Gating pore currents and the resting state of Nav1.4 voltage sensor domains

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 47, 2012, Pages 19250-19255

  Gosselin Badaroudine, Pascal ^a   Delemotte, Lucie ^b   Moreau, Adrien ^a   Klein, Michael L ^b   Chahine, Mohamed ^a,c  

^a CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^b Temple University   (United States)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

Ion channel; Molecular dynamics simulations; Omega currents; pH; Voltage clamp

Indexed keywords

AMINO ACID; HISTIDINE; ION CHANNEL; PROTON; SODIUM CHANNEL; TETRODOTOXIN; VOLTAGE GATED SODIUM CHANNEL; WATER;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; HYDROPHOBICITY; HYPERPOLARIZATION; MAMMAL; MOLECULAR DYNAMICS; MOLECULE; MUTATION; NONHUMAN; OOCYTE; PH; PRIORITY JOURNAL; PROTON TRANSPORT; SODIUM TRANSPORT; STRUCTURE ANALYSIS; XENOPUS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ELECTRIC CONDUCTIVITY; ION CHANNEL GATING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NAV1.4 VOLTAGE-GATED SODIUM CHANNEL; OOCYTES; POROSITY; PROTEIN STRUCTURE, TERTIARY; PROTONS; SEQUENCE ALIGNMENT; XENOPUS;

MAMMALIA;

EID: 84869806065     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1217990109     Document Type: Article

References (38)

1. Stühmer W, et al. (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature 339(6226):597-603.
2. Yang N, George AL, Jr., Horn R (1996) Molecular basis of charge movement in voltage-gated sodium channels. Neuron 16(1):113-122.
3. Chanda B, Bezanilla F (2002) Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J Gen Physiol 120(5):629-645.
4. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage- gated sodium channel. Nature 475(7356):353-358.
5. Yarov-Yarovoy V, et al. (2012) Structural basis for gating charge movement in the voltage sensor of a sodium channel. Proc Natl Acad Sci USA 109(2):E93-E102.
6. Tikhonov DB, Zhorov BS (2012) Architecture and pore block of eukaryotic voltage-gated sodium channels in view of NavAb bacterial sodium channel structure. Mol Pharmacol 82(1):97-104.
7. Sokolov S, Scheuer T, Catterall WA (2007) Gating pore current in an inherited ion channelopathy. Nature 446(7131):76-78.
8. Struyk AF, Cannon SC (2007) A Na+ channel mutation linked to hypokalemic periodic paralysis exposes a proton-selective gating pore. J Gen Physiol 130(1):11-20.
9. Sokolov S, Scheuer T, Catterall WA (2008) Depolarization-activated gating pore current conducted by mutant sodium channels in potassium-sensitive normokalemic periodic paralysis. Proc Natl Acad Sci USA 105(50):19980-19985.
10. Gosselin-Badaroudine P, et al. (2012) A proton leak current through the cardiac sodium channel is linked to mixed arrhythmia and the dilated cardiomyopathy phenotype. PLoS ONE 7(5):e38331.
11. Sokolov S, Scheuer T, Catterall WA (2005) Ion permeation through a voltage-sensitive gating pore in brain sodium channels having voltage sensor mutations. Neuron 47(2):183-189.
12. Starace DM, Bezanilla F (2004) A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427(6974):548-553.
13. Tombola F, Pathak MM, Isacoff EY (2005) Voltage-sensing arginines in a potassium channel permeate and occlude cation-selective pores. Neuron 45(3):379-388.
14. Delemotte L, Treptow W, Klein ML, Tarek M (2010) Effect of sensor domain mutations on the properties of voltage-gated ion channels: Molecular dynamics studies of the potassium channel Kv1.2. Biophys J 99(2):L72-L74.
15. Delemotte L, Tarek M, Klein ML, Amaral C, Treptow W (2011) Intermediate states of the Kv1.2 voltage sensor from atomistic molecular dynamics simulations. Proc Natl Acad Sci USA 108(15):6109-6114.
16. Jensen MØ, et al. (2012) Mechanism of voltage gating in potassium channels. Science 336(6078):229-233.
17. Khalili-Araghi F, Tajkhorshid E, Roux B, Schulten K (2012) Molecular dynamics investigation of the ω-current in the Kv1.2 voltage sensor domains. Biophys J 102(2):258-267.
18. Geissler PL, Dellago C, Chandler D, Hutter J, Parrinello M (2001) Autoionization in liquid water. Science 291(5511):2121-2124.
19. Hassanali A, Prakash MK, Eshet H, Parrinello M (2011) On the recombination of hydronium and hydroxide ions in water. Proc Natl Acad Sci USA 108(51):20410-20415.
20. Chen H, Wu Y, Voth GA (2006) Origins of proton transport behavior from selectivity domain mutations of the aquaporin-1 channel. Biophys J 90(10):L73-L75.
21. Starace DM, Bezanilla F (2001) Histidine scanning mutagenesis of basic residues of the S4 segment of the shaker k+ channel. J Gen Physiol 117(5):469-490.
22. Pomès R, Roux B (2002) Molecular mechanism of H+ conduction in the single-file water chain of the gramicidin channel. Biophys J 82(5):2304-2316.
23. Francis DG, Rybalchenko V, Struyk A, Cannon SC (2011) Leaky sodium channels from voltage sensor mutations in periodic paralysis, but not paramyotonia. Neurology 76(19):1635-1641.
24. Capes DL, Arcisio-Miranda M, Jarecki BW, French RJ, Chanda B (2012) Gating transitions in the selectivity filter region of a sodium channel are coupled to the domain IV voltage sensor. Proc Natl Acad Sci USA 109(7):2648-2653.
25. Chahine M, et al. (1994) Sodium channel mutations in paramyotonia congenita uncouple inactivation from activation. Neuron 12(2):281-294.
26. Bezanilla F (2005) The voltage-sensor structure in a voltage-gated channel. Trends Biochem Sci 30(4):166-168.
27. Treptow W, Tarek M (2006) Environment of the gating charges in the Kv1.2 Shaker potassium channel. Biophys J 90(9):L64-L66.
28. Krepkiy D, et al. (2009) Structure and hydration of membranes embedded with voltage-sensing domains. Nature 462(7272):473-479.
29. Pless SA, Galpin JD, Niciforovic AP, Ahern CA (2011) Contributions of counter-charge in a potassium channel voltage-sensor domain. Nat Chem Biol 7(9):617-623.
30. Jogini V, Roux B (2007) Dynamics of the Kv1.2 voltage-gated K+ channel in a membrane environment. Biophys J 93(9):3070-3082.
31. Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R (2010) A gating charge transfer center in voltage sensors. Science 328(5974):67-73.
32. Freites JA, Tobias DJ, White SH (2006) A voltage-sensor water pore. Biophys J 91(11):L90-L92.
33. MacCallum JL, Bennett WFD, Tieleman DP (2007) Partitioning of amino acid side chains into lipid bilayers: Results from computer simulations and comparison to experiment. J Gen Physiol 129(5):371-377.
34. Jurkat-Rott K, Groome J, Lehmann-Horn F (2012) Pathophysiological role of omega pore current in channelopathies. Front Pharmacol 3:112.
35. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403-410.
36. Pavlov E, Bladen C, Diao C, French RJ (2005) Bacterial Ion Channels and Their Eukaryotic Homologs, eds Kubalski A, Martinac B (ASM Press, Washington, DC), pp 191-207.
37. Payandeh J, Gamal El-Din TM, Scheuer T, Zheng N, Catterall WA (2012) Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486(7401):135-139.
38. Zhang X, et al. (2012) Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486(7401):130-134.