Skip to main content
SpringerLink
Log in

Biological Activities and Assays of the Snake Venom Metalloproteinases (SVMPs)

  • Reference work entry
  • First Online:
Venom Genomics and Proteomics

Part of the book series: Toxinology ((TOXI))

Abstract

Snake venom metalloproteases (SVMP) are a key group of enzymes abundant in Viperidae venoms. Structurally, secreted SVMPs are typically organized into three main groups based on the presence or absence of domains: PI – which contains only a metalloproteinase domain; PII – includes also a disintegrin domain; and PIII – in addition to the first two domains, possesses a cysteine-rich domain. Diverse functions have been described to this group of proteases including their well-known hemorrhagic activity. Fibrin(ogen)olysis, prothrombin activation, interaction and lysis of von Willebrand factor, cytotoxicity, obstruction of angiogenesis, interference with platelet aggregation, myotoxicity, and proinflammatory are some of the other activities described by SVMPs. The SVMPs possess a broad range of biological activities, many with pathological consequences, that a brief description of the more common assays for biological activity associated with these proteins is of value to those entering the field. This chapter discusses the numerous activities attributed to the SVMPs and outlines the major assays utilized in systematic investigations of SVMPs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 299.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Achê DC, Gomes MSR, de Souza DLN, Silva MA, Brandeburgo MIH, Yoneyama KAG, et al. Biochemical properties of a new PI SVMP from Bothrops pauloensis: inhibition of cell adhesion and angiogenesis. Int J Biol Macromol [Internet]. Elsevier B.V. 2014 [cited 10 Oct 2014];72C:445–53. Available from http://www.ncbi.nlm.nih.gov/pubmed/25199868

    Google Scholar 

  • Baldo C, Tanjoni I, León IR, Batista IFC, Della-Casa MS, Clissa PB, et al. BnP1, a novel P-I metalloproteinase from Bothrops neuwiedi venom: biological effects benchmarking relatively to jararhagin, a P-III SVMP. Toxicon [Internet]. 2008 [cited 21 Aug 2014];51(1):54–65. Available from http://www.ncbi.nlm.nih.gov/pubmed/17889921

  • Baldo C, Ferreira M, Lopes D, Izidoro L, Gomes A, Ferro E, et al. Action of neuwiedase, a metalloproteinase isolated from Bothrops neuwiedi venom, on skeletal muscle: an ultrastructural and immunocytochemistry study. J Venom Anim Toxins Incl Trop Dis [Internet]. 2010;16(3):462–9. Available from http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1678-91992010000300013&lng=en&nrm=iso&tlng=en

  • Baramova EN, Shannon JD, Bjarnason JB, Fox JW. Degradation of extracellular matrix proteins by hemorrhagic metalloproteinases. Arch Biochem Biophys [Internet]. 1989;275(1):63–71. Available from http://linkinghub.elsevier.com/retrieve/pii/0003986189903500

    Google Scholar 

  • Barrantes A, Solís V, Bolaños R. Alteración de los mecanismos de la coagulación en el envenenamiento por Bothrops asper(Terciopelo). Toxicon [Internet]. 1985 [cited 30 Oct 2014];(fibrina I):399–407. Available from http://www.sciencedirect.com/science/article/pii/0041010185900248

  • Bello CA, Hermogenes ALN, Magalhaes A, Veiga SS, Gremski LH, Richardson M, et al. Isolation and biochemical characterization of a fibrinolytic proteinase from Bothrops leucurus (white-tailed jararaca) snake venom. Biochimie [Internet]. 2006 [cited 21 Aug 2014];88(2):189–200. Available from http://www.ncbi.nlm.nih.gov/pubmed/16139412

  • Berger M, Pinto AFM, Guimarães JA. Purification and functional characterization of bothrojaractivase, a prothrombin-activating metalloproteinase isolated from Bothrops jararaca snake venom. Toxicon [Internet]. 2008 [cited 21 Aug 2014];51(4):488–501. Available from http://www.ncbi.nlm.nih.gov/pubmed/18262582

    Google Scholar 

  • Bernardes CP, Santos-Filho NA, Costa TR, Gomes MSR, Torres FS, Costa J, et al. Isolation and structural characterization of a new fibrin(ogen)olytic metalloproteinase from Bothrops moojeni snake venom. Toxicon [Internet]. 2008 [cited 21 Aug 2014];51(4):574–84. Available from http://www.ncbi.nlm.nih.gov/pubmed/18187176

    Google Scholar 

  • Bernardes CP, Menaldo DL, Camacho E, Rosa JC, Escalante T, Rucavado A, et al. Proteomic analysis of Bothrops pirajai snake venom and characterization of BpirMP, a new P-I metalloproteinase. J Proteomics [Internet]. Elsevier B.V. 2013 [cited 5 Jun 2014];80:250–67. Available from http://www.ncbi.nlm.nih.gov/pubmed/23385358

  • Bjarnason JB, Fox JW. Hemorrhagic metalloproteinases from snake venoms. Pharmacol Ther [Internet]. 1994;62(3):325–72. Available from http://linkinghub.elsevier.com/retrieve/pii/0163725894900493

    Google Scholar 

  • Bjarnason JB, Tu AT. Hemorrhagic toxins from Western diamondback rattlesnake (Crotalus atrox) venom: isolation and characterization of five toxins and the role of zinc in hemorrhagic toxin e. Biochemistry [Internet]. 1978;17(16):3395–404. Available from http://www.ncbi.nlm.nih.gov/pubmed/210790

    Google Scholar 

  • Camacho E, Villalobos E, Sanz L, Pérez A, Escalante T, Lomonte B, et al. Understanding structural and functional aspects of PII snake venom metalloproteinases: Characterization of BlatH1, a hemorrhagic dimeric enzyme from the venom of Bothriechis lateralis. Biochimie [Internet]. Elsevier Masson SAS. 2014 [cited 9 May 2014];101:145–55. Available from http://www.ncbi.nlm.nih.gov/pubmed/24457155

    Google Scholar 

  • Chaim OM, Sade YB, da Silveira RB, Toma L, Kalapothakis E, Chávez-Olórtegui C, et al. Brown spider dermonecrotic toxin directly induces nephrotoxicity. Toxicol Appl Pharmacol [Internet]. 2006 [cited 12 Nov 2014];211(1):64–77. Available from http://www.ncbi.nlm.nih.gov/pubmed/16005484

    Google Scholar 

  • Chen R-Q, Jin Y, Wu J-B, Zhou X-D, Li D, Lu Q-M, et al. A novel high molecular weight metalloproteinase cleaves fragment F1 of activated human prothrombin. Toxicon [Internet]. 2004 [cited 10 Sept 2014];44(3):281–7. Available from http://www.ncbi.nlm.nih.gov/pubmed/15302534

    Google Scholar 

  • Chen H-S, Tsai H-Y, Wang Y-M, Tsai I-H. P-III hemorrhagic metalloproteinases from Russell’s viper venom: cloning, characterization, phylogenetic and functional site analyses. Biochimie [Internet]. 2008 [cited 10 Sept 2014];90(10):1486–98. Available from http://www.ncbi.nlm.nih.gov/pubmed/18554518

  • Cheresh DA. Human endothelial cells synthesize and express an Arg-Gly-Asp-directed adhesion receptor involved in attachment to fibrinogen and von Willebrand factor. Proc Natl Acad Sci U S A [Internet]. 1987;84(18):6471–5. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=299099&tool=pmcentrez&rendertype=abstract

  • Cintra CO, De Toni LGB, Sartim MA, Franco JJ, Caetano RC, Murakami MT, et al. Batroxase, a new metalloproteinase from B. atrox snake venom with strong fibrinolytic activity. Toxicon [Internet]. Elsevier Ltd; 2012 [cited 22 Oct 2014];60(1):70–82. Available from http://www.ncbi.nlm.nih.gov/pubmed/22483847

  • Clissa P, Laing G, Theakston R. The effect of jararhagin, a metalloproteinase from Bothrops jararaca venom, on pro-inflammatory cytokines released by murine peritoneal adherent cells. Toxicon [Internet]. 2001 [cited 2 Dec 2014];39. Available from http://www.sciencedirect.com/science/article/pii/S0041010101001313

  • Clissa PB, Lopes-Ferreira M, Della-Casa MS, Farsky SHP, Moura-da-Silva AM. Importance of jararhagin disintegrin-like and cysteine-rich domains in the early events of local inflammatory response. Toxicon [Internet]. 2006 [cited 30 Nov 2014];47(5):591–6. Available from http://www.ncbi.nlm.nih.gov/pubmed/16564063

    Google Scholar 

  • Costa EP, Clissa PB, Teixeira CFP. Importance of metalloproteinases and macrophages in viper snake envenomation – induced local inflammation. Inflammation. 2002;26(1):13–17.

    Article  CAS  PubMed  Google Scholar 

  • Da Silva M, Lucena S, Aguilar I, Rodríguez-Acosta A, Salazar AM, Sánchez EE, et al. Anti-platelet effect of cumanastatin 1, a disintegrin isolated from venom of South American Crotalus rattlesnake. Thromb Res [Internet]. 2009 [cited 26 Mar 2014];123(5):731–9. Available from http://www.ncbi.nlm.nih.gov/pubmed/18835011

    Google Scholar 

  • De Morais NCG, Neves Mamede CC, Fonseca KC, de Queiroz MR, Gomes-Filho SA, Santos-Filho NA, et al. Isolation and characterization of moojenin, an acid-active, anticoagulant metalloproteinase from Bothrops moojeni venom. Toxicon [Internet]. 2012;60(7):1251–8. Available from http://www.ncbi.nlm.nih.gov/pubmed/22975266

    Google Scholar 

  • Edgar W, Prentice C. The proteolytic action of ancrod on human fibrinogen and its polypeptide chains. Thromb Res [Internet]. 1973 [cited 22 Oct 2014]. Available from http://www.sciencedirect.com/science/article/pii/0049384873900820

  • Escalante T, Franceschi A, Rucavado A, Gutiérrez JM. Effectiveness of batimastat, a synthetic inhibitor of matrix metalloproteinases, in neutralizing local tissue damage induced by BaP1, a hemorrhagic metalloproteinase from the venom of the snake Bothrops asper. Biochem Pharmacol [Internet]. 2000;60(2):269–74. Available from http://linkinghub.elsevier.com/retrieve/pii/S0006295200003026

    Google Scholar 

  • Escalante T, Shannon J, Moura-da-Silva AM, Gutiérrez JM, Fox JW. Novel insights into capillary vessel basement membrane damage by snake venom hemorrhagic metalloproteinases: a biochemical and immunohistochemical study. Arch Biochem Biophys [Internet]. 2006 [cited 31 July 2014];455(2):144–53. Available from http://www.ncbi.nlm.nih.gov/pubmed/17055999

    Google Scholar 

  • Escalante T, Rucavado A, Pinto AFM, Terra RMS, Fox JW. Wound exudate as a proteomic window to reveal different mechanisms of tissue damage by snake venom toxins research articles. Journal of Proteome Research. 2009(8);5120–31.

    Article  CAS  PubMed  Google Scholar 

  • Escalante T, Rucavado A, Fox JW, Gutiérrez JM. Key events in microvascular damage induced by snake venom hemorrhagic metalloproteinases. J Proteomics [Internet]. 2011 [cited 19 June 2014];74(9):1781–94. Available from http://www.ncbi.nlm.nih.gov/pubmed/21447411

    Google Scholar 

  • Fernandes CM, Zamuner SR, Zuliani JP, Rucavado A, Gutiérrez JM, Teixeira CDFP. Inflammatory effects of BaP1 a metalloproteinase isolated from Bothrops asper snake venom: leukocyte recruitment and release of cytokines. Toxicon [Internet]. 2006 [cited 30 Nov 2014];47(5):549–59. Available from http://www.ncbi.nlm.nih.gov/pubmed/16529786

    Google Scholar 

  • Fox JW, Serrano SMT. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J [Internet]. 2008 [cited 26 Apr 2012];275(12):3016–30. Available from http://www.ncbi.nlm.nih.gov/pubmed/18479462

    Google Scholar 

  • Friedl P, Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol [Internet]. 2010 [cited 11 July 2014];188(1):11–9. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2812848&tool=pmcentrez&rendertype=abstract

  • Gallagher P, Bao Y, Serrano SMT, Laing GD, Theakston RDG, Gutiérrez JM, et al. Role of the snake venom toxin jararhagin in proinflammatory pathogenesis: in vitro and in vivo gene expression analysis of the effects of the toxin. Arch Biochem Biophys [Internet]. 2005 [cited 2 Dec 2014];441(1):1–15. Available from http://www.ncbi.nlm.nih.gov/pubmed/16083850

    Google Scholar 

  • Gené JA, Roy A, Rojas G, Gutiérrez JM, Cerdas L. Comparative study on coagulant, defibrinating, fibrinolyic and fibrinogenolytic activities of Costa Rican crotaline snake venoms and their neutralization by a polyvalent antivenom. Toxicon. 1989;27(8):841–8.

    Article  PubMed  Google Scholar 

  • Girón ME, Rodríguez-Acosta A, Salazar AM, Sánchez EE, Galán J, Ibarra C, et al. Isolation and characterization of two new non-hemorrhagic metalloproteinases with fibrinogenolytic activity from the mapanare (Bothrops colombiensis) venom. Arch Toxicol [Internet]. 2013 [cited 9 May 2014];87(1):197–208. Available from http://www.ncbi.nlm.nih.gov/pubmed/22918489

  • Gomes MSR, de Queiroz MR, Mamede CCN, Mendes MM, Hamaguchi A, Homsi-Brandeburgo MI, et al. Purification and functional characterization of a new metalloproteinase (BleucMP) from Bothrops leucurus snake venom. Comp Biochem Physiol C Toxicol Pharmacol [Internet]. Elsevier B.V. 2011 [cited 26 Apr 2012];153(3):290–300. Available from http://www.ncbi.nlm.nih.gov/pubmed/21130897

  • Gremski LH, Chaim OM, Paludo KS, Sade YB, Otuki MF, Richardson M, et al. Cytotoxic, thrombolytic and edematogenic activities of leucurolysin-a, a metalloproteinase from Bothrops leucurus snake venom. Toxicon [Internet]. 2007 [cited 23 Sept 2014];50(1):120–34. Available from http://www.ncbi.nlm.nih.gov/pubmed/17482228

    Google Scholar 

  • Guan H-H, Goh K-S, Davamani F, Wu P-L, Huang Y-W, Jeyakanthan J, et al. Structures of two elapid snake venom metalloproteases with distinct activities highlight the disulfide patterns in the D domain of ADAMalysin family proteins. J Struct Biol [Internet]. Elsevier Inc. 2010 [cited 14 Aug 2014];169(3):294–303. Available from http://www.ncbi.nlm.nih.gov/pubmed/19932752

    Google Scholar 

  • Guo X-X, Zeng L, Lee W-H, Zhang Y, Jin Y. Isolation and cloning of a metalloproteinase from king cobra snake venom. Toxicon [Internet]. 2007 [cited 10 Sept 2014];49(7):954–65. Available from http://www.ncbi.nlm.nih.gov/pubmed/17337026

    Google Scholar 

  • Gutiérrez JM, Rucavado A. Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage. Biochimie. 2000;82:841–850.

    Article  PubMed  Google Scholar 

  • Gutiérrez J, Gené J, Rojas G, Cerdas L. Neutralization of proteolytic and hemorrhagic activities of Costa Rican snake venoms by a polyvalent antivenom. Toxicon Elsevier. 1985;23(6):887–93.

    Article  Google Scholar 

  • Gutiérrez J, Romero M, Díaz C, Borkow G, Ovadia M. Isolation and characterization of a metalloproteinase with weak hemorrhagic activity from the venom of the snake Bothrops asper (terciopelo). Toxicon [Internet]. 1995 [cited 1 Dec 2014];33(I):19–29. Available from http://www.sciencedirect.com/science/article/pii/004101019400138X

  • Gutiérrez JM, Rucavado A, Escalante T, Díaz C. Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage. Toxicon [Internet]. 2005 [cited 17 June 2014];45(8):997–1011. Available from http://www.ncbi.nlm.nih.gov/pubmed/15922771

    Google Scholar 

  • Han Y-P, Lu X-Y, Wang X-F, Xu J. Isolation and characterization of a novel P-II class snake venom metalloproteinase from Trimeresurus stejnegeri. Toxicon [Internet]. 2007 [cited 19 Aug 2014];49(7):889–98. Available from http://www.ncbi.nlm.nih.gov/pubmed/17403531

    Google Scholar 

  • Howes J-M, Kamiguti AS, Theakston RDG, Wilkinson MC, Laing GD. Effects of three novel metalloproteinases from the venom of the West African saw-scaled viper, Echis ocellatus on blood coagulation and platelets. Biochim Biophys Acta [Internet]. 2005 [cited 10 Sept 2014];1724(1–2):194–202. Available from http://www.ncbi.nlm.nih.gov/pubmed/15863354

    Google Scholar 

  • Hynes RO, Naba A. Overview of the matrisome – an inventory of extracellular matrix constituents and functions. Cold Spring Harb Perspect Biol [Internet]. 2012;4(1):a004903. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3249625&tool=pmcentrez&rendertype=abstract

  • Jia L, Shimokawa K, Bjarnason J, Fox J. Snake venom metalloproteinases: structure, function and relationship to the ADAMs family of proteins. Toxicon [Internet]. 1996 [cited 7 Mar 2014];34(1269):1269–76. Available from http://www.sciencedirect.com/science/article/pii/S0041010196001080

  • Jia LG, Wang X-M, Shannon JD, Bjarnason JB, Fox JW. Function of disintegrin-like/cysteine-rich domains of atrolysin A. Inhibition of platelet aggregation by recombinant protein and peptide antagonists. J Biol Chem. 1997;272(20):13094–102.

    Article  CAS  PubMed  Google Scholar 

  • Jia LG, Wang XM, Shannon JD, Bjarnason JB, Fox JW. Inhibition of platelet aggregation by the recombinant cysteine-rich domain of the hemorrhagic snake venom metalloproteinase, atrolysin A. Arch Biochem Biophys [Internet]. 2000;373(1):281–6. Available from http://www.ncbi.nlm.nih.gov/pubmed/10620350

    Google Scholar 

  • Jia Y, Lucena S, Jr EC, Sánchez E, Pérez J. cDNA cloning, expression and fibrin (ogen) olytic activity of two low-molecular weight snake venom metalloproteinases. Toxicon [Internet]. 2009 [cited 9 Sept 2014];54(3):233–43. Available from http://www.sciencedirect.com/science/article/pii/S0041010109002153

    Google Scholar 

  • Kamiguti AS, Slupsky JR, Zuzel M, Hay CR. Properties of fibrinogen cleaved by Jararhagin, a metalloproteinase from the venom of Bothrops jararaca. Thromb Haemost [Internet]. 1994 [cited 18 Aug 2014];72(2):244–9. Available from http://www.ncbi.nlm.nih.gov/pubmed/7831660

    Google Scholar 

  • Kamiguti A, Hay C, Zuzel M. Inhibition of collagen-induced platelet aggregation as the result of cleavage of alpha 2 beta 1-integrin by the snake venom metalloproteinase jararhagin. Biochem J. 1996;320:635–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamiguti AS, Gallagher P, Marcinkiewicz C, Theakston RDG, Zuzel M, Fox JW. Identification of sites in the cysteine-rich domain of the class P-III snake venom metalloproteinases responsible for inhibition of platelet function. FEBS Lett [Internet]. 2003 [cited 29 Oct 2014];549(1–3):129–34. Available from http://linkinghub.elsevier.com/retrieve/pii/S0014579303007993

    Google Scholar 

  • Kim J-S, Jin Y, Lemasters JJ. Reactive oxygen species, but not Ca2+ overloading, trigger pH- and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. Am J Physiol Heart Circ Physiol [Internet]. 2006 [cited 12 Nov 2014];290(5):H2024–34. Available from http://www.ncbi.nlm.nih.gov/pubmed/16399872

    Google Scholar 

  • Kleinman HK, Martin GR. Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol [Internet]. 2005[cited 18 July 2014];15(5):378–86. Available from http://www.ncbi.nlm.nih.gov/pubmed/15975825

    Google Scholar 

  • Kondo H, Kondo S, Ikezawa H, Murata R. Studies on the quantitative method for determination of hemorrhagic activity of Habu snake venom. Jpn J Med Sci Biol [Internet]. 1960 [cited 13 Aug 2014];13:43–52. Available from http://www.ncbi.nlm.nih.gov/pubmed/13853435

    Google Scholar 

  • Kroll M, Harris T, Moake J. von Willebrand factor binding to platelet Gplb initiates signals for platelet activation. J Clin … [Internet]. 1991 [cited 12 Dec 2014];88:1568–73. Available from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC295673/

    Google Scholar 

  • Kunitz M. Crystalline soybean trypsin inhibitor II. General properties. J Gen Physiol [Internet]. 1947 [cited 29 Oct 2014];291–310. Available from http://jgp.rupress.org/content/30/4/291.short

  • Kurtović T, Brgles M, Leonardi A, Balija ML, Križaj I, Allmaier G, et al. Ammodytagin, a heterodimeric metalloproteinase from Vipera ammodytes ammodytes venom with strong hemorrhagic activity. Toxicon [Internet]. 2011 [cited 10 Sept 2014];58(6–7):570–82. Available from http://www.ncbi.nlm.nih.gov/pubmed/21933678

    Google Scholar 

  • Leonardi A, Fox JW, Trampus-Bakija A, Krizaj I. Two coagulation factor X activators from Vipera a. ammodytes venom with potential to treat patients with dysfunctional factors IXa or VIIa. Toxicon [Internet]. 2008 [cited 10 Sept 2014];52(5):628–37. Available from http://www.ncbi.nlm.nih.gov/pubmed/18760294

  • Lomonte B, Lundgren J, Johansson B, Bagge U. The dynamics of local tissue damage induced by Bothrops asper snake venom and myotoxin II on the mouse cremaster muscle: an intravital and elecron microscopy study. Toxicon [Internet]. 1994 [cited 15 Dec 2014];41–55. Available from http://www.sciencedirect.com/science/article/pii/0041010194900205

  • Marcussi S, Bernardes CP, Santos-Filho NA, Mazzi MV, Oliveira CZ, Izidoro LFM, et al. Molecular and functional characterization of a new non-hemorrhagic metalloprotease from Bothrops jararacussu snake venom with antiplatelet activity. Peptides [Internet]. 2007 [cited 21 Aug 2014];28(12):2328–39. Available from http://www.ncbi.nlm.nih.gov/pubmed/18006118

    Google Scholar 

  • Markland F. Snake venom fibrinogenolytic and fibrinolytic enzymes: an updated inventory. Thromb Haemost [Internet]. 1998a [cited 29 Oct 2014];(ii). Available from http://th.schattauer.de/en/contents/archive/issue/911/manuscript/4463/download.html

  • Markland FS. Snake venoms and the hemostatic system. Toxicon. Elsevier; 1998b;36(12):1749–800.

    Google Scholar 

  • Marsh NA, Arocha-Piñango CL. Evaluation of the fibrin plate method for estimating plasminogen activators. Thromb Diath Haemorrh. 1972;28(1):75.

    CAS  PubMed  Google Scholar 

  • Mazzi M, Marcussi S, Carlos G. A new hemorrhagic metalloprotease from Bothrops jararacussu snake venom: isolation and biochemical characterization. Toxicon [Internet]. 2004 [cited 27 Oct 2012]; Available from http://www.sciencedirect.com/science/article/pii/S0041010104002405

  • Menezes MC, Paes Leme AF, Melo RL, Silva CA, Della Casa M, Bruni FM, et al. Activation of leukocyte rolling by the cysteine-rich domain and the hyper-variable region of HF3, a snake venom hemorrhagic metalloproteinase. FEBS Lett [Internet]. 2008 [cited 29 Apr 2014];582(28):3915–21. Available from http://www.ncbi.nlm.nih.gov/pubmed/18977230

    Google Scholar 

  • Mosesson MW. Fibrinogen and fibrin structure and functions. Journal of Thrombosis and Haemostasis. 2005(3);1894–904.

    Article  CAS  PubMed  Google Scholar 

  • Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of immunological methods. 1983;65:55–63.

    Article  CAS  PubMed  Google Scholar 

  • Moura-da-Silva A, Butera D, Tanjoni I. Importance of snake venom metalloproteinases in cell biology: effects on platelets, inflammatory and endothelial cells. Curr Pharm Des [Internet]. 2007 [cited 11 Nov 2014];13(28):2893–905. Available from http://www.eurekaselect.com/openurl/content.php?genre=article&issn=1381-6128&volume=13&issue=28&spage=2893

  • Osler W. On certain problems in the physiology of the blood corpuscles…. Br Med J [Internet]. 1886 [cited 30 Oct 2014];917–9. Available from http://scholar.google.com/scholar?hl=en&btnG=Search&q=intitle:On+certain+problems+in+the+physiology+of+the+blood+corpuscles.#0

  • Patiño AC, Pereañez JA, Núñez V, Benjumea DM, Fernandez M, Rucavado A, et al. Isolation and biological characterization of Batx-I, a weak hemorrhagic and fibrinogenolytic PI metalloproteinase from Colombian Bothrops atrox venom. Toxicon [Internet]. Elsevier Ltd. 2010 [cited 26 Apr 2012];56(6):936–43. Available from http://www.ncbi.nlm.nih.gov/pubmed/20600221

  • Punchard NA, Whelan CJ, Adcock I. J Inflamm (Lond) [Internet]. 2004 [cited 6 Dec 2014];1(1):1. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1074343&tool=pmcentrez&rendertype=abstract

  • Qianyun S, Min L, Fumei Y. Purification and characterization of a metalloproteinase with weak fibrinogenolytic activity from Naja atra venom. 2007 [cited 22 Dec 2014];835–43. Available from http://europepmc.org/abstract/CBA/645169

  • Rucavado A, Núñez J, Gutiérrez JM. Blister formation and skin damage induced by BaP1, a haemorrhagic metalloproteinase from the venom of the snake Bothrops asper. Int J Exp Pathol [Internet]. 1998 [cited 2 Dec 2014];79(4):245–54. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3230865&tool=pmcentrez&rendertype=abstract

  • Rucavado A, Flores-sa E, Gutie ÂM. Characterization of the local tissue damage induced by LHF-II, a metalloproteinase with weak hemorrhagic activity isolated from Lachesis muta muta snake venom. Toxicon. 1999;37:1297–312.

    Article  CAS  PubMed  Google Scholar 

  • Rucavado A, Escalante T, Teixeira CFP, Fernándes CM, Diaz C, Gutiérrez JM. Increments in cytokines and matrix metalloproteinases in skeletal muscle after injection of tissue-damaging toxins from the venom of the snake Bothrops asper. Mediators Inflamm [Internet]. 2002 [cited 2 Dec 2014];11(2):121–8. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1781651&tool=pmcentrez&rendertype=abstract

  • Sajevic T, Leonardi A, Križaj I. Haemostatically active proteins in snake venoms. Toxicon [Internet]. 2011 [cited 13 Oct 2014];57(5):627–45. Available from http://www.ncbi.nlm.nih.gov/pubmed/21277886

  • Sanchez EF, Gabriel LM, Gontijo S, Gremski LH, Veiga SS, Evangelista KS, et al. Structural and functional characterization of a P-III metalloproteinase, leucurolysin-B, from Bothrops leucurus venom. Arch Biochem Biophys [Internet]. 2007 [cited 10 Sept 2014];468(2):193–204. Available from http://www.ncbi.nlm.nih.gov/pubmed/17963685

    Google Scholar 

  • Sanchez EF, Schneider FS, Yarleque A, Borges MH, Richardson M, Figueiredo SG, et al. The novel metalloproteinase atroxlysin-I from Peruvian Bothrops atrox (Jergón) snake venom acts both on blood vessel ECM and platelets. Arch Biochem Biophys [Internet]. Elsevier Inc. 2010 [cited 9 Sept 2014];496(1):9–20. Available from http://www.ncbi.nlm.nih.gov/pubmed/20102699

  • Scott A. What is “inflammation”? Are we ready to move beyond Celsus? Br J Sports Med [Internet]. 2004 [cited 15 Dec 2014];38(3):248–9. Available from http://bjsm.bmj.com/cgi/doi/10.1136/bjsm.2003.011221

  • Serrano SMT, Wang D, Shannon JD, Pinto AFM, Polanowska-Grabowska RK, Fox JW. Interaction of the cysteine-rich domain of snake venom metalloproteinases with the A1 domain of von Willebrand factor promotes site-specific proteolysis of von Willebrand factor and inhibition of von Willebrand factor-mediated platelet aggregation. FEBS J [Internet]. 2007 [cited 16 Apr 2013];274(14):3611–21. Available from http://www.ncbi.nlm.nih.gov/pubmed/17578514

    Google Scholar 

  • Sharma JN, Samud AM, Asmawi MZ. Short communication comparison between plethysmometer and micrometer methods to measure acute paw oedema for screening anti-in è ammatory activity in mice. Inflammopharmacology. 2004;12(1):89–94.

    Article  CAS  PubMed  Google Scholar 

  • Shoibonov BB, Osipov AV, Kryukova EV, Zinchenko AA, Lakhtin VM, Tsetlin VI, et al. Oxiagin from the Naja oxiana cobra venom is the first reprolysin inhibiting the classical pathway of complement. Mol Immunol [Internet]. 2005 [cited 11 Sept 2014];42(10):1141–53. Available from http://www.ncbi.nlm.nih.gov/pubmed/15829304

    Google Scholar 

  • Sørensen B, Larsen OH, Rea CJ, Tang M, Foley JH, et al. Fibrinogen as a hemostatic agent. Seminars in Thrombosis and Hemostasis. 2012;1(212):268–73.

    Google Scholar 

  • Souza DHF, Iemma MRC, Ferreira LL, Faria JP, Oliva MLV, Zingali RB, et al. The disintegrin-like domain of the snake venom metalloprotease alternagin inhibits α2β1 integrin-mediated cell adhesion. Arch Biochem Biophys Elsevier. 2000;384(2):341–50.

    Article  CAS  Google Scholar 

  • Starke RD, Ferraro F, Paschalaki KE, Dryden NH, McKinnon TAJ, Sutton RE, et al. Endothelial von Willebrand factor regulates angiogenesis. Blood [Internet]. Am Soc Hematol. 2011[cited 11 Nov 2014];117(3):1071–80. Available from http://www.bloodjournal.org/content/117/3/1071.abstract

    Google Scholar 

  • Sun Q-Y, Bao J. Purification, cloning and characterization of a metalloproteinase from Naja atra venom. Toxicon [Internet]. Elsevier Ltd. 2010 [cited 24 July 2014];56(8):1459–69. Available from http://www.ncbi.nlm.nih.gov/pubmed/20837040

  • Suntravat M, Jia Y, Lucena SE, Sánchez EE, Pérez JC. cDNA cloning of a snake venom metalloproteinase from the eastern diamondback rattlesnake (Crotalus adamanteus), and the expression of its disintegrin domain with anti-platelet effects. Toxicon [Internet]. 2013;64:43–54. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3570744&tool=pmcentrez&rendertype=abstract

  • Tanjoni I, Weinlich R, Della-Casa MS, Clissa PB, Saldanha-Gama RF, de Freitas MS, et al. Jararhagin, a snake venom metalloproteinase, induces a specialized form of apoptosis (anoikis) selective to endothelial cells. Apoptosis [Internet]. 2005;10(4):851–61. Available from http://www.ncbi.nlm.nih.gov/pubmed/16133875

    Google Scholar 

  • Tanjoni I, Evangelista K, Della-Casa MS, Butera D, Magalhães GS, Baldo C, et al. Different regions of the class P-III snake venom metalloproteinase jararhagin are involved in binding to alpha2beta1 integrin and collagen. Toxicon [Internet]. 2010 [cited 29 Apr 2014];55(6):1093–9. Available from http://www.ncbi.nlm.nih.gov/pubmed/20056118

  • Teixeira C, Fernandes C, Zuliani J, Zamuner S. Inflammatory effects of snake venom metalloproteinases. Memórias do Inst … [Internet]. 2005 [cited 1 Dec 2014];100:181–4. Available from http://www.scielo.br/scielo.php?pid=S0074-02762005000900031&script=sci_arttext

  • Teklemariam T, Seoane AI, Ramos CJ, Sanchez EE, Lucena SE, Perez JC, et al. Functional analysis of a recombinant PIII-SVMP, GST-acocostatin; an apoptotic inducer of HUVEC and HeLa, but not SK-Mel-28 cells. Toxicon [Internet]. Elsevier Ltd. 2011 [cited 29 Apr 2014];57(5):646–56. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3073737&tool=pmcentrez&rendertype=abstract

  • Teng CM, Huang TF. Inventory of exogenous inhibitors of platelet aggregation. For the Subcommittee on Nomenclature of Exogenous Hemostatic Factors of the Scientific and Standardization Committee of the International Society on Thrombosis and Haemostasis. Thromb Haemost [Internet]. 1991 [cited 31 Oct 2014];65(5):624–6. Available from http://www.ncbi.nlm.nih.gov/pubmed/1871725

    Google Scholar 

  • Torres-Huaco FD, Ponce-Soto LA, Martins-de-Souza D, Marangoni S. Purification and characterization of a new weak hemorrhagic metalloproteinase BmHF-1 from Bothrops marajoensis snake venom. Protein J [Internet]. 2010 [cited 9 Sept 2014];29(6):407–16. Available from http://www.ncbi.nlm.nih.gov/pubmed/20607373

    Google Scholar 

  • Trummal K, Tõnismägi K, Siigur E, Aaspõllu A, Lopp A, Sillat T, et al. A novel metalloprotease from Vipera lebetina venom induces human endothelial cell apoptosis. Toxicon [Internet]. 2005 [cited 10 Sept 2014];46(1):46–61. Available from http://www.ncbi.nlm.nih.gov/pubmed/15922394

    Google Scholar 

  • Tu AT. Overview of Snake Venom Chemistry, Nature toxins, vol. 2. Berlin: Springer US; 1996. p. 37–62.

    Google Scholar 

  • Wagner DD. Cell biology of von Willebrand factor. Annu Rev Cell Biol [Internet]. 1990 [cited 25 Nov 2014];6:217–46. Available from http://www.ncbi.nlm.nih.gov/pubmed/2275814

    Google Scholar 

  • Wahby AF, Abdel-Aty AM, El-Kady EM. Purification of hemorrhagic SVMPs from venoms of three vipers of Egypt. Toxicon [Internet]. Elsevier Ltd. 2012 [cited 9 May 2014];59(2):329–37. Available from http://www.ncbi.nlm.nih.gov/pubmed/22138485

  • Wan S-G, Jin Y, Lee W-H, Zhang Y. A snake venom metalloproteinase that inhibited cell proliferation and induced morphological changes of ECV304 cells. Toxicon [Internet]. 2006 [cited 10 Sept 2014];47(4):480–9. Available from http://www.ncbi.nlm.nih.gov/pubmed/16487560

  • Wang W-J. Purification and functional characterization of AAV1, a novel P-III metalloproteinase, from Formosan Agkistrodon acutus venom. Biochimie [Internet]. 2007 [cited 11 Sept 2014];89(1):105–15. Available from http://www.ncbi.nlm.nih.gov/pubmed/17029743

  • Wang W-J, Shih C-H, Huang T-F. A novel P-I class metalloproteinase with broad substrate-cleaving activity, agkislysin, from Agkistrodon acutus venom. Biochem Biophys Res Commun [Internet]. 2004 [cited 29 Oct 2014];324(1):224–30. Available from http://www.ncbi.nlm.nih.gov/pubmed/15465006

    Google Scholar 

  • Warrell DA. Snake bite. Lancet [Internet]. Elsevier Ltd. 2010 [cited 27 Oct 2014];375(9708):77–88. Available from http://www.ncbi.nlm.nih.gov/pubmed/20109866

    Google Scholar 

  • Wei J-F, Mo Y-Z, Qiao L-Y, Wei X-L, Chen H-Q, Xie H, et al. Potent histamine-releasing activity of atrahagin, a novel snake venom metalloproteinase. Int J Biochem Cell Biol [Internet]. 2006 [cited 10 Sept 2014];38(4):510–20. Available from http://www.ncbi.nlm.nih.gov/pubmed/16310401

    Google Scholar 

  • White J. Snake venoms and coagulopathy. Toxicon [Internet]. 2005 [cited 13 Oct 2014];45(8):951–67. Available from http://www.ncbi.nlm.nih.gov/pubmed/15922768

    Google Scholar 

  • Whittaker CA, Hynes RO. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell [Internet]. 2002 [cited 30 Nov 2014];13(10):3369–87. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=129952&tool=pmcentrez&rendertype=abstract

  • Yamashita KM, Alves AF, Barbaro KC, Santoro ML. Bothrops jararaca venom metalloproteinases are essential for coagulopathy and increase plasma tissue factor levels during envenomation. PLoS Negl Trop Dis [Internet]. 2014 [cited 28 July 2014];8(5):e2814. Available from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4022520&tool=pmcentrez&rendertype=abstract

  • Ye Q, Sun Q, Li M. Inflammatory mediators releasing and apotosis of endothelial cell induced by cobra venom metalloproteinase atrase A. Chinese Pharmacol Bull. 2009;8:6.

    Google Scholar 

  • Yeh C, Peng H, Yang R, Huang T (2001) Rhodostomin, a snake venom disintegrin, inhibits angiogenesis elicited by basic fibroblast growth factor and suppresses tumor growth by a selective α(v) β(3) blockade of endothelial cells. Molecular pharmacology. 2001;59(5):1333–42.

    CAS  PubMed  Google Scholar 

  • Zhou Y-F, Eng ET, Zhu J, Lu C, Walz T, Springer TA. Sequence and structure relationships within von Willebrand factor. Blood. 2012;120(2):449–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Immunology and Cancer Biology, University of Virginia School of Medicine, Charlottesville, VA, 434-924-0050, USA

    Jéssica K. A. Macêdo & Jay W. Fox

  2. Department of Cell Biology, Institute of Biology, Brazilian Center for Protein Research, University of Brasília, 70910-900, Brasília, DF, Brazil

    Jéssica K. A. Macêdo

Authors
  1. Jéssica K. A. Macêdo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jay W. Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jay W. Fox .

Editor information

Editors and Affiliations

  1. Venom and Toxin Research Programme, Department of Anatomy, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore

    P. Gopalakrishnakone

  2. Structural and Functional Venomics Lab, Instituto de Biomedicina de Valencia (CSIC), Valencia, Spain

    Juan J. Calvete

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Dordrecht

About this entry

Cite this entry

Macêdo, J.K.A., Fox, J.W. (2016). Biological Activities and Assays of the Snake Venom Metalloproteinases (SVMPs). In: Gopalakrishnakone, P., Calvete, J. (eds) Venom Genomics and Proteomics. Toxinology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6416-3_21

Download citation

Publish with us

Policies and ethics

Search

Navigation