Dynamics of internal pore opening in KV channels probed by a fluorescent unnatural amino acid

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

Volumn 110, Issue 20, 2013, Pages 8272-8277

  Kalstrup, Tanja ^a   Blunck, Rikard ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Anap; Two color VCF

Indexed keywords

AMINO ACID DERIVATIVE; FLUORESCENT UNNATURAL AMINO ACID; TRANSFER RNA; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CRYSTALLOGRAPHY; ELECTROPHYSIOLOGY; FLUOROMETRY; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; VOLTAGE CLAMP FLUOROMETRY;

ANAP; TWO-COLOR VCF;

AMINO ACIDS; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DROSOPHILA MELANOGASTER; ELECTROPHYSIOLOGY; FLUORESCENT DYES; FLUOROMETRY; ION CHANNEL GATING; MOLECULAR DYNAMICS SIMULATION; MUTATION; OOCYTES; PATCH-CLAMP TECHNIQUES; PLASMIDS; PROTEIN STRUCTURE, TERTIARY; RNA, TRANSFER; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; XENOPUS LAEVIS;

EID: 84877847896     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220398110     Document Type: Article

References (53)

1. Long SB, Tao X, Campbell EB, MacKinnon R (2007) Atomic structure of a voltagedependent K+ channel in a lipid membrane-like environment. Nature 450(7168): 376-382. (Pubitemid 350126743)
2. Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltagedependent Shaker family K+ channel. Science 309(5736):897-903. (Pubitemid 41099919)
3. 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.
4. 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.
5. Jensen MO, et al. (2012) Mechanism of voltage gating in potassium channels. Science 336(6078):229-233.
6. Faure E, Starek G, McGuire H, Bernèche S, Blunck R (2012) A limited 4 Å radial displacement of the S4-S5 linker is sufficient for internal gate closing in Kv channels. J Biol Chem 287(47):40091-40098.
7. Bezanilla F, Perozo E, Stefani E (1994) Gating of Shaker K+ channels: II. The components of gating currents and a model of channel activation. Biophys J 66(4):1011-1021.
8. Zagotta WN, Hoshi T, Aldrich RW (1994) Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J Gen Physiol 103(2):321-362. (Pubitemid 24068562)
9. Schoppa NE, Sigworth FJ (1998) Activation of Shaker potassium channels. III. An activation gating model for wild-type and V2 mutant channels. J Gen Physiol 111(2):313-342. (Pubitemid 28113080)
10. Blunck R, Batulan Z (2012) Mechanism of electromechanical coupling in voltage-gated potassium channels. Front Pharmacol 3:166.
11. Cha A, Bezanilla F (1997) Characterizing voltage-dependent conformational changes in the Shaker K+ channel with fluorescence. Neuron 19(5):1127-1140. (Pubitemid 27512372)
12. Mannuzzu LM, Moronne MM, Isacoff EY (1996) Direct physical measure of conformational rearrangement underlying potassium channel gating. Science 271(5246): 213-216. (Pubitemid 26033303)
13. Cha A, Bezanilla F (1998) Structural implications of fluorescence quenching in the Shaker K+ channel. J Gen Physiol 112(4):391-408. (Pubitemid 28467597)
14. Bannister JP, Chanda B, Bezanilla F, Papazian DM (2005) Optical detection of ratedetermining ion-modulated conformational changes of the ether-à-go-go K+ channel voltage sensor. Proc Natl Acad Sci USA 102(51):18718-18723. (Pubitemid 43011292)
15. Savalli N, Kondratiev A, Toro L, Olcese R (2006) Voltage-dependent conformational changes in human Ca(2+)-and voltage-activated K(+) channel, revealed by voltageclamp fluorometry. Proc Natl Acad Sci USA 103(33):12619-12624. (Pubitemid 44267308)
16. Claydon TW, Fedida D (2007) Voltage clamp fluorimetry studies of mammalian voltage-gated K(+) channel gating. Biochem Soc Trans 35(Pt 5):1080-1082. (Pubitemid 350206434)
17. Blunck R, Starace DM, Correa AM, Bezanilla F (2004) Detecting rearrangements of shaker and NaChBac in real-time with fluorescence spectroscopy in patch-clamped mammalian cells. Biophys J 86(6):3966-3980. (Pubitemid 38780273)
18. Zheng J, Zagotta WN (2000) Gating rearrangements in cyclic nucleotide-gated channels revealed by patch-clamp fluorometry. Neuron 28(2):369-374.
19. Cha A, Ruben PC, George AL, Jr., Fujimoto E, Bezanilla F (1999) Voltage sensors in domains III and IV, but not I and II, are immobilized by Na+ channel fast inactivation. Neuron 22(1):73-87. (Pubitemid 29070095)
20. Meinild AK, Hirayama BA, Wright EM, Loo DD (2002) Fluorescence studies of ligandinduced conformational changes of the Na(+)/glucose cotransporter. Biochemistry 41(4):1250-1258. (Pubitemid 34083777)
21. Gagnon DG, et al. (2005) Membrane topology of loop 13-14 of the Na+/glucose cotransporter (SGLT1): A SCAM and fluorescent labelling study. Biochim Biophys Acta 1712(2):173-184. (Pubitemid 40799303)
22. Li M, Farley RA, Lester HA (2000) An intermediate state of the gamma-aminobutyric acid transporter GAT1 revealed by simultaneous voltage clamp and fluorescence. J Gen Physiol 115(4):491-508. (Pubitemid 30196596)
23. Li M, Lester HA (2002) Early fluorescence signals detect transitions at mammalian serotonin transporters. Biophys J 83(1):206-218. (Pubitemid 34694732)
24. Dahan DS, et al. (2004) A fluorophore attached to nicotinic acetylcholine receptor beta M2 detects productive binding of agonist to the alpha delta site. Proc Natl Acad Sci USA 101(27):10195-10200. (Pubitemid 38891218)
25. Nowak MW, et al. (1995) Nicotinic receptor binding site probed with unnatural amino acid incorporation in intact cells. Science 268(5209):439-442.
26. Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R (2010) A gating charge transfer center in voltage sensors. Science 328(5974):67-73.
27. 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.
28. Pantoja R, Rodriguez EA, Dibas MI, Dougherty DA, Lester HA (2009) Single-molecule imaging of a fluorescent unnatural amino acid incorporated into nicotinic receptors. Biophys J 96(1):226-237.
29. Lee HS, Guo J, Lemke EA, Dimla RD, Schultz PG (2009) Genetic incorporation of a small, environmentally sensitive, fluorescent probe into proteins in Saccharomyces cerevisiae. J Am Chem Soc 131(36):12921-12923.
30. Haddad GA, Blunck R (2011) Mode shift of the voltage sensors in Shaker K+ channels is caused by energetic coupling to the pore domain. J Gen Physiol 137(5):455-472.
31. Baker OS, Larsson HP, Mannuzzu LM, Isacoff EY (1998) Three transmembrane conformations and sequence-dependent displacement of the S4 domain in shaker K+ channel gating. Neuron 20(6):1283-1294. (Pubitemid 28293143)
32. Mannuzzu LM, Isacoff EY (2000) Independence and cooperativity in rearrangements of a potassium channel voltage sensor revealed by single subunit fluorescence. J Gen Physiol 115(3):257-268.
33. Cole KS, Moore JW (1960) Potassium ion current in the squid giant axon: Dynamic characteristic. Biophys J 1:1-14.
34. Sigg D, Bezanilla F, Stefani E (2003) Fast gating in the Shaker K+ channel and the energy landscape of activation. Proc Natl Acad Sci USA 100(13):7611-7615. (Pubitemid 36760017)
35. Freites JA, Schow EV, White SH, Tobias DJ (2012) Microscopic origin of gating current fluctuations in a potassium channel voltage sensor. Biophys J 102(11):L44-L46.
36. Ledwell JL, Aldrich RW (1999) Mutations in the S4 region isolate the final voltagedependent cooperative step in potassium channel activation. J Gen Physiol 113(3): 389-414. (Pubitemid 29219810)
37. 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. (Pubitemid 27255942)
38. McCormack K, Joiner WJ, Heinemann SH (1994) A characterization of the activating structural rearrangements in voltage-dependent Shaker K+ channels. Neuron 12(2): 301-315.
39. Loboda A, Armstrong CM (2001) Resolving the gating charge movement associated with late transitions in K channel activation. Biophys J 81(2):905-916. (Pubitemid 32721461)
40. Lu Z, Klem AM, Ramu Y (2001) Ion conduction pore is conserved among potassium channels. Nature 413(6858):809-813. (Pubitemid 33026842)
41. Labro AJ, et al. (2008) Kv channel gating requires a compatible S4-S5 linker and bottom part of S6, constrained by non-interacting residues. J Gen Physiol 132(6): 667-680.
42. Long SB, Campbell EB, Mackinnon R (2005) Voltage sensor of Kv1.2: Structural basis of electromechanical coupling. Science 309(5736):903-908. (Pubitemid 41099920)
43. Pantazis A, Olcese R (2012) Relative transmembrane segment rearrangements during BK channel activation resolved by structurally assigned fluorophore-quencher pairing. J Gen Physiol 140(2):207-218.
44. Pathak M, Kurtz L, Tombola F, Isacoff E (2005) The cooperative voltage sensor motion that gates a potassium channel. J Gen Physiol 125(1):57-69. (Pubitemid 40130098)
45. Gandhi CS, Loots E, Isacoff EY (2000) Reconstructing voltage sensor-pore interaction from a fluorescence scan of a voltage-gated K+ channel. Neuron 27(3):585-595.
46. Claydon TW, Vaid M, Rezazadeh S, Kehl SJ, Fedida D (2007) 4-aminopyridine prevents the conformational changes associated with p/c-type inactivation in shaker channels. J Pharmacol Exp Ther 320(1):162-172. (Pubitemid 46025731)
47. Villalba-Galea CA, Sandtner W, Starace DM, Bezanilla F (2008) S4-based voltage sensors have three major conformations. Proc Natl Acad Sci USA 105(46): 17600-17607.
48. Batulan Z, Haddad GA, Blunck R (2010) An intersubunit interaction between S4-S5 linker and S6 is responsible for the slow off-gating component in Shaker K+ channels. J Biol Chem 285(18):14005-14019.
49. 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.
50. Ding S, Horn R (2003) Effect of S6 tail mutations on charge movement in Shaker potassium channels. Biophys J 84(1):295-305. (Pubitemid 36026398)
51. Schoppa NE, Sigworth FJ (1998) Activation of Shaker potassium channels. II. Kinetics of the V2 mutant channel. J Gen Physiol 111(2):295-311. (Pubitemid 28113079)
52. Hoshi T, Zagotta WN, Aldrich RW (1990) Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250(4980):533-538. (Pubitemid 120031778)
53. Bezanilla F, Armstrong CM (1977) Inactivation of the sodium channel. I. Sodium current experiments. J Gen Physiol 70(5):549-566. (Pubitemid 8239321)