Description of Hutmannin-1, a new piii-metalloprotease from the venom of the neotropical lansberg’s hognose Viper (Porthidium lansbergii hutmanni) With fibrino(geno) lytic and haemorrhagic activities
Descripción de Hutmannin-1, una nueva metaloproteasa piii del veneno de la serpiente neotropical mapanare de lansberg (Porthidium lansbergii Hutmanni) con actividades fibrino (geno) líticas y hemorrágicas
Keywords:
Anticoagulant, antivenin, coagulation, haemostasis, haemorrhage, snake venom
Abstract
The objective was to characterise hutmannin-1 (hut-1), a new~62 kDa P-III-class metalloprotease from Porthidium lansbergii hutmanni(P.l.h) (Margarita Island, Venezuela). To characterise this protein, the crude venom of P.l.h was fractionated by size exclusion chromatography, anion exchange chromatography and High Performance Liquid Chromatography (HPLC). Hutmannin-1 was identified by MALDI-TOF/TOF mass spectrometry, and the venom was analysed by SDS-PAGE. The lethality, minimum haemorrhagic dose (MHD), effect of temperature on the activity, procoagulant activity on human plasma, and anticoagulant, defibrinating, gelatinolytic fibrinolytic, and fibrinogenolytic and platelet aggregation activities of hut-1 were determined. Antigenic recognition assays were performed on P.l.h crude venom and hut-1 by a venezuelan polyvalent anti-ophidic serum (PAOS) Hut-1 had strong fibrinogenolytic and moderate fibrinolytic activity. These activities and the haemorrhagic activity of hut-1 were completely inhibited by EDTA. P.l.h crude venom had potent anticoagulant activity on recalcified plasma and inhibited the platelet aggregation induced by thrombin, ADP, collagen and ristocetin. In contrast, the anticoagulant, coagulant and platelet aggregation inhibition of hut-1 were not observed with any of the agonists. This result suggests that other proteins in the crude venom, markedly impact platelet functions and/or coagulation factors. Commercial venezuelan antivenin showed limited ability to neutralise the haemorrhagic activity of hut-1.
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References
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JIA, L.G.; WANG, X.M.; SHANNON, J.D.; BJARNASON, J.B.; FOX, J.W.; Function of disintegrin-like/cysteine-rich domains of atrolysin A Inhibition of platelet aggregation by recombinant protein and peptide antagonists. J.Biol. Chem. 272: 13094-13102. 1997.
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KAMIGUTI, A. Platelets as targets of snake venom metallo-proteinases. Toxicon. 45: 1041-1049. 2005;
KINI, M.; KOH, C. Metalloproteases Affecting blood coagulation fibrinolysis and platelet aggregation from snake venoms: definition and nomenclature of interaction sites. Toxins. 8: 330-338. 2016.
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CAMPBELL, JA.; LAMAR, W. Porthidium genus. Venomous reptiles of Latin America, Cornell. Univ. Press, Cornell (USA). Pp. 313-329. 1989.
CANDIANO, G.; BRUSCHI, M.; MUSANTE, L.; SANTUC- CI, L.; GHIGGERI, G.M.; CARNEMOLLA, B.; ORECCHIA, P.; ZARDI, L.; RIGHETTI, P. Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophor. 25: 1327-1333. 2004.
CASTOE, A.; SASA, M.; PARKINSON, C. Modeling nucleotide evolution at the mesoscale: The phylogeny of the Neo- tropicalpitvipers of the Porthidium group (Viperidae: Crotalinae). Mol. Phylogenet. Evol. 37: 881–898. 2005.
DA SILVA, M.; LUCENA, S.; AGUILAR, I.; RODRÍGUEZ-ACOSTA, A.; SALAZAR, A.M.; SÁNCHEZ, E.E.; GIRÓN, M.E.; CARVAJAL, Z.; AROCHA-PIÑANGO, C.; GUERRERO, B. Anti-platelet effect of cumanastatin 1 a disintegrin isolated from venom of South American Crotalus rattlesnake. Thromb. Res. 123: 731-739. 2009.
ESCALANTE, T.; NÚÑEZ, J.; MOURA DA SILVA, A.M.; RUCAVADO, A.; THEAKSTON, R.D.; GUTIÉRREZ, J.M. Pulmonary hemorrhage induced by jararhagin a metalloproteinase from Bothrops jararaca snake venom. Toxicol. Appl. Pharmacol. 193: 17–28. 2003.
ESCALANTE, T.; RUCAVADO, A.; FOX, J.; GUTIÉRREZ, J.M. Key events in microvascular damage induced by snake venom hemorrhagic metalloproteinases. J. Proteomics. 74: 1781-1794 2011.
FREITAS DE SOUSA, L.A.; COLOMBINI, M.; LOPES-FERREIRA, M.; SERRANO, S.M.T.; MOURA DA-SILVA, A.M. Insights into the mechanisms involved in strong hemorrhage and dermonecrosis induced by AtroxlysinIa a PI-Class snake venom metalloproteinase. Toxins. 9: 239. 2017.
FUENTES, O.; RODRIGUEZ-ACOSTA, A. Sobre los géneros Bothriechis Bothriopsis Bothrops y Porthidium (Serpentes: Crotalidae) existentes en Venezuela. Claves para su identificación de interés biomédico. Acta. Biol. Venez. 17: 31-38. 1997.
GAY, C.; LEIVA, L.; TEIBLER, P.; ACOSTA DE P, O. Proteolytic edematogenic and miotoxic activities of a hemorrhagic metalloproteinase isolated from Bothrops alternatus venom. Toxicon. 46: 546-554. 2005;
GENE, J.A.; ROY, A.; ROJAS, G.; GUTIÉRREZ, J.M.; CERDAS, L. Comparative study on the coagulant desfibrinating fibrinolytic and fibrinogenolytic activities of Costa Rican Crotalinae snake venoms and their neutralization by polyvalent antivenom. Toxicon. 27: 841-848. 1989.
GIDDEN J, DENSON J, LIYANAGE R, IVEY DM, LAY JO. Lipid Compositions in Escherichia coli and Bacillus subtilis During Growth as Determined by MALDI-TOF and TOF/TOF Mass Spectrometry. Int. J. Mass. Spectrom. 2009;283:178- 184.
GIRÓN, M.E.; ESTRELLA, A.; SÁNCHEZ, E.E.; GALAN, J.; TAO, A.; GUERRERO, B.; SALAZAR, A.M.; RODRÍGUEZ-ACOSTA, A. Purification and characterization of a metalloproteinase Porthidin-1 from the venom of Lansberg’s hog-nosed pitvipers (Porthidium lansbergii hutmanni). Toxi- con. 57: 608-618. 2011.
GIRÓN, M.E.; RODRÍGUEZ-ACOSTA, A.; SALAZAR, A.M.; SÁNCHEZ, E.E.; GALAN, J.; IBARRA, C.; GUERRERO, B. Isolation and characterization of two new non-hemorrhagic metalloproteinases with fibrinogenolytic activity from the mapanare (Bothrops colombiensis) Venom. Arch. Toxicol. 87: 197-208. 2013.
GIRÓN, M.E.; SALAZAR, A.M.; AGUILAR, I.; PÉREZ, J.; SÁNCHEZ, E.E.; AROCHA-PIÑANGO, C.; RODRÍGUEZ-ACOSTA, A.; GUERRERO, B. Hemorrhagic coagulant and fibrino(geno)lytic activities of crude venom and fractions from mapanare (Bothrops colombiensis) snakes Comp. Biochem. Physiol. Toxicol. Pharmacol. 147: 113-121. 2008.
GRILLO, O.; SCANNONE, H. Fractionation of Crotalus durissus cumanensis venom by gel filtration. Toxicon. 14: 400-403. 1976.
GUTIÉRREZ, J.M.; LEÓN, G.; LOMONTE, B.; ANGULO, Y. Antivenoms for snakebite envenomings. Inflamm. Allergy. Drug. Targets. 10: 369-380. 2011.
HAMZA, L.; GARGIOLI, C.; CASTELLI, S.; RUFINI, S.; LARABA-DJEBARI, F. Purification and characterization of a fibrinogenolytic and hemorrhagic metalloproteinase isolated from Vipera lebetina venom. Biochimie. 92: 797- 805. 2010.
HERNÁNDEZ, M.; SCANNONE, H.; FINOL, H.J.; PINEDA, M.E.; FERNÁNDEZ, I.; GIRÓN, M.E.; AGUILAR, I.; RODRÍGUEZ-ACOSTA, A. Alterations in the ultrastructure of cardiac autonomic nervous system triggered by crotoxin from rattlesnake (Crotalus durissus cumanensis) Venom. Exp. Toxicol. Pathol. 59:129-37. 2007.
HERRERA, C.; ESCALANTE, T.; VOISIN, M.; RUCAVADO, A.; MORAZÁN, D.; KELE, J.; CALVETE, J.J.; SANZ, L.; NOURSHARGH, S.; GUTIÉRREZ, J.M.; FOX, J.W Tissue localization and extracellular matrix degradation by PI PII and PIII snake venom metalloproteinases: Clues on the mechanisms of venom-induced haemorrhage. PLoS. Negl. Trop. Dis. 29: 1-20. 2015.
JIA, L.G.; WANG, X.M.; SHANNON, J.D.; BJARNASON, J.B.; FOX, J.W.; Function of disintegrin-like/cysteine-rich domains of atrolysin A Inhibition of platelet aggregation by recombinant protein and peptide antagonists. J.Biol. Chem. 272: 13094-13102. 1997.
JIMÉNEZ-CHARRIS, E.; MONTEALEGRE-SANCHEZ, L.; SOLANO-REDONDO, L.; MORA-OBANDO, D.; CAMACHO, E.; CASTRO-HERRERA, F.; FIERRO-PÉREZ, L.; LOMONTE, B. Proteomic and functional analyses of the venom of Porthidium lansbergii lansbergii (Lansberg’s hognose viper) from the Atlantic Department of Colombia. J. Proteom. 114: 287-299. 2015;
KAMIGUTI, A. Platelets as targets of snake venom metallo-proteinases. Toxicon. 45: 1041-1049. 2005;
KINI, M.; KOH, C. Metalloproteases Affecting blood coagulation fibrinolysis and platelet aggregation from snake venoms: definition and nomenclature of interaction sites. Toxins. 8: 330-338. 2016.
KONDO, H.; KONDO, S.; IKEZAWA, Y.; MURATA, R.; OHSAKA, A. Studies on the quantitative method for the determination of hemorrhagic activity of Habu snake venom. Japan J. Med. Sci. Biol. 13: 43-51. 1960.
LAEMMLI, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680-85. 1970.
LANCINI, A. Familia Viperidae. Genero Bothrops. Serpientes de Venezuela. 2nd Ed. Ediciones Ernesto Armitano, Venezuela. Pp. 203-204. 1986.
LEE J.H.; CHOI, H.S.; NASR, K.A.; HA, M.; KIM, Y.; FRANGIONI, J.V. High-throughput small molecule identification using MALDI-TOF and a nanolayered substrate. Analytical Chemistry. 83 (13):5283-5289. 2011.
LOMONTE, B.; REY-SUÁREZ, P.; TSAIA, W.; ANGULO, Y.; SASA, M.; GUTIÉRREZ, J.M.; CALVETE, J. Snake venomics of the pit vipers Porthidium nasutum Porthidium ophryo-megas and Cerrophidion godmani from Costa Rica: Toxicological and taxonomical insights. J. Proteom. 75:1675- 1689. 2012.
LOWRY, O.; ROSEBROUGH, N.; FARR, A.; RANDALL, R. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 93: 265-275. 1951.
MARKLAND, F.; SWENSON, S. Snake venom metalloproteinases. Toxicon. 62: 3–18. 2013.
MARSH, N.A.; AROCHA-PIÑANGO, C.L. Evaluation of the fibrin plate method for estimating plasminogen activators. Thromb. Diath. Haemorrh. 28: 75–88. 1972.
MOURA-DA-SILVA, A.M.; BALDO, C. Jararhagin a hemorrhagic snake venom metalloproteinase from Bothrops jararaca. Toxicon. 60: 280-289. 2012;
OYAMA, E.; TAKAHASHI, H. Structures and functions of snake venom metalloproteinases (SVMP) from Protobothrops venom collected in Japan. Molecules. 22: E1305/1- 11. 2017.
PIFANO, F. Investigación y docencia en Medicina Tropical. Arch. Ven. Med. Trop. Parasitol. Med. 4: 1-203. 1961.
REY-SUÁREZ, P.; NÚÑEZ, V.; GUTIÉRREZ, J.M.; LOMONTE, B. Proteomic and biological characterization of the venom of the red-tail coral snake Micrurus mipartitus (Elapidae) from Colombia and Costa Rica. J. Proteom. 75: 655-667. 2011.
RODRÍGUEZ-ACOSTA, A.; SÁNCHEZ, E.E.; MÁRQUEZ, A.; CARVAJAL, Z.; SALAZAR, A.M.; GIRÓN, M.E.; ESTRELLA, A.; GIL, A.; GUERRERO, B. Hemostatic properties of Venezuelan Bothrops snake venoms with special reference to Bothrops isabelae Venom. Toxicon. 56: 926-935.2010.
ROKYTA, D.R.; WRAY, K.P.; LEMMON, A.R.; LEMMON, E.M.; CAUDLE, S.B. High-throughput venom-gland transcriptome for the Eastern Diamondback Rattlesnake (Crotalus adamanteus) and evidence for pervasive positive selection across toxin classes. Toxicon. 57: 657-671. 2011.
SALAZAR, A.M.; RODRÍGUEZ-ACOSTA, A.; GIRÓN, M.E.; AGUILAR, I.; GUERRERO, B. A comparative analysis of the clotting and fibrinolytic activities of the snake venom (Bothrops atrox) from different geographical areas in Venezuela. Thromb. Res. 120: 95-104. 2007.
SÁNCHEZ, E.E.; GIRÓN, M.E.; UZCÁTEGUI, N.L.; GUERRERO, B.; SAUCEDO, M.; CUEVAS, E.; RODRÍGUEZ-ACOSTA, A. Biochemical and biological characterisation of lancehead (Bothrops venezuelensis Sandner 1952) snake venom from the Venezuelan Central Coastal range. Bol. Malariol. San. Ambient. 54:138-149. 2014.
SANDNER-MONTILLA, F. Una nueva especie de Bothrops lansbergii de la familia Crotalidae. Mem. Cient. Ofidiol. 9:1- 16. 1989.
TAKEDA, S. Adam and Adamts family proteins and snake venom metalloproteinases: A structural overview. Toxins. 8:155. 2016.
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Published
2021-04-23
How to Cite
1.
Eugenia Pineda M, Perales J, Sánchez EE, Hermoso T, Narvaez M, Chapeaurouge A, Vargas AM, Rodríguez-Acosta A. Description of Hutmannin-1, a new piii-metalloprotease from the venom of the neotropical lansberg’s hognose Viper (Porthidium lansbergii hutmanni) With fibrino(geno) lytic and haemorrhagic activities: Descripción de Hutmannin-1, una nueva metaloproteasa piii del veneno de la serpiente neotropical mapanare de lansberg (Porthidium lansbergii Hutmanni) con actividades fibrino (geno) líticas y hemorrágicas. Rev. Cient. FCV-LUZ [Internet]. 2021Apr.23 [cited 2024Nov.22];30(3):142-56. Available from: https://produccioncientificaluz.org/index.php/cientifica/article/view/35747
Section
Wild Life
