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Toxins 2017, 9(5), 171; doi:10.3390/toxins9050171

Coagulating Colubrids: Evolutionary, Pathophysiological and Biodiscovery Implications of Venom Variations between Boomslang (Dispholidus typus) and Twig Snake (Thelotornis mossambicanus)

1
Venom Evolution Lab, School of Biological Sciences, University of Queensland, St. Lucia, QLD 4072, Australia
2
Alistair Reid Venom Research Unit, Parasitology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
3
Vertebrate Palaeontology and Biomechanics Laboratory, School of Biological Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia
4
Faculty of Health Sciences, University of Macau, Avenida da Universidade, Taipa, Macau SAR
5
Centre for Advanced Imaging, University of Queensland, St. Lucia, QLD 4072, Australia
6
School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, QLD 4072, Australia
*
Author to whom correspondence should be addressed.
Academic Editor: Anita Malhotra
Received: 16 January 2017 / Revised: 15 May 2017 / Accepted: 15 May 2017 / Published: 19 May 2017
(This article belongs to the Section Animal Venoms)
View Full-Text   |   Download PDF [5755 KB, uploaded 19 May 2017]   |  

Abstract

Venoms can deleteriously affect any physiological system reachable by the bloodstream, including directly interfering with the coagulation cascade. Such coagulopathic toxins may be anticoagulants or procoagulants. Snake venoms are unique in their use of procoagulant toxins for predatory purposes. The boomslang (Dispholidus typus) and the twig snakes (Thelotornis species) are iconic African snakes belonging to the family Colubridae. Both species produce strikingly similar lethal procoagulant pathologies. Despite these similarities, antivenom is only produced for treating bites by D. typus, and the mechanisms of action of both venoms have been understudied. In this study, we investigated the venom of D. typus and T. mossambicanus utilising a range of proteomic and bioactivity approaches, including determining the procoagulant properties of both venoms in relation to the human coagulation pathways. In doing so, we developed a novel procoagulant assay, utilising a Stago STA-R Max analyser, to accurately detect real time clotting in plasma at varying concentrations of venom. This approach was used to assess the clotting capabilities of the two venoms both with and without calcium and phospholipid co-factors. We found that T. mossambicanus produced a significantly stronger coagulation response compared to D. typus. Functional enzyme assays showed that T. mossambicanus also exhibited a higher metalloprotease and phospholipase activity but had a much lower serine protease activity relative to D. typus venom. The neutralising capability of the available boomslang antivenom was also investigated on both species, with it being 11.3 times more effective upon D. typus venom than T. mossambicanus. In addition to being a faster clotting venom, T. mossambicanus was revealed to be a much more complex venom composition than D. typus. This is consistent with patterns seen for other snakes with venom complexity linked to dietary complexity. Consistent with the external morphological differences in head shape between the two species, CT and MRI analyses revealed significant internal structural differences in skull architecture and venom gland anatomy. This study increases our understanding of not only the biodiscovery potential of these medically important species but also increases our knowledge of the pathological relationship between venom and the human coagulation cascade. View Full-Text
Keywords: procoagulant; boomslang; Dispholidus typus; Thelotornis mossambicanus; colubridae; enzyme activity; biodiscovery; evolution procoagulant; boomslang; Dispholidus typus; Thelotornis mossambicanus; colubridae; enzyme activity; biodiscovery; evolution
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This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. (CC BY 4.0).

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MDPI and ACS Style

Debono, J.; Dobson, J.; Casewell, N.R.; Romilio, A.; Li, B.; Kurniawan, N.; Mardon, K.; Weisbecker, V.; Nouwens, A.; Kwok, H.F.; Fry, B.G. Coagulating Colubrids: Evolutionary, Pathophysiological and Biodiscovery Implications of Venom Variations between Boomslang (Dispholidus typus) and Twig Snake (Thelotornis mossambicanus). Toxins 2017, 9, 171.

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