Open- and closed-state fast inactivation in sodium channels: Differential effects of a site-3 anemone toxin

Channels

Volumn 5, Issue 1, 2011, Pages 65-78

  Groome, James R ^a   Lehmann Horn, Frank ^b   Holzherr, Boris D ^b  

^a Nucl Eng Idaho State University   (United States)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Anthopleurin; Charge immobilization; Fast inactivation; Sodium channel; Voltage gated

Indexed keywords

ANTHOPLEURIN A; DOMAIN FOUR TRANSMEMBRANE SEGMENT FOUR PROTEIN; MEMBRANE PROTEIN; SODIUM CHANNEL NAV1.4; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; ELECTRICITY; FEMALE; ION CURRENT; MEMBRANE DEPOLARIZATION; NONHUMAN; SKELETAL MUSCLE;

ANEMONE;

EID: 79551500632     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.5.1.14031     Document Type: Article

References (55)

1. Armstrong CM, Hille B. Voltage-gated ion channels and electrical excitability. Neuron 1998; 20:371-80.
2. Catterall WA. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000; 26:13-25.
3. George AL. Inherited disorders of voltage-gated sodium channels. J Clin Invest 2005; 115:1990-9.
4. Jurkat-Rott K, Lehmann-Horn F. Muscle channelopathies and critical points in functional and genetic studies. J Clin Invest 2005; 115:2000-9.
5. Cannon SC. Pathomechanisms in channelopathies of skeletal muscle and brain. Ann Rev Neurosci 2006; 29:387-415.
6. Bean BP. Sodium channel inactivation in the crayfish giant axon. Must channels open before inactivating? Biophys J 1981; 35:595-614.
7. Aldrich RW, Corey DP, Stevens CF. A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature 1983; 306:436-41.
8. Kambouris NG, Nuss HB, Johns DC, Marban E, Tomaselli GF, Balser JR. A revised view of cardiac sodium channel blockade in the long-QT syndrome. J Clin Invest 2000; 105:1133-40.
9. Chen T, Sheets MF. Enhancement of closed-state inactivation in long QT syndrome sodium channel mutation delta KPQ. Am J Physiol Heart Circ Physiol 2002; 283:966-75.
10. Chen T, Inoue M, Sheets MF. Reduced voltage dependence of inactivation in the SCN5A sodium channel mutation dleF1617. Am J Physiol Heart Circ Physiol 2005; 288:2666-76.
11. Bendahhou S, Cummins TR, Kwiecinski H, Waxman SG, Ptacek LJ. Characterization of a new sodium channel mutatioin at arginine 1,448 associated with moderate paramyotonia congenita in humans. J Physiol 1999; 518:337-44.
12. Mohammadi B, Jurkat-Rott K, Alekov A, Dengler R, Bufler J, Lehmann-Horn F. Preferred mexiletine block of human sodium channels with IVS4 mutations and its pH-dependence. Pharmacogen Genomics 2005; 15:235-44.
13. Wu FF, Gordon E, Hoffman EP, Cannon SC. A C-terminal skeletal muscle sodium channel mutation associated with myotonia disrupts fast inactivation. J Physiol 2005; 565:371-80.
14. Groome JR, Larsen MF, Coonts A. Differential effects of paramyotonia congenita mutants F1473S and F1705I on sodium channel gating. Channels 2008; 2:39-49.
15. Vassilev PM, Scheurer T, Catterall WA. Identification of an intracellular peptide segment involved in sodium channel inactivation. Science 1988; 241:1658-66.
16. + channel inactivation. Proc Natl Acad Sci USA 1992; 89:10910-4.
17. Stuhmer W, Conti F, Suzuki H, Wang X, Noda N, Yahagi N, et al. Structural parts involved in activation and inactivation of the sodium channel. Nature 1989; 339:597-604.
18. Noda MS, Shizimu S, Tanabe T, Takai T, Kayano T, Ikeda T, et al. Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature 1984; 312:121-7.
19. Chahine M, George AL Jr, Zhou M, Ji S, Sun W, Barchi RL, Horn R. Sodium channel mutations in paramyotonia congenita uncouple inactivation from activation. Neuron 1994; 12:281-94.
20. Chen LQ, Santarelli V, Horn R, Kallen RG. A unique role for the S4 segment of domain 4 in the inactivation of sodium channels. J Gen Physiol 1996; 108:549-56.
21. Hanck DA, Sheets MF. Site-3 toxins and cardiac sodium channels. Toxicon 2007; 49:181-93.
22. Armstrong CM, Bezanilla F. Inactivation of the sodium channel. II. Gating current experiments. J Gen Physiol 1977; 70:567-90.
23. + channel fast inactivation. Neuron 1999; 22:73-87.
24. Kuhn FJP, Greef NG. Movement of voltage sensor S4 in domain IV is tightly coupled to sodium channel fast inactivation and gating charge immobilization. J Gen Physiol 1999; 114:167-83.
25. Sheets MF, Kyle JW, Hanck DA. The role of the putative inactivation lid in sodium channel gating current immobilization. J Gen Physiol 2000; 115:609-19.
26. Chanda B, Bezanilla F. Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J Gen Physiol 2002; 120:629-45.
27. Armstrong CM. Na channel inactivation from open and closed states. Proc Natl Acad Sci USA 2006; 103:17991-6.
28. Groome JR. Charge immobilization from the open and closed states of voltage-gated sodium channels. Biophys Abstr 2009; 248.
29. Sheets MF, Hanck DA. Gating of skeletal and cardiac muscle sodium channels in mammalian cells. J Physiol 1999; 514:425-36.
30. Campos FV, Chanda B, Beirao PSL, Bezanilla F. α scorpion toxin impairs a conformational change that leads to fast inactivation in sodium channels. J Gen Physiol 2008; 251-63.
31. Cannon SC, Brown RH, Corey DP. Theoretical reconstruction of myotonia and paralysis caused by incomplete inactivation of sodium channels. Biophys J 1993; 65:270-88.
32. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1952; 117:500-44.
33. Horn R, Ding S, Gruber HJ. Immobilizing the moving parts of voltage-gated ion channels. J Gen Physiol 2000; 116:461-75.
34. Sheets MF, Hanck DA. Voltage-dependent open-state inactivation of cardiac sodium channels: gating current studies with Anthopleurin-A. J Gen Physiol 1995; 106:617-40.
35. Catterall WA, Cestele S, Yaorv-Yarovy V, Yu FH, Konoki KK, Scheurer T. Voltage-gated ion channels and gating modifier toxins. Toxicon 2007; 49:124-41.
36. Santarelli VP, Eastwood AL, Dougherty DA, Horn R, Ahern CA. A cation-pi interaction discriminates among sodium channels that are either sensitive or resistant to tetrodotoxin block. J Biol Chem 2007; 282:8044-51.
37. + channel alpha subunit. J Biol Chem 1996: 271:15950-62.
38. Cestele S, Qu Y, Rogers JC, Bochat H, Scheurer T, Catterall WA. Voltage-sensor trapping: enchanced activation of sodium channels by β-scorpion toxin bound to the S3-S4 loop in domain II. Neuron 1998; 21:919-31.
39. Campos FV, Chana B, Beirao PSL, Bezanilla F. β-scorpion toxin modifies gating transitions in all four voltage sensors of the sodium channel. J Gen Physiol 2007; 130:257-68.
40. Khera PK, Benzinger GR, Lipkind G, Drum CL, Hanck DA, Blumenthal KM. Multiple cationic residues of anthopleurin B that determine high affinity and channel isoform discrimination. Biochem 1995; 34:8533-41.
41. Campos FV, Coronas FIV, Beirao PSL. Voltage-dependent displacement of the scorpion toxin Tx3 from sodium channels and its implication on the control of inactivation. Brit J Pharamacol 2004; 142:1115-22.
42. Hanck DA, Sheets MF. Modification of inactivation in cardiac sodium channels: ionic current studies with anthopleurin-A toxin. J Gen Physiol 1995; 106:601-16.
43. + channels: role of residues in the inactivation linker. Biophys J 2007; 93:1-15.
44. Sheets MF, Kyle JW, Krueger S, Hanck DA. Optimization of a mammalian expression system for the measurement of sodium channel gating currents. Amer J Physiol 1996; 271:1001-6.
45. El-Sherif N, Fozzard HA, Hanck DA. Dose-dependent modulation of the cardiac sodium channel by sea anemone toxin ATXII. Circ Res 1992; 70:285-301.
46. + channels must deactivate to recover from inactivation. Neuron 1994; 12:819-29.
47. Kontis KJ, Goldin AL. Sodium channel inactivation is altered by substitution of voltage sensor positive charges. J Gen Physiol 1997; 110:403-13.
48. Groome JR, Fujimoto E, Walter L, Ruben PC. Outer and central charged residues in DIVS4 of skeletal muscle sodium channels have differing roles in deactivation. Biophys J 2002; 82:1293-307.
49. Groome JR, Alexander HM, Fujiimoto E, Sherry M, Petty D. Central charged residues in DIIIS4 regulate deactivation gating in skeletal muscle sodium channels. Cell Mol Neurobiol 2007; 27:87-106.
50. Benzinger GR, Tonkovich GS, Hanck DA. Augmentation of recovery from inactivation by site-3 Na channel toxins. J Gen Physiol 1999; 113:333-46.
51. V1.7 sodium channels in mouse spinal sensory neurons. J Physiol 2003; 551:741-50.
52. V1.3 sodium channels: rapid repriming and slow closed-state inactivation display quantitative differences after expression in a mammalian cell line and in spinal sensory neurons. J Neurosci 2001; 21:5952-61.
53. V1.7 sodium channels in a painful inherited neuropathy. J Neurosci 2004; 24:8232-6.
54. Nuss HB, Kambouris NG, Marban E, Tomaselli GF, Balser JR. Isoform-specific lidocaine block of sodium channels explained by differences in gating. Biophys J 2000; 78:200-10.
55. Filatov GN, Pinter MJ, Rich MM. Resting potential-dependent regulation of the voltage sensitivity of sodium channel gating in rat skeletal muscle in vivo. J Gen Physiol 2005; 126:161-72.