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Molecular Description of Scorpion Toxin Interaction with Voltage-Gated Sodium Channels

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Scorpion Venoms

Part of the book series: Toxinology ((TOXI,volume 4))

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Abstract

Scorpion alpha and beta toxins interact with voltage-gated sodium channels (Navs) at two pharmacologically distinct sites. Alpha toxins bind at receptor site 3 and inhibit channel inactivation, whereas beta toxins bind at receptor site 4 and shift the voltage-dependent activation toward more hyperpolarizing potentials. The two toxin classes are subdivided to distinct pharmacological groups according to their binding preferences and competition for receptor sites at Nav subtypes. To elucidate the surface of interaction of the two toxin classes with Navs and clarify the molecular basis of varying toxin preferences, an efficient expression system was established. Mutagenesis accompanied by toxicity, binding, and electrophysiological assays, in parallel to determination of the three-dimensional structure using NMR and X-ray crystallography, uncovered the bioactive surfaces of toxin representatives of all pharmacological groups. Exchange of external loops between channels that exhibit marked differences in sensitivity to various toxins accompanied by point mutagenesis highlighted channel determinants that play a role in toxin selectivity. These data were used in further mapping of the brain channel rNav1.2a receptor sites for the beta-toxin Css4 (from Centruroides suffusus suffusus) and the alpha-toxin Lqh2 (from Leiurus quinquestriatus hebraeus). On the basis of channel mutations that affected Css4 activity, the known structure of the toxin and its bioactive surface, and using the structure of a potassium channel as template, a structural model of Css4 interaction with the gating module of domain II was constructed. This initial model was the first step in the identification of part of receptor site 4. In parallel, a swapping and a mutagenesis approach employing the rNav1.2a mammalian and DmNav1 insect Navs and the toxin Lqh2 as a probe were used to search for receptor site 3. The channel mapping along with toxin dissociation assays and double-mutant cycle analyses using toxin and channel mutants identified the gating module of domain IV as the site of interaction with the toxin core domain, thus describing the docking orientation of an alpha toxin at the channel surface.

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Authors and Affiliations

  1. Department of Plant Molecular Biology & Ecology, George S. Wise Faculty of Life Sciences, Tel-Aviv University, Ramat-Aviv, Tel-Aviv, 69978, Israel

    Michael Gurevitz, Dalia Gordon, Maya Gur Barzilai, Roy Kahn, Hagit Altman-Gueta, Michael Turkov & Izhar Karbat

  2. Department of Neurobiology, Silberman Institute of Life Sciences, Hebrew University of Jerusalem, Jerusalem, 91904, Israel

    Lior Cohen

  3. Department of Ecology, Evolution and Behavior, Silberman Institute of Life Sciences, Hebrew University of Jerusalem, Jerusalem, 91904, Israel

    Yehu Moran

  4. Department of Life Sciences, Ben Gurion University, Beer Sheva, 84105, Israel

    Noam Zilberberg

  5. Institute of Biochemistry, Food Science and Nutrition, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, 76100, Israel

    Oren Froy

  6. Department of Entomology and the Genetics and Neuroscience Programs, Michigan State University, East Lansing, MI, 48824, USA

    Ke Dong

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  1. Michael Gurevitz
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  2. Dalia Gordon
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  10. Michael Turkov
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  11. Ke Dong
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  12. Izhar Karbat
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Correspondence to Michael Gurevitz .

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Editors and Affiliations

  1. Venom and Toxin Research Programme Department of Anatomy, Yong Loo Lin School of Medicine National University of Singapore, Singapore, Singapore

    P. Gopalakrishnakone

  2. Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnologı´a Universidad Nacional Autonoma de Mexico (UNAM), Cuernavaca, Morelos, Mexico

    Lourival D. Possani

  3. Departamento de Ciências Fisiológicas -, Universidade de Brasília Laboratório de Toxinologia, Brasilia, DF, Brasília, Brazil

    Elisabeth F. Schwartz

  4. Laboratoire Ecologie, Systématique et Evolution Université Paris-Sud, CNRS, ORSAY, France

    Ricardo C. Rodríguez de la Vega

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Gurevitz, M. et al. (2015). Molecular Description of Scorpion Toxin Interaction with Voltage-Gated Sodium Channels. In: Gopalakrishnakone, P., Possani, L., F. Schwartz, E., Rodríguez de la Vega, R. (eds) Scorpion Venoms. Toxinology, vol 4. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6404-0_10

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