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In Vitro Evaluation of Neutral Aryloximes As Reactivators for Electrophorus Eel Acetylcholinesterase Inhibited by Paraoxon

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In Vitro Evaluation of Neutral Aryloximes As Reactivators for Electrophorus Eel Acetylcholinesterase Inhibited by Paraoxon biomolecules Article In Vitro Evaluation of Neutral Aryloximes as Reactivators for Electrophorus eel Acetylcholinesterase Inhibited by Paraoxon Daniel A. S. Kitagawa 1,2 , Samir F. de A. Cavalcante 2,3,4,5,* , Reuel L. de Paula 2,6 , Rafael B. Rodrigues 2, Leandro B. Bernardo 2, Munique C. J. da Silva 2 , Thiago N. da Silva 4, Wellington V. dos Santos 7,8, José M. Granjeiro 6, Joyce S. F. D. de Almeida 1 , Marcos C. Barcellos 2, Ana Beatriz de A. Correa 2 , Tanos C. C. França 1,5 , Kamil Kuˇca 5,* and Alessandro B. C. Simas 3,* 1 Laboratory of Molecular Modelling Applied to Chemical and Biological Defense (LMACBD), Military Institute of Engineering (IME), Praça General Tibúrcio 80, Rio de Janeiro 22290-270, Brazil 2 Brazilian Army Institute of Chemical, Biological, Radiological and Nuclear Defense (IDQBRN), Brazilian Army Technological Center (CTEx), Avenida das Américas 28705, Rio de Janeiro 23020-470, Brazil 3 Walter Mors Institute of Research on Natural Products (IPPN), Federal University of Rio de Janeiro (UFRJ), CCS, Bloco H, Rio de Janeiro 21941-902, Brazil 4 Castelo Branco University (UCB), School of Pharmacy, Avenida Santa Cruz 1631, Rio de Janeiro 21710-255, Brazil 5 Department of Chemistry, Faculty of Science, University of Hradec Králové, Rokitanskeho 62, 50003 Hradec Králové, Czech Republic 6 National Institute of Metrology, Standardization and Industrial Quality (INMETRO), Avenida Nossa Senhora das Graças 50, Duque de Caxias 25250-020, Brazil 7 Emergency and Rescue Department (DSE), Rio de Janeiro State Fire Department (CBMERJ), Praça São Salvador 4, Rio de Janeiro 22231-170, Brazil 8 School of Biomedicine, University Universus Veritas (UNIVERITAS), Rua Marquês de Abrantes 55, Rio de Janeiro 22230-060, Brazil * Correspondence: [email protected] (S.F.d.A.C.); [email protected] (K.K.); [email protected] (A.B.C.S.) Received: 9 September 2019; Accepted: 4 October 2019; Published: 8 October 2019 Abstract: Casualties caused by organophosphorus pesticides are a burden for health systems in developing and poor countries. Such compounds are potent acetylcholinesterase irreversible inhibitors, and share the toxic profile with nerve agents. Pyridinium oximes are the only clinically available antidotes against poisoning by these substances, but their poor penetration into the blood-brain barrier hampers the efficient enzyme reactivation at the central nervous system. In searching for structural factors that may be explored in future SAR studies, we evaluated neutral aryloximes as reactivators for paraoxon-inhibited Electrophorus eel acetylcholinesterase. Our findings may result into lead compounds, useful for development of more active compounds for emergencies and supportive care. Keywords: acetylcholinesterase; pesticides; neutral oximes; antidotes; drug design 1. Introduction Acetylcholinesterase (AChE, EC 3.1.1.7, 1) is a serine-esterase, a key enzyme for the parasympathetic neurotransmission. This enzyme can be found in the brain, erythrocytes, and muscles, being responsible for the hydrolysis of the neurotransmitter acetylcholine (ACh, 2) into Biomolecules 2019, 9, 583; doi:10.3390/biom9100583 www.mdpi.com/journal/biomolecules BiomoleculesBiomolecules 2019 2019, ,9 9, ,x x 22 of of 13 13 1.1. Introduction Introduction Acetylcholinesterase (AChE, EC 3.1.1.7, 1) is a serine-esterase, a key enzyme for the BiomoleculesAcetylcholinesterase2019, 9, 583 (AChE, EC 3.1.1.7, 1) is a serine-esterase, a key enzyme for 2 ofthe 13 parasympatheticparasympathetic neurotransmission.neurotransmission. ThisThis enzymeenzyme cancan bebe foundfound inin thethe brain,brain, erythrocyteserythrocytes, , andand muscles,muscles, being being responsible responsible for for the the hydrolysis hydrolysis of of the the neurotransmitter neurotransmitter acetylcholine acetylcholine (ACh, (ACh, 2 2)) into into it itss twotwoits two precursors,precursors, precursors, acetateacetate acetate ((33)) ( and3and) and cholinecholine choline ((44) (),4 , ending),ending ending thethe the potentialpotential potential actionaction action atat at thethe the postpost post-synaptic--synapticsynaptic cleft cleft (Scheme(Scheme 11) 1))[ [1 [11––44]] SchemeScheme 1. 1. Hydrolysis Hydrolysis of of ACh ACh by by AChE. AChE. TheThe h h hydrolysisydrolysisydrolysis of of ACh ACh by by AChE AChE is is accomplished accomplished at at the the esteratic esteratic site site (a (a catalytic catalytic triad triad composed composed byby residues residues serine, serine, histidinehistidine histidine,, , andand glutamate),glutamate), whichwhich which isis is highlyhighly highly conservedconserved conserved throughoutthroughout throughout thethe the species.species. species. InhibitionInhibition of of the the catalytic catalytic serine serine residueresidue via via phosphorylation phosphorylation leads leads to to accumulation accumulation of of ACh, ACh, causing causing overstimulationoverstimulation ofof cholinergic cholinergic innervations innervations andand ultimately, ultimately, death deathdeath [5 [[55–––888]].]. OrganophosphorusOrganophosphorus (OP)(OP) (OP) compoundscompounds are areare wellwell-studiedwell--studiedstudied AChE AChEAChE inhibitors. inhibitors.inhibitors. The TThehe nerve nervenerve agents agentsagents sarin sarinsarin (5 (),(55), soman), somansoman (6 ), ((66 tabun),), tabuntabun (7 ), ((7 VX7),), VXVX (8), ((and88),), and and pesticides pesticides pesticides such such such as as paraoxonas paraoxon paraoxon (9 ( )(99 and)) and and malathion malathion malathion ( 10( (1010),)), are ,are are relevantrelevant relevant examplesexamples examples of of such suchsuch compounds compounds (Figure1)[ 8,9]. While nerve agents are strictly regulated by the Chemical Weapons Convention (Figure(Figure 1)1) [8,9][8,9]. .WhileWhile nervenerve agentsagents areare strictlystrictly regulatedregulated byby thethe ChemicalChemical WeaponsWeapons ConventionConvention (CWC)(CWC) [10][10] [10,], , aa a multilateralmultilateral multilateral treatytreaty treaty thatthat that enteredentered entered intointo into forceforce force inin 1997, in1997, 1997, pesticidespesticides pesticides areare not arenot re notregulatedgulated regulated byby anyany by internationalinternationalany international agency agency agency,, ,and and their their and theiruse use is is use still still is subjected subjected still subjected to to each each to country eachcountry country’s’s’s discretion discretion discretion.. .Consequently Consequently Consequently,, ,non non-- developeddevelopednon-developed andand eveneven and developing evendeveloping developing countriescountries countries still still useuse still pesticidespesticides use pesticides already already already forbidden forbidden forbidden in in thethe U inUnitednited the United SStatestates andandStates EuropeEurope and Europe [11[11––1414]]. [ .11 Recently,Recently,–14]. Recently, thethe BrazilianBrazilian the Brazilian ParliamentParliament Parliament hashas discusseddiscussed has discussed aa controversialcontroversial a controversial liftlift ofof thethe lift banban of forforthe using banusing for somesome using aggressiveaggressive some aggressive pesticides,pesticides, pesticides, raisingraising raising fearsfears fears ofof pollutionpollution of pollution ofof oflands,lands, lands, waterwater water coursescourses courses,, , and and groundwater,groundwater, as as well well well as as as the the the intoxication intoxication intoxication of of of workers workers workers and and and animals animals animals [15 [15 [15––1818–18]]. .Beside ].Beside Besidesss economic economic economic impact impact impact in in tradetradein trade agreements,agreements, agreements, environmentalenvironmental environmental andand and occupationaloccupational occupational issues,issues, issues, accidentalaccidental accidental poisoningpoisoning poisoning ofof of childrenchildren children,, , and and suicidesuicide attemptsattempts are areare also alsoalso additional additionaladditional costs costcost forss theforfor governmental thethe governmentalgovernmental health healthhealth systems systemssystems [8,19–27 [8,19[8,19]. These––2727]]. harmful . TheseThese harmfulharmfulchemicals chemicals chemicals are also are associatedare also also associated associated with neurodegenerative with with n neurodegenerativeeurodegenerative diseases diseases [diseases28]. [28] [28]. FigureFigure 1. 1. Toxic ToxicToxic organophosphorus organophosphorus compounds. compounds. Aiming to control mosquito vectors in densely populated areas of the tropical countries, insecticides AimingAiming toto controlcontrol mosquitomosquito vectorsvectors inin denselydensely populatedpopulated areasareas ofof thethe tropicaltropical countriescountries, , have been aerosolized. Despite of the inefficiency of this methodology and studies accounting for insecticidesinsecticides havehave beenbeen aerosolizedaerosolized. DespiteDespite ofof thethe inefficiencyinefficiency ofof thisthis methodologymethodology andand studiesstudies development of vector’s resistance, it is still used. Tropical diseases are a burden for health systems in developing and under-developed countries. For example, arboviruses in Brazil transmitted by Aedes aegypti (Dengue, Yellow Fever, Zika, and Chikungunya) and Anopheles sp. (Malaria) have high rate of mortality and morbidity, among other mosquito-borne diseases. Brazilian National Health Biomolecules 2019, 9, x 3 of 13 Biomolecules 2019, 9, x 3 of 13 accounting for development of vector’s resistance, it is still used. Tropical diseases are a burden for
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