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Identification and Characterization of Novel Proteins from Arizona Bark toxins Article Identification and Characterization of Novel Proteins from Arizona Bark Scorpion Venom That Inhibit Nav1.8, a Voltage-Gated Sodium Channel Regulator of Pain Signaling Tarek Mohamed Abd El-Aziz 1,2,† , Yucheng Xiao 3,†, Jake Kline 4, Harold Gridley 4, Alyse Heaston 4, Klaus D. Linse 5, Micaiah J. Ward 6 , Darin R. Rokyta 6 , James D. Stockand 1, Theodore R. Cummins 3, Luca Fornelli 4 and Ashlee H. Rowe 4,* 1 Department of Cellular & Integrative Physiology, University of Texas Health Science Center San Antonio, San Antonio, TX 78229, USA; [email protected] (T.M.A.E.-A.); [email protected] (J.D.S.) 2 Zoology Department, Faculty of Science, Minia University, El-Minia 61519, Egypt 3 Department of Biology, School of Science, Indiana University-Purdue University Indianapolis, Indianapolis, IN 46202, USA; [email protected] (Y.X.); [email protected] (T.R.C.) 4 Department of Biology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA; [email protected] (J.K.); [email protected] (H.G.); [email protected] (A.H.); [email protected] (L.F.) 5 Bio-Synthesis Inc., 612 E. Main Street, Lewisville, TX 75057, USA; [email protected] 6 Department of Biological Sciences, Florida State University, 319 Stadium Drive, Tallahassee, FL 32306, USA; [email protected] (M.J.W.); [email protected] (D.R.R.) * Correspondence: [email protected]; Tel.: +1-936-577-5782 † These authors contributed equally. Citation: Abd El-Aziz, T.M.; Xiao, Y.; Abstract: The voltage-gated sodium channel Nav1.8 is linked to neuropathic and inflammatory pain, Kline, J.; Gridley, H.; Heaston, A.; highlighting the potential to serve as a drug target. However, the biophysical mechanisms that Linse, K.D.; Ward, M.J.; Rokyta, D.R.; regulate Nav1.8 activation and inactivation gating are not completely understood. Progress has been Stockand, J.D.; Cummins, T.R.; et al. hindered by a lack of biochemical tools for examining Nav1.8 gating mechanisms. Arizona bark Identification and Characterization of scorpion (Centruroides sculpturatus) venom proteins inhibit Nav1.8 and block pain in grasshopper Novel Proteins from Arizona Bark mice (Onychomys torridus). These proteins provide tools for examining Nav1.8 structure–activity Scorpion Venom That Inhibit Nav1.8, relationships. To identify proteins that inhibit Nav1.8 activity, venom samples were fractioned a Voltage-Gated Sodium Channel using liquid chromatography (reversed-phase and ion exchange). A recombinant Nav1.8 clone Regulator of Pain Signaling. Toxins expressed in ND7/23 cells was used to identify subfractions that inhibited Nav1.8 Na+ current. 2021, 13, 501. https://doi.org/ Mass-spectrometry-based bottom-up proteomic analyses identified unique peptides from inhibitory 10.3390/toxins13070501 subfractions. A search of the peptides against the AZ bark scorpion venom gland transcriptome Received: 24 June 2021 revealed four novel proteins between 40 and 60% conserved with venom proteins from scorpions in Accepted: 16 July 2021 four genera (Centruroides, Parabuthus, Androctonus, and Tityus). Ranging from 63 to 82 amino acids, Published: 18 July 2021 each primary structure includes eight cysteines and a “CXCE” motif, where X = an aromatic residue (tryptophan, tyrosine, or phenylalanine). Electrophysiology data demonstrated that the inhibitory Publisher’s Note: MDPI stays neutral effects of bioactive subfractions can be removed by hyperpolarizing the channels, suggesting that with regard to jurisdictional claims in proteins may function as gating modifiers as opposed to pore blockers. published maps and institutional affil- iations. Keywords: voltage-gated sodium channel; Nav1.8; hyperpolarization; pain signaling; scorpion venom; neurotoxin; bioactive proteins; drug discovery; Onychomys torridus; Centruroides sculpturatus Key Contribution: Few venom proteins have been identified that modify Nav1.8 gating to inhibit Copyright: © 2021 by the authors. activity. Novel AZ bark scorpion venom proteins provide tools for investigating the biophysical Licensee MDPI, Basel, Switzerland. mechanisms underlying Nav1.8 activation and inactivation gating—the first step toward engineering This article is an open access article proteins that inhibit Nav1.8 activity in humans to block pain. distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Toxins 2021, 13, 501. https://doi.org/10.3390/toxins13070501 https://www.mdpi.com/journal/toxins Toxins 2021, 13, 501 2 of 21 Toxins 2021, 13, x FOR PEER REVIEW 2 of 21 1.1. IntroductionIntroduction PrimaryPrimary sensory nociceptive nociceptive neurons, neurons, whose whose cell cell bodies bodies reside reside in the in dorsal the dorsal root gan- root gangliaglia (DRG) (DRG) of the of the body body and and limbs limbs or orin inthe the trigeminal trigeminal ganglia ganglia (TG) (TG) of of the the head head and and face, face, transmittransmit painpain signalssignals toto thethe centralcentral nervous system (CNS) (CNS) [1–4]. [1–4]. Tissue Tissue damage damage due due to to injury,injury, aging,aging, oror diseasedisease causescauses biochemicalbiochemical changes in in nociceptive nociceptive neurons neurons that that activate activate thethe voltage-gatedvoltage-gated sodiumsodium channelchannel (VGSC)(VGSC) Nav1.7,Nav1.7, whichwhich thenthen recruitsrecruitsNav1.8 Nav1.8 [[1,5–8].1,5–8]. Ac- Acti- + vationtivation of of Nav1.8 Nav1.8 generates generates the the majority majority of of the the Na Nacurrent+ current underlying underlying the the action action potentials poten- thattials carry that paincarry signals pain signals to the brain; to the inactivation brain; inactivation terminates terminates the action-potential-driven the action-potential- pain signalsdriven pain [5–8]. signals Chronic [5–8]. pain Chronic results pain from result prolongeds from prolonged activation oractivation failed inactivation or failed inacti- [1,9]. Nav1.8vation [1,9]. activity Nav1.8 is linked activity to mechanical, is linked to mechanical, neuropathic, neuropathic, and inflammatory and inflammatory pain, highlighting pain, thehighlighting potential the for Nav1.8potential to for serve Nav1.8 as a to drug serve target as a [drug7,8,10 target–18]. However,[7,8,10–18]. the However, biophysical the mechanismsbiophysical mechanisms that regulate that Nav1.8 regulate gating Nav1.8 are not gating completely are not completely understood, understood, particularly par- the mechanismsticularly the mechanisms that regulate that Nav1.8 regu inactivationlate Nav1.8 [inactivation9]. [9]. + TheThe functionfunction ofof a VGSC is to open briefly, briefly, allowing an influx influx of Na Na+ ionsions to to depolarize depolarize cellcell membranesmembranes andand generating the action potentials potentials that that underlie underlie neuronal neuronal signaling signaling and and musclemuscle contractioncontraction [[19–21].19–21]. VGSC alpha alpha subuni subunitsts have have four four domains, domains, DI–DIV DI–DIV (Figure (Figure 1).1). EachEach domaindomain hashas six six membrane-spanning membrane-spanning helices helices (S1–S6) (S1–S6) and and re-entrant re-entrant loops loops that that connect con- S5nect and S5 S6 and (Pore). S6 (Pore). The domainsThe domains are organized are organiz suched such that thethat re-entrant the re-entrant loops loops face eachface each other toother form to an form ion-permeating an ion-permeating pore with pore an with activation an activation gate. When gate. a cellWhen is ata rest,cell is the at activationrest, the gateactivation is closed. gate The is closed. S4 segments The S4 of eachsegments domain of each have domain alternating have positively alternating charged positively amino acidscharged that amino function acids as voltagethat function sensors. as Biochemicalvoltage sensors. changes Biochemical in damaged changes tissues in depolarizedamaged membranes,tissues depolarize imposing membranes, electrostatic imposing forces electros on thesetatic positive forces on charges. these positive The voltage charges. sensors The movevoltage outward sensors and move open outward the channel and (activated)open the channel [20,22]. (activated) The outward [20,22]. movements The outward of S4 in DI–DIIImovements initiate of S4 channel in DI–DIII activation initiate (opening); channel activation the S4 in (opening); the fourth domainthe S4 in detectsthe fourth channel do- openingmain detects and channel initiates opening fast inactivation. and initiates During fast inactivation. fast inactivation, During fast part inactivation, of the DIII–DIV part intracellularof the DIII–DIV loop intracellular forms a “hinged loop forms lid” inactivation a “hinged lid” gate inactivation that moves gate into thethat mouth moves ofinto the channelthe mouth toblock of the the channel pore. Ato secondblock the type pore. of inactivation, A second type slow of inactivation, inactivation, occurs slow inactiva- when the poretion, loopsoccurs change when the conformation pore loops tochange block conformation the flow of ions to block [23]. Failedthe flow inactivation of ions [23]. prolongs Failed theinactivation action potentials prolongs that the carryaction pain potentials signals that to the carry brain. pain signals to the brain. FigureFigure 1.1. StructureStructure ofof aa voltage-gatedvoltage-gated sodiumsodium channelchannel (VGSC). (VGSC). The The channel channel consists consists of of four four repeating repeat- domainsing domains (DI–DIV), (DI–DIV), each each having having six six transmembrane
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