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Venoms and Toxins

Editor-in-Chief

ISSN (Print): 2666-1217
ISSN (Online): 2666-1225

Research Article

Evaluation of the Toxicological Effects from Bothrops Jararacussu Snake Venom on Zebrafish (Danio Rerio) Embryos and Larvae

Author(s): Layssa Gualberto da Silva, Pierri Emanoel De Abreu Oliveira, Pedro Gabriel Nascimento dos Santos, Juliana Alves Costa Ribeiro Souza, Rafael Xavier Martins, Maria Caroline Lourenço de Lima, Erica de Souza Falcão, Davi Felipe Farias and Daniela Priscila Marchi-Salvador*

Volume 3, 2023

Published on: 12 July, 2023

Article ID: e150523216919 Pages: 12

DOI: 10.2174/2666121703666230515122901

Price: $65

Abstract

Introduction: Approximately 90% of reported and identified cases of snakebites in Brazil are caused by species belonging to the Bothrops genus. These snakes have clinical relevance due to their venom composition, which contains substances capable of triggering local and systemic effects, leading to morbidities and/or mortality.

Objective: The objective of this study was to evaluate the toxic and toxinological effects of Bothrops Jararacussu snake venom on zebrafish embryos and larvae.

Methods: The stability of B. Jararacussu snake venom under the conditions used in the toxicity experiments in zebrafish embryos and larvae was evaluated on citrated human plasma. Zebrafish embryos and/or larvae mortality, morphological alterations, spontaneous tail movements and heartbeat caused by the venom were quantified within 96 hours. Toxicity parameters and activity of enzyme-related toxicity biomarkers were evaluated in zebrafish after 96 hours of semi-static exposure to the venom.

Results: The results indicated that the venom causes toxicity in zebrafish embryos and larvae, inducing embryonic mortality, alteration in the number of spontaneous tail movements and activity of biomarker enzymes. The results suggested that the toxic effects caused by the venom in the early stages of zebrafish development are mediated, in part, by neurotoxic action, induction of oxidative and metabolic stress caused by low molecular weight components, and proteins present in this venom.

Conclusion: Toxinological evaluations using the zebrafish as a model are scarce; however, this study presented promising results that encourage the development of future research in toxinology using this animal as a model organism.

[1]
Paixão-Júnior OB, Silva DP, Ferreira SS, et al. Comparative protein composition and biological effects caused by Bothrops Jararacussu and B. moojeni crude venoms. Venoms Toxins 2021; 1(1): 67-84.
[http://dx.doi.org/10.2174/2666121701999200618102634]
[2]
Silva JL, Siva AM, Amaral GLG, Ortega GP, Monteiro WM, Bernarde PS. The deadliest snake according to ethnobiological perception of the population of the Alto Juruá region, western Brazilian Amazonia. Rev Soc Bras Med Trop 2020; 53: e20190305.
[http://dx.doi.org/10.1590/0037-8682-0305-2019] [PMID: 31859953]
[3]
Suraweera W, Warrell D, Whitaker R, et al. Trends in snakebite deaths in India from 2000 to 2019 in a nationally representative mortality study. eLife 2020; 9: e54076.
[http://dx.doi.org/10.7554/eLife.54076] [PMID: 32633232]
[4]
Gutiérrez JM, Calvete JJ, Habib AG, Harrison RA, Williams DJ, Warrell DA. Correction: Snakebite envenoming. Nat Rev Dis Primers 2017; 3(1): 17079.
[http://dx.doi.org/10.1038/nrdp.2017.79]
[5]
Casewell NR, Jackson TNW, Laustsen AH, Sunagar K. Causes and consequences of snake venom variation. Trends Pharmacol Sci 2020; 41(8): 570-81.
[http://dx.doi.org/10.1016/j.tips.2020.05.006] [PMID: 32564899]
[6]
Williams D. Snakebite. World Health Organization. 2023. Available From: https://www.who.int/health-topics/snakebite#tab=tab_1
[7]
Brasil, Ministério da Saúde. Acidente por animais peçonhentos - Notificações registradas no sistema de informação de agravos de notificação – Sinan Net. Banco de dados do Sistema Único de Saúde-DATASUS 2023. Available From: http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sinannet/animaisp/bases/animaisbrnet.def
[8]
Oliveira SS, Alves EC, Santos AS, et al. Factors associated with systemic bleeding in Bothrops envenomation in a tertiary hospital in the Brazilian Amazon. Toxins 2019; 11(1): 22.
[http://dx.doi.org/10.3390/toxins11010022] [PMID: 30621001]
[9]
Larréché S, Chippaux JP, Chevillard L, et al. Bleeding and thrombosis: Insights into pathophysiology of Bothrops venom-related hemostasis disorders. Int J Mol Sci 2021; 22(17): 9643.
[http://dx.doi.org/10.3390/ijms22179643] [PMID: 34502548]
[10]
Albuquerque PLMM, Jacinto CN, Silva GB. Junior, Lima JB, Veras MDSB, Daher EF. Lesão renal aguda causada pelo veneno das cobras Crotalus e Bothrops: Revisão da epidemiologia, das manifestações clínicas e do tratamento. Rev Inst Med Trop São Paulo 2013; 55(5): 295-301.
[http://dx.doi.org/10.1590/S0036-46652013000500001] [PMID: 24037282]
[11]
Renally Santos de Moraes RCA, Costa e Silva R, Cav-alcante Santos E. Aspectos Epidemiológicos Dos Acidentes Ofídicos na Região Nordeste no Período Entre 2016-2019. Revista interdisciplinar emsaúde 2021; 8(Único): 226-38.
[http://dx.doi.org/10.35621/23587490.v8.n1.p226-238]
[12]
Spolaore B, Fernández J, Lomonte B, Massimino ML, Tonello F. Enzymatic labelling of snake venom phospholipase A2 toxins. Toxicon 2019; 170: 99-107.
[http://dx.doi.org/10.1016/j.toxicon.2019.09.019] [PMID: 31563525]
[13]
Silva GM, Souza DHB, Waitman KB, et al. Design, synthesis, and evaluation of Bothrops venom serine protease peptidic inhibitors. J Venom Anim Toxins Incl Trop Dis 2021; 27: e20200066.
[http://dx.doi.org/10.1590/1678-9199-jvatitd-2020-0066] [PMID: 33488681]
[14]
Marcussi S, Bernardes CP, Santos-Filho NA, et al. Molecular and functional characterization of a new non-hemorrhagic metalloprotease from Bothrops Jararacussu snake venom with antiplatelet activity. Peptides 2007; 28(12): 2328-39.
[http://dx.doi.org/10.1016/j.peptides.2007.10.010] [PMID: 18006118]
[15]
Barbosa LG, Costa TR, Borges IP, et al. A comparative study on the leishmanicidal activity of the L-amino acid oxidases BjussuLAAO-II and BmooLAAO-II isolated from Brazilian Bothrops snake venoms. Int J Biol Macromol 2021; 167(167): 267-78.
[http://dx.doi.org/10.1016/j.ijbiomac.2020.11.146] [PMID: 33242552]
[16]
Pires WL, Kayano AM, de Castro OB, et al. Lectin isolated from Bothrops Jararacussu venom induces IL-10 release by TCD4+ cells and TNF-α release by monocytes and natural killer cells. J Leukoc Biol 2019; 106(3): 595-605.
[http://dx.doi.org/10.1002/JLB.MA1118-463R] [PMID: 31087703]
[17]
Kashima S, Roberto PG, Soares AM, et al. Analysis of Bothrops Jararacussu venomous gland transcriptome focusing on structural and functional aspects: I--gene expression profile of highly expressed phospholipases A2. Biochimie 2004; 86(3): 211-9.
[http://dx.doi.org/10.1016/j.biochi.2004.02.002] [PMID: 15134836]
[18]
Correa-Netto C, Teixeira-Araujo R, Aguiar AS, et al. Immunome and venome of Bothrops Jararacussu: A proteomic approach to study the molecular immunology of snake toxins. Toxicon 2010; 55(7): 1222-35.
[http://dx.doi.org/10.1016/j.toxicon.2009.12.018] [PMID: 20060013]
[19]
Jorge RJB, Monteiro HSA, Gonçalves-Machado L, et al. Venomics and antivenomics of Bothrops erythromelas from five geographic populations within the Caatinga ecoregion of northeastern Brazil. J Proteomics 2015; 114: 93-114.
[http://dx.doi.org/10.1016/j.jprot.2014.11.011] [PMID: 25462430]
[20]
Segura Á, Herrera M, Vargas M, et al. Preclinical efficacy against toxic activities of medically relevant Bothrops sp. (Serpentes: Viperidae) snake venoms by a polyspecific antivenom produced in Mexico. Rev Biol Trop 2016; 65(1): 345-50.
[http://dx.doi.org/10.15517/rbt.v65i1.18908] [PMID: 29466649]
[21]
Garcia Soares. Stockand, Stockand JD. Mohamed Abd El-Aziz. Snake venoms in drug discovery: Valuable therapeutic tools for life saving. Toxins 2019; 11(10): 564.
[http://dx.doi.org/10.3390/toxins11100564] [PMID: 31557973]
[22]
Lazarovici P, Marcinkiewicz C, Lelkes PI. From snake venom’s disintegrins and C-type lectins to anti-platelet drugs. Toxins 2019; 11(5): 303.
[http://dx.doi.org/10.3390/toxins11050303] [PMID: 31137917]
[23]
Lin F, Reid PF, Qin Z. Cobrotoxin could be an effective therapeutic for COVID-19. Acta Pharmacol Sin 2020; 41(9): 1258-60.
[http://dx.doi.org/10.1038/s41401-020-00501-7] [PMID: 32843715]
[24]
Andersen ML, Winter LMF. Animal models in biological and biomedical research - experimental and ethical concerns. An Acad Bras Cienc 2019; 91 (Suppl. 1): e20170238.
[http://dx.doi.org/10.1590/0001-3765201720170238] [PMID: 28876358]
[25]
Fernandes MR, Pedroso AR. Animal experimentation: A look into ethics, welfare and alternative methods. Rev Assoc Med Bras 2017; 63(11): 923-8.
[http://dx.doi.org/10.1590/1806-9282.63.11.923] [PMID: 29451652]
[26]
Hickman DL, Johnson J, Vemulapalli TH, Crisler JR, Shepherd R. Commonly used animal models, principles of animal research for graduate and undergraduate students. Cambridge: Academic Press 2017; pp. 117-75.
[27]
Coghlan A. Just 2.5% of DNA turns mice into men. New Scientist 2002. Available From: https://www.newscientist.com/article/dn2352-just-2-5-of-dna-turns-mice-into-men/#ixzz7LUxxMiEO
[28]
Zon LI, Peterson RT. In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 2005; 4(1): 35-44.
[http://dx.doi.org/10.1038/nrd1606] [PMID: 15688071]
[29]
Bailone RL, Fukushima HCS, Ventura Fernandes BH, et al. Zebrafish as an alternative animal model in human and animal vaccination research. Lab Anim Res 2020; 36(1): 13.
[http://dx.doi.org/10.1186/s42826-020-00042-4] [PMID: 32382525]
[30]
Ali S, Mil HGJ, Richardson MK. Large-scale assessment of the zebrafish embryo as a possible predictive model in toxicity testing. PLoS One 2011; 6(6): e21076.
[http://dx.doi.org/10.1371/journal.pone.0021076] [PMID: 21738604]
[31]
Cassar S, Adatto I, Freeman JL, et al. Use of zebrafish in drug discovery toxicology. Chem Res Toxicol 2020; 33(1): 95-118.
[http://dx.doi.org/10.1021/acs.chemrestox.9b00335] [PMID: 31625720]
[32]
Choi TY, Choi TI, Lee YR, Choe SK, Kim CH. Zebrafish as an animal model for biomedical research. Exp Mol Med 2021; 53(3): 310-7.
[http://dx.doi.org/10.1038/s12276-021-00571-5] [PMID: 33649498]
[33]
Ducharme NA, Reif DM, Gustafsson JA, Bondesson M. Comparison of toxicity values across zebrafish early life stages and mammalian studies: Implications for chemical testing. Reprod Toxicol 2015; 55: 3-10.
[http://dx.doi.org/10.1016/j.reprotox.2014.09.005] [PMID: 25261610]
[34]
Polaka S, Koppisetti HP, Pande S, Tekade M, Sharma MC, Tekade RK. Zebrafish models for toxicological screening. Pharmacokinetics and toxicokinetic considerations. (1st ed.). Cambridge: Academic Press 2022; Vol. II: pp. 221-40.
[http://dx.doi.org/10.1016/B978-0-323-98367-9.00011-1]
[35]
Bauer B, Mally A, Liedtke D. Zebrafish embryos and larvae as alternative animal models for toxicity testing. Int J Mol Sci 2021; 22(24): 13417.
[http://dx.doi.org/10.3390/ijms222413417] [PMID: 34948215]
[36]
Lieschke GJ, Currie PD. Animal models of human disease: Zebrafish swim into view. Nat Rev Genet 2007; 8(5): 353-67.
[http://dx.doi.org/10.1038/nrg2091] [PMID: 17440532]
[37]
Howe K, Clark MD, Torroja CF, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496(7446): 498-503.
[http://dx.doi.org/10.1038/nature12111] [PMID: 23594743]
[38]
Vieira LR, Hissa DC, Souza TM, et al. Proteomics analysis of zebrafish larvae exposed to 3,4dichloroaniline using the fish embryo acute toxicity test. Environ Toxicol 2020; 35(8): 849-60.
[http://dx.doi.org/10.1002/tox.22921] [PMID: 32170993]
[39]
Langova V, Vales K, Horka P, Horacek J. The role of zebrafish and laboratory rodents in schizophrenia research. Front Psychiatry 2020; 11: 703.
[http://dx.doi.org/10.3389/fpsyt.2020.00703] [PMID: 33101067]
[40]
Sousa IDL, Barbosa AR, Salvador GHM, et al. Secondary hemostasis studies of crude venom and isolated proteins from the snake Crotalus durissus terrificus. Int J Biol Macromol 2019; 131: 127-33.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.03.059] [PMID: 30867125]
[41]
[42]
Finney DJ. Probit analysis: A statistical treatment of the sigmoid response curve. Cambridge: University Press 1952.
[43]
Muniz MS, Halbach K, Alves Araruna IC, et al. Moxidectin toxicity to zebrafish embryos: Bioaccumulation and biomarker responses. Environ Pollut 2021; 283: 117096.
[http://dx.doi.org/10.1016/j.envpol.2021.117096] [PMID: 33866217]
[44]
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72(1-2): 248-54.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[45]
Ellman GL, Courtney KD, Andres V Jr, Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961; 7(2): 88-95.
[http://dx.doi.org/10.1016/0006-2952(61)90145-9] [PMID: 13726518]
[46]
Claiborne A. Catalase Activity. Handbook of methods for oxygen radical research. Boca Raton: CRC Press 1985; pp. 283-4.
[47]
Domingues I, Gravato C. Oxidative stress assessment in zebrafish larvae. Methods Mol Biol 2018; 1797: 477-86.
[http://dx.doi.org/10.1007/978-1-4939-7883-0_26] [PMID: 29896710]
[48]
Schneider MC, Min K, Hamrick PN, et al. Overview of snakebite in Brazil: Possible drivers and a tool for risk mapping. PLoS Negl Trop Dis 2021; 15(1): e0009044.
[http://dx.doi.org/10.1371/journal.pntd.0009044] [PMID: 33513145]
[49]
Silva FS, Ibiapina HNS, Neves JCF, et al. Severe tissue complications in patients of Bothrops snakebite at a tertiary health unit in the Brazilian Amazon: Clinical characteristics and associated factors. Rev Soc Bras Med Trop 2021; 54: e0374-2020.
[http://dx.doi.org/10.1590/0037-8682-0374-2020] [PMID: 33656146]
[50]
Paiva DDAMRD. Serpentes de interesse em saúde. Revista Científica Multidisciplinar Núcleo do Conhecimento 2020; 7(4): 144-70.
[http://dx.doi.org/10.32749/nucleodoconhecimento.com.br/biologia/interesse-em-saude]
[51]
Silva EO, Pardal PPO. Envenenamento por serpente Bothrops no município de Afuá, Ilha de Marajó, estado do Pará, Brasil. Rev Panamazonica Saude 2018; 9(3): 57-62.
[http://dx.doi.org/10.5123/S2176-62232018000300007]
[52]
Sousa L, Zdenek C, Dobson J, et al. Coagulotoxicity of Bothrops (lancehead pit-vipers) venoms from Brazil: Differential biochemistry and antivenom efficacy resulting from prey-driven venom variation. Toxins 2018; 10(10): 411.
[http://dx.doi.org/10.3390/toxins10100411] [PMID: 30314373]
[53]
Kini RM, Rao VS, Joseph JS. Procoagulant proteins from snake venoms. Haemostasis 2001; 31(3-6): 218-24.
[PMID: 11910188]
[54]
Kini R, Koh C. Metalloproteases affecting blood coagulation, fibrinolysis and platelet aggregation from snake venoms: Definition and nomenclature of interaction sites. Toxins 2016; 8(10): 284.
[http://dx.doi.org/10.3390/toxins8100284] [PMID: 27690102]
[55]
Carvalho BMA, Santos JDL, Xavier BM, et al. Snake venom PLA2s inhibitors isolated from Brazilian plants: Synthetic and natural molecules. BioMed Res Int 2013; 2013: 153045.
[http://dx.doi.org/10.1155/2013/153045] [PMID: 24171158]
[56]
Singh S, Dodt J, Volkers P, et al. Structure functional insights into calcium binding during the activation of coagulation factor XIII A. Sci Rep 2019; 9(1): 11324.
[http://dx.doi.org/10.1038/s41598-019-47815-z] [PMID: 31383913]
[57]
Barmore W, Bajwa T, Burns B. Biochemistry, Clotting Factors. StatPearls. Treasure Island, FL: StatPearls Publishing 2022. Available From: https://www.ncbi.nlm.nih.gov/books/NBK507850/
[58]
Metairon S, Zamboni CB, Suzuki MF, da Silva LFFL, Rizzutto MA. Inorganic elements in blood of mice immunized with snake venom using NAA and XRF techniques. J Radioanal Nucl Chem 2016; 309(1): 59-64.
[http://dx.doi.org/10.1007/s10967-016-4770-0]
[59]
Bortoleto RK, Murakami MT, Watanabe L, Soares AM, Arni RK. Purification, characterization and crystallization of Jararacussin-I, a fibrinogen-clotting enzyme isolated from the venom of Bothrops Jararacussu. Toxicon 2002; 40(9): 1307-12.
[http://dx.doi.org/10.1016/S0041-0101(02)00140-X] [PMID: 12220716]
[60]
Mazzi MV, Marcussi S, Carlos GB, et al. A new hemorrhagic metalloprotease from Bothrops Jararacussu snake venom: Isolation and biochemical characterization. Toxicon 2004; 44(2): 215-23.
[http://dx.doi.org/10.1016/j.toxicon.2004.06.002] [PMID: 15246772]
[61]
Sant’Ana CD, Bernardes CP, Izidoro LFM, et al. Molecular characterization of BjussuSP-I, a new thrombin-like enzyme with procoagulant and kallikrein-like activity isolated from Bothrops Jararacussu snake venom. Biochimie 2008; 90(3): 500-7.
[http://dx.doi.org/10.1016/j.biochi.2007.10.005] [PMID: 17996740]
[62]
Hamm J, Ceger P, Allen D, et al. Characterizing sources of variability in zebrafish embryo screening protocols. Altern Anim Exp 2019; 36(1): 103-20.
[http://dx.doi.org/10.14573/altex.1804162] [PMID: 30415271]
[63]
Ali MK, Saber SP, Taite DR, Emadi S, Irving R. The Protective Layer of Zebrafish Embryo Changes Continuously with Advancing Ages of Embryo Development (AGED). J Toxicol Pharmacol 2017; 1(2): e009.
[64]
Chen ZY, Li NJ, Cheng FY, et al. The effect of the chorion on size-dependent acute toxicity and underlying mechanisms of amine-modified silver nanoparticles in zebrafish embryos. Int J Mol Sci 2020; 21(8): 2864.
[http://dx.doi.org/10.3390/ijms21082864] [PMID: 32325940]
[65]
Alberto-Silva C, Portaro FCV, Kodama RT, et al. Novel neuroprotective peptides in the venom of the solitary scoliid wasp Scolia decorata ventralis. J Venom Anim Toxins Incl Trop Dis 2021; 27(27): e20200171.
[http://dx.doi.org/10.1590/1678-9199-jvatitd-2020-0171] [PMID: 34194483]
[66]
da Silva Caldeira CA, Diniz-Sousa R, Pimenta DC, et al. Antimicrobial peptidomes of Bothrops atrox and Bothrops Jararacussu snake venoms. Amino Acids 2021; 53(10): 1635-48.
[http://dx.doi.org/10.1007/s00726-021-03055-y] [PMID: 34482475]
[67]
Xu X, Li B, Zhu S, Rong R. Hypotensive peptides from snake venoms: Structure, function and mechanism. Curr Top Med Chem 2015; 15(7): 658-69.
[http://dx.doi.org/10.2174/1568026615666150217113835] [PMID: 25686732]
[68]
Sciani JM, Pimenta DC. The modular nature of bradykinin-potentiating peptides isolated from snake venoms. J Venom Anim Toxins Incl Trop Dis 2017; 23(1): 45.
[http://dx.doi.org/10.1186/s40409-017-0134-7] [PMID: 29090005]
[69]
Pinheiro-Júnior EL, Boldrini-França J, de Campos Araújo LMP, et al. LmrBPP9: A synthetic bradykinin-potentiating peptide from Lachesis muta rhombeata venom that inhibits the angiotensin-converting enzyme activity in vitro and reduces the blood pressure of hypertensive rats. Peptides 2018; 102: 1-7.
[http://dx.doi.org/10.1016/j.peptides.2018.01.015] [PMID: 29410030]
[70]
Legradi JB, Di Paolo C, Kraak MHS, et al. An ecotoxicological view on neurotoxicity assessment. Environ Sci Eur 2018; 30(1): 46.
[http://dx.doi.org/10.1186/s12302-018-0173-x] [PMID: 30595996]
[71]
Zindler F, Beedgen F, Brandt D, et al. Analysis of tail coiling activity of zebrafish (Danio rerio) embryos allows for the differentiation of neurotoxicants with different modes of action. Ecotoxicol Environ Saf 2019; 186: 109754.
[http://dx.doi.org/10.1016/j.ecoenv.2019.109754] [PMID: 31606639]
[72]
González-Fraga J, Dipp-Alvarez V, Bardullas U. Quantification of spontaneous tail movement in zebrafish embryos using a novel open-source MATLAB Application. Zebrafish 2019; 16(2): 214-6.
[http://dx.doi.org/10.1089/zeb.2018.1688] [PMID: 30615594]
[73]
Kiper KG, Freeman JL. Zebrafish as a tool to assess developmental neurotoxicity. Cell culture techniques neuromethods. New York: Humana Press Inc. 2019; Vol. 145: pp. 169-93.
[http://dx.doi.org/10.1007/978-1-4939-9228-7_9]
[74]
Knogler LD, Ryan J, Saint-Amant L, Drapeau P. A hybrid electrical/chemical circuit in the spinal cord generates a transient embryonic motor behavior. J Neurosci 2014; 34(29): 9644-55.
[http://dx.doi.org/10.1523/JNEUROSCI.1225-14.2014] [PMID: 25031404]
[75]
Ogino K, Hirata H. Defects of the glycinergic synapse in zebrafish. Front Mol Neurosci 2016; 9: 50.
[http://dx.doi.org/10.3389/fnmol.2016.00050] [PMID: 27445686]
[76]
de Oliveira A, Brigante T, Oliveira D. Tail coiling assay in zebrafish (Danio rerio) embryos: Stage of development, promising positive control candidates, and selection of an appropriate organic solvent for screening of developmental neurotoxicity (DNT). Water 2021; 13(2): 119.
[http://dx.doi.org/10.3390/w13020119]
[77]
Munawar A, Ali S, Akrem A, Betzel C. Snake venom peptides: Tools of biodiscovery. Toxins 2018; 10(11): 474.
[http://dx.doi.org/10.3390/toxins10110474] [PMID: 30441876]
[78]
Gierten J, Pylatiuk C, Hammouda OT, et al. Automated high-throughput heartbeat quantification in medaka and zebrafish embryos under physiological conditions. Sci Rep 2020; 10(1): 2046.
[http://dx.doi.org/10.1038/s41598-020-58563-w] [PMID: 32029752]
[79]
Sifuentes DN, El-Kik CZ, Ricardo HD, et al. Ability of suramin to antagonize the cardiotoxic and some enzymatic activities of Bothrops Jararacussu venom. Toxicon 2008; 51(1): 28-36.
[http://dx.doi.org/10.1016/j.toxicon.2007.07.002] [PMID: 18023464]
[80]
Ricardo HD, Martins VV, Monteiro-Machado M, et al. Ability of polyanions to antagonize the cardiotoxic effect of the Bothrops Jararacussu venom. Toxicon 2012; 60(2): 205-6.
[http://dx.doi.org/10.1016/j.toxicon.2012.04.216] [PMID: 22178782]
[81]
Eissa MA, Hashim YZHY, Mohd Nasir MH, et al. Fabrication and characterization of Agarwood extract-loaded nanocapsules and evaluation of their toxicity and anti-inflammatory activity on RAW 264.7 cells and in zebrafish embryos. Drug Deliv 2021; 28(1): 2618-33.
[http://dx.doi.org/10.1080/10717544.2021.2012307] [PMID: 34894947]
[82]
Dalzochio T, Rodrigues GZP, Petry IE, Gehlen G, da Silva LB. The use of biomarkers to assess the health of aquatic ecosystems in Brazil: A review. Int Aquatic Research 2016; 8(4): 283-98.
[http://dx.doi.org/10.1007/s40071-016-0147-9]
[83]
McHardy SF, Wang HYL, McCowen SV, Valdez MC. Recent advances in acetylcholinesterase Inhibitors and Reactivators: An update on the patent literature (2012-2015). Expert Opin Ther Pat 2017; 27(4): 455-76.
[84]
Koenig JA, Dao TL, Kan RK, Shih TM. Zebrafish as a model for acetylcholinesterase-inhibiting organophosphorus agent exposure and oxime reactivation. Ann N Y Acad Sci 2016; 1374(1): 68-77.
[http://dx.doi.org/10.1111/nyas.13051] [PMID: 27123828]
[85]
Massarsky A, Kozal JS, Di Giulio RT. Glutathione and zebrafish: Old assays to address a current issue. Chemosphere 2017; 168: 707-15.
[http://dx.doi.org/10.1016/j.chemosphere.2016.11.004] [PMID: 27836271]
[86]
Huang Y, Ma J, Meng Y, et al. Exposure to Oxadiazon-Butachlor causes cardiac toxicity in zebrafish embryos. Environ Pollut 2020; 265(Pt A): 114775.
[http://dx.doi.org/10.1016/j.envpol.2020.114775] [PMID: 32504889]
[87]
Singh RR, Reindl KM. Glutathione S-Transferases in Cancer. Antioxidants 2021; 10(5): 701.
[http://dx.doi.org/10.3390/antiox10050701] [PMID: 33946704]
[88]
Al-Asmari A, Anvarbatcha R, Al-Shahrani M, Islam M. Snake venom causes apoptosis by increasing the reactive oxygen species in colorectal and breast cancer cell lines. OncoTargets Ther 2016; 9: 6485-98.
[http://dx.doi.org/10.2147/OTT.S115055] [PMID: 27799796]
[89]
Tang H, Chen J, Nie L, Yao S, Kuang Y. Electrochemical oxidation of glutathione at well-aligned carbon nanotube array electrode. Electrochim Acta 2006; 51(15): 3046-51.
[http://dx.doi.org/10.1016/j.electacta.2005.08.038]
[90]
Machado ART, Aissa AF, Ribeiro DL, et al. Cytotoxic, genotoxic, and oxidative stress-inducing effect of an l-amino acid oxidase isolated from Bothrops Jararacussu venom in a co-culture model of HepG2 and HUVEC cells. Int J Biol Macromol 2019; 127: 425-32.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.01.059] [PMID: 30654040]
[91]
Abdelglil MI, Abdallah SO, El-Desouky MA, Alfaifi MY, Elbehairi SEI, Mohamed AF. Evaluation of the anticancer potential of crude, irradiated Cerastes cerastes snake venom and propolis ethanolic extract & related biological alterations. Molecules 2021; 26(22): 7057.
[http://dx.doi.org/10.3390/molecules26227057] [PMID: 34834153]
[92]
Toyama MH, Costa CRC, Belchor MN, et al. Evaluation of Thiol-dependent Enzymes on the Pharmacological Effects Induced by the Catalytically Active PLA2 from Bothrops Jararacussu. Preprints 2021; 2021050012.
[93]
Klein R, Nagy O, Tóthová C, Chovanová F. Clinical and diagnostic dignificance of Lactate Dehydrogenase and its isoenzymes in Animals. Vet Med Int 2020; 2020: 5346483.
[http://dx.doi.org/10.1155/2020/5346483] [PMID: 32607139]
[94]
Dar OI, Sharma S, Singh K, Sharma A, Bhardwaj R, Kaur A. Biomarkers for the toxicity of sublethal concentrations of triclosan to the early life stages of carps. Sci Rep 2020; 10(1): 17322.
[http://dx.doi.org/10.1038/s41598-020-73042-y] [PMID: 33057045]
[95]
Quintaneiro C, Patrício D, Novais SC, Soares AMVM, Monteiro MS. Endocrine and physiological effects of linuron and S-metolachlor in zebrafish developing embryos. Sci Total Environ 2017; 586: 390-400.
[http://dx.doi.org/10.1016/j.scitotenv.2016.11.153] [PMID: 28209406]
[96]
Young A, Oldford C, Mailloux RJ. Lactate dehydrogenase supports lactate oxidation in mitochondria isolated from different mouse tissues. Redox Biol 2020; 28: 101339.
[http://dx.doi.org/10.1016/j.redox.2019.101339] [PMID: 31610469]
[97]
Yu H, Yin Y, Yi Y, et al. Targeting lactate dehydrogenase A (LDHA) exerts antileukemic effects on Tcell acute lymphoblastic leukemia. Cancer Commun (Lond) 2020; 40(10): 501-17.
[http://dx.doi.org/10.1002/cac2.12080] [PMID: 32820611]
[98]
Silva LMG, Silva CAA, Silva A, et al. Photobiomodulation protects and promotes differentiation of C2C12 myoblast cells exposed to snake venom. PLoS One 2016; 11(4): e0152890.
[http://dx.doi.org/10.1371/journal.pone.0152890] [PMID: 27058357]
[99]
Aebi H. Catalase in vitro. Methods Enzymol 1984; 105: 121-6.
[http://dx.doi.org/10.1016/S0076-6879(84)05016-3] [PMID: 6727660]
[100]
Costal-Oliveira F, Stransky S, Guerra-Duarte C, et al. L-amino acid oxidase from Bothrops atrox snake venom triggers autophagy, apoptosis and necrosis in normal human keratinocytes. Sci Rep 2019; 9(1): 781.
[http://dx.doi.org/10.1038/s41598-018-37435-4] [PMID: 30692577]
[101]
Morás AM, Steffens L, Nordio BE, et al. Cytotoxic mechanism of Bothrops jararaca venom mediated by mitochondrial depolarization. Adv Toxicol Toxic Eff 2020; 4(1): 001-8.
[102]
Burin SM, Cacemiro MC, Cominal JG, et al. Bothrops moojeni L-amino acid oxidase induces apoptosis and epigenetic modulation on Bcr-Abl+ cells. J Venom Anim Toxins Incl Trop Dis 2020; 26: e20200123.
[http://dx.doi.org/10.1590/1678-9199-jvatitd-2020-0123] [PMID: 33354202]
[103]
de Ornellas Strapazzon J, Benedetti Parisotto E, Moratelli AM, et al. Systemic oxidative stress in victims of Bothrops snakebites. J Appl Biomed 2015; 13(2): 161-7.
[http://dx.doi.org/10.1016/j.jab.2014.11.002]
[104]
Agostinetto D, Tarouco CP, Nohatto MA, Oliveira C, Fraga DS. Metabolic activity of wheat and ryegrass plants in competition. Planta Daninha 2017; 35(0): e017155463.
[http://dx.doi.org/10.1590/s0100-83582017350100044]
[105]
Hiu JJ, Yap MKK. Cytotoxicity of snake venom enzymatic toxins: Phospholipase A2 and l -amino acid oxidase. Biochem Soc Trans 2020; 48(2): 719-31.
[http://dx.doi.org/10.1042/BST20200110] [PMID: 32267491]
[106]
Teixeira C, Fernandes CM, Leiguez E, Chudzinski-Tavassi AM. Inflammation induced by platelet-activating viperid snake venoms: Perspectives on thromboinflammation. Front Immunol 2019; 10: 2082.
[http://dx.doi.org/10.3389/fimmu.2019.02082] [PMID: 31572356]
[107]
Moreira V, Leiguez E, Janovits PM, Maia-Marques R, Fernandes CM, Teixeira C. Inflammatory Effects of Bothrops Phospholipases A2: Mechanisms involved in biosynthesis of lipid mediators and lipid accumulation. Toxins 2021; 13(12): 868.
[http://dx.doi.org/10.3390/toxins13120868] [PMID: 34941706]
[108]
Carone SEI, Costa TR, Burin SM, et al. A new l-amino acid oxidase from Bothrops Jararacussu snake venom: Isolation, partial characterization, and assessment of pro-apoptotic and antiprotozoal activities. Int J Biol Macromol 2017; 103: 25-35.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.05.025] [PMID: 28495622]

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