Expression and mutagenesis of the sea anemone toxin Av2 reveals key amino acid residues important for activity on voltage-gated sodium channels

Biochemistry

Volumn 45, Issue 29, 2006, Pages 8864-8873

  Moran, Yehu ^a   Cohen, Lior ^a   Kahn, Roy ^a   Karbat, Izhar ^a   Gordon, Dalia ^a   Gurevitz, Michael ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ASSAYS; BIOCHEMISTRY; PROBES; SPECTROSCOPIC ANALYSIS; SURFACE PHENOMENA;

ANEMONIA VIRIDIS; SEA ANEMONE TOXIN AV2; TOXIN MUTANT; VOLTAGE-GATED NA-CHANNELS (NAVS);

MUTAGENESIS;

ALPHA TOXIN; ANTHOPLEURINE B; ARGININE; ASPARAGINE; GLYCINE; ISOLEUCINE; LEUCINE; SEA ANEMONE TOXIN; SEA ANEMONE TOXIN AV2; UNCLASSIFIED DRUG; VALINE; VOLTAGE GATED CALCIUM CHANNEL;

AMINO ACID ANALYSIS; ANEMONIA VIRIDIS; ANTHOPLEURA XANTHOGRAMMICA; ARTICLE; CHANNEL GATING; CIRCULAR DICHROISM; CONTROLLED STUDY; INSECTICIDAL ACTIVITY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; RESIDUE ANALYSIS; SEA ANEMONE; SODIUM TRANSPORT; STRUCTURE ANALYSIS; TOXIN ANALYSIS; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; CNIDARIAN VENOMS; DIPTERA; HUMANS; LARVA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; MUTAGENESIS, SITE-DIRECTED; RECOMBINANT PROTEINS; SEA ANEMONES; SEQUENCE ALIGNMENT; SODIUM CHANNELS;

ACTINIARIA; ANEMONIA VIRIDIS; ANTHOPLEURA XANTHOGRAMMICA; HEXAPODA; INSECTA; MAMMALIA; SCORPIONES;

EID: 33746220061     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060386b     Document Type: Article

References (47)

1. Whittington, H. B. (1985) The Burgess Shale, Yale University Press, New Haven, CT.
2. Blumenthal, K. M., and Seibert, A. L. (2003) Voltage-gated sodium channel toxins: poison, probes, and future promise, Cell. Biochem. Biophys. 38, 215-238.
3. Catterall, W. A. (1992) Cellular and molecular biology of voltage-gated sodium channels, Physiol. Rev. 72, 15-48.
4. Catteral, W. A., Goldin, A. L., and Waxman, S. G., (2003) International union of pharmacology, XXXIX, compendium of voltage-gated ion channels: sodium channels, Pharmacol. Rev. 55, 575-578.
5. Norton, R. S. (1991) Structure and structure-function relationships of sea anemone proteins that interact with the sodium channel, Toxicon 29, 1051-1084.
6. 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.
7. Gordon, D., and Zlotkin, E. (1993) Binding of alpha scorpion toxin to insect sodium channels is not dependent on membrane potential, FEBS Lett. 315, 125-128.
8. Gordon, D., Martin-Eauclaire, M.-F., Cestele, S., Kopeyan, C., Carlier, E., Ben Khalifa, R., 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.
9. + channel α subunit, J. Biol. Chem. 271, 15950-15962.
10. Beress, L., Beress, R., and Wunderer G. (1975) Isolation and characterization of three polypeptides with neurotoxic activity from Anemonia sulcata, FEBS Lett. 50, 311-314.
11. Csaba, G., Dobozy, O., Darvas, Z., Laszlo, V., and Beress, L. (1984) Phylogenetic change in sensitivity to Anemonia sulcata toxin (ATX II), and impact of first interaction with the toxin (imprinting) on later response to it, Comp. Biochem. Physiol., C. 77, 153-155.
12. Warmke, J. W., Reenan, A. G. R., Wang, P., Qian, S., Arena, J. P., Wang, J., Wunderler, D., Liu, K., Kaczorowski, G. J., Van der Ploeg, L. H. T., Ganetzky, B., and Cohen, C. J. (1997) Functional expression of Drosophila para sodium channels. Modulation by membrane protein TipE and toxin pharmacology, J. Gen. Physiol. 110, 119-133.
13. Alsen, C., Beress, L., Fischer, K., Proppe D., Reinberg, T., and Sattler, R. W. (1976) The action of a toxin from the sea anemone Anemonia sulcata upon mammalian heart muscles, Naunyn-Schmiedeberg's Arch. Pharmacol. 295, 55-62.
14. Chahine, M. Plante, E., and Kallen, R. G. (1996) Sea anemone toxin (ATX II) modulation of heart and skeletal muscle sodium channel alpha-subunits expressed in tsA201 cells, J. Membr. Biol. 152, 39-48.
15. Barhanin, J., Hugues, M., Schweitz, H., Vincent, J.-P., and Lazdunski, M. (1981) Structure-function relationships of sea anemone toxin II from Anemonia sulcata, J. Biol. Chem. 256, 5764-5769.
16. Gallagher, M. J., and Blumenthal, K. M. (1992) Cloning and expression of wild-type and mutant forms of the cardiotonic polypeptide Anthopleurin B, J. Biol. Chem. 267, 13958-13963.
17. Wang, L., Ou, J., Peng, L., Zhong, X., Du, J., Liu, Y., Zhang, Y., Dong, M., and Xu, A.-L. (2004) Functional expression and characterization of four novel neurotoxins from sea anemone Anthopleura sp, Biochem. Biophys. Res. Commun. 313, 163-170.
18. Benzinger, G. R., Kyle, J. W., Blumethal, 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.
19. Loret, E. P., Menendez, R., Mansuelle, P., Sampieri, F., and Rochat, H. (1994) Positively charged amino acid residues located similarly in sea anemone and scorpion toxins, J. Biol. Chem. 269, 16785-16788.
20. Froy, O., Zilberberg, N., Gordon, D., Turkov, M., Gilles, N., Stankiewicz, M., Plehate, M., Loret, E., Oren, D. A., Shaanan, B., and Gurevitz, M. (1999) The putative bioactive surface of insect-selective scorpion excitatory neurotoxins, J. Biol. Chem. 274, 5769-5776.
21. Cohen, L., Karbat, I., Gilles, N., Ilan, N., Benveniste, M., Gordon, D., and Gurevitz, M. (2005) Common features in the functional surface of scorpion /?-toxins and elements that confer specificity for insect and mammalian voltage-gated sodium channels, J. Biol. Chem. 280, 5045-5053.
22. Wunderer, G., Fritz, H., Wachter, E., and Machleidt, W. (1976) Amino acid sequence of a coelenterate toxin: toxin II from Anemonia sulcata, Eur. J. Biochem. 68, 193-198.
23. Turkov, M., Rashi, S., Zilberberg, N., Gordon, D., Ben-Khalifa, R., Stankiewicz, M., Pelhate, M., and Gurevitz, M. (1997) In vitro folding and functional analysis of an anti-insect selective scorpion depressant neurotoxin produced in Escherichia coli, Protein Expression Purif. 10, 123-131.
24. Reed, L., and Muench, H. (1938) A simple method of estimating fifty-percent endpoint, Am. J. Hyg. 27, 493-497.
25. Gilles, N., Krimm, I., Bouet, F., Froy, O., Gurevitz, M., Lancelin, J.-M., and Gordon, D. (2000) Structural implications on the interaction of scorpion α-like toxins with the sodium channel receptor site inferred from toxin iodination and pH-dependent binding, J. Neurochem. 75, 1735-1745.
26. Rochat, C., Tessier, M., Miranda, F., and Lissitzky, S. (1977) Radioiodination of scorpion and snake neurotoxins, Anal. Biochem. 82, 532-548.
27. + current in Xenopus oocytes, J. Neurosci. 12, 3743-3752.
28. Wallner, M., Weigl, L., Meera, P., and Lotan, I. (1993) Modulation of the skeletal muscle sodium channel alpha-subunit by the beta-1 subunit, FEBS Lett. 336, 535-539.
29. 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.
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. Seibert, A. L., Liu, J., Hanck, D. A., and Blumenthal, K. M. (2003) Arg-14 loop of site 3 anemone toxins: effects of glycine replacement on toxin affinity, Biochemistry 42, 14515-14521.
32. v site 3, Biochemistry 43, 7082-7089.
33. Dias-Kadambi, B. L., Drum, C. I., Hanck, D. A., and Blumenthal K. M. (1996) Leucine 18, a hydrophobic residue essential for high affinity binding of Anthopleurin B to the voltage-sensitive sodium channel, J. Biol. Chem. 271, 9422-9428.
34. Wang, C. G., Gilles, N., Hamon, A., Le Gall, F., Stankiewicz, M., Pelhate, M., Xiong, Y. M., Wang, D. C., and Chi C. W. (2003) Exploration of the functional site of a scorpion alpha-like toxin by site-directed mutagenesis, Biochemistry, 42, 4699-4708.
35. 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 alpha-toxins, J. Biol. Chem. 279, 31679-31686.
36. Liu, L., Bosmans, F., Maertens, C., Zhu, R. H., Wang, D. C., and Tytgat, J. (2005) Molecular basis of the mammalian potency of the scorpion alpha-like toxin, BmK M1, FASEB J. 19, 594-596.
37. Khera, P. K., and Blumenthal, K. M. (1996) Importance of highly conserved anionic residues and electrostatic interactions in the activity and structure of the cardiotonic polypeptide Anthopleurin B, Biochemistry 35, 3503-3507.
38. Bosmans, F., Aneiros, A., and Tytgat, J. (2002) The sea anemone Bunodosoma granulifera contains surprisingly efficacious and potent insect-selective toxins, FEBS Lett. 532, 131-134.
39. Dias-Kadambi, B. L., Combs, K. A., Drum, C. L., Hanck, D. A., and Blumenthal, K. M. (1996) The role of exposed tryptophan residues in the activity of the cardiotonic polypeptide Anthopleurin B, J. Biol. Chem. 271, 23828-23835.
40. Benzinger, G. R., Drum, C. L., Chen, L.-Q., Kallen, R. G., and Hanck, D. A. (1997) Differences in the binding sites of two site-3 sodium channel toxins, Pflugers Arch. 424, 742-749.
41. Ali, S. A., Wang, B., Alam, M., Beck, A., Stoeva, S., Voelter, W., Abbasi, A., and Duszenko, M. (2006) Structure-activity relationship of an alpha-toxin Bs-Tx28 from scorpion (Buthus sindicus) venom suggests a new alpha-toxin subfamily, Arch. Biochem. Biophys. 445, 81-94.
42. Pallaghy, P. K., Scanlon, M. J., and Norton, R. S. (1995) Three-dimensional structure in solution of the polypeptide cardiac stimulant Anthopleurin-A, Biochemistry 34, 3782-3794.
43. Monks, S. A., Pallaghy, P. K., Scanlon, M. J., and Norton, R. S. (1995) Solution structure of the cardiostimulant polypeptide Anthopleurin-B and comparison with Anthopleurin-A, Structure 15, 791-803.
44. Fogh, R. H., Kem, W. R., and Norton R. S. (1990) Solution structure of neurotoxin I from the sea anemone Stichodactyla helianthus. A nuclear magnetic resonance, distance geometry, and restrained molecular dynamics study, J. Biol. Chem. 265, 13016-13028.
45. Wilcox, G. R., Fogh, R. H., and Norton, R. S. (1993) Refinement of the solution structure of the sea anemone neurotoxin Sh I, J. Biol. Chem. 268, 24707-24719.
46. Koshland, D. E. (1958) Application of a theory of enzyme specificity to protein synthesis, Proc. Natl. Acad. Sci. U.S.A. 44, 98-104.
47. Buck, E., and Iyengar, R. (2003) Organization and functions of interacting domains for signaling by protein-protein interactions. Sci. STKE 209, 14-18.