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A Taxon-Specific and High-Throughput Method For toxins Article A Taxon-Specific and High-Throughput Method for Measuring Ligand Binding to Nicotinic Acetylcholine Receptors 1, 1, 2, 1 Christina N. Zdenek y , Richard J. Harris y , Sanjaya Kuruppu y, Nicholas J. Youngman , James S. Dobson 1 , Jordan Debono 1, Muzaffar Khan 3, Ian Smith 2, Mike Yarski 4, David Harrich 5, Charlotte Sweeney 6, Nathan Dunstan 7, Luke Allen 7 and Bryan G. Fry 1,* 1 Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia; [email protected] (C.N.Z.); [email protected] (R.J.H.); [email protected] (N.J.Y.); [email protected] (J.S.D.); [email protected] (J.D.) 2 Department of Biochemistry & Molecular Biology, Biomedicine Discovery Institute, Monash University, Clayton, VIC 3800, Australia; [email protected] (S.K.); [email protected] (I.S.) 3 Institute of Biology, Leiden University (IBL), Sylvius Laboratory, Sylviusweg 72, 2333 BE Leiden, The Netherlands; [email protected] 4 Millennium Science, 4 Miles Street Mulgrave, VIC 3170, Australia; [email protected] 5 QIMR Berghofer, Royal Brisbane Hospital QLD 4029, Australia; [email protected] 6 Translational Research Institute, University of Queensland, QLD 4072, Australia; [email protected] 7 Venom Supplies Pty Ltd., Stonewell Rd, Tanunda, SA 5352, Australia; [email protected] (N.D.); [email protected] (L.A.) * Correspondence: [email protected]; Tel.: +61-7-336-58515 Co-first author; contributed equally. y Received: 16 September 2019; Accepted: 1 October 2019; Published: 16 October 2019 Abstract: The binding of compounds to nicotinic acetylcholine receptors is of great interest in biomedical research. However, progress in this area is hampered by the lack of a high-throughput, cost-effective, and taxonomically flexible platform. Current methods are low-throughput, consume large quantities of sample, or are taxonomically limited in which targets can be tested. We describe a novel assay which utilizes a label-free bio-layer interferometry technology, in combination with adapted mimotope peptides, in order to measure ligand binding to the orthosteric site of nicotinic acetylcholine receptor alpha-subunits of diverse organisms. We validated the method by testing the evolutionary patterns of a generalist feeding species (Acanthophis antarcticus), a fish specialist species (Aipysurus laevis), and a snake specialist species (Ophiophagus hannah) for comparative binding to the orthosteric site of fish, amphibian, lizard, snake, bird, marsupial, and rodent alpha-1 nicotinic acetylcholine receptors. Binding patterns corresponded with diet, with the Acanthophis antarcticus not showing bias towards any particular lineage, while Aipysurus laevis showed selectivity for fish, and Ophiophagus hannah a selectivity for snake. To validate the biodiscovery potential of this method, we screened Acanthophis antarcticus and Tropidolaemus wagleri venom for binding to human alpha-1, alpha-2, alpha-3, alpha-4, alpha-5, alpha-6, alpha-7, alpha-9, and alpha-10. While A. antarcticus was broadly potent, T. wagleri showed very strong but selective binding, specifically to the alpha-1 target which would be evolutionarily selected for, as well as the alpha-5 target which is of major interest for drug design and development. Thus, we have shown that our novel method is broadly applicable for studies including evolutionary patterns of venom diversification, predicting potential neurotoxic effects in human envenomed patients, and searches for novel ligands of interest for laboratory tools and in drug design and development. Keywords: venom; ligand; evolution; biosensor; nicotinic acetylcholine receptor Toxins 2019, 11, 600; doi:10.3390/toxins11100600 www.mdpi.com/journal/toxins Toxins 2019, 11, 600 2 of 11 Key Contribution: This paper presents a novel method that allows for the first time high-throughput, flexible testing of ligand binding to taxon-specific nicotinic acetylcholine receptors. 1. Introduction Nicotinic acetylcholine receptors (nAChRs) are a family of ligand-gated ion channels located throughout the body for many different physiological functions. One of their most vital roles is signaling between neuronal junctions to skeletal-muscle cells [1–3]. At the neuromuscular junction, the binding of acetylcholine to the 14-amino acid orthosteric site (i.e., active site) of the α-1 subtype triggers the contraction of muscles [2,3]. In addition to their central role at the neuromuscular junction, nAChR α-subunits are also widely distributed in the central nervous system and therefore of pharmacological interest. There are approximately 17 characterized nAChR subunits (α-1-10, β1-4, γ, ", σ), which structurally link to form a pentamer in homomeric or heteromeric combinations. Nicotinic acetylcholine receptors are of broad interest due to their central involvement in disease states and in mediating the paralysis of prey and human victims upon envenoming by some venomous animals. α-nAChR subunits are targeted by toxins within venoms from a diverse range of animals including cone snails, scorpions, snakes, and spiders, as well as poisonous organisms such as dart frogs and cyanobacteria [4–8]. The targeting of α-1 nAChR by these toxins allows effective immobilisation of prey through the flaccid paralysis of voluntary muscles, leading to death by respiratory failure. Toxins targeting the α-1 nAChR have evolved in snake venom on at least four separate occasions: three finger toxins (e.g., α-bungarotoxin), which are widespread in the advanced snakes (Caenophidia), waglerin peptides from the Tropidolaemus genus of Asian pit vipers, azemiopsin peptides from the Asian viper genus Azemiops, and phospholipase A2 toxins from vipers within the Bitis genus [9–12]. As these four neurotoxin classes are structurally unrelated to each other and possess different protein scaffolds, they represent a remarkable functional convergence of toxins independently targeting the same neurological target (α-1 nAChRs) at the neuromuscular junction of various prey types. Furthermore, due to variations in the amino acid sequence alignments of nAChR subunits within different taxa, these neurotoxin classes represent excellent study systems for investigating how prey specific toxins evolve and, in parallel, how resistance evolves in prey and predators of venomous snakes. A lack of high-throughput assays that measure effects upon specific-species nAChRs or receptor subtypes has been a major limitation hampering studies on the evolution of these neurotoxins, their clinical effects, and their biodiscovery. Current analytical methods to determine the binding of toxins to nAChRs are either low-throughput (in vitro skeletal muscle preparations, such as the chick biventer cervicis nerve-muscle preparation or mouse/rat phrenic nerve hemidiaphragm), cumbersome (oocyte patch-clamp systems), and/or taxonomically limited (cellular screening techniques such as Fluorescence Imaging Plate Reader (FLIPR)) [13]. In addition to limitations such as requiring animal dissections and high consumption of precious venoms and pure toxins, these assays cannot test for taxon-specific venom effects upon prey or the evolution of toxin resistance by prey. Thus, there is an unmet need for a flexible, high-throughput method that can accurately measure such biomolecular interactions. A newer, more robust biomolecular detection method of analyte-ligand binding of nAChRs is vital to overcome these hindrances. Short synthetic peptides (mimotopes) corresponding to the orthosteric site of nAChRs have been utilized in ligand binding studies of α-bungarotoxin to investigate their use as first aid or antivenom supplements [14–17]. These studies include the use of surface plasmon resonance (SPR), a microfluidics delivery system which clogs easily, requires experienced operators and expensive gold sensor chips, is low throughput, and has high running and maintenance costs. Consequently, the use of mimotopes to study ligand binding to nAChR orthosteric sites has remained dormant for over 15 years. Previous approaches using mimotope peptides also did not take a taxonomically diverse approach, investigating only human and rodent chimeric analogs. Toxins 2019, 11, 600 3 of 11 More recent research used the mollusk acetylcholine binding protein [18] and chimeric forms with human α-7 residues at the orthosteric site [19] to investigate snake venom relative potencies and the potential therapeutic usefulness as ‘decoy proteins’. In both cases, studies were hampered by the fact that snake venom nAChR targeting neurotoxins have been evolutionarily selected for the muscle-type α-1 subunit [8]. Thus, human α-7 orthosteric sequence results may be misleading for evolutionary or potential clinical effects studies and the dramatically lower affinity relative to the α-1 orthosteric site would limit the usefulness of α-7 based proteins as antivenom supplements. The mollusk acetylcholine binding protein is vastly more evolutionarily distant and therefore studies which investigated snake venom evolutionary patterns using this assay would be skewed, as was shown in one such study in which known neurotoxic snakes, such as within the Boiga genus, did not bind in the assay [18]. We have developed a high-throughput method which has many advantages that overcome the aforementioned limitations of current analytical approaches of nAChR binding. Our method is based upon mimotope peptides corresponding to α-nAChR subunit orthosteric sites spanning the full range of nAChR α-subunits
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