Domain IV voltage-sensor movement is both sufficient and rate limiting for fast inactivation in sodium channels

Journal of General Physiology

Volumn 142, Issue 2, 2013, Pages 101-112

  Capes, Deborah L ^a,c   Goldschen Ohm, Marcel P ^a   Arcisio Miranda, Manoel ^a,d   Bezanilla, Francisco ^b   Chanda, Baron ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84883277214     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201310998     Document Type: Article

References (44)

1. Ackerman, M.J. 1998. The long QT syndrome: ion channel diseases of the heart. Mayo Clin. Proc. 73:250-269. http://dx.doi.org/10.4065/73.3.250
2. Aldrich, R.W., D.P. Corey, and C.F. Stevens. 1983. A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature. 306:436-441. http://dx.doi.org/10.1038/ 306436a0
3. Armstrong, C.M. 2006. Na channel inactivation from open and closed states. Proc. Natl. Acad. Sci. USA. 103:17991-17996. http:// dx.doi.org/10.1073/pnas.0607603103
4. Armstrong, C.M., and F. Bezanilla. 1977. Inactivation of the sodium channel. II. Gating current experiments. J. Gen. Physiol. 70:567- 590. http://dx.doi.org/10.1085/jgp.70.5.567
5. Bao, H., A. Hakeem, M. Henteleff, J.G. Starkus, and M.D. Rayner 1999. Voltage-insensitive gating after charge-neutralizing mutations in the S4 segment of Shaker channels. J. Gen. Physiol 113:139-151. http://dx.doi.org/10.1085/jgp.113.1.139
6. Bezanilla, F. 2000. The voltage sensor in voltage-dependent ion channels. Physiol. Rev. 80:555-592
7. Bosmans, F., M.-F. Martin-Eauclaire, and K.J. Swartz. 2008 Deconstructing voltage sensor function and pharmacology in sodium channels. Nature. 456:202-208. http://dx.doi.org/10.1038/ nature07473
8. Cannon, S.C. 1996. Sodium channel defects in myotonia and periodic paralysis. Annu. Rev. Neurosci. 19:141-164. http://dx.doi.org/10.1146/annurev.ne.19.030196.001041
9. Capes, D.L., M. Arcisio-Miranda, B.W. Jarecki, R.J. French, and B Chanda. 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. 109:2648-2653. http://dx.doi.org/ 10.1073/pnas.1115575109.
10. Catterall, W.A. 2010. Ion channel voltage sensors: structure, function, and pathophysiology. Neuron. 67:915-928. http://dx.doi.org/10.1016/j.neuron.2010.08.021.
11. Cha, A., P.C. Ruben, A.L. George Jr., E. Fujimoto, and F. Bezanilla. 1999. Voltage sensors in domains III and IV, but not I and II, are immobilized by Na+ channel fast inactivation. Neuron. 22:73-87 http://dx.doi.org/10.1016/S0896-6273(00)80680-7
12. Chahine, M., A.L. George Jr., M. Zhou, S. Ji, W. Sun, R.L. Barchi, and R. Horn. 1994. Sodium channel mutations in paramyotonia congenita uncouple inactivation from activation. Neuron. 12:281- 294. http://dx.doi.org/10.1016/0896-6273(94)90271-2
13. Chanda, B., and F. Bezanilla. 2002. Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J. Gen. Physiol. 120:629-645. http://dx.doi.org/ 10.1085/jgp.20028679
14. Chen, L.Q., V. Santarelli, R. Horn, and R.G. Kallen. 1996. A unique role for the S4 segment of domain 4 in the inactivation of sodium channels. J. Gen. Physiol. 108:549-556. http://dx.doi.org/10.1085/jgp.108.6.549
15. Colquhoun, D., and A.G. Hawkes. 1995. A Q-matrix cookbook. In Single-Channel Recording. B. Sakmann and E. Neher, editors Plenum Press, New York. 589-633
16. Eaholtz, G., T. Scheuer, and W.A. Catterall. 1994. Restoration of inactivation and block of open sodium channels by an inactivation gate peptide. Neuron. 12:1041-1048. http://dx.doi.org/10.1016/0896-6273(94)90312-3
17. Gagnon, D.G., and F. Bezanilla. 2009. A single charged voltage sensor is capable of gating the Shaker K+ channel. J. Gen. Physiol 133:467-483. http://dx.doi.org/10.1085/jgp.200810082
18. Goldschen-Ohm, M.P., D.L. Capes, K.M. Oelstrom, and B. Chanda. 2013. Multiple pore conformations driven by asynchronous movements of voltage sensors in a eukaryotic sodium channel Nat Commun. 4:1350. http://dx.doi.org/10.1038/ncomms2356
19. Gonoi, T., and B. Hille. 1987. Gating of Na channels. Inactivation modifiers discriminate among models. J. Gen. Physiol. 89:253-274 http://dx.doi.org/10.1085/jgp.89.2.253
20. Hanck, D.A., and M.F. Sheets. 2007. Site-3 toxins and cardiac sodium channels. Toxicon. 49:181-193. http://dx.doi.org/10.1016/j.toxicon.2006.09.017
21. Hayward, L.J., R.H. Brown Jr., and S.C. Cannon. 1996. Inactivation defects caused by myotonia-associated mutations in the sodium channel III-IV linker. J. Gen. Physiol. 107:559-576. http://dx.doi.org/10.1085/jgp.107.5.559
22. Hodgkin, A.L., and A.F. Huxley. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500-544 Horn, R., and C.A. Vandenberg. 1984. Statistical properties of single sodium channels. J. Gen. Physiol. 84:505-534. http://dx.doi.org/10.1085/jgp.84.4.505
23. Horn, R., and C.A. Vandenberg. 1984. Statistical properties of single sodium channels. J. Gen. Physiol. 84:505-534. http://dx.doi .org/10.1085/jgp.84.4.505
24. Horn, R., J. Patlak, and C.F. Stevens. 1981. Sodium channels need not open before they inactivate. Nature. 291:426-427. http:// dx.doi.org/10.1038/291426a0
25. Jurkat-Rott, K., N. Mitrovic, C. Hang, A. Kouzmekine, P. Iaizzo, J Herzog, H. Lerche, S. Nicole, J. Vale-Santos, D. Chauveau, et al. 2000. Voltage-sensor sodium channel mutations cause hypokalemic periodic paralysis type 2 by enhanced inactivation and reduced current. Proc. Natl. Acad. Sci. USA. 97:9549-9554. http:// dx.doi.org/10.1073/pnas.97.17.9549
26. Jurkat-Rott, K., B. Holzherr, M. Fauler, and F. Lehmann-Horn. 2010. Sodium channelopathies of skeletal muscle result from gain or loss of function. Pflugers Arch. 460:239-248. http:// dx.doi.org/10.1007/s00424-010-0814-4
27. Kambouris, N.G., H.B. Nuss, D.C. Johns, G.F. Tomaselli, E. Marban, and J.R. Balser. 1998. Phenotypic characterization of a novel long-QT syndrome mutation (R1623Q) in the cardiac sodiumchannel. Circulation. 97:640-644. http://dx.doi.org/10.1161/01.CIR.97.7.640
28. Kontis, K.J., and A.L. Goldin. 1997. Sodium channel inactivation is altered by substitution of voltage sensor positive charges. J. Gen Physiol. 110:403-413. http://dx.doi.org/10.1085/jgp.110.4.403
29. Kühn, F.J., and N.G. Greeff. 1999. Movement of voltage sensor S4 in domain 4 is tightly coupled to sodium channel fast inactivation and gating charge immobilization. J. Gen. Physiol. 114:167-183 http://dx.doi.org/10.1085/jgp.114.2.167
30. Kuo, C.C., and B.P. Bean. 1994. Na+ channels must deactivate to recover from inactivation. Neuron. 12:819-829. http://dx.doi.org/10.1016/0896-6273(94)90335-2
31. Lerche, H., W. Peter, R. Fleischhauer, U. Pika-Hartlaub, T. Malina, N. Mitrovic, and F. Lehmann-Horn. 1997. Role in fast inactivation of the IV/S4-S5 loop of the human muscle Na+ channel probed by cysteine mutagenesis. J. Physiol. 505:345-352. http:// dx.doi.org/10.1111/j.1469-7793.1997.345bb.x
32. McPhee, J.C., D.S. Ragsdale, T. Scheuer, and W.A. Catterall. 1998 A critical role for the S4-S5 intracellular loop in domain IV of the sodium channel alpha-subunit in fast inactivation. J. Biol. Chem 273:1121-1129. http://dx.doi.org/10.1074/jbc.273.2.1121
33. Muroi, Y., M. Arcisio-Miranda, S. Chowdhury, and B. Chanda. 2010 Molecular determinants of coupling between the domain III voltage sensor and pore of a sodium channel. Nat. Struct. Mol. Biol 17:230-237. http://dx.doi.org/10.1038/nsmb.1749
34. Richard Benzinger, G., G.S. Tonkovich, and D.A. Hanck. 1999 Augmentation of recovery from inactivation by site-3 Na channel toxins. A single-channel and whole-cell study of persistent currents J. Gen. Physiol. 113:333-346. http://dx.doi.org/10.1085/ jgp.113.2.333
35. Sheets, M.F., J.W. Kyle, R.G. Kallen, and D.A. Hanck. 1999 The Na channel voltage sensor associated with inactivation is localized to the external charged residues of domain IV, S4. Biophys J. 77:747-757. http://dx.doi.org/10.1016/S0006-3495(99) 76929-8
36. Sheets, M.F., J.W. Kyle, and D.A. Hanck. 2000. The role of the putative inactivation lid in sodium channel gating currentimmobilization. J. Gen. Physiol. 115:609-620. http://dx.doi org/10.1085/jgp.115.5.609
37. Smith, M.R., and A.L. Goldin. 1997. Interaction between the sodium channel inactivation linker and domain III S4-S5 Biophys. J. 73:1885-1895. http://dx.doi.org/10.1016/S0006-3495 (97)78219-5
38. Vandenberg, C.A., and F. Bezanilla. 1991. A sodium channel gating model based on single channel, macroscopic ionic, and gating currents in the squid giant axon. Biophys. J. 60:1511-1533. http:// dx.doi.org/10.1016/S0006-3495(91)82186-5
39. Wallace, R.H., D.W. Wang, R. Singh, I.E. Scheffer, A.L. George Jr., H.A. Phillips, K. Saar, A. Reis, E.W. Johnson, G.R. Sutherland, et al. 1998. Febrile seizures and generalized epilepsy associated with a mutation in the Na+-channel beta1 subunit gene SCN1B Nat. Genet. 19:366-370 http://dx.doi.org/10.1038/448
40. Wang, D.W., K. Yazawa, A.L. George Jr., and P.B. Bennett. 1996 Characterization of human cardiac Na+ channel mutations in the congenital long QT syndrome. Proc. Natl. Acad. Sci. USA 93:13200-13205. http://dx.doi.org/10.1073/pnas.93.23.13200
41. Wang, Q., J. Shen, Z. Li, K. Timothy, G.M. Vincent, S.G. Priori, P.J. Schwartz, and M.T. Keating. 1995a. Cardiac sodium channel mutations in patients with long QT syndrome, an inherited cardiac arrhythmia. Hum. Mol. Genet. 4:1603-1607. http://dx.doi.org/10.1093/hmg/4.9.1603
42. Wang, Q., J. Shen, I. Splawski, D. Atkinson, Z. Li, J.L. Robinson, A.J. Moss, J.A. Towbin, and M.T. Keating. 1995b. SCN5A mutations associated with an inherited cardiac arrhythmia, long QT syndrome. Cell. 80:805-811. http://dx.doi.org/10.1016/ 0092-8674(95)90359-3
43. West, J.W., D.E. Patton, T. Scheuer, Y. Wang, A.L. Goldin, and W.A. Catterall. 1992. A cluster of hydrophobic amino acid residues required for fast Na(+)-channel inactivation. Proc. Natl Acad. Sci. USA. 89:10910-10914. http://dx.doi.org/10.1073/ pnas.89.22.10910
44. Yang, N., and R. Horn. 1995. Evidence for voltage-dependent S4 movement in sodium channels. Neuron. 15:213-218. http:// dx.doi.org/10.1016/0896-6273(95)90078-0