β-Scorpion toxin modifies gating transitions in all four voltage sensors of the sodium channel

Journal of General Physiology

Volumn 130, Issue 3, 2007, Pages 257-268

  Campos, Fabiana V ^a,b   Chanda, Baron ^c   Beirão, Paulo S L ^b   Bezanilla, Francisco ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TOXIN; NEUROTOXIN; POLYPEPTIDE; SCORPION VENOM; TS1 TOXIN; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FLUORESCENCE SPECTROSCOPY; HYPERPOLARIZATION; NONHUMAN; PROTEIN DOMAIN; TOXIN ANALYSIS; TOXIN STRUCTURE;

ALLOSTERIC REGULATION; ANIMALS; BINDING SITES; FEMALE; INSECT PROTEINS; ION CHANNEL GATING; KINETICS; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; NEUROTOXINS; OOCYTES; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RATS; SCORPION VENOMS; SODIUM CHANNELS; SPECTROMETRY, FLUORESCENCE; XENOPUS;

EID: 34548847505     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200609719     Document Type: Article

References (37)

1. Armstrong, C.M., and F. Bezanilla. 1977. Inactivation of the sodium channel. II. Gating current experiments. J. Gen. Physiol. 70:567-590.
2. + channel. J. Biol. Chem. 257:12553-12558.
3. Cahalan, M.D. 1975. Modification of sodium channel gating in frog myelinated nerve fibres by Centruroides sculpturatus scorpion venom. J. Physiol. 244:511-534.
4. Catterall, W.A., S. Cestele, V. Yarov-Yarovoy, F.H. Yu, K. Konoki, and T. Scheuer. 2007. Voltage gated ion channels and gating modifier toxins. Toxicon. 49:124-141.
5. Cestèle, S., Q. Yusheng, J.C. Rogers, H. Rochat, T. Scheuer, and W.A. Catterall. 1998. Voltage sensor-trapping: enhanced activation of sodium channels by β-scorpion toxin bound to the S3-S4 loop in domain II. Neuron. 21:919-931.
6. Cestèle, S., T. Scheuer, M. Mantegazza, H. Rochat, and W.A. Catterall. 2001. Neutralization of gating charges in domain II of the sodium channel α-subunit enhances voltage sensor trapping by a β-scorpion toxin. J. Gen. Physiol. 118:291-302.
7. Cestèle, S., and W.A. Catterall. 2000. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie. 82:883-892.
8. Cestèle, S., V. Yarov-Yarovoy, Y. Qu, F. Sampieri, T. Scheuer, and W.A. Catterall. 2006. Structure and function of the voltage sensor of sodium channels probed by a β scorpion toxin. J. Biol. Chem. 281:21332-21344.
9. Cha, A., and F. Bezanilla. 1998. Structural implications of fluorescence quenching in the Shaker K1 channel. J. Gen. Physiol. 112:391-408.
10. Cha, A., P.C. Ruben, A.L. George, 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.
11. Chanda, B., and F. Bezanilla. 2002. Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J. Gen. Physiol. 120:629-645.
12. Chanda, B., O.K. Asamoah, and F. Bezanilla. 2004. Coupling interactions between voltage sensors of the sodium channel as revealed by site-specific measurements. J. Gen. Physiol. 123:217-230.
13. Cohen, L., I. Karbat, N. Gilles, N. Ilan, M. Benveniste, D. Gordon, and M. Gurevitz. 2005. Common features in the functional surface of scorpion β toxins and elements that confer specificity for insect and mammalian voltage-gated sodium channels. J. Biol. Chem. 280:5045-5053.
14. Cohen, L., N. Lipstein, and D. Gordon. 2006. Allosteric interactions between scorpion toxin receptor sites on voltage-gated Na channels imply a novel role for weakly active components in arthropod venom. FASEB J. 20:1933-1935.
15. Cole, K.S., and J.W. Moore. 1960. Potassium ion current in the squid giant axon: dynamic characteristic. Biophys. J. 1:1-14.
16. French, R.J., and R. Horn. 1983. Sodium channel gating: models, mimics, and modifiers. Annu. Rev. Biophys. Bioeng. 12:319-356.
17. Hanck, D.A., and M.F. Sheets. 1995. Modification of inactivation in cardiac sodium channels: ionic current studies with Anthopleurin-A toxin. J. Gen. Physiol. 106:601-616.
18. 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.
19. Horn, R., S. Ding, and H.J. Gruber. 2000. Immobilizing the moving parts of voltage-gated ion channels. J. Gen. Physiol. 116:461-476.
20. Keynes, R.D. 1994. The kinetics of voltage-gated ion channels. Q. Rev. Biophys. 27:339-434.
21. Ledwell, J.L., and R.W. Aldrich. 1999. Mutations in the S4 region isolate the final voltage-dependent cooperative step in potassium channel activation. J. Gen. Physiol. 113:389-414.
22. + channel. Science. 309:897-903.
23. Mannuzzu, L.M., and E.Y. Isacoff. 2000. Independence and cooperativity in rearrangements of a potassium channel voltage sensor revealed by single subunit fluorescence. J. Gen. Physiol. 115:257-268.
24. + channels. Circ. Res. 80:363-369.
25. Meves, H., N. Rubly, and D.D. Watt. 1987. Gating current experiments on frog nodes of Ranvier treated with Centruroides sculpturatus toxins or aconitine. Pflugers Arch. 409:381-393.
26. Pathak, M., L. Kurtz, F. Tombola, and E. Isacoff. 2005. The cooperative voltage sensor motion that gates a potassium channel. J. Gen. Physiol. 125:57-69.
27. + channels. Physiol. Rev. 71:1047-1080.
28. + channels. Acta Crystallogr. D Biol. Crystallogr. 59:405-415.
29. Possani, L., W.E. Steinmetz, M.A. Dent, A.C. Alagon, and K. Wuthrich. 1981. Preliminary spectroscopic characterization of six toxins from Latin American scorpions. Biochim. Biophys. Acta. 669:183-192.
30. Sack, J.T., and R.W. Aldrich. 2006. Binding of a gating modifier toxin induces intersubunit cooperativity early in the Shaker K channel's activation pathway. J. Gen. Physiol. 128:119-132.
31. Schoppa, N.E., and F.J. Sigworth. 1998. Activation of Shaker potassium channels. III. An activation gating model for wild-type and V2 mutant channels. J. Gen. Physiol. 111:313-342.
32. Sheets, M.F., and D.A. Hanck. 1995. Voltage-dependent open-state inactivation of cardiac sodium channels: gating current studies with Anthopleurin-A toxin. J. Gen. Physiol. 106:617-640.
33. Taylor, R.E., and F. Bezanilla. 1983. Sodium and gating current time shifts resulting from changes in initial conditions. J. Gen. Physiol. 81:773-784.
34. 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.
35. Vijverberg, H.P., D. Pauron, and M. Lazdunski. 1984. The effect of Tityus serrulatus scorpion toxin gamma on Na channels in neuroblastoma cells. Pflugers Arch. 401:297-303.
36. Yatani, A., G.E. Kirsch, L.D. Possani, and A.M. Brown. 1988. Effects of New World scorpion toxins on single-channel and whole cell cardiac sodium currents. Am. J. Physiol. 254:H443-H451.
37. Zagotta, W.N., T. Hoshi, and R.W. Aldrich. 1994. Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J. Gen. Physiol. 103:321-362.