Binding modes and functional surface of anti-mammalian scorpion α-toxins to sodium channels

Biochemistry

Volumn 51, Issue 39, 2012, Pages 7775-7782

  Chen, Rong ^a   Chung, Shin Ho ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMISTIC MOLECULAR DYNAMICS SIMULATIONS; BINDING MODES; BINDING POCKETS; C-TERMINUS; DISSOCIATION CONSTANT; EXTRACELLULAR; FUNCTIONAL SURFACES; HYDROPHOBIC CLUSTERS; INACTIVATION MECHANISMS; MOLECULAR DYNAMICS SIMULATIONS; SALT BRIDGES; SODIUM CHANNEL;

BINDING ENERGY; DISSOCIATION; MAMMALS; METABOLITES; MOLECULAR DYNAMICS; NEURONS;

TOXIC MATERIALS;

ALPHA TOXIN; SCORPION VENOM; SODIUM CHANNEL NAV1.2;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; HYDROPHOBICITY; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MUTAGENESIS; NERVE CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; TOXIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; NAV1.2 VOLTAGE-GATED SODIUM CHANNEL; PROTEIN STRUCTURE, TERTIARY; RATS; SCORPION VENOMS; SCORPIONS; SEQUENCE ALIGNMENT;

HEXAPODA; MAMMALIA; RATTUS; SCORPIONES;

EID: 84867093419     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300776g     Document Type: Article

References (52)

1. Catterall, W. A., Cestele, S., Yarov-Yarovoy, V., Yu, F. H., Konoki, K., and Scheuer, T. (2007) Voltage-gated ion channels and gating modifier toxins Toxicon 49, 124-141
2. Stevens, M., Peigneur, S., and Tytgat, J. (2011) Neurotoxins and their binding areas on voltage-gated sodium channels Front. Pharmacol. 2, 71
3. Chen, H., Gordon, D., and Heinemann, S. H. (2000) Modulation of cloned skeletal muscle sodium channels by the scorpion toxins Lqh II, Lqh III, and Lqh alphaIT Pflügers Arch. 439, 423-432
4. Chen, H. and Heinemann, S. H. (2001) Interaction of scorpion α-toxins with cardiac sodium channels: binding properties and enhancement of slow inactivation J. Gen. Physiol. 117, 505-518
5. + channels but not in skeletal and cardiac muscle J. Biol. Chem. 279, 4680-4685
6. West, P. J., Bulaj, G., and Yoshikami, D. (2005) Effects of δ-conotoxins PVIA and SVIE on sodium channels in the amphibian sympathetic nervous system J. Neurophysiol. 94, 3916-3924
7. Gurevitz, M., Karbat, I., Cohen, L., Ilan, N., Kahn, R., Turkov, M., Stankiewicz, M., Stühmer, W., Dong, K., and Gordon, D. (2007) The insecticidal potential of scorpion β-toxins Toxicon 49, 473-489
8. Gordon, D., Karbat, I., Ilan, N., Cohen, L., Kahn, R., Gilles, N., Dong, K., Stuhmer, W., Tytgat, J., and Gurevitz, M. (2007) The differential preference of scorpion α-toxins for insect or mammalian sodium channels: implications for improved insect control Toxicon 49, 452-472
9. Bosmans, F. and Tytgat, J. (2007) Voltage-gated sodium channel modulation by scorpion α-toxins Toxicon 49, 142-158
10. Housset, D., Habersetzer-Rochat, C., Astier, J. P., and Fontecilla-Camps, J. C. (1994) Crystal structure of toxin II from the scorpion Androctonus australis Hector refined at 1.3 Å resolution J. Mol. Biol. 238, 88-103
11. Tugarinov, V., Kustanovich, I., Zilberberg, N., Gurevitz, M., and Anglister, J. (1997) Solution structures of a highly insecticidal recombinant scorpion α-toxin and a mutant with increased activity Biochemistry 36, 2414-2424
12. Miranda, F., Kupeyan, C., Rochat, H., Rochat, C., and Lissitzky, S. (1970) Purification of animal neurotoxins. Isolation and characterization of eleven neurotoxins from the venoms of the scorpions Androctonus australis Hector, Buthus occitanus tunetanus and Leiurus quinquestriatus quinquestriatus Eur. J. Biochem. 16, 514-523
13. Gordon, D., Martin-Eauclaire, M. F., Cestèle, S., Kopeyan, C., Carlier, E., Khalifa, R. B., Pelhate, M., and Rochat, H. (1996) Scorpion toxins affecting sodium current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels J. Biol. Chem. 271, 8034-8045
14. Benkhadir, K., Kharrat, R., Cestele, S., Mosbah, A., Rochat, H., El Ayeb, M., and Karoui, H. (2004) Molecular cloning and functional expression of the alpha-scorpion toxin BotIII: pivotal role of the C-terminal region for its interaction with voltage-dependent sodium channels Peptides 25, 151-161
15. Kahn, R., Karbat, I., Ilan, N., Cohen, L., Sokolov, S., Catterall, W. A., Gordon, D., and Gurevitz, M. (2009) Molecular requirements for recognition of brain voltage-gated sodium channels by scorpion α-toxins J. Biol. Chem. 284, 20684-20691
16. Sautière, P., Cestele, S., Kopeyan, C., Martinage, A., Drobecq, H., Doljansky, Y., and Gordon, D. (1998) New toxins acting on sodium channels from the scorpion Leiurus quinquestriatus hebraeus suggest a clue to mammalian vs insect selectivity Toxicon 36, 1141-1154
17. Eitan, M., Fowler, E., Herrmann, R., Duval, A., Pelhate, M., and Zlotkin, E. (1990) A scorpion-venom neurotoxin paralytic to insects that affects sodium current inactivation: purification, primary structure, and mode of action Biochemistry 29, 5941-5947
18. Karbat, I., Kahn, R., Cohen, L., Ilan, N., Gilles, N., Corzo, G., Froy, O., Gur, M., Albrecht, G., Heinemann, S. H., Gordon, D., and Gurevitz, M. (2007) The unique pharmacology of the scorpion α-like toxin Lqh3 is associated with its flexible C-tail FEBS J. 274, 1918-1931
19. Tejedor, F. J. and Catterall, W. A. (1988) Site of covalent attachment of α-scorpion toxin derivatives in domain I of the sodium channel α subunit Proc. Natl. Acad. Sci. U. S. A. 85, 8742-8746
20. + channel α subunit J. Biol. Chem. 271, 15950-15962
21. Benzinger, G. R., Kyle, J. W., Blumenthal, K. M., and Hanck, D. A. (1998) A specific interaction between the cardiac sodium channel and site-3 toxin anthopleurin B J. Biol. Chem. 273, 80-84
22. Leipold, E., Lu, S., Gordon, D., Hansel, A., and Heinemann, S. H. (2004) Combinatorial interaction of scorpion toxins Lqh-2, Lqh-3, and LqhαIT with sodium channel receptor sites-3 Mol. Pharmacol. 65, 685-691
23. Gur, M., Kahn, R., Karbat, I., Regev, N., Wang, J. T., Catterall, W. A., Gordon, D., and Gurevitz, M. (2011) Elucidation of the molecular basis of selective recognition uncovers the interaction site for the core domain of scorpion α-toxins on sodium channels J. Biol. Chem. 286, 35209-35217
24. + channel voltage sensor Proc. Natl. Acad. Sci. U. S. A. 108, 15426-15431
25. Payandeh, J., Scheuer, T., Zheng, N., and Catterall, W. A. (2011) The crystal structure of a voltage-gated sodium channel Nature 475, 353-358
26. Zilberberg, N., Froy, O., Loret, E., Cestèle, S., Arad, D., Gordon, D., and Gurevitz, M. (1997) Identification of structural elements of a scorpion α-neurotoxin important for receptor site recognition J. Biol. Chem. 272, 14810-14816
27. Karbat, I., Frolow, F., Froy, O., Gilles, N., Cohen, L., Turkov, M., Gordon, D., and Gurevitz, M. (2004) Molecular basis of the high insecticidal potency of scorpion α-toxins J. Biol. Chem. 279, 31679-31686
28. Chen, R. and Chung, S. H. (2012) Conserved functional surface of anti-mammalian scorpion β-toxins J. Phys. Chem. B 116, 4796-4800
29. Guex, N. and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18, 2714-2723
30. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: an automated protein homology-modeling server Nucleic Acids Res. 31, 3381-3385
31. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL Workspace: a web-based environment for protein structure homology modeling Bioinformatics 22, 195-201
32. Hillisch, A., Pineda, L. F., and Hilgenfeld, R. (2004) Utility of homology models in the drug discovery process Drug Discovery Today 9, 659-669
33. Chakrapani, S., Cuello, L. G., Cortes, D. M., and Perozo, E. (2008) Structural dynamics of an isolated voltage-sensor domain in a lipid bilayer Structure 16, 398-409
34. + ionophore. Studies with a toxin derivative prepared by lactoperoxidase-catalyzed iodination J. Biol. Chem. 252, 8660-8668
35. Mozhayeva, G. N., Naumov, A. P., Nosyreva, E. D., and Grishin, E. V. (1980) Potential-dependent interaction of toxin from venom of the scorpion Buthus eupeus with sodium channels in myelinated fibre: voltage clamp experiments Biochim. Biophys. Acta 597, 587-602
36. Benoit, E. and Dubois, J. M. (1987) Properties of maintained sodium current induced by a toxin from Androctonus scorpion in frog node of Ranvier J. Physiol. 383, 93-114
37. Chen, H., Gordon, D., and Heinemann, S. H. (2000) Modulation of cloned skeletal muscle sodium channels by the scorpion toxins Lqh II, Lqh III, and LqhαIT Pflügers Arch. 439, 423-432
38. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD J. Comput. Chem. 26, 1781-1802
39. MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiórkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102, 3586-3616
40. Klauda, J. B., Venable, R. M., Freites, J. A., O'Connor, J. W., Tobias, D. J., Mondragon-Ramirez, C., Vorobyov, I., MacKerell, A. D., Jr., and Pastor, R. W. (2010) Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114, 7830-7843
41. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1982) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
42. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n -alkanes J. Comput. Phys. 23, 327-341
43. Miyamoto, S. and Kollman, P. A. (1992) SETTLE: An analytical version of the SHAKE and RATTLE algorithm for rigid water models J. Comput. Chem. 13, 952-962
44. Kumar, S., Bouzida, D., Swendsen, R. H., Kollman, P. A., and Rosenberg, J. M. (1992) The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 13, 1011-1021
45. Allen, T. W., Andersen, O. S., and Roux, B. (2004) Energetics of ion conduction through the gramicidin channel Proc. Natl. Acad. Sci. U. S. A. 101, 117-122
46. Chen, R., Robinson, A., Gordon, D., and Chung, S. H. (2011) Modeling the binding of three toxins to the voltage-gated potassium channel (Kv1.3) Biophys. J. 101, 2652-2660
47. + channel: a computational approach based on experimental distance restraints extracted from thermodynamic mutant cycles Biophys. J. 83, 2595-2609
48. Legros, C., Ceard, B., Vacher, H., Marchot, P., Bougis, P. E., and Martin-Eauclaire, M. F. (2005) Expression of the standard scorpion alpha-toxin AaH II and AaH II mutants leading to the identification of some key bioactive elements Biochim. Biophys. Acta 1723, 91-99
49. Wang, C., Bradley, P., and Baker, D. (2007) Protein-protein docking with backbone flexibility J. Mol. Biol. 373, 503-519
50. Leipold, E., Hansel, A., Olivera, B. M., Terlau, H., and Heinemann, S. H. (2005) Molecular interaction of δ-conotoxins with voltage-gated sodium channels FEBS Lett. 579, 3881-3884
51. + channels J. Biol. Chem. 279, 21356-21366
52. Pintar, A., Possani, L. D., and Delepierre, M. (1999) Solution structure of toxin 2 from centruroides noxius Hoffmann, a β-scorpion neurotoxin acting on sodium channels J. Mol. Biol. 287, 359-367