Moving gating charges through the gating pore in a Kv channel voltage sensor

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

Volumn 111, Issue 19, 2014, Pages

  Lacroix, Jérôme J ^a   Clark Hyde, H ^a   Campos, Fabiana V ^a   Bezanilla, Francisco ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Energy landscape; Global fit; Kinetic model

Indexed keywords

AMINO ACID; MEMBRANE PROTEIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV1.2;

ARTICLE; CELL STRUCTURE; CHANNEL GATING; DEPOLARIZATION; ENERGY; HYDROPHOBICITY; ION CURRENT; KINETICS; MUTAGENESIS; MUTANT; MUTATION; PHENOTYPE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN CONFORMATION; SENSOR;

ENERGY LANDSCAPE; GLOBAL FIT; KINETIC MODEL;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ION CHANNEL GATING; KINETICS; KV1.1 POTASSIUM CHANNEL; KV1.2 POTASSIUM CHANNEL; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; OOCYTES; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, SECONDARY; XENOPUS LAEVIS;

EID: 84900508031     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1406161111     Document Type: Article

References (69)

1. El Chemaly A, Demaurex N (2012) Do Hv1 proton channels regulate the ionic and redox homeostasis of phagosomes? Mol Cell Endocrinol 353(1-2):82-87.
2. Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435(7046):1239-1243.
3. Ben-Chaim Y, et al. (2006) Movement of "gating charge" is coupled to ligand binding in a G-protein-coupled receptor. Nature 444(7115):106-109.
4. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarization- activated cation channels: From genes to function. Physiol Rev 89(3):847-885.
5. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117(4):500-544.
6. Jensen MO, et al. (2012) Mechanism of voltage gating in potassium channels. Science 336(6078):229-233.
7. Jacobson DA, et al. (2010) Calcium-activated and voltage-gated potassium channels of the pancreatic islet impart distinct and complementary roles during secretagogue induced electrical responses. J Physiol 588(Pt 18):3525-3537.
8. Zhu X, Mose E, Zimmermann N (2013) Proton channel HVCN1 is required for effector functions of mouse eosinophils. BMC Immunol 14:24.
9. + channel. Science 309(5736):897-903.
10. Sasaki M, Takagi M, Okamura Y (2006) A voltage sensor-domain protein is a voltage-gated proton channel. Science 312(5773):589-592.
11. Ramsey IS, Moran MM, Chong JA, Clapham DE (2006) A voltage-gated proton-selective channel lacking the pore domain. Nature 440(7088):1213-1216.
12. + channel. Neuron 16(6):1159-1167.
13. + channel. Neuron 16(6):1169-1177.
14. 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.
15. Chanda B, Bezanilla F (2008) A common pathway for charge transport through voltage-sensing domains. Neuron 57(3):345-351.
16. Starace DM, Bezanilla F (2004) A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427(6974):548-553.
17. Campos FV, Chanda B, Roux B, Bezanilla F (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(19):7904-7909.
18. Ahern CA, Horn R (2005) Focused electric field across the voltage sensor of potassium channels. Neuron 48(1):25-29.
19. Asamoah OK, Wuskell JP, Loew LM, Bezanilla F (2003) A fluorometric approach to local electric field measurements in a voltage-gated ion channel. Neuron 37(1):85-97.
20. Islas LD, Sigworth FJ (2001) Electrostatics and the gating pore of Shaker potassium channels. J Gen Physiol 117(1):69-89.
21. Chen X, Wang Q, Ni F, Ma J (2010) Structure of the full-length Shaker potassium channel Kv1.2 by normal-mode-based X-ray crystallographic refinement. Proc Natl Acad Sci USA 107(25):11352-11357.
22. Chamberlin A, et al. (2014) Hydrophobic plug functions as a gate in voltage-gated proton channels. Proc Natl Acad Sci USA 111(2):E273-E282.
23. + channel in a lipid membrane-like environment. Nature 450(7168): 376-382.
24. Khalili-Araghi F, et al. (2010) Calculation of the gating charge for the Kv1.2 voltage-activated potassium channel. Biophys J 98(10):2189-2198.
25. 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.
26. Vargas E, Bezanilla F, Roux B (2011) In search of a consensus model of the resting state of a voltage-sensing domain. Neuron 72(5):713-720.
27. Vargas E, et al. (2012) An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations. J Gen Physiol 140(6): 587-594.
28. Imbrici P, D'Adamo MC, Kullmann DM, Pessia M (2006) Episodic ataxia type 1 mutations in the KCNA1 gene impair the fast inactivation properties of the human potassium channels Kv1.4-1.1/Kvbeta1.1 and Kv1.4-1.1/Kvbeta1.2. Eur J Neurosci 24(11): 3073-3083.
29. Browne DL, et al. (1995) Identification of two new KCNA1 mutations in episodic ataxia/myokymia families. Hum Mol Genet 4(9):1671-1672.
30. Adelman JP, Bond CT, Pessia M, Maylie J (1995) Episodic ataxia results from voltage-dependent potassium channels with altered functions. Neuron 15(6):1449-1454.
31. Zhu J, Alsaber R, Zhao J, Ribeiro-Hurley E, Thornhill WB (2012) Characterization of the Kv1.1 I262T and S342I mutations associated with episodic ataxia 1 with distinct phenotypes. Arch Biochem Biophys 524(2):99-105.
32. Singh NA, et al. (2009) A role of SCN9A in human epilepsies, as a cause of febrile seizures and as a potential modifier of Dravet syndrome. PLoS Genet 5(9):e1000649.
33. Yang P, et al. (2002) Allelic variants in long-QT disease genes in patients with drug-associated torsades de pointes. Circulation 105(16):1943-1948.
34. Paulussen AD, et al. (2004) Genetic variations of KCNQ1, KCNH2, SCN5A, KCNE1, and KCNE2 in drug-induced long QT syndrome patients. J Mol Med (Berl) 82(3):182-188.
35. Fujiwara T, et al. (2003) Mutations of sodium channel alpha subunit type 1 (SCN1A) in intractable childhood epilepsies with frequent generalized tonic-clonic seizures. Brain 126(Pt 3):531-546.
36. Petitprez S, et al. (2008) A novel dominant mutation of the Nav1.4 alpha-subunit domain I leading to sodium channel myotonia. Neurology 71(21):1669-1675.
37. Kwong AK, Fung CW, Chan SY, Wong VC (2012) Identification of SCN1A and PCDH19 mutations in Chinese children with Dravet syndrome. PLoS One 7(7):e41802.
38. + channel voltage sensor. Proc Natl Acad Sci USA 108(16):6444-6449.
39. + channel. J Gen Physiol 115(1):33-50.
40. Muroi Y, Arcisio-Miranda M, Chowdhury S, Chanda B (2010) Molecular determinants of coupling between the domain III voltage sensor and pore of a sodium channel. Nat Struct Mol Biol 17(2):230-237.
41. Soler-Llavina GJ, Chang TH, Swartz KJ (2006) Functional interactions at the interface between voltage-sensing and pore domains in the Shaker K(v) channel. Neuron 52(4): 623-634.
42. + channel. J Gen Physiol 119(6):521-532.
43. + channel. Neuron 25(2):411-423.
44. + channels. Neuron 18(4):675-682.
45. + channel. Cell 111(2):231-239.
46. Lacroix JJ, Campos FV, Frezza L, Bezanilla F (2013) Molecular bases for the asynchronous activation of sodium and potassium channels required for nerve impulse generation. Neuron 79(4):651-657.
47. Lacroix JJ, et al. (2012) Intermediate state trapping of a voltage sensor. J Gen Physiol 140(6):635-652.
48. Stefani E, Bezanilla F (1998) Cut-open oocyte voltage-clamp technique. Methods Enzymol 293:300-318.
49. Mathur R, Zhou J, Babila T, Koren G (1999) Ile-177 and Ser-180 in the S1 segment are critically important in Kv1.1 channel function. J Biol Chem 274(17):11487-11493.
50. + channels. Neuron 11(2):353-358.
51. Yang Y, Yan Y, Sigworth FJ (1997) How does the W434F mutation block current in Shaker potassium channels? J Gen Physiol 109(6):779-789.
52. Pless SA, Galpin JD, Niciforovic AP, Kurata HT, Ahern CA (2013) Hydrogen bonds as molecular timers for slow inactivation in voltage-gated potassium channels. Elife 2: e01289.
53. Lacroix JJ, Labro AJ, Bezanilla F (2011) Properties of deactivation gating currents in Shaker channels. Biophys J 100(5):L28-L30.
54. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157(1):105-132.
55. Hessa T, et al. (2005) Recognition of transmembrane helices by the endoplasmic re-ticulum translocon. Nature 433(7024):377-381.
56. Wimley WC, White SH (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 3(10):842-848.
57. Miller S, Janin J, Lesk AM, Chothia C (1987) Interior and surface of monomeric proteins. J Mol Biol 196(3):641-656.
58. Darby NJ, Creighton TE (1993) Protein Structure (Oxford Univ Press, Oxford).
59. Lacroix JJ, Bezanilla F (2012) Tuning the voltage-sensor motion with a single residue. Biophys J 103(3):L23-L25.
60. Musset B, et al. (2011) Aspartate 112 is the selectivity filter of the human voltage-gated proton channel. Nature 480(7376):273-277.
61. Lin MC, Hsieh JY, Mock AF, Papazian DM (2011) R1 in the Shaker S4 occupies the gating charge transfer center in the resting state. J Gen Physiol 138(2):155-163.
62. Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R (2010) A gating charge transfer center in voltage sensors. Science 328(5974):67-73.
63. Ledwell JL, Aldrich RW (1999) Mutations in the S4 region isolate the final voltage-dependent cooperative step in potassium channel activation. J Gen Physiol 113(3): 389-414.
64. + channel voltage-sensor domain creates a barrier with unidirectional effects. Bio-phys J 104(1):75-84.
65. Donald JE, Kulp DW, DeGrado WF (2011) Salt bridges: Geometrically specific, de-signable interactions. Proteins 79(3):898-915.
66. Papazian DM, Timpe LC, Jan YN, Jan LY (1991) Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence. Nature 349(6307):305-310.
67. + channels. J Biol Chem 285(18):14005-14019.
68. Bezanilla F, Villalba-Galea CA (2013) The gating charge should not be estimated by fitting a two-state model to a Q-V curve. J Gen Physiol 142(6):575-578.
69. + channel. J Gen Physiol 117(5):469-490.