Brevetoxin and Conotoxin Interactions with Single-Domain Voltage-Gated Sodium Channels from a Diatom and Coccolithophore
Abstract
:1. Introduction
2. Results and Discussion
3. Materials and Methods
3.1. Plasmid Cloning and Purification
3.2. HEK293 Cell Culturing
3.3. Plasmid Transfection into HEK293 Cells
3.4. HEK293 Whole-Cell Patch Clamp Electrophysiology
3.5. Pharmacological Treatments for Electrophysiological Experiments
3.6. Statistical Analysis
3.7. Bioinformatic Analysis
3.8. Model of Changes in Membrane Potential
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Taylor, A.R. A fast Na+/Ca2+-based action potential in a marine diatom. PLoS ONE 2009, 4, e4966. [Google Scholar] [CrossRef] [Green Version]
- Helliwell, K.E.; Chrachri, A.; Koester, J.A.; Wharam, S.; Taylor, A.R.; Wheeler, G.L.; Brownlee, C. A Novel Single-Domain Na+-selective voltage-gated channel in photosynthetic eukaryotes. Plant Physiol. 2020, 184, 1674–1683. [Google Scholar] [CrossRef]
- Helliwell, K.E.; Chrachri, A.; Koester, J.A.; Wharam, S.; Verret, F.; Taylor, A.R.; Wheeler, G.L.; Brownlee, C. Alternative mechanisms for fast Na+/Ca2+ signaling in eukaryotes via a novel class of single-domain voltage-gated channels. Curr. Biol. 2019, 29, 1503. [Google Scholar] [CrossRef] [Green Version]
- Verret, F.; Wheeler, G.; Taylor, A.R.; Farnham, G.; Brownlee, C. Calcium channels in photosynthetic eukaryotes: Implications for evolution of calcium-based signalling. New Phytol. 2010, 187, 23–43. [Google Scholar] [CrossRef]
- Liebeskind, B.J.; Hillis, D.M.; Zakon, H.H. Independent acquisition of sodium selectivity in bacterial and animal sodium channels. Curr. Biol. 2013, 23, R948–R949. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ren, D.; Navarro, B.; Xu, H.; Yue, L.; Shi, Q.; Clapham, D.E. A prokaryotic voltage-gated sodium channel. Science 2001, 294, 2372–2375. [Google Scholar] [CrossRef] [Green Version]
- Shimomura, T.; Yonekawa, Y.; Nagura, H.; Tateyama, M.; Fujiyoshi, Y.; Irie, K. A native prokaryotic voltage-dependent calcium channel with a novel selectivity filter sequence. eLife 2020, 9. [Google Scholar] [CrossRef] [PubMed]
- Chen, R.; Chung, S.-H. Binding modes of μ-conotoxin to the bacterial sodium channel (NaVAb). Biophys. J. 2012, 102, 483–488. [Google Scholar] [CrossRef] [Green Version]
- Finol-Urdaneta, R.K.; McArthur, J.R.; Korkosh, V.S.; Huang, S.; McMaster, D.; Glavica, R.; Tikhonov, D.B.; Zhorov, B.S.; French, R.J. Extremely potent block of bacterial voltage-gated sodium channels by µ-conotoxin PIIIA. Mar. Drugs 2019, 17, 510. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trainer, V.L.; Baden, D.G.; Catterall, W.A. Identification of peptide components of the brevetoxin receptor site of rat brain sodium channels. J. Biol. Chem. 1994, 269, 19904–19909. [Google Scholar] [CrossRef]
- Konoki, K.; Baden, D.G.; Scheuer, T.; Catterall, W.A. Molecular determinants of brevetoxin binding to voltage-gated sodium channels. Toxins 2019, 11, 513. [Google Scholar] [CrossRef] [Green Version]
- Mio, K.; Mio, M.; Arisaka, F.; Sato, M.; Sato, C. The C-terminal coiled-coil of the bacterial voltage-gated sodium channel NaChBac is not essential for tetramer formation, but stabilizes subunit-to-subunit interactions. Prog. Biophys. Mol. Biol. 2010, 103, 111–121. [Google Scholar] [CrossRef]
- Bagneris, C.; DeCaen, P.G.; Hall, B.A.; Naylor, C.E.; Clapham, D.E.; Kay, C.W.M.; Wallace, B.A. Role of the C-terminal domain in the structure and function of tetrameric sodium channels. Nat. Commun. 2013, 4. [Google Scholar] [CrossRef] [Green Version]
- Irie, K.; Shimomura, T.; Fujiyoshi, Y. The C-terminal helical bundle of the tetrameric prokaryotic sodium channel accelerates the inactivation rate. Nat. Commun. 2012, 3, 793. [Google Scholar] [CrossRef] [Green Version]
- Catterall, W.A.; Zheng, N. Deciphering voltage-gated Na+ and Ca2+ channels by studying prokaryotic ancestors. Trends Biochem. Sci. 2015, 40, 526–534. [Google Scholar] [CrossRef] [Green Version]
- Catterall, W.A.; Wisedchaisri, G.; Zheng, N. The chemical basis for electrical signaling. Nat. Chem. Biol. 2017, 13, 455–463. [Google Scholar] [CrossRef] [Green Version]
- Yue, L.; Navarro, B.; Ren, D.; Ramos, A.; Clapham, D.E. The cation selectivity filter of the bacterial sodium channel, NaChBac. J. Gen. Physiol. 2002, 120, 845–853. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, B.M.; Peng, C.; Yang, J.A.; Yi, Y.H.; Zhang, J.Q.; Shi, Q. Cone snails: A big store of conotoxins for novel drug discovery. Toxins 2017, 9, 397. [Google Scholar] [CrossRef] [Green Version]
- Shon, K.J.; Olivera, B.M.; Watkins, M.; Jacobsen, R.B.; Gray, W.R.; Floresca, C.Z.; Cruz, L.J.; Hillyard, D.R.; Brink, A.; Terlau, H.; et al. μ-conotoxin PIIIA, a new peptide for discriminating among tetrodotoxin-sensitive Na channel subtypes. J. Neurosci. 1998, 18, 4473–4481. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, R.; Robinson, A.; Chung, S.-H. Mechanism of μ-conotoxin PIIIA binding to the voltage-gated Na+ channel NaV1.4. PLoS ONE 2014, 9, e93267. [Google Scholar] [CrossRef] [PubMed]
- Kirkpatrick, B.; Fleming, L.E.; Squicciarini, D.; Backer, L.C.; Clark, R.; Abraham, W.; Benson, J.; Cheng, Y.S.; Johnson, D.; Pierce, R.; et al. Literature review of Florida red tide: Implications for human health effects. Harmful Algae 2004, 3, 99–115. [Google Scholar] [CrossRef] [Green Version]
- Pierce, R.H.; Henry, M.S. Harmful algal toxins of the Florida red tide (Karenia brevis): Natural chemical stressors in South Florida coastal ecosystems. Ecotoxicology 2008, 17, 623–631. [Google Scholar] [CrossRef]
- Dechraoui, M.-Y.B.; Ramsdell, J.S. Type B brevetoxins show tissue selectivity for voltage-gated sodium channels: Comparison of brain, skeletal muscle and cardiac sodium channels. Toxicon 2003, 41, 919–927. [Google Scholar] [CrossRef]
- Huang, J.M.; Wu, C.H.; Baden, D.G. Depolarizing action of a red-tide dinoflagellate brevetoxin on axonal membranes. J. Pharm. Exp. 1984, 229, 615–621. [Google Scholar]
- Atchison, W.D.; Luke, V.S.; Narahashi, T.; Vogel, S.M. Nerve membrane sodium channels as the target site of brevetoxins at neuromuscular junctions. Br. J. Pharmacol. 1986, 89, 731–738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeglitsch, G.; Rein, K.; Baden, D.G.; Adams, D.J. Brevetoxin-3 (PbTx-3) and its derivatives modulate single tetrodotoxin-sensitive sodium channels in rat sensory neurons. J. Pharm. Exp. 1998, 284, 516–525. [Google Scholar]
- Kitchen, S.A.; Bourdelais, A.J.; Taylor, A.R. Interaction of a dinoflagellate neurotoxin with voltage-activated ion channels in a marine diatom. PeerJ 2018, 6, e4533. [Google Scholar] [CrossRef] [Green Version]
- Prince, E.K.; Myers, T.L.; Kubanek, J. Effects of harmful algal blooms on competitors: Allelopathic mechanisms of the red tide dinoflagellate Karenia brevis. Limnol. Oceanogr. 2008, 53, 531–541. [Google Scholar] [CrossRef]
- Poulson-Ellestad, K.L.; Jones, C.M.; Roy, J.; Viant, M.R.; Fernández, F.M.; Kubanek, J.; Nunn, B.L. Metabolomics and proteomics reveal impacts of chemically mediated competition on marine plankton. Proc. Natl. Acad. Sci. USA 2014, 111, 9009. [Google Scholar] [CrossRef] [Green Version]
- Poulin, R.X.; Hogan, S.; Poulson-Ellestad, K.L.; Brown, E.; Fernández, F.M.; Kubanek, J. Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors. Sci. Rep. 2018, 8, 9572. [Google Scholar] [CrossRef]
- Hille, B. Ion Channels of Excitable Membranes; Sinauer: Sunderland, MA, USA, 2001. [Google Scholar]
- Horn, R.; Korn, S.J. Prevention of rundown in electrophysiological recording. Methods Enzymol. 1992, 207, 149–155. [Google Scholar]
- Liberona, J.L.; Cárdenas, J.C.; Reyes, R.; Hidalgo, J.; Molgó, J.; Jaimovich, E. Sodium-dependent action potentials induced by brevetoxin-3 trigger both IP3 increase and intracellular Ca2+ release in rat skeletal myotubes. Cell Calcium 2008, 44, 289–297. [Google Scholar] [CrossRef]
- Mantegazza, M.; Yu, F.H.; Catterall, W.A.; Scheuer, T. Role of the C-terminal domain in inactivation of brain and cardiac sodium channels. Proc. Natl. Acad. Sci. USA 2001, 98, 15348–15353. [Google Scholar] [CrossRef] [Green Version]
- Wang, C.J.; Chung, B.C.; Yan, H.D.; Lee, S.Y.; Pitt, G.S. Crystal structure of the ternary complex of a NaV C-terminal domain, a fibroblast growth factor homologous factor, and calmodulin. Structure 2012, 20, 1167–1176. [Google Scholar] [CrossRef] [Green Version]
- Hull, J.M.; Isom, L.L. Voltage-gated sodium channel β-subunits: The power outside the pore in brain development and disease. Neuropharmacology 2018, 132, 43–57. [Google Scholar] [CrossRef]
- Moran, Y.; Zakon, H.H. The evolution of the four subunits of voltage-gated calcium channels: Ancient roots, increasing complexity, and multiple losses. Genome Biol. Evol. 2014, 6, 2210–2217. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Ren, W.; DeCaen, P.; Yan, C.; Tao, X.; Tang, L.; Wang, J.; Hasegawa, K.; Kumasaka, T.; He, J.; et al. Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 2012, 486, 130. [Google Scholar] [CrossRef]
- Bagneris, C.; Naylor, C.E.; McCusker, E.C.; Wallace, B.A. Structural model of the open-closed-inactivated cycle of prokaryotic voltage-gated sodium channels. J. Gen. Physiol. 2015, 145, 5–16. [Google Scholar] [CrossRef] [Green Version]
- Zhao, Y.; Scheuer, T.; Catterall, W.A. Reversed voltage-dependent gating of a bacterial sodium channel with proline substitutions in the S6 transmembrane segment. Proc. Natl. Acad. Sci. USA 2004, 101, 17873. [Google Scholar] [CrossRef] [Green Version]
- Chatterjee, S.; Vyas, R.; Chalamalasetti, S.V.; Sahu, I.D.; Clatot, J.; Wan, X.; Lorigan, G.A.; Deschênes, I.; Chakrapani, S. The voltage-gated sodium channel pore exhibits conformational flexibility during slow inactivation. J. Gen. Physiol. 2018, 150, 1333–1347. [Google Scholar] [CrossRef] [Green Version]
- Irie, K.; Kitagawa, K.; Nagura, H.; Imai, T.; Shimomura, T.; Fujiyoshi, Y. Comparative study of the gating motif and C-type inactivation in prokaryotic voltage-gated sodium channels. J. Biol. Chem. 2010, 285, 3685–3694. [Google Scholar] [CrossRef] [Green Version]
- Zeberg, H.; Dannemann, M.; Sahlholm, K.; Tsuo, K.; Maricic, T.; Wiebe, V.; Hevers, W.; Robinson, H.P.C.; Kelso, J.; Pääbo, S. A Neanderthal sodium channel increases pain sensitivity in present-day humans. Curr. Biol. 2020, 30, 3465–3469.e3464. [Google Scholar] [CrossRef] [PubMed]
- Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [Green Version]
- Korkosh, V.S.; Zhorov, B.S.; Tikhonov, D.B. Folding similarity of the outer pore region in prokaryotic and eukaryotic sodium channels revealed by docking of conotoxins GIIIA, PIIIA, and KIIIA in a NavAb-based model of Nav1.4. J. Gen. Physiol. 2014, 144, 231–244. [Google Scholar] [CrossRef] [Green Version]
- Waterhouse, A.M.; Procter, J.B.; Martin, D.M.A.; Clamp, M.; Barton, G.J. Jalview Version 2—A multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25, 1189–1191. [Google Scholar] [CrossRef] [Green Version]
- Dixon, L.K.; Kirkpatrick, G.J.; Hall, E.R.; Nissanka, A. Nitrogen, phosphorus and silica on the West Florida Shelf: Patterns and relationships with Karenia spp. occurrence. Harmful Algae 2014, 38, 8–19. [Google Scholar] [CrossRef]
Control | PbTx-2 | Control | PbTx-3 | Control | µ-CTx PIIIA | |
---|---|---|---|---|---|---|
Vact (mV) | −18.8 ± 7.7 (n = 5) | −23.6 ± 7.8 (n = 5) | −21.6 ± 5.7 (n = 6) | −30.7 ± 7.5 ** (n = 6) | −19.5 ± 2.9 (n = 6) | −33.5 ± 9.0 * (n = 6) |
Vinact (mV) | −34.1 ± 0.8 (n = 4) | −42.4 ± 1.5 ** (n = 4) | −37.0 ± 2.7 (n = 5) | −44.6 ± 6.4 * (n = 5) | −35.5 ± 1.1 (n = 3) | −42.6 ± 3.0 * (n = 3) |
τact (ms) | 1.7 ± 0.9 (n = 4) | 1.6 ± 0.9 (n = 4) | 1.3 ± 0.7 (n = 6) | 1.1 ± 0.6 * (n = 6) | 2.0 ± 1.1 (n = 10) | 1.4 ± 0.9 * (n = 10) |
τinact (ms) | 51.5 ± 14.3 (n = 4) | 48.5 ± 13.2 * (n = 4) | 54.4 ± 7.7 (n = 6) | 50.0 ± 9.9 (n = 6) | 62.6 ± 24.5 (n = 10) | 55.0 ± 20.0 * (n = 10) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yates, P.; Koester, J.A.; Taylor, A.R. Brevetoxin and Conotoxin Interactions with Single-Domain Voltage-Gated Sodium Channels from a Diatom and Coccolithophore. Mar. Drugs 2021, 19, 140. https://doi.org/10.3390/md19030140
Yates P, Koester JA, Taylor AR. Brevetoxin and Conotoxin Interactions with Single-Domain Voltage-Gated Sodium Channels from a Diatom and Coccolithophore. Marine Drugs. 2021; 19(3):140. https://doi.org/10.3390/md19030140
Chicago/Turabian StyleYates, Ping, Julie A. Koester, and Alison R. Taylor. 2021. "Brevetoxin and Conotoxin Interactions with Single-Domain Voltage-Gated Sodium Channels from a Diatom and Coccolithophore" Marine Drugs 19, no. 3: 140. https://doi.org/10.3390/md19030140