Preclinical Immuno-recognition and Neutralization of Lethality Assessment of a New Polyvalent Antivenom, VINS Snake Venom Antiserum – African IHS®, against Envenomation of Ten African Viperid and Elapid Snakes
Journal of Scientific Research and Reports,
Page 25-43
DOI:
10.9734/jsrr/2021/v27i1130456
Abstract
Snakebite envenomation is a major health concern in developing countries causing significant mortality and morbidity. With over 1.2 million cases annually caused by medically important snake species belonging to the two families Viperidae (Echis spp. and Bitis spp.) and Elapidae (Naja spp. and Dendroaspis spp.). Several antivenoms are being produced and distributed to western sub-Saharan Africa for treatment of envenomation with the absence of preclinical efficacy studies. The present study evaluated the preclinical efficacy of venoms from Echis leucogaster, Echis ocellatus, Bitis arietans, Bitis gabonica, Naja haje, Naja melanoleuca, Naja nigricollis, Dendroaspis jamesoni, Dendroaspis polylepis and Dendroaspis viridis against a polyvalent Snake Venom Antiserum - African IHS (lyophilised), manufactured by VINS Bioproducts Limited (Telangana, India). Our in vitro results showed that, the SVA- AIHS contains antibodies that are capable of recognizing and binding majority of protein components representative of all eight major protein families of venoms of the snake species tested by double immunodiffusion assay and confirmed by western blot. The venom antiserum exhibited high neutralization efficacy against all the viperid and elapid snake species venoms in in vivo studies and confirmed the manufacturer’s recommended neutralization capacity. This is clear evidence that the VINS polyvalent SVA-AIHS batch tested has strong neutralizing capacity and will be useful in treating envenoming by most African viperid and some elapid snake species.
Keywords:
- Snake venoms
- venom antiserum
- neutralization
- elapids
- viperids
- protein profile
How to Cite
Georgina I., D., Samuel, N., Mark, T.-T., Frances M., M., Samuel, A., Emmanuel A., B., Abraham K., A., & Irene, A. (2021). Preclinical Immuno-recognition and Neutralization of Lethality Assessment of a New Polyvalent Antivenom, VINS Snake Venom Antiserum – African IHS®, against Envenomation of Ten African Viperid and Elapid Snakes. Journal of Scientific Research and Reports, 27(11), 25-43. https://doi.org/10.9734/jsrr/2021/v27i1130456
References
DOI:https://doi.org/10.1038/nrdp.2017.63.1
Musah Y, Ameade EPK, Attuquayefio DK, Holbech LH. Epidemiology, ecology and human perceptions of snakebites in a savanna community of northern Ghana. PLoS Neglected Tropical Diseases. 2019;13:e0007221. DOI:https://doi.org/10.1371/journal.pntd.0007221
Williams DJ, Faiz MA, Abela-Ridder B, Ainsworth S, Bulfone TC, Nickerson AD, et al. Strategy for a globally coordinated response to a priority neglected tropical disease: Snakebite envenoming. PLoS Neglected Tropical Diseases. 2019;13. DOI:https://doi.org/10.1371/journal.pntd.0007059.
Chippaux JP. Estimate of the burden of snakebites in sub-Saharan Africa: A meta-analytic approach. Toxicon. 2011;57:586–99. DOI:https://doi.org/10.1016/j.toxicon.2010.12.022
Harrison RA, Hargreaves A, Wagstaff SC, Faragher B, Lalloo DG. Snake envenoming: A disease of poverty. PLoS Neglected Tropical Diseases. 2009;3. DOI:https://doi.org/10.1371/journal.pntd.0000569.
Alirol E, Sharma SK, Bawaskar HS, Kuch U, Chappuis F. Snake bite in south asia: A review. PLoS Neglected Tropical Diseases. 2010;4:e603.
DOI:https://doi.org/10.1371/journal.pntd.0000603.
Gutiérrez JM, Warrell DA, Williams DJ, Jensen S, Brown N, Calvete JJ, et al. The Need for Full Integration of Snakebite Envenoming within a Global Strategy to Combat the Neglected Tropical Diseases: The Way Forward. PLoS Neglected Tropical Diseases. 2013;7:e2162. DOI:https://doi.org/10.1371/journal.pntd.0002162.
Ferraz CR, Arrahman A, Xie C, Casewell NR, Lewis RJ, Kool J, et al. Multifunctional toxins in snake venoms and therapeutic implications: From pain to hemorrhage and necrosis. Frontiers in Ecology and Evolution. 2019;7:1–19.
DOI:https://doi.org/10.3389/fevo.2019.00218.
Slagboom J, Kool J, Harrison RA, Casewell NR. Haemotoxic snake venoms: their functional activity, impact on snakebite victims and pharmaceutical promise. British Journal of Haematology. 2017;177:947–59. DOI:https://doi.org/10.1111/bjh.14591.
Habib AG. Public health aspects of snakebite care in West Africa: Perspectives from Nigeria. Journal of Venomous Animals and Toxins Including Tropical Diseases. 2013;19:1. DOI:https://doi.org/10.1186/1678-9199-19-27.
Osipov A V., Utkin YN. Snake Venom Toxins Targeted at the Nervous System. Snake Venoms, Springer Netherlands; 2015; 1–21.
DOI:https://doi.org/10.1007/978-94-007-6648-8_23-1.
Méndez I, Gutiérrez JM, Angulo Y, Calvete JJ, Lomonte B. Comparative study of the cytolytic activity of snake venoms from African spitting cobras (Naja spp., Elapidae) and its neutralization by a polyspecific antivenom. Toxicon. 2011;58:558–64. DOI:https://doi.org/10.1016/j.toxicon.2011.08.018.
Bougis PE, Marchot P, Rochat H. Characterization of Elapidae Snake Venom Components Using Optimized Reverse-Phase High-Performance Liquid Chromatographic Conditions and Screening Assays for α-Neurotoxin and Phospholipase A2 Activities. Biochemistry. 1986;25:7235–43. DOI:https://doi.org/10.1021/bi00370a070.
Chippaux J-P. Snakebite in Africa. Handbook of Venoms and Toxins of Reptiles, CRC Press. 2009;453–73. DOI:https://doi.org/10.1201/9781420008661.ch22.
Kularatne SAM, Senanayake N. Venomous snake bites, scorpions, and spiders. 1st ed. Elsevier B.V. 2014;120.
DOI:https://doi.org/10.1016/B978-0-7020-4087-0.00066-8.
Marsh N. Snake Venoms and Envenomations. By Jean‐Philippe Chippaux; translated by , F W Huchzermeyer. Malabar (Florida): Krieger Publishing. $58.50. xii + 287 p; ill.; index. ISBN: 1‐57524‐272‐9. [Originally published in French as Venins de Serpent et Enveninmati. The Quarterly Review of Biology 2007;82:61–61.
DOI:https://doi.org/10.1086/513371.
El-Aziz TMA, Soares AG, Stockand JD. Snake venoms in drug discovery: Valuable therapeutic tools for life saving. Toxins 2019;11. DOI:https://doi.org/10.3390/toxins11100564.
Vineetha MS, Bhavya J, More SS. Inhibition of pharmacological and toxic effects of echis carinatus venom by tabernaemontana alternifolia root extract. Indian Journal of Natural Products and Resources. 2019;10:48–58.
Guidolin FR, Caricati CP, Marcelino JR, da Silva WD. Development of equine IgG antivenoms against major snake groups in mozambique. PLoS Neglected Tropical Diseases. 2016;10:1–17.
DOI:https://doi.org/10.1371/journal.pntd.0004325.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 1976;72:248–54.
DOI:https://doi.org/10.1016/0003-2697(76)90527-3.
Ouchterlony OT. Immunochemistry. vol. 15. Pergamon Press; 1978.
He F. Laemmli SDS PAGE Fanglian He Carnegie Institution at Stanford. Bio-ProtocolOrg. 2011;1:3–6.
Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America. 1979;76:4350–4. DOI:https://doi.org/10.1073/pnas.76.9.4350.
National Institute of Health N. Guide for Grants and Contracts. vol. 14. No.8. Special Ed. Laboratory Animal Welfare; 1985.
Institute of Laboratory Animal Resource (US) Committee on care use of laboratory A. Guide for the care and use of laboratory animals. US: US Department of Health and Human services, Public Health Service, National Institute of Health; 1986.
Act AW. Public Law 89-544 Act. 89th Congr; 1966.
DOI:https://www.nal.usda.gov/awic/animal-welfare-act-public-law-89-544-act-august-24-1966 (accessed October 6, 2021).
World Health Organisation. WHO guidelines for the Production, Control and Regulation of Snake Antivenom Immunoglobulins. 2016:17–21.
Sanhajariya S, Duffull SB, Isbister GK. Pharmacokinetics of snake venom. Toxins. 2018;10. DOI:https://doi.org/10.3390/toxins10020073
Malih I, Ahmad rusmili MR, Tee TY, Saile R, Ghalim N, Othman I. Proteomic analysis of moroccan cobra naja haje legionis venom using tandem mass spectrometry. Journal of Proteomics. 2014;96:240–52. DOI:https://doi.org/10.1016/j.jprot.2013.11.012
Lauridsen LP, Laustsen AH, Lomonte B, Gutiérrez JM. Exploring the venom of the forest cobra snake: Toxicovenomics and antivenom profiling of Naja melanoleuca. Journal of Proteomics. 2017;150:98–108. DOI:https://doi.org/10.1016/j.jprot.2016.08.024.
Petras D, Sanz L, Segura Á, Herrera M, Villalta M, Solano D, et al. Snake venomics of African spitting cobras: Toxin composition and assessment of congeneric cross-reactivity of the Pan-African EchiTAb-Plus-ICP antivenom by antivenomics and neutralization approaches. Journal of Proteome Research. 2011;10:1266–80.
DOI:https://doi.org/10.1021/pr101040f.
Laustsen AH, Lomonte B, Lohse B, Fernández J, Gutiérrez JM. Unveiling the nature of black mamba (Dendroaspis polylepis) venom through venomics and antivenom immunoprofiling: Identification of key toxin targets for antivenom development. Journal of Proteomics. 2015;119:126–42. DOI:https://doi.org/10.1016/j.jprot.2015.02.002.
Williams HF, Layfield HJ, Vallance T, Patel K, Bicknell AB, Trim SA, et al. The urgent need to develop novel strategies for the diagnosis and treatment of snakebites. Toxins. 2019;11:1–29.
DOI:https://doi.org/10.3390/toxins11060363.
Ainsworth S, Petras D, Engmark M, Süssmuth RD, Whiteley G, Albulescu LO, et al. The medical threat of mamba envenoming in sub-Saharan Africa revealed by genus-wide analysis of venom composition, toxicity and antivenomics profiling of available antivenoms. Journal of Proteomics. 2018;172:173–89. DOI:https://doi.org/10.1016/j.jprot.2017.08.016.
Calvete JJ, Escolano J, Sanz L. Snake venomics of Bitis species reveals large intragenus venom toxin composition variation: Application to taxonomy of congeneric taxa. Journal of Proteome Research. 2007;6:2732–45.
DOI:https://doi.org/10.1021/pr0701714.
Casewell NR, Harrison RA, Wüster W, Wagstaff SC. Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genomics. 2009;10:1–12. DOI:https://doi.org/10.1186/1471-2164-10-564.
Calvete JJ. Proteomic tools against the neglected pathology of snake bite envenoming. Expert Review of Proteomics. 2011;8:739–58. DOI:https://doi.org/10.1586/epr.11.61.
Toyama MH, Soares AM, Wen-Hwa L, Polikarpov I, Giglio JR, Marangoni S. Amino acid sequence of piratoxin-II, a myotoxic Lys49 phospholipase A2 homologue from Bothrops pirajai venom. Biochimie. 2000;82:245–50.
DOI:https://doi.org/10.1016/S0300-9084(00)00202-9.
Huang MZ, Gopalakrishnakone P, Chung MCM, Kini RM. Complete amino acid sequence of an acidic, cardiotoxic phospholipase A2 from the venom of Ophiophagus hannah (King cobra): A novel cobra venom enzyme with “pancreatic loop.” Archives of Biochemistry and Biophysics. 1997;338:150–6.
DOI:https://doi.org/10.1006/abbi.1996.9814.
Arni RK, Ward RJ. Phospholipase A2 - A structural review. Toxicon. 1996;34:827–41. DOI:https://doi.org/10.1016/0041-0101(96)00036-0.
Tasoulis T, Isbister GK. A review and database of snake venom proteomes. Toxins. 2017;9.
DOI:https://doi.org/10.3390/toxins9090290.
Bjarnason JB, Fox JW. Hemorrhagic metalloproteinases from snake venoms. Pharmacology and Therapeutics. 1994; 62:325–72. DOI:https://doi.org/10.1016/0163-7258(94)90049-3.
Tosin O, Karina P, Selistre-de-araujo HS, Helena D, Souza F De. Toxicon : X snake venom metalloproteinases ( SVMPs ): A structure-function update. Toxicon: X. 2020;7:100052. DOI:https://doi.org/10.1016/j.toxcx.2020.100052
Gutiérrez JM, Vargas M, Segura Á, Herrera M, Villalta M, Solano G, et al. In Vitro tests for assessing the neutralizing ability of snake antivenoms: Toward the 3Rs principles. Frontiers in Immunology 2021;11:1–13. DOI:https://doi.org/10.3389/fimmu.2020.617429
Takeda S, Takeya H, Iwanaga S. Snake venom metalloproteinases: Structure, function and relevance to the mammalian ADAM/ADAMTS family proteins. Biochimica et Biophysica Acta - Proteins and Proteomics. 2012;1824:164–76.
DOI:https://doi.org/10.1016/j.bbapap.2011.04.009.
Gutiérrez JM, Rucavado A. Snake venom metalloproteinases: Their role in the pathogenesis of local tissue damage. Biochimie. 2000;82:841–50.
DOI:https://doi.org/10.1016/S0300-9084(00)01163-9.
Serrano SMT, Maroun RC. Snake venom serine proteinases: Sequence homology vs. substrate specificity, a paradox to be solved. Toxicon. 2005;45:1115–32. DOI:https://doi.org/10.1016/j.toxicon.2005.02.020.
Roldan-Padron O, Castro-Guillen JL, Garcia-Arredondo JA, Cruz-Perez SM, Diaz-Pena LF, Saldaña C, et al. Snake venom hemotoxic enzymes : Biochemical Comparison between Crotalus Species from. Molecules. 2019;24:1–16.
DOI:https://doi.org/10.3390/molecules24081489.
Du XY, Clemetson KJ. Snake venom L-amino acid oxidases. Toxicon. 2002; 40:659–65. DOI:https://doi.org/10.1016/S0041-0101(02)00102-2
Tan KK, Bay BH, Gopalakrishnakone P. L-amino acid oxidase from snake venom and its anticancer potential. Toxicon. 2018;144:7–13. DOI:https://doi.org/10.1016/j.toxicon.2018.01.015.
Guo C, Liu S, Yao Y, Zhang Q, Sun MZ. Past decade study of snake venom l-amino acid oxidase. Toxicon. 2012;60:302–11. DOI:https://doi.org/10.1016/j.toxicon.2012.05.001.
Mackessy S. Section I. Reptile Toxinology, Systematics, and Venom Gland Structure. Structure 2010:1–13.
Iwanaga S, Susuki T. Enzymes in Snake Venoms. Venomous Animals and their Venoms, Springer, Berlin, Heidelberg; 1979;62–157. DOI:https://doi.org/10.1016/b978-1-4832-2949-2.50015-1.
Aird SD. Ophidian envenomation strategies and the role of purines. Toxicon. 2002;40:335–93. DOI:https://doi.org/10.1016/S0041-0101(01)00232-X.
Kang TS, Georgieva D, Genov N, Murakami MT, Sinha M, Kumar RP, et al. Enzymatic toxins from snake venom: Structural characterization and mechanism of catalysis. FEBS Journal. 2011; 278:4544–76. DOI:https://doi.org/10.1111/j.1742-4658.2011.08115.x.
Frobert Y, Créminon C, Cousin X, Rémy MH, Chatel JM, Bon S, et al. Acetylcholinesterases from Elapidae snake venoms: Biochemical, immunological and enzymatic characterization. Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology. 1997;1339:253–67.
DOI:https://doi.org/10.1016/S0167-4838(97)00009-5.
Fox JW. A brief review of the scientific history of several lesser-known snake venom proteins: L-amino acid oxidases, hyaluronidases and phosphodiesterases. Toxicon. 2013;62:75–82.
DOI:https://doi.org/10.1016/j.toxicon.2012.09.009.
Kini RM, Doley R. Structure, function and evolution of three-finger toxins: Mini proteins with multiple targets. Toxicon 2010;56:855–67. DOI:https://doi.org/10.1016/j.toxicon.2010.07.010.
Mukherjee AK, Mackessy SP, Dutta S. International Journal of Biological Macromolecules Characterization of a Kunitz-type protease inhibitor peptide ( Rusvikunin ) purified from Daboia russelii russelii venom. International Journal of Biological Macromolecules. 2014;67:154–62. DOI:https://doi.org/10.1016/j.ijbiomac.2014.02.058.
Willmott N, Gaffney P, Masci P, Whitaker A. A novel serine protease inhibitor from the Australian brown snake, Pseudonaja textilis textilis: Inhibition kinetics. Fibrinolysis and Proteolysis. 1995;9: 1–8.
DOI:https://doi.org/10.1016/S0268-9499(08)80040-9.
Yamazaki Y, Morita T. Structure and function of snake venom cysteine-rich secretory proteins. Toxicon. 2004;44:227–31. DOI:https://doi.org/10.1016/j.toxicon.2004.05.023.
Morita T. Structures and functions of snake venom CLPs (C-type lectin-like proteins) with anticoagulant-, procoagulant-, and platelet-modulating activities. Toxicon. 2005;45:1099–114. DOI:https://doi.org/10.1016/j.toxicon.2005.02.021.
Ogawa T, Chijiwa T, Oda-Ueda N, Ohno M. Molecular diversity and accelerated evolution of C-type lectin-like proteins from snake venom. Toxicon. 2005;45:1–14. DOI:https://doi.org/10.1016/j.toxicon.2004.07.028.
Kamiguti AS, Zuzel M, Theakston RDG. Snake venom metalloproteinases and disintegrins: Interactions with cells. Brazilian Journal of Medical and Biological Research. 1998;31:853–62.
DOI:https://doi.org/10.1590/S0100-879X1998000700001.
St Pierre L, Flight S, Masci PP, Hanchard KJ, Lewis RJ, Alewood PF, et al. Cloning and characterisation of natriuretic peptides from the venom glands of Australian elapids. Biochimie. 2006;88:1923–31. DOI:https://doi.org/10.1016/j.biochi.2006.06.014
Zhang Y, Wu J, Yu G, Chen Z, Zhou X, Zhu S, et al. Toxicon A novel natriuretic peptide from the cobra venom. Toxicon. 2011;57:134–40. DOI:https://doi.org/10.1016/j.toxicon.2010.10.014.
Levin ER, Gardner DG, Samson WK. Natriuretic Peprides. The New England Journal of Medicine. 1998;339:321–8. DOI:https://doi.org/10.1300/J123v27n02_05.
Zhao Y, Wu J, Wang X, Jia H, Chen DN, Li J Da. Prokineticins and their G protein-coupled receptors in health and disease. 1st ed. Elsevier Inc.; 2019;161. DOI:https://doi.org/10.1016/bs.pmbts.2018.09.006.
Fry BG. From genome to “venome”: Molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Research. 2005;15:403–20.
DOI:https://doi.org/10.1101/gr.3228405.
Yamazaki Y, Matsunaga Y, Tokunaga Y, Obayashi S, Saito M, Morita T. Snake venom vascular endothelial growth factors (VEGF-Fs) exclusively vary their structures and functions among species. Journal of Biological Chemistry. 2009;284:9885–91. DOI:https://doi.org/10.1074/jbc.M809071200.
Chippaux JP, Goyffon M. Venoms, antivenoms and immunotherapy. Toxicon. 1998;36:823–46. DOI:https://doi.org/10.1016/S0041-0101(97)00160-8.
Katali O, Shipingana L, Nyarangó P, Pääkkönen M, Haindongo E, Rennie T, et al. Protein identification of venoms of the African spitting cobras, Naja mossambica and Naja nigricincta nigricincta. Toxins. 2020;12. DOI:https://doi.org/10.3390/toxins12080520.
Chotwiwatthanakun C, Pratanaphon R, Akesowan S, Sriprapat S, Ratanabanangkoon K. Production of potent polyvalent antivenom against three elapid venoms using a low dose, low volume, multi-site immunization protocol. Toxicon. 2001;39:1487–94.
DOI:https://doi.org/10.1016/S0041-0101(01)00108-8.
Potet J, Smith J, McIver L. Reviewing evidence of the clinical effectiveness of commercially available antivenoms in sub-saharan africa identifies the need for a multi-centre, multi-antivenom clinical trial. PLoS Neglected Tropical Diseases. 2019;13:1–17. DOI:https://doi.org/10.1371/journal.pntd.0007551
Wong KY, Tan KY, Tan NH, Tan CH. A Neurotoxic Snake Venom without Phospholipase A2: Proteomics and Cross-Neutralization of the Venom from Senegalese Cobra, Naja senegalensis (Subgenus: Uraeus). Toxins. 2021;13. DOI:https://doi.org/10.3390/toxins13010060.
Williams CA, Chase MW. Precipitation analysis by diffusion in gels. Methods in immunology and immunochemistry, vol. 3, Academic Press New York. 1971;103–374.
DOI:https://doi.org/10.1016/b978-0-12-754403-8.50008-3.
Oudin J. [9] Immunochemical Analysis by Antigen-Antibody Precipitation in Gels. Methods in Enzymology. Academic Press, Inc., New York. 1980;70:166–98. DOI:https://doi.org/10.1016/S0076-6879(80)70048-4.
Bailey GS. Ouchterlony double immunodiffusion. Humana Press Inc., Totowa, NJ; 1996. DOI:https://doi.org/10.1007/978-1-60327-259-9_135.
Calvete JJ, Arias AS, Rodríguez Y, Quesada-Bernat S, Sánchez L V., Chippaux JP, et al. Preclinical evaluation of three polyspecific antivenoms against the venom of Echis ocellatus: Neutralization of toxic activities and antivenomics. Toxicon. 2016;119:280–8. DOI:https://doi.org/10.1016/j.toxicon.2016.06.022.
Pla D, Sanz L, Quesada-Bernat S, Villalta M, Baal J, Chowdhury MAW, et al. Phylovenomics of Daboia russelii across the Indian subcontinent. Bioactivities and comparative in vivo neutralization and in vitro third-generation antivenomics of antivenoms against venoms from India, Bangladesh and Sri Lanka. Journal of Proteomics. 2019;207:103443.
DOI:https://doi.org/10.1016/j.jprot.2019.103443.
Casewell NR, Cook DAN, Wagstaff SC, Nasidi A, Durfa N, Wüster W, et al. Pre-clinical assays predict Pan-African Echis viper efficacy for a species-specific antivenom. PLoS Neglected Tropical Diseases. 2010;4.
DOI:https://doi.org/10.1371/journal.pntd.0000851.
Paixão-Cavalcante D, Kuniyoshi AK, Portaro FCV, da Silva WD, Tambourgi D V. African adders: Partial characterization of snake venoms from three bitis species of medical importance and their neutralization by experimental equine antivenoms. PLoS Neglected Tropical Diseases. 2015;9:1–18.
DOI:https://doi.org/10.1371/journal.pntd.0003419.
Andrejccaronáková Z, Petrilla V, Tomečková V, Tóth Š, Pekárová T, Komanický V, et al. New approaches in monitoring venom of genus Dendroaspis. Spectroscopy Letters. 2015;48:462–72. DOI:https://doi.org/10.1080/00387010.2014.906471.
Currier R. Investigating venom synthesis: exploring the composition, variation and gene expression dynamics of Bitis arietans venom. PhD Thesis, LSTM 2012.
Casewell NR, Jackson TNW, Laustsen AH, Sunaga K. Europe PMC Funders Group Causes and Consequences of Snake Venom Variation. 2020;41:570–81.
DOI:https://doi.org/10.1016/j.tips.2020.05.006.Causes.
Giorgianni MW, Dowell NL, Griffin S, Kassner VA, Selegue JE. The origin and diversification of a novel protein family in venomous snakes. 2020;117.
DOI:https://doi.org/10.1073/pnas.1920011117.
Post Y, Puschhof J, Beumer J, Richardson MK, Casewell NR, Clevers H. Article Snake Venom Gland Organoids. Cell. 2020;180:233-247.e21. DOI:https://doi.org/10.1016/j.cell.2019.11.038.
Tanaka GD, Furtado MDFD, Portaro FCV, Sant’Anna OA, Tambourgi D v. Diversity of Micrurus snake species related to their venom toxic effects and the prospective of antivenom neutralization. PLoS Neglected Tropical Diseases. 2010;4:1–12.
DOI:https://doi.org/10.1371/journal.pntd.0000622.
Tanaka GD, Pidde-Queiroz G, Furtado M de FD, van den Berg C, Tambourgi D V. Micrurus snake venoms activate human complement system and generate anaphylatoxins. BMC Immunology. 2012;13.
DOI:https://doi.org/10.1186/1471-2172-13-4.
Musah Y, Ameade EPK, Attuquayefio DK, Holbech LH. Epidemiology, ecology and human perceptions of snakebites in a savanna community of northern Ghana. PLoS Neglected Tropical Diseases. 2019;13:e0007221. DOI:https://doi.org/10.1371/journal.pntd.0007221
Williams DJ, Faiz MA, Abela-Ridder B, Ainsworth S, Bulfone TC, Nickerson AD, et al. Strategy for a globally coordinated response to a priority neglected tropical disease: Snakebite envenoming. PLoS Neglected Tropical Diseases. 2019;13. DOI:https://doi.org/10.1371/journal.pntd.0007059.
Chippaux JP. Estimate of the burden of snakebites in sub-Saharan Africa: A meta-analytic approach. Toxicon. 2011;57:586–99. DOI:https://doi.org/10.1016/j.toxicon.2010.12.022
Harrison RA, Hargreaves A, Wagstaff SC, Faragher B, Lalloo DG. Snake envenoming: A disease of poverty. PLoS Neglected Tropical Diseases. 2009;3. DOI:https://doi.org/10.1371/journal.pntd.0000569.
Alirol E, Sharma SK, Bawaskar HS, Kuch U, Chappuis F. Snake bite in south asia: A review. PLoS Neglected Tropical Diseases. 2010;4:e603.
DOI:https://doi.org/10.1371/journal.pntd.0000603.
Gutiérrez JM, Warrell DA, Williams DJ, Jensen S, Brown N, Calvete JJ, et al. The Need for Full Integration of Snakebite Envenoming within a Global Strategy to Combat the Neglected Tropical Diseases: The Way Forward. PLoS Neglected Tropical Diseases. 2013;7:e2162. DOI:https://doi.org/10.1371/journal.pntd.0002162.
Ferraz CR, Arrahman A, Xie C, Casewell NR, Lewis RJ, Kool J, et al. Multifunctional toxins in snake venoms and therapeutic implications: From pain to hemorrhage and necrosis. Frontiers in Ecology and Evolution. 2019;7:1–19.
DOI:https://doi.org/10.3389/fevo.2019.00218.
Slagboom J, Kool J, Harrison RA, Casewell NR. Haemotoxic snake venoms: their functional activity, impact on snakebite victims and pharmaceutical promise. British Journal of Haematology. 2017;177:947–59. DOI:https://doi.org/10.1111/bjh.14591.
Habib AG. Public health aspects of snakebite care in West Africa: Perspectives from Nigeria. Journal of Venomous Animals and Toxins Including Tropical Diseases. 2013;19:1. DOI:https://doi.org/10.1186/1678-9199-19-27.
Osipov A V., Utkin YN. Snake Venom Toxins Targeted at the Nervous System. Snake Venoms, Springer Netherlands; 2015; 1–21.
DOI:https://doi.org/10.1007/978-94-007-6648-8_23-1.
Méndez I, Gutiérrez JM, Angulo Y, Calvete JJ, Lomonte B. Comparative study of the cytolytic activity of snake venoms from African spitting cobras (Naja spp., Elapidae) and its neutralization by a polyspecific antivenom. Toxicon. 2011;58:558–64. DOI:https://doi.org/10.1016/j.toxicon.2011.08.018.
Bougis PE, Marchot P, Rochat H. Characterization of Elapidae Snake Venom Components Using Optimized Reverse-Phase High-Performance Liquid Chromatographic Conditions and Screening Assays for α-Neurotoxin and Phospholipase A2 Activities. Biochemistry. 1986;25:7235–43. DOI:https://doi.org/10.1021/bi00370a070.
Chippaux J-P. Snakebite in Africa. Handbook of Venoms and Toxins of Reptiles, CRC Press. 2009;453–73. DOI:https://doi.org/10.1201/9781420008661.ch22.
Kularatne SAM, Senanayake N. Venomous snake bites, scorpions, and spiders. 1st ed. Elsevier B.V. 2014;120.
DOI:https://doi.org/10.1016/B978-0-7020-4087-0.00066-8.
Marsh N. Snake Venoms and Envenomations. By Jean‐Philippe Chippaux; translated by , F W Huchzermeyer. Malabar (Florida): Krieger Publishing. $58.50. xii + 287 p; ill.; index. ISBN: 1‐57524‐272‐9. [Originally published in French as Venins de Serpent et Enveninmati. The Quarterly Review of Biology 2007;82:61–61.
DOI:https://doi.org/10.1086/513371.
El-Aziz TMA, Soares AG, Stockand JD. Snake venoms in drug discovery: Valuable therapeutic tools for life saving. Toxins 2019;11. DOI:https://doi.org/10.3390/toxins11100564.
Vineetha MS, Bhavya J, More SS. Inhibition of pharmacological and toxic effects of echis carinatus venom by tabernaemontana alternifolia root extract. Indian Journal of Natural Products and Resources. 2019;10:48–58.
Guidolin FR, Caricati CP, Marcelino JR, da Silva WD. Development of equine IgG antivenoms against major snake groups in mozambique. PLoS Neglected Tropical Diseases. 2016;10:1–17.
DOI:https://doi.org/10.1371/journal.pntd.0004325.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 1976;72:248–54.
DOI:https://doi.org/10.1016/0003-2697(76)90527-3.
Ouchterlony OT. Immunochemistry. vol. 15. Pergamon Press; 1978.
He F. Laemmli SDS PAGE Fanglian He Carnegie Institution at Stanford. Bio-ProtocolOrg. 2011;1:3–6.
Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America. 1979;76:4350–4. DOI:https://doi.org/10.1073/pnas.76.9.4350.
National Institute of Health N. Guide for Grants and Contracts. vol. 14. No.8. Special Ed. Laboratory Animal Welfare; 1985.
Institute of Laboratory Animal Resource (US) Committee on care use of laboratory A. Guide for the care and use of laboratory animals. US: US Department of Health and Human services, Public Health Service, National Institute of Health; 1986.
Act AW. Public Law 89-544 Act. 89th Congr; 1966.
DOI:https://www.nal.usda.gov/awic/animal-welfare-act-public-law-89-544-act-august-24-1966 (accessed October 6, 2021).
World Health Organisation. WHO guidelines for the Production, Control and Regulation of Snake Antivenom Immunoglobulins. 2016:17–21.
Sanhajariya S, Duffull SB, Isbister GK. Pharmacokinetics of snake venom. Toxins. 2018;10. DOI:https://doi.org/10.3390/toxins10020073
Malih I, Ahmad rusmili MR, Tee TY, Saile R, Ghalim N, Othman I. Proteomic analysis of moroccan cobra naja haje legionis venom using tandem mass spectrometry. Journal of Proteomics. 2014;96:240–52. DOI:https://doi.org/10.1016/j.jprot.2013.11.012
Lauridsen LP, Laustsen AH, Lomonte B, Gutiérrez JM. Exploring the venom of the forest cobra snake: Toxicovenomics and antivenom profiling of Naja melanoleuca. Journal of Proteomics. 2017;150:98–108. DOI:https://doi.org/10.1016/j.jprot.2016.08.024.
Petras D, Sanz L, Segura Á, Herrera M, Villalta M, Solano D, et al. Snake venomics of African spitting cobras: Toxin composition and assessment of congeneric cross-reactivity of the Pan-African EchiTAb-Plus-ICP antivenom by antivenomics and neutralization approaches. Journal of Proteome Research. 2011;10:1266–80.
DOI:https://doi.org/10.1021/pr101040f.
Laustsen AH, Lomonte B, Lohse B, Fernández J, Gutiérrez JM. Unveiling the nature of black mamba (Dendroaspis polylepis) venom through venomics and antivenom immunoprofiling: Identification of key toxin targets for antivenom development. Journal of Proteomics. 2015;119:126–42. DOI:https://doi.org/10.1016/j.jprot.2015.02.002.
Williams HF, Layfield HJ, Vallance T, Patel K, Bicknell AB, Trim SA, et al. The urgent need to develop novel strategies for the diagnosis and treatment of snakebites. Toxins. 2019;11:1–29.
DOI:https://doi.org/10.3390/toxins11060363.
Ainsworth S, Petras D, Engmark M, Süssmuth RD, Whiteley G, Albulescu LO, et al. The medical threat of mamba envenoming in sub-Saharan Africa revealed by genus-wide analysis of venom composition, toxicity and antivenomics profiling of available antivenoms. Journal of Proteomics. 2018;172:173–89. DOI:https://doi.org/10.1016/j.jprot.2017.08.016.
Calvete JJ, Escolano J, Sanz L. Snake venomics of Bitis species reveals large intragenus venom toxin composition variation: Application to taxonomy of congeneric taxa. Journal of Proteome Research. 2007;6:2732–45.
DOI:https://doi.org/10.1021/pr0701714.
Casewell NR, Harrison RA, Wüster W, Wagstaff SC. Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genomics. 2009;10:1–12. DOI:https://doi.org/10.1186/1471-2164-10-564.
Calvete JJ. Proteomic tools against the neglected pathology of snake bite envenoming. Expert Review of Proteomics. 2011;8:739–58. DOI:https://doi.org/10.1586/epr.11.61.
Toyama MH, Soares AM, Wen-Hwa L, Polikarpov I, Giglio JR, Marangoni S. Amino acid sequence of piratoxin-II, a myotoxic Lys49 phospholipase A2 homologue from Bothrops pirajai venom. Biochimie. 2000;82:245–50.
DOI:https://doi.org/10.1016/S0300-9084(00)00202-9.
Huang MZ, Gopalakrishnakone P, Chung MCM, Kini RM. Complete amino acid sequence of an acidic, cardiotoxic phospholipase A2 from the venom of Ophiophagus hannah (King cobra): A novel cobra venom enzyme with “pancreatic loop.” Archives of Biochemistry and Biophysics. 1997;338:150–6.
DOI:https://doi.org/10.1006/abbi.1996.9814.
Arni RK, Ward RJ. Phospholipase A2 - A structural review. Toxicon. 1996;34:827–41. DOI:https://doi.org/10.1016/0041-0101(96)00036-0.
Tasoulis T, Isbister GK. A review and database of snake venom proteomes. Toxins. 2017;9.
DOI:https://doi.org/10.3390/toxins9090290.
Bjarnason JB, Fox JW. Hemorrhagic metalloproteinases from snake venoms. Pharmacology and Therapeutics. 1994; 62:325–72. DOI:https://doi.org/10.1016/0163-7258(94)90049-3.
Tosin O, Karina P, Selistre-de-araujo HS, Helena D, Souza F De. Toxicon : X snake venom metalloproteinases ( SVMPs ): A structure-function update. Toxicon: X. 2020;7:100052. DOI:https://doi.org/10.1016/j.toxcx.2020.100052
Gutiérrez JM, Vargas M, Segura Á, Herrera M, Villalta M, Solano G, et al. In Vitro tests for assessing the neutralizing ability of snake antivenoms: Toward the 3Rs principles. Frontiers in Immunology 2021;11:1–13. DOI:https://doi.org/10.3389/fimmu.2020.617429
Takeda S, Takeya H, Iwanaga S. Snake venom metalloproteinases: Structure, function and relevance to the mammalian ADAM/ADAMTS family proteins. Biochimica et Biophysica Acta - Proteins and Proteomics. 2012;1824:164–76.
DOI:https://doi.org/10.1016/j.bbapap.2011.04.009.
Gutiérrez JM, Rucavado A. Snake venom metalloproteinases: Their role in the pathogenesis of local tissue damage. Biochimie. 2000;82:841–50.
DOI:https://doi.org/10.1016/S0300-9084(00)01163-9.
Serrano SMT, Maroun RC. Snake venom serine proteinases: Sequence homology vs. substrate specificity, a paradox to be solved. Toxicon. 2005;45:1115–32. DOI:https://doi.org/10.1016/j.toxicon.2005.02.020.
Roldan-Padron O, Castro-Guillen JL, Garcia-Arredondo JA, Cruz-Perez SM, Diaz-Pena LF, Saldaña C, et al. Snake venom hemotoxic enzymes : Biochemical Comparison between Crotalus Species from. Molecules. 2019;24:1–16.
DOI:https://doi.org/10.3390/molecules24081489.
Du XY, Clemetson KJ. Snake venom L-amino acid oxidases. Toxicon. 2002; 40:659–65. DOI:https://doi.org/10.1016/S0041-0101(02)00102-2
Tan KK, Bay BH, Gopalakrishnakone P. L-amino acid oxidase from snake venom and its anticancer potential. Toxicon. 2018;144:7–13. DOI:https://doi.org/10.1016/j.toxicon.2018.01.015.
Guo C, Liu S, Yao Y, Zhang Q, Sun MZ. Past decade study of snake venom l-amino acid oxidase. Toxicon. 2012;60:302–11. DOI:https://doi.org/10.1016/j.toxicon.2012.05.001.
Mackessy S. Section I. Reptile Toxinology, Systematics, and Venom Gland Structure. Structure 2010:1–13.
Iwanaga S, Susuki T. Enzymes in Snake Venoms. Venomous Animals and their Venoms, Springer, Berlin, Heidelberg; 1979;62–157. DOI:https://doi.org/10.1016/b978-1-4832-2949-2.50015-1.
Aird SD. Ophidian envenomation strategies and the role of purines. Toxicon. 2002;40:335–93. DOI:https://doi.org/10.1016/S0041-0101(01)00232-X.
Kang TS, Georgieva D, Genov N, Murakami MT, Sinha M, Kumar RP, et al. Enzymatic toxins from snake venom: Structural characterization and mechanism of catalysis. FEBS Journal. 2011; 278:4544–76. DOI:https://doi.org/10.1111/j.1742-4658.2011.08115.x.
Frobert Y, Créminon C, Cousin X, Rémy MH, Chatel JM, Bon S, et al. Acetylcholinesterases from Elapidae snake venoms: Biochemical, immunological and enzymatic characterization. Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology. 1997;1339:253–67.
DOI:https://doi.org/10.1016/S0167-4838(97)00009-5.
Fox JW. A brief review of the scientific history of several lesser-known snake venom proteins: L-amino acid oxidases, hyaluronidases and phosphodiesterases. Toxicon. 2013;62:75–82.
DOI:https://doi.org/10.1016/j.toxicon.2012.09.009.
Kini RM, Doley R. Structure, function and evolution of three-finger toxins: Mini proteins with multiple targets. Toxicon 2010;56:855–67. DOI:https://doi.org/10.1016/j.toxicon.2010.07.010.
Mukherjee AK, Mackessy SP, Dutta S. International Journal of Biological Macromolecules Characterization of a Kunitz-type protease inhibitor peptide ( Rusvikunin ) purified from Daboia russelii russelii venom. International Journal of Biological Macromolecules. 2014;67:154–62. DOI:https://doi.org/10.1016/j.ijbiomac.2014.02.058.
Willmott N, Gaffney P, Masci P, Whitaker A. A novel serine protease inhibitor from the Australian brown snake, Pseudonaja textilis textilis: Inhibition kinetics. Fibrinolysis and Proteolysis. 1995;9: 1–8.
DOI:https://doi.org/10.1016/S0268-9499(08)80040-9.
Yamazaki Y, Morita T. Structure and function of snake venom cysteine-rich secretory proteins. Toxicon. 2004;44:227–31. DOI:https://doi.org/10.1016/j.toxicon.2004.05.023.
Morita T. Structures and functions of snake venom CLPs (C-type lectin-like proteins) with anticoagulant-, procoagulant-, and platelet-modulating activities. Toxicon. 2005;45:1099–114. DOI:https://doi.org/10.1016/j.toxicon.2005.02.021.
Ogawa T, Chijiwa T, Oda-Ueda N, Ohno M. Molecular diversity and accelerated evolution of C-type lectin-like proteins from snake venom. Toxicon. 2005;45:1–14. DOI:https://doi.org/10.1016/j.toxicon.2004.07.028.
Kamiguti AS, Zuzel M, Theakston RDG. Snake venom metalloproteinases and disintegrins: Interactions with cells. Brazilian Journal of Medical and Biological Research. 1998;31:853–62.
DOI:https://doi.org/10.1590/S0100-879X1998000700001.
St Pierre L, Flight S, Masci PP, Hanchard KJ, Lewis RJ, Alewood PF, et al. Cloning and characterisation of natriuretic peptides from the venom glands of Australian elapids. Biochimie. 2006;88:1923–31. DOI:https://doi.org/10.1016/j.biochi.2006.06.014
Zhang Y, Wu J, Yu G, Chen Z, Zhou X, Zhu S, et al. Toxicon A novel natriuretic peptide from the cobra venom. Toxicon. 2011;57:134–40. DOI:https://doi.org/10.1016/j.toxicon.2010.10.014.
Levin ER, Gardner DG, Samson WK. Natriuretic Peprides. The New England Journal of Medicine. 1998;339:321–8. DOI:https://doi.org/10.1300/J123v27n02_05.
Zhao Y, Wu J, Wang X, Jia H, Chen DN, Li J Da. Prokineticins and their G protein-coupled receptors in health and disease. 1st ed. Elsevier Inc.; 2019;161. DOI:https://doi.org/10.1016/bs.pmbts.2018.09.006.
Fry BG. From genome to “venome”: Molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Research. 2005;15:403–20.
DOI:https://doi.org/10.1101/gr.3228405.
Yamazaki Y, Matsunaga Y, Tokunaga Y, Obayashi S, Saito M, Morita T. Snake venom vascular endothelial growth factors (VEGF-Fs) exclusively vary their structures and functions among species. Journal of Biological Chemistry. 2009;284:9885–91. DOI:https://doi.org/10.1074/jbc.M809071200.
Chippaux JP, Goyffon M. Venoms, antivenoms and immunotherapy. Toxicon. 1998;36:823–46. DOI:https://doi.org/10.1016/S0041-0101(97)00160-8.
Katali O, Shipingana L, Nyarangó P, Pääkkönen M, Haindongo E, Rennie T, et al. Protein identification of venoms of the African spitting cobras, Naja mossambica and Naja nigricincta nigricincta. Toxins. 2020;12. DOI:https://doi.org/10.3390/toxins12080520.
Chotwiwatthanakun C, Pratanaphon R, Akesowan S, Sriprapat S, Ratanabanangkoon K. Production of potent polyvalent antivenom against three elapid venoms using a low dose, low volume, multi-site immunization protocol. Toxicon. 2001;39:1487–94.
DOI:https://doi.org/10.1016/S0041-0101(01)00108-8.
Potet J, Smith J, McIver L. Reviewing evidence of the clinical effectiveness of commercially available antivenoms in sub-saharan africa identifies the need for a multi-centre, multi-antivenom clinical trial. PLoS Neglected Tropical Diseases. 2019;13:1–17. DOI:https://doi.org/10.1371/journal.pntd.0007551
Wong KY, Tan KY, Tan NH, Tan CH. A Neurotoxic Snake Venom without Phospholipase A2: Proteomics and Cross-Neutralization of the Venom from Senegalese Cobra, Naja senegalensis (Subgenus: Uraeus). Toxins. 2021;13. DOI:https://doi.org/10.3390/toxins13010060.
Williams CA, Chase MW. Precipitation analysis by diffusion in gels. Methods in immunology and immunochemistry, vol. 3, Academic Press New York. 1971;103–374.
DOI:https://doi.org/10.1016/b978-0-12-754403-8.50008-3.
Oudin J. [9] Immunochemical Analysis by Antigen-Antibody Precipitation in Gels. Methods in Enzymology. Academic Press, Inc., New York. 1980;70:166–98. DOI:https://doi.org/10.1016/S0076-6879(80)70048-4.
Bailey GS. Ouchterlony double immunodiffusion. Humana Press Inc., Totowa, NJ; 1996. DOI:https://doi.org/10.1007/978-1-60327-259-9_135.
Calvete JJ, Arias AS, Rodríguez Y, Quesada-Bernat S, Sánchez L V., Chippaux JP, et al. Preclinical evaluation of three polyspecific antivenoms against the venom of Echis ocellatus: Neutralization of toxic activities and antivenomics. Toxicon. 2016;119:280–8. DOI:https://doi.org/10.1016/j.toxicon.2016.06.022.
Pla D, Sanz L, Quesada-Bernat S, Villalta M, Baal J, Chowdhury MAW, et al. Phylovenomics of Daboia russelii across the Indian subcontinent. Bioactivities and comparative in vivo neutralization and in vitro third-generation antivenomics of antivenoms against venoms from India, Bangladesh and Sri Lanka. Journal of Proteomics. 2019;207:103443.
DOI:https://doi.org/10.1016/j.jprot.2019.103443.
Casewell NR, Cook DAN, Wagstaff SC, Nasidi A, Durfa N, Wüster W, et al. Pre-clinical assays predict Pan-African Echis viper efficacy for a species-specific antivenom. PLoS Neglected Tropical Diseases. 2010;4.
DOI:https://doi.org/10.1371/journal.pntd.0000851.
Paixão-Cavalcante D, Kuniyoshi AK, Portaro FCV, da Silva WD, Tambourgi D V. African adders: Partial characterization of snake venoms from three bitis species of medical importance and their neutralization by experimental equine antivenoms. PLoS Neglected Tropical Diseases. 2015;9:1–18.
DOI:https://doi.org/10.1371/journal.pntd.0003419.
Andrejccaronáková Z, Petrilla V, Tomečková V, Tóth Š, Pekárová T, Komanický V, et al. New approaches in monitoring venom of genus Dendroaspis. Spectroscopy Letters. 2015;48:462–72. DOI:https://doi.org/10.1080/00387010.2014.906471.
Currier R. Investigating venom synthesis: exploring the composition, variation and gene expression dynamics of Bitis arietans venom. PhD Thesis, LSTM 2012.
Casewell NR, Jackson TNW, Laustsen AH, Sunaga K. Europe PMC Funders Group Causes and Consequences of Snake Venom Variation. 2020;41:570–81.
DOI:https://doi.org/10.1016/j.tips.2020.05.006.Causes.
Giorgianni MW, Dowell NL, Griffin S, Kassner VA, Selegue JE. The origin and diversification of a novel protein family in venomous snakes. 2020;117.
DOI:https://doi.org/10.1073/pnas.1920011117.
Post Y, Puschhof J, Beumer J, Richardson MK, Casewell NR, Clevers H. Article Snake Venom Gland Organoids. Cell. 2020;180:233-247.e21. DOI:https://doi.org/10.1016/j.cell.2019.11.038.
Tanaka GD, Furtado MDFD, Portaro FCV, Sant’Anna OA, Tambourgi D v. Diversity of Micrurus snake species related to their venom toxic effects and the prospective of antivenom neutralization. PLoS Neglected Tropical Diseases. 2010;4:1–12.
DOI:https://doi.org/10.1371/journal.pntd.0000622.
Tanaka GD, Pidde-Queiroz G, Furtado M de FD, van den Berg C, Tambourgi D V. Micrurus snake venoms activate human complement system and generate anaphylatoxins. BMC Immunology. 2012;13.
DOI:https://doi.org/10.1186/1471-2172-13-4.
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