7715
55. Kandasamy, S. K. and Larson, R. G. (2006) Molecular dynamics simulations of model trans-membrane peptides in lipid bilayers: a systematic investigation of hydrophobic mismatch Biophys. J. 90, 2326-2343
56. Zhou, H.-X. and Cross, T. A. (2013) Influences of membrane mimetic environments on membrane protein structures Annu. Rev. Biophys. 42 42, 361-392
57. Sanders, C. R. and Mittendorf, K. F. (2011) Tolerance to changes in membrane lipid composition as a selected trait of membrane proteins Biochemistry 50, 7858-7867