Insights into the binding mode and functional components of the analgesic-antitumour peptide from Buthus martensii Karsch to human voltage-gated sodium channel 1.7 based on dynamic simulation analysis

References

• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, s1–2(C), p, S2352711015000059.
   Google Scholar
• Ahuja, S., Mukund, S., Deng, L., Khakh, K., Chang, E., Ho, H., … Payandeh, J. (2015). Structural basis of Nav1.7 inhibition by an isoform-selective small-molecule antagonist. Science, 350(6267), aac5464. doi:10.1126/science.aac5464
   PubMed Web of Science ®Google Scholar
• Amira, S., Spangberg, D., & Hermansson, K. (2004). Derivation and evaluation of a flexible SPC model for liquid water. Chemical Physics, 303(3), 327–334. doi:10.1016/j.chemphys.2004.04.024
   Web of Science ®Google Scholar
• Berendsen, H. J. C., Spoel, D. V. D., & Drunen, R. V. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91(1–3), 43–56. doi:10.1016/0010-4655(95)00042-E
   Web of Science ®Google Scholar
• Berger, O., Edholm, O., & Jahnig, F. (1997). Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophysical Journal., 72(5), 2002–2013. doi:10.1016/S0006-3495(97)78845-3
   PubMed Web of Science ®Google Scholar
• Cahalan, M. D. (1975). Modification of sodium channel gating in frog myelinated nerve fibres by Centruroides sculpturatus scorpion venom. The Journal of Physiology, 244(2), 511–534. doi:10.1113/jphysiol.1975.sp010810
   PubMed Web of Science ®Google Scholar
• Cestèle, S., Qu, Y., Rogers, J. C., Rochat, H., Scheuer, T., & Catterall, W. A. (1998). Voltage sensor-trapping: Enhanced activation of sodium channels by beta-scorpion toxin bound to the S3-S4 loop in domain II. Neuron, 21(4), 919–931.
   PubMed Web of Science ®Google Scholar
• Cestèle, S., & Catterall, W. A. (2000). Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie, 82(9-10), 883–892.
   PubMed Web of Science ®Google Scholar
• Chen, R., Li, L., & Weng, Z. (2010). ZDOCK: An initial-stage protein-docking algorithm. Proteins: Structure, Function, and Genetics, 52(1), 80–87. doi:10.1002/prot.10389
   Google Scholar
• Clairfeuille, T., Cloake, A., Infield, D. T., Llongueras, J. P., Arthur, C. P., Li, Z. R., … Payandeh, J. (2019). Structural basis of alpha-scorpion toxin action on Nav channels. Science, doi:10.1126/science.aav8573
   PubMed Web of Science ®Google Scholar
• Consortium, U. P. (2015). UniProt: A hub for protein information. Nucleic Acids Research, 43 (Database issue), p, D204.
   PubMed Web of Science ®Google Scholar
• Cui, Y., Guo, G.-L., Ma, L., Hu, N., Song, Y.-B., Liu, Y.-F., … Zhang, J.-H. (2010). Structure and function relationship of toxin from Chinese scorpion Buthus martensii Karsch (BmKAGAP): Gaining insight into related sites of analgesic activity. Peptides, 31(6), 995. p doi:10.1016/j.peptides.2010.03.017
   PubMed Web of Science ®Google Scholar
• Cui, Y., Li, S., Chen, Y., Hu, S., Song, Y., He, W., … Zhang, J. (2015). Investigation of the role of disulphide bond in modulating internal motions of BmK AGAP protein by molecular dynamics simulation. Molecular Simulation, 42(9), 1–5.
   Web of Science ®Google Scholar
• Daura, X., Gademann, K., Jaun, B., Seebach, D., Gunsteren, W. F. V., & Mark, A. E. (1999). Peptide folding: When simulation meets experiment. Angewandte Chemie International Edition, 38(1-2), 236–240. doi:10.1002/(SICI)1521-3773(19990115)38:1/2<236::AID-ANIE236>3.3.CO;2-D
   Web of Science ®Google Scholar
• Drenth, J. P., & Waxman, S. G. (2007). Mutations in sodium-channel gene SCN9A cause a spectrum of human genetic pain disorders. Journal of Clinical Investigation, 117(12), 3603–3609. doi:10.1172/JCI33297
   PubMed Web of Science ®Google Scholar
• Goldberg, Y. P., MacFarlane, J., MacDonald, M. L., Thompson, J., Dube, M.-P., Mattice, M., … Hayden, M. R. (2007). Loss-of-function mutations in the Nav1.7 gene underlie congenital indifference to pain in multiple human populations. Clinical Genetics, 71(4), 311. p doi:10.1111/j.1399-0004.2007.00790.x
   PubMed Web of Science ®Google Scholar
• Goldin, A. L. (2001). Resurgence of sodium channel research. Annual Review of Physiology, 63(1), 871–894. doi:10.1146/annurev.physiol.63.1.871
   PubMedGoogle Scholar
• Gurevitz, M. (2012). Mapping of scorpion toxin receptor sites at voltage-gated sodium channels. Toxicon, 60(4), 502–511. doi:10.1016/j.toxicon.2012.03.022
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 4(1), 1463–1472. doi:10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L
   Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. 27–38.
   PubMedGoogle Scholar
• Isralewitz, B., Gao, M., & Schulten, K. (2001). Steered molecular dynamics and mechanical functions of proteins. Current Opinion in Structural Biology, 11(2), 224–230.
   PubMed Web of Science ®Google Scholar
• Kandt, C., Ash, W. L., & Tieleman, D. P. (2007). Setting up and running molecular dynamics simulations of membrane proteins. Methods, 41(4), 475–488. doi:10.1016/j.ymeth.2006.08.006
   PubMed Web of Science ®Google Scholar
• Lemak, A. S., & Balabaev, N. K. (1994). On The Berendsen Thermostat. Molecular Simulation, 13(3), 177–187. doi:10.1080/08927029408021981
   Web of Science ®Google Scholar
• Liu, Y. F., Ma, R. L., Wang, S. L., Duan, Z. Y., Zhang, J. H., Wu, L. J., & Wu, C. F. (2003). Expression of an antitumor-analgesic peptide from the venom of Chinese scorpion Buthus martensii Karsch in Escherichia coli. Protein Expression and Purification, 27(2), 253–258. doi:10.1016/S1046-5928(02)00609-5
   PubMed Web of Science ®Google Scholar
• Ma, R., Cui, Y., Zhou, Y., Bao, Y. M., Yang, W. Y., Liu, Y. F., … Zhang, J. H. (2010). Location of the analgesic domain in Scorpion toxin BmK AGAP by mutagenesis of disulfide bridges. Biochemical & Biophysical Research Communications, 394(2), 330. doi:10.1016/j.bbrc.2010.02.179
   PubMed Web of Science ®Google Scholar
• Makarewicz, T., & Kaźmierkiewicz, R. (2013). Molecular dynamics simulation by GROMACS using GUI plugin for PyMOL. Journal of Chemical Information and Modeling, 53(5), 1229–1234. doi:10.1021/ci400071x
   PubMed Web of Science ®Google Scholar
• Mantegazza, M., & Cestèle, S. (2005). Beta-scorpion toxin effects suggest electrostatic interactions in domain II of voltage-dependent sodium channels. The Journal of Physiology, 568(1), 13–30. doi:10.1113/jphysiol.2005.093484
   PubMed Web of Science ®Google Scholar
• Mao, Q., Ruan, J., Cai, X., Lu, W., Ye, J., Yang, J., … Cao, P. (2013). Antinociceptive effects of analgesic-antitumor peptide (AGAP), a neurotoxin from the scorpion Buthus martensii Karsch, on formalin-induced inflammatory pain through a mitogen-activated protein kinases-dependent mechanism in mice. Plos One, 8(11), e78239. p doi:10.1371/journal.pone.0078239
   PubMed Web of Science ®Google Scholar
• Matteo, T., & Elena, P. (2011). Dynamic properties of extremophilic subtilisin-like serine-proteases. Journal of Structural Biology, 174(1), 69–83.
   PubMed Web of Science ®Google Scholar
• Meves, H., Rubly, N., & Watt, D. D. (1982). Effect of toxins isolated from the venom of the scorpion Centruroides sculpturatus on the Na currents of the node of Ranvier. Pflügers Archiv: European Journal of Physiology, 393(1), 56. p doi:10.1007/BF00582392
   PubMed Web of Science ®Google Scholar
• Noda, M., Shimizu, S., Tanabe, T., Takai, T., Kayano, T., Ikeda, T., … Numa, S. (1984). Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature, 312(5990), 121–127. doi:10.1038/312121a0
   PubMed Web of Science ®Google Scholar
• Oostenbrink, C., Soares, T. A., van Der Vegt, N. F., & Van Gunsteren, W. F. (2005). Validation of the 53A6 GROMOS force field. European Biophysics Journal, 34(4), 273. p doi:10.1007/s00249-004-0448-6
   PubMed Web of Science ®Google Scholar
• Pedraza, E. M., & Possani, L. D. (2013). Scorpion beta-toxins and voltage-gated sodium channels: Interactions and effects. Frontiers in Bioscience, 18(1)p, 572.
   Google Scholar
• Petersen, H. G. (1995). Accuracy and efficiency of the particle mesh Ewald method. Journal of Chemical Physics, 103(9), 3668–3679. doi:10.1063/1.470043
   Web of Science ®Google Scholar
• Rodríguez de la Vega, R. C., & Possani, L. D. (2005). Overview of scorpion toxins specific for Na+ channels and related peptides: Biodiversity, structure-function relationships and evolution. Toxicon, 46(8), 831–844. doi:10.1016/j.toxicon.2005.09.006
   PubMed Web of Science ®Google Scholar
• Sandrine, C., Vladimir, Y. Y., Yusheng, Q., François, S., Todd, S., & Catterall, W. A. (2006). Structure and function of the voltage sensor of sodium channels probed by a beta-scorpion toxin. Journal of Biological Chemistry, 281(30), 21332–21344. doi:10.1074/jbc.M603814200
   PubMed Web of Science ®Google Scholar
• Smith, E. R., Snook, I. K., & Megen, W. V. (1987). Hydrodynamic interactions in Brownian dynamics: I. Periodic boundary conditions for computer simulations. Physica A Statistical Mechanics & Its Applications, 143(3), 441–467. doi:10.1016/0378-4371(87)90160-9
   Google Scholar
• Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2002). Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics, Chapter, 2(Unit 2), Unit 2.3.
   PubMedGoogle Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. doi:10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Wang, Y., Song, Y.-B., Yang, G.-Z., Cui, Y., Zhao, Y.-S., Liu, Y.-F., … Zhang, J.-H. (2012). Arginine residues in the C-terminal and their relationship with the analgesic activity of the toxin from the Chinese scorpion Buthus martensii Karsch (BmK AGP-SYPU1). Applied Biochemistry and Biotechnology, 168(2), 247–255. doi:10.1007/s12010-012-9768-7
   PubMed Web of Science ®Google Scholar
• Webb, B., & Sali, A. (2016). Comparative protein structure modeling using MODELLER. Current Protocols in Protein Science, 86(1), 2.9.1.
   Google Scholar
• Xu, H., Li, T., Rohou, A., Arthur, C. P., Tzakoniati, F., Wong, E., … Payandeh, J. (2019). Structural basis of Nav1.7 inhibition by a gating-modifier spider toxin. Cell, 176(4), 702–715. e714. doi:10.1016/j.cell.2018.12.018
   PubMed Web of Science ®Google Scholar
• Xu, Y. J., Meng, X. X., Hou, X., Sun, J. F., Kong, X. H., Sun, Y. Q., … Zhang, J. H. (2017). A mutant of the BmK antitumor-analgesic peptide exhibits reduced inhibition to hNav1.4 and hNav1.5 channels while retaining analgesic activity. Journal of Biological Chemistry, 292 p, jbc.M117.792697.
   Web of Science ®Google Scholar
• Zhang, J. Z., Yarov-Yarovoy, V., Scheuer, T., Karbat, I., Cohen, L., Gordon, D., … Catterall, W. A. (2011). Structure-function map of the receptor site for beta-scorpion toxins in domain II of voltage-gated sodium channels. Journal of Biological Chemistry, 286(38), 33641–33651. doi:10.1074/jbc.M111.282509
   PubMed Web of Science ®Google Scholar