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Phoneutria Nigriventer Spider Toxin Pntx2-1 (Δ-Ctenitoxin-Pn1a) Is a Modulator of Sodium Channel Gating

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Phoneutria Nigriventer Spider Toxin Pntx2-1 (Δ-Ctenitoxin-Pn1a) Is a Modulator of Sodium Channel Gating toxins Article Phoneutria nigriventer Spider Toxin PnTx2-1 (δ-Ctenitoxin-Pn1a) Is a Modulator of Sodium Channel Gating Steve Peigneur 1,2,*,† ID , Ana Luiza B. Paiva 3,†, Marta N. Cordeiro 3,Márcia H. Borges 3, Marcelo R. V. Diniz 3, Maria Elena de Lima 2,4 and Jan Tytgat 1,* 1 Toxicology and Pharmacology, University of Leuven (KU Leuven), Campus Gasthuisberg, P.O. Box 922, Herestraat 49, 3000 Leuven, Belgium 2 Laboratório de Venenos e Toxinas Animais, Dept de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte 31270-901, Brazil; [email protected] 3 Departamento de Pesquisa e Desenvolvimento, Fundação Ezequiel Dias, Minas Gerais, Belo Horizonte 30510-010, Brazil; [email protected] (A.L.B.P.); [email protected] (M.N.C.); [email protected] (M.H.B.); [email protected] (M.R.V.D.) 4 Programa de Pós-graduação em Ciências da Saúde, Biomedicina e Medicina, Instituto de Ensino e Pesquisa da Santa Casa de Belo Horizonte, Grupo Santa Casa de Belo Horizonte, Minas Gerais, Belo Horizonte 31270-901, Brazil * Correspondence: [email protected] or [email protected] (S.P.); [email protected] (J.T.); Tel.: +321-632-3404 (J.T.) † These two authors contribute equally to this work. Received: 26 July 2018; Accepted: 16 August 2018; Published: 21 August 2018 Abstract: Spider venoms are complex mixtures of biologically active components with potentially interesting applications for drug discovery or for agricultural purposes. The spider Phoneutria nigriventer is responsible for a number of envenomations with sometimes severe clinical manifestations in humans. A more efficient treatment requires a comprehensive knowledge of the venom composition and of the action mechanism of the constituting components. PnTx2-1 (also called δ-ctenitoxin-Pn1a) is a 53-amino-acid-residue peptide isolated from the venom fraction PhTx2. Although PnTx2-1 is classified as a neurotoxin, its molecular target has remained unknown. This study describes the electrophysiological characterization of PnTx2-1 as a modulator of voltage-gated sodium channels. PnTx2-1 is investigated for its activity on seven mammalian NaV-channel isoforms, one insect NaV channel and one arachnid NaV channel. Furthermore, comparison of the activity of both PnTx2-1 and PnTx2-6 on NaV1.5 channels reveals that this family of Phoneutria toxins modulates the cardiac NaV channel in a bifunctional manner, resulting in an alteration of the inactivation process and a reduction of the sodium peak current. Keywords: Phoneutria nigriventer; voltage-gated sodium channel; spider; insecticide; peptide toxin PnTx2-1; gating modifier toxin Key Contribution: Phoneutria nigriventer toxin PnTx2-1 modulates both the activation and inactivation gating processes of voltage-gated sodium channels. PnTx2-1 exhibits a strong insecticidal activity. 1. Introduction Spiders can be considered one of the most successful venomous animals ever to inhabit the planet with over 47,000 species characterized to date [1]. Despite this diversity, no more than 100 spider species Toxins 2018, 10, 337; doi:10.3390/toxins10090337 www.mdpi.com/journal/toxins Toxins 2018, 10, x FOR PEER REVIEW 2 of 12 1. Introduction ToxinsSpiders2018, 10, 337can be considered one of the most successful venomous animals ever to inhabit2 ofthe 12 planet with over 47,000 species characterized to date [1]. Despite this diversity, no more than 100 spider species have had their venom investigated [2]. With over ten million estimated biologically activehave had peptides their venom in spider investigated venoms [3], [2]. this With means over tenthat million less than estimated 0.01% of biologically spider peptides active peptideshave been in studiedspider venoms [3,4], making [3], this spider means venom that less an than untapped 0.01% of treasure spider peptidesof biologically have been active studied compounds [3,4], making with promisingspider venom discoveries an untapped in drug treasure and bioinsecticide of biologically development active compounds [1,5,6]. Phoneutria with promising nigriventer discoveries are very aggressive,in drug and solitary bioinsecticide spiders. developmentThey are active [1 ,hunter5,6]. Phoneutrias, relying nigriventeron their fast-actingare very and aggressive, efficient solitaryvenom forspiders. prey capture They are and active defense. hunters, They relying prey normal on theirly fast-acting on insects, and although efficient there venom are reports for prey of capture Phoneutria and huntingdefense. on They other prey spiders normally and on small insects, rodent althoughs as well there [6,7]. are reportsHuman of envenomationPhoneutria hunting by Phoneutria on other nigriventerspiders and is smallcommon rodents in Brazil, as well with [6,7 0.5]. Human–1% resulting envenomation in severe by envenomation,Phoneutria nigriventer with mostis commonof these occurringin Brazil, within children 0.5–1% resulting[8]. Cysteine-rich in severe peptide envenomation, toxins with mostaction of on these ion occurring channels inare children the most [8]. abundantCysteine-rich components peptide toxinsin its venom with action [9]. A onrecent ion channelsreview describes are the mostthe complexity abundant componentsof this venom in [6]. its Historically,venom [9]. A the recent Phoneutria review describestoxins are the annotated complexity based of thison venomtheir occurrence [6]. Historically, in the thevenomPhoneutria when followingtoxins are the annotated venom basedpurification on their methods occurrence used in in the the venom first studies when [10], following that is, the based venom on purificationa particular chromatographicmethods used in thestep first and studies in the [10order], that of is,elutio basedn of on the a particular toxin, in chromatographicthis step. However, step a and new in nomenclaturethe order of elution has been of theproposed toxin, based in this on step. the However,genus of the a newspider, nomenclature the target of has the been toxin proposed and the isoformbased on [11]. the According genus of theto this spider, nomenclature, the target ofPnTx2-1 the toxin is also and called the isoform δ-ctenitoxin-Pn1a [11]. According and it can to this be accessednomenclature, in the PnTx2-1Arachnoserver is also calleddatabankδ-ctenitoxin-Pn1a (http://www.arachnoserver.org) and it can be accessed [2]. inIn-vivo the Arachnoserver studies have showndatabank that (http://www.arachnoserver.org the PhTx2 fraction is toxic to both)[ 2mice]. In-vivo and insects studies [12]. have Nine shown peptides that coul the PhTx2d be identified fraction fromis toxic the to PhTx2 both micefraction. and These insects peptides [12]. Nine were peptides named could accordingly be identified PnTx2-1 from to thePnTx2-9. PhTx2 PnTx2-1, fraction. PnTx2-5These peptides and PnTx2-6 were named showed accordingly higher toxicity PnTx2-1 after to PnTx2-9. intracerebral PnTx2-1, (i.c.) PnTx2-5 injection and in PnTx2-6mice [13]. showed Both PnTx2-5higher toxicity and PnTx2-6 after intracerebral have been characterized (i.c.) injection as in micemodulators [13]. Both of the PnTx2-5 inactivation and PnTx2-6 of voltage-gated have been sodiumcharacterized (NaV) aschannels modulators [14,15]. of the Toxin inactivation PnTx2-1 of(5838.8 voltage-gated Da) shares sodium up to (Na 77%V) channelsidentity with [14,15 PnTx2-5]. Toxin andPnTx2-1 PnTx2-6 (5838.8 (Figure Da) shares 1) [13]. up When to 77% injected identity in with mice PnTx2-5, PnTx2-1 and causes PnTx2-6 pruritus, (Figure lacrimation,1)[ 13]. When increased injected salivation,in mice, PnTx2-1 sweating causes and pruritus, agitation lacrimation, followed increased by spastic salivation, paralysis sweating of the and limbs agitation [12]. followed A recent by transcriptomicspastic paralysis and of theproteomic limbs [12 investigation]. A recent transcriptomic of P. nigriventer and venom proteomic showed investigation that PnTx2-1, of P. altogether nigriventer withvenom its showedisoforms, that is PnTx2-1,among the altogether most expressed with its isoforms,toxins in isthis among venom the [9], most suggesting expressed that toxins thisin toxin this mayvenom play [9], an suggesting important that role this in the toxin envenoming may play an of important natural preys. role inBased the envenoming on the in-vivo of naturaltests in preys.mice andBased the on sequence the in-vivo homology tests in mice with and PnTx2-5 the sequence and PnTx2-6, homology this withpeptide PnTx2-5 is classified and PnTx2-6, as a Na thisV-channel peptide toxin.is classified However, as a Nait hasV-channel never been toxin. tested However, on any it hasNaV never-channel been isoform. tested on Therefore, any NaV -channelin this study isoform. the NaTherefore,V-channel in subtype this study selectivity the NaV -channeland species subtype specific selectivityity of PnTx2-1 and species are investigated. specificity of Furthermore, PnTx2-1 are comparisoninvestigated. of Furthermore, the activity comparison of both PnTx2-1 of the activity and PnTx2-6 of both PnTx2-1on NaV1.5 and reveals PnTx2-6 that on NathisV 1.5family reveals of Phoneutriathat this family toxins of modulatesPhoneutria thetoxins cardiac modulates NaV channel the cardiac in a NabifunctionalV channel inmanner, a bifunctional resulting manner, in an alterationresulting inof anthe alteration inactivation of the process inactivation and a reduction process and of the a reduction sodium peak of the current. sodium peak current. Figure 1. SequenceSequence
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