The specificity of Av3 sea anemone toxin for arthropods is determined at linker DI/SS2-S6 in the pore module of target sodium channels

Biochemical Journal

Volumn 463, Issue 2, 2014, Pages 271-277

  Gur Barzilai, Maya ^a   Kahn, Roy ^a   Regev, Noa ^a   Gordon, Dalia ^a,b   Moran, Yehu ^a,c   Gurevitz, Michael ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Av3; Insecticidal toxin; Receptor binding site; Sea anemone; Selectivity; Voltage gated sodium channel

Indexed keywords

AV3 SEA ANEMONE TOXIN; SEA ANEMONE TOXIN; SODIUM CHANNEL; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; MARINE TOXIN; NEUROTOXIN; PARA PROTEIN, DROSOPHILA; SODIUM CHANNEL BLOCKING AGENT;

ARTHROPOD; ARTICLE; BINDING COMPETITION; CHIMERA; DROSOPHILA MELANOGASTER; MUTAGENESIS; NONHUMAN; ANIMAL; BINDING SITE; CHEMISTRY; DROSOPHILA; DRUG EFFECTS; GENETICS; METABOLISM; SEA ANEMONE; TOXICITY; XENOPUS LAEVIS;

ANIMALS; BINDING SITES; DROSOPHILA; DROSOPHILA PROTEINS; MARINE TOXINS; NEUROTOXINS; SEA ANEMONES; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; XENOPUS LAEVIS;

EID: 84907222942     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140576     Document Type: Article

References (43)

1. Catterall, W. A. (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26, 13-25 CrossRef PubMed
2. Stühmer, W., Conti, F., Suzuki, H., Wang, X., Noda, M., Yahagi, N., Kubo, H and Numa, S. (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature 339, 597-603 CrossRef PubMed
3. Yang, N., George, A. L. and Horn, R. (1996) Molecular basis of charge movement in voltage-gated sodium channels. Neuron 16, 113-122 CrossRef PubMed
4. Kontis, K. J., Rounaghi, A. and Goldin, A. L. (1997) Sodium channel activation gating is affected by substitutions of voltage sensor positive charges in all four domains. J. Gen. Physiol. 110, 391-401 CrossRef PubMed
5. Kontis, K. J. and Goldin, A. L. (1997) Sodium channel inactivation is altered by substitution of voltage sensor positive charges. J. Gen. Physiol. 110, 403-413 CrossRef PubMed
6. Armstrong, C. M. and Hille, B. (1998) Voltage-gated ion channels and electrical excitability. Neuron 20, 371-380 CrossRef PubMed
7. Chanda, B., Asamoah, O. K. and Bezanilla, F. J. (2004) Coupling interactions between voltage sensors of the sodium channel as revealed by site-specific measurements. J. Gen. Physiol. 123, 217-230 CrossRef PubMed
8. Chahine, M., George, Jr, A. L., Zhou, M., Ji, S., Sun, W., Barchi, R. L. and Horn, R. (1994) Sodium channel mutations in paramyotonia congenita uncouple inactivation from activation. Neuron 12, 281-294 CrossRef PubMed
9. Cha, A., Ruben, P. C., George, Jr, A. L., Fujimoto, E. and Bezanilla, F. (1999) Voltage sensors in domains III and IV, but not I and II, are immobilized by Na+ channel fast inactivation. Neuron 22, 73-87 CrossRef PubMed
10. Cha, A., Snyder, G. E., Selvin, P. R. and Bezanilla, F. (1999) Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy. Nature 402, 809-813 CrossRef PubMed
11. Motoike, H. K., Liu, H., Glaaser, I. W., Yang, A. S., Tateyama, M. and Kass, R. S. (2004) The Na+ channel inactivation gate is a molecular complex: a novel role of the COOH-terminal domain. J. Gen. Physiol. 123, 155-165 CrossRef PubMed
12. Rogers, J. C., Qu, Y., Tanada, T. N., Scheuer, T. and Catterall, W. A. (1996) Molecular determinants of high affinity binding of scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the Na+ channel subunit. J. Biol. Chem. 271, 15950-15962 CrossRef PubMed
13. Sheets, M. F., Kyle, J. W., Kallen, R. G. and Hanck, D. A. (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 CrossRef PubMed
14. Campos, F. V., Chanda, B., Beirão, P. S. and Bezanilla, F. (2008) Scorpion toxin impairs a conformational change that leads to fast inactivation of muscle sodium channels. J. Gen. Physiol. 132, 251-263 CrossRef PubMed
15. Catterall, W. A. (1992) Cellular and molecular biology of voltage-gated sodium channels. Physiol. Rev. 72, S15-S48 PubMed
16. Possani, L. D., Becerril, B., Delepierre, M. and Tytgat, J. (1999) Scorpion toxins specific for Na+-channels. Eur. J. Biochem. 264, 287-300 CrossRef PubMed
17. Gordon, D., Karbat, I., Ilan, N., Cohen, L., Kahn, R., Gilles, N., Dong, K., Stühmer, W., Tytgat, J. and Gurevitz, M. (2007) The differential preference of scorpion toxins for insect or mammalian sodium channels: implications for improved insect control. Toxicon 49, 452-472 CrossRef PubMed
18. Gilles, N., Harrison, G., Karbat, I., Gurevitz, M., Nicholson, G. and Gordon, D. (2002) Variations in receptor site-3 on rat brain and insect sodium channels highlighted by binding of a funnel-web spider atracotoxin. Eur. J. Biochem. 269, 1500-1510 CrossRef PubMed
19. Nicholson, G. M., Little, M. J. and Birinyi-Strachan, L. C. (2004) Structure and function of atracotoxins: lethal neurotoxins targeting the voltage-gated sodium channel. Toxicon 43, 587-599 CrossRef PubMed
20. Catterall, W. A. and Beress, L. (1978) Sea anemone toxin and scorpion toxin share a common receptor site associated with the action potential sodium ionophore. J. Biol. Chem. 253, 7393-7396 PubMed
21. Moran, Y., Gordon, D. and Gurevitz, M. (2009) Sea anemone toxins affecting voltage-gated sodium channels: molecular and evolutionary features. Toxicon 54, 1089-1101 CrossRef PubMed
22. Gurevitz, M., Gordon, D., Barzilai, M. G., Kahn, R., Cohen, L., Moran, Y., Zilberberg, N., Froy, O., Altman-Gueta, H., Turkov, M. et al. (2014) Molecular description of scorpion toxin interaction with voltage-gated sodium channels. In Toxinology: Scorpion Venoms (Gopalakrishnakone, P., Schwartz, E. F., Possani, L. D. and Rodrguez de la Vega, R. C., eds), pp. 1-19, Springer, Dordrecht
23. Moran, Y., Cohen, L., Kahn, R., Karbat, I., Gordon, D. and Gurevitz, M. (2006) Expression and mutagenesis of the sea anemone toxin Av2 reveals key amino acid residues important for activity on voltage-gated sodium channels. Biochemistry 45, 8864-8873 CrossRef PubMed
24. Honma, T. and Shiomi, K. (2006) Peptide toxins in sea anemones: structural and functional aspects. Mar. Biotechnol. (N.Y.) 8, 1-10 CrossRef
25. 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 CrossRef PubMed
26. Manoleras, N. and Norton, R. S. (1994) Three-dimensional structure in solution of neurotoxin III from the sea anemone Anemonia sulcata. Biochemistry 33, 11051-11061 CrossRef PubMed
27. Moran, Y., Kahn, R., Cohen, L., Gur, M., Karbat, I., Gordon, D. and Gurevitz, M. (2007) Molecular analysis of the sea anemone toxin Av3 reveals selectivity to insects and demonstrates the heterogeneity of receptor site-3 on voltage-gated Na+ channels. Biochem. J. 406, 41-48 CrossRef PubMed
28. Schnur, E., Turkov, M., Kahn, R., Gordon, D., Gurevitz, M. and Anglister, J. (2007) NMR analysis of Lqh-IT scorpion toxin interaction with a peptide corresponding to the D4/S3-S4 loop of insect para voltage-gated sodium channel. Biochemistry 47, 911-921 CrossRef PubMed
29. Gur, M., Kahn, R., Regev, N., Wang, J., 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 toxins on sodium channels. J. Biol. Chem. 286, 35209-35217 CrossRef PubMed
30. Wang, J., Yarov-Yarovoy, V., Kahn, R., Gordon, D., Gurevitz, M., Scheuer, T. and Catterall, W. A. (2011) Mapping the receptor site for scorpion toxins on a sodium channel voltage sensor. Proc. Natl. Acad. Sci. U.S.A. 108, 15426-15431 CrossRef PubMed
31. Shichor, I., Zlotkin, E., Ilan, N., Chikashvili, D., Stuhmer, W., Gordon, D. and Lotan, I. (2002) Domain 2 of Drosophila para voltage-gated sodium channel confers insect properties to a rat brain channel. J. Neurosci. 22, 4364-4371 PubMed
32. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. and Ferrin, T. E. (2004) UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 CrossRef PubMed
33. Tugarinov, V., Kustanovitz, I., Zilberberg, N., Gurevitz, M. and Anglister, J. (1997) Solution structures of a highly insecticidal recombinant scorpion toxin and a mutant with increased activity. Biochemistry 36, 2414-2424 CrossRef PubMed
34. Leipold, E., Hansel, A., Olivera, B. M., Terlau, H. and Heinemann, S. H. (2005) Molecular interaction of conotoxins with voltage-gated sodium channels. FEBS Lett. 579, 3881-3884 CrossRef PubMed
35. Beress, L., Beress, R. and Wunderer, G. (1975) Isolation and characterisation of three polypeptides with neurotoxic activity from Anemonia sulcata. FEBs Lett. 50, 311-314 PubMed
36. Schweitz, H., Vincent, J. P., Barhanin, J., Frelin, C., Linden, G., Hugues, M. and Lazdunski, M. (1981) Purification and pharmacological properties of eight sea anemone toxins from Anemonia sulcata, Anthopleura xanthogrammica, Stoichactis giganteus, and Actinodendron plumosum. Biochemistry 20, 5245-5252 CrossRef PubMed
37. Yan, F., Cheng, X., Ding, X., Yao, T., Chen, H., Li, W., Hu, S., Yu, Z., Sun, Y., Zhang, Y. and Xia, L. (2014) Improved insecticidal toxicity by fusing Cry1Ac of Bacillus thuringiensis with Av3 of Anemonia viridis. Curr. Microbiol. 68, 604-609 CrossRef PubMed
38. Erxleben, C. and Rathmayer, W. (1984) Effects of Anemonia sulcata toxin II on neuromuscular transmission and skeletal muscle. Toxicon 22, 387-399 CrossRef PubMed
39. 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 toxins. J. Biol. Chem. 279, 31679-31686 CrossRef PubMed
40. Erwin, D. H., Laflamme, M., Tweedt, S. M., Sperling, E. A., Pisani, D. and Peterson, K. J. (2011) The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091-1097 CrossRef PubMed
41. Richardson, J., Blunck, R., Ge, P., Selvin, P. R., Bezanilla, F., Papazian, D. M. and Correa, A. M. (2006) Distance measurements reveal a common topology of prokaryotic voltage-gated ion channels in the lipid bilayer. Proc. Natl. Acad. Sci. U.S.A. 103, 15865-15870 CrossRef PubMed
42. Cohen, L., Ilan, N., Gur, M., Stühmer, W., Gordon, D. and Gurevitz, M. (2007) Design of a specific activator for skeletal muscle voltage-gated sodium channels uncovers channel architecture. J. Biol. Chem. 282, 29424-29430 CrossRef PubMed
43. Long, S. B., Campbell, E. B. and MacKinnon, R. (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309, 897-903 CrossRef PubMed