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Inhibitory effect of the red seaweed Plocamium brasiliense against the toxic effects of Lachesis muta snake venom

  • IV Latin American Congress of Algae Biotechnology (CLABA) and IV Redealgas Workshop
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Abstract

The ability of extracts and fractions of the red seaweed Plocamium brasiliense to inhibit hemorrhagic, edematogenic, hemolytic, clotting and proteolytic activities of Lachesis muta snake venom was analyzed. In Brazil, snakebites by L. muta are low (2 %) when compared to Bothrops genus (90 %); however, their lethality indexes are three times higher than Bothrops. Envenomation by L. muta venom results in hemorrhage, pain, necrosis, hemolysis, myotoxicity, and death. Since antivenom does not efficiently neutralize local effects, a large number of researchers have attempted to identify molecule(s) from natural sources to inhibit such activities to use them as an alternative treatment for snakebite. We tested four extracts of seaweed P. brasiliense obtained with solvents of increasing polarities: n-hexane (HEX), dichloromethane (DCM), ethyl acetate (ACE), and hydroalcohol (HYD). Extracts of alga or fractions were incubated with L. muta venom, and then, biological assays were performed. The extracts, except the HYD, inhibited all the assays but with different potencies. The DCM extract fully inhibited all activities. Moreover, DCM and HEX extracts inhibited hemolysis induced by a phospholipase A2 isolated from L. muta venom (LM-PLA2-I). A fraction from HEX enriched in cholesterol isolated from HEX extract inhibited proteolysis by L. muta venom and hemolysis by LM-PLA2-I; in contrast, monoterpenes isolated from DCM extract did not inhibit both activities. Seaweeds may be a promising source of natural inhibitors of the toxic effects caused by snakebite by L. muta venom, and they may be used to develop new strategies for antivenom treatment.

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References

  • Arruda EZ, Silva NM, Moraes RA, Melo PA (2002) Effect of suramin on myotoxicity of some crotalid snake venoms. Braz J Med Biol Res 35:723–736

    Article  PubMed  CAS  Google Scholar 

  • Cardoso JLC, França FOS, Wen FH, Málaque SA, Haddad VJ (2003) Animais peçonhentos no Brasil; Biologia, Clínica e Terapêutica dos acidentes ofídicos. Editora Sarvier, São Paulo

    Google Scholar 

  • Chippaux JP (1988) Snake-bites: appraisal of the global situation. Bull World Health Organ 76:515–524

    Google Scholar 

  • Cirne-Santos CC, Souza TM, Teixeira VL, Fontes CF, Rebello MA, Castello-Branco LR, Abreu CM, Tanuri A, Frugulhetti IC, Bou-Habib DC (2008) The dolabellane diterpene dolabelladienetriol is a typical noncompetitive inhibitor of HIV-1 reverse transcriptase enzyme. Antivir Res 77:64–71

    Article  PubMed  CAS  Google Scholar 

  • Coe FG, Anderson GJ (2005) Snakebite ethnopharmacopoeia of eastern Nicaragua. J Ethnopharmacol 96:303–323

    Article  PubMed  Google Scholar 

  • da Silva NM, Arruda EZ, Murakami YL, Moraes RA, El-Kik CZ, Tomaz MA, Fernandes FF, Oliveira CZ, Soares AM, Giglio JR, Melo PA (2007) Evaluation of three Brazilian antivenom ability to antagonize myonecrosis and hemorrhage induced by Bothrops snake venoms in a mouse model. Toxicon 50:196–205

    Article  PubMed  Google Scholar 

  • de Andrade Moura L, Bianco EM, Pereira RC, Teixeira VL, Fuly AL (2011a) Anticoagulation and antiplatelet effects of a dolastane diterpene isolated from the marine brown alga Canistrocarpus cervicornis. J Thromb Thrombolysis 31:235–240

    Article  PubMed  CAS  Google Scholar 

  • de Andrade Moura L, Ortiz-Ramirez FA, Cavalcanti DN, Ribeiro SM, Muricy G, Teixeira VL, Fuly AL (2011b) Evaluation of marine brown algae and sponges from Brazil as anticoagulant and antiplatelet products. Mar Drugs 9:1346–1358

    Article  PubMed  PubMed Central  Google Scholar 

  • de Paula RC, Castro HC, Rodrigues CR, Melo PA, Fuly AL (2009) Structural and pharmacological features of phospholipases A2 from snake venoms. Protein Pept Lett 16:899–907

    Article  PubMed  Google Scholar 

  • Domingos TFS, Vallim MA, Carvalho C, Sanchez EF, Teixeira VL, Fuly AL (2011) Anti-snake venom effect of secodolastane diterpenes isolated from Brazilian marine brown alga Canistrocarpus cervicornis against Lachesis muta venom. Braz J Pharm 2:234–238

    Google Scholar 

  • Domingos TFS, Ortiz-Ramirez FA, Villaça RC, Cavalcanti DN, Sanchez EF, Teixeira VL, Fuly AL (2012) Inhibitory effect of a Brazilian marine brown alga Spatoglossum schröederi upon biological activities of Lachesis muta snake venom. Braz J Pharm 4:741–747

    Google Scholar 

  • Ferreira T, Camargo EA, Ribela MT, Damico DC, Marangoni S, Antunes E, De Nucci G, Landucci EC (2009) Inflammatory oedema induced by L. muta muta (Surucucu) venom and LmTX-I in the rat paw and dorsal skin. Toxicon 53:69–77

    Article  PubMed  CAS  Google Scholar 

  • Ferreira WJ, Amaro R, Cavalcanti DN, de Rezende CM, da Silva VA, Barbosa JE, Paixão IC, Teixeira VL (2010) Antiherpetic activities of chemical components from the Brazilian red alga Plocamium brasiliense. Nat Prod Commun 5:1167–1170

    PubMed  CAS  Google Scholar 

  • Fonseca RR, Ortiz-Ramírez FA, Cavalcanti DN, Ramos CJB, Teixeira VL, Souza Filho APS (2012) Allelopathic potential of extracts from marine macroalga Plocamium brasiliense and their effects on pasture weed. Braz J Pharm 22:850–853

    Google Scholar 

  • Fuly AL, Francischetti IM, Zingali RB, Carlini CR (1993) Partial purification and some physicochemical properties of phospholipases A2 from the venom of the bushmaster snake (Lachesis muta). Braz J Med Biol Res 5:459–463

    Google Scholar 

  • Fuly AL, Machado OL, Alves EW, Carlini CR (1997) Mechanism of inhibitory action on platelet activation of a phospholipase A2 isolated from Lachesis muta (Bushmaster) snake venom. Thromb Haemost 78:1372–1380

    PubMed  CAS  Google Scholar 

  • Fuly AL, de Miranda AL, Zingali RB, Guimarães JA (2002) Purification and characterization of a phospholipase A2 isoenzyme isolated from Lachesis muta snake venom. Biochem Pharmacol 63:1589–1597

    Article  PubMed  CAS  Google Scholar 

  • Garcia ES, Guimarães JA, Prado JL (1978) Purification and characterization of a sulfhydryl-dependent protease from Rhodnius prolixus midgut. Arch Biochem Biophys 2:315–322

    Google Scholar 

  • González del Val A, Platas G, Basilio A, Cabello A, Gorrochategui J, Suay I, Vicente F, Portillo E, Jiménez del Río M, Reina GG, Peláez F (2011) Screening of antimicrobial activities in red, green and brown macroalgae from Gran Canaria (Canary Islands, Spain). Int Microbiol 4:35–40

    Google Scholar 

  • Gressler V, Fujii MT, Martins AP, Colepicolo P, Mancini-Filho J, Pinto E (2011) Biochemical composition of two red seaweed species grown on the Brazilian coast. J Sci Food Agric 91:1687–1692

    Article  PubMed  CAS  Google Scholar 

  • Gutiérrez JM, Ownby CL (2003) Skeletal muscle degeneration induced by venom phospholipases A2: insights into the mechanisms of local and systemic myotoxicity. Toxicon 42:915–931

    Article  PubMed  Google Scholar 

  • Gutiérrez JM, Lomonte B, León G, Alape-Girón A, Flores-Díaz M, Sanz L, Ângulo Y, Calvete JJ (2009) Snake venomics and antivenomics: proteomic tools in the design and control of antivenoms for the treatment of snakebite envenoming. J Proteome 72:165–182

    Article  Google Scholar 

  • Havsteen B (1983) Flavonoids, a class of natural products of high pharmacological potency. Biochem Pharmacol 32:1141–1148

    Article  PubMed  CAS  Google Scholar 

  • Jorge MT, Sano Martins SI, Tomy SC, Castro SC, Ferrari RA, Ribeiro LA, Warrell DA (1997) Snake bite by the bushmaster (Lachesis muta) in Brazil: case report and review of the literature. Toxicon 35:545–554

    Article  PubMed  CAS  Google Scholar 

  • Kini RM (2003) Excitement ahead: structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon 42:827–840

    Article  PubMed  CAS  Google Scholar 

  • Kini RM (2006) Anticoagulant proteins from snake venoms: structure, function and mechanism. Biochem J 397:377–387

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kladi M, Vagias C, Roussis V (2004) Volatile halogenated metabolites from marine red algae. Phytochem Rev 3:337–366

    Article  CAS  Google Scholar 

  • Kondo H, Kondo S, Ikezawa H, Murata R (1960) Studies on the quantitative methods for determination of hemorrhagic activity of Habu snake venom. Jpn J Med Sci Biol 13:43–52

    Article  PubMed  CAS  Google Scholar 

  • Magalhães A, Monteiro MR, Magalhães HPB, Mares-Guia M, Rogana E (1997) Thrombin-like enzyme from Lachesis muta muta venom: isolation and topographical analysis of its active site structure by means of the binding of amidines and guanidines as competitive inhibitors. Toxicon 35:1549–1559

    Article  PubMed  Google Scholar 

  • Markland FS (1998) Snake venoms and the hemostatic system. Toxicon 12:1749–1800

    Article  Google Scholar 

  • Martz W (1992) Plants with a reputation against snakebite. Toxicon 30:1131–1142

    Article  PubMed  CAS  Google Scholar 

  • Melo PA, do Nascimento MC, Mors WB, Suarez-Kurtz G (1994) Inhibition of the myotoxic and hemorrhagic activities of crotalid venoms by Eclipta prostrata (Asteraceae) extracts and constituents. Toxicon 32:595–603

    Article  PubMed  CAS  Google Scholar 

  • Mors WB, Nascimento MC, Pereira BM, Pereira NA (2000) Plant natural products active against snake bite—the molecular approach. Phytochemistry 55:627–642

    Article  PubMed  CAS  Google Scholar 

  • MS (Ministério da Saúde) / Funasa (Fundação Nacional de Saúde) (2001) Manual de Diagnóstico e Tratamento de Acidentes por Animais Peçonhentos. MS/Funasa, Brasília

    Google Scholar 

  • Murakami MT, Arruda EZ, Melo PA, Martinez AB, Calil-Eliás S, Tomaz MA, Lomonte B, Gutiérrez JM, Arni RK (2005) Inhibition of myotoxic activity of Bothrops asper myotoxin II by the anti-trypanosomal drug suramin. J Mol Biol 350:416–426

    Article  PubMed  CAS  Google Scholar 

  • Nikai T, Mori N, Kishyda M, Sugihara H, Tu AT (1984) Isolation and biochemical characterization of hemorrhagic toxin f from the venom of Crotalus atrox (western diamondback rattlesnake). Arch Biochem Biophys 2:309–319

    Article  Google Scholar 

  • Owuor BO, Kisangau DP (2006) Kenyan medicinal plants used as antivenin: a comparison of plant usage. J Ethnobiol Ethnomed 2:1–8

    Article  Google Scholar 

  • Pereira RC, Pinheiro MD, Teixeira VL, da Gama BA (2010) Feeding preferences of the endemic gastropod Astraea latispina in relation to chemical defenses of Brazilian tropical seaweeds. Braz J Biol 62:33–40

    Google Scholar 

  • Picolo G, Chacur M, Gutiérrez JM, Teixeira CFP, Cury Y (2002) Evaluation of antivenoms in the neutralization of hyperalgesia and edema induced by Bothrops jararaca and Bothrops asper snake venoms. Braz J Med Biol Res 35:1221–1228

    Article  PubMed  CAS  Google Scholar 

  • Rocha HA, Moraes FA, Trindade ES, Franco CR, Torquato RJ, Veiga SS, Valente AP, Mourão PA, Leite EL, Nader HB, Dietrich CP (2005) Structural and hemostatic activities of a sulfated galactofucan from the brown alga Spatoglossum schroederi. An ideal antithrombotic agent? J Biol Chem 280:41278–41288

    Article  PubMed  CAS  Google Scholar 

  • Rocha FD, Soares AR, Houghton PJ, Pereira RC, Kaplan MA, Teixeira VL (2007) Potential cytotoxic activity of some Brazilian seaweeds on human melanoma cells. Phytother Res 21:170–175

    Article  PubMed  Google Scholar 

  • Rucavado A, Sanchez EF, Franceschi A, Magalhães A, Gutiérrez JM (1999) Characterization of the local tissue damage induced by LHF-II, a metalloproteinase with weak hemorrhagic activity isolated from Lachesis muta muta snake venom. Toxicon 37:1297–1312

    Article  PubMed  CAS  Google Scholar 

  • Sakata K, Iwase Y, Ina K, Fujita D (1991) Chemical studies on feeding inhibitors for marine herbivores. 2. Halogenated terpenes isolated from the red alga Plocamium leptophyllum as feeding inhibitors for marine herbivores. Nippon Suisan Gakkaishi 57:743–746

    Google Scholar 

  • Saunders GW, Lehmkuhl KV (2005) Molecular divergence and morphological diversity among four cryptic species of Plocamium (Plocamiales, Florideophyceae) in northern Europe. Eur J Phycol 40:293–312

    Article  CAS  Google Scholar 

  • Selvanayagam ZE, Gnanavendhan SG, Balakrishna K, Rao RB, Sivaraman J, Subramanian K, Puri R, Puri RK (1996) Ehretian one, a novel quinonoid xanthene from Ehretia buxifolia with antisnake venom activity. J Nat Prod 59:664–667

    Article  PubMed  CAS  Google Scholar 

  • Soares AM, Januario AH, Lourenco MV, Pereira AM, Pereira OS (2004) Neutralizing effects of Brazilian plants against snake venoms. Drugs Future 29:1105–1117

    Article  CAS  Google Scholar 

  • Soares AM, Ticli FK, Marcussi S, Lourenço MV, Januário AH, Sampaio SV, Giglio JR, Lomonte B, Pereira PS (2005) Medicinal plants with inhibitory properties against snake venoms. Curr Med Chem 12:2625–2641

    Article  PubMed  CAS  Google Scholar 

  • Swaroop S, Grab B (1954) Snakebite mortality in the world. Bull World Health Organ 10:35–76

    PubMed  CAS  PubMed Central  Google Scholar 

  • Teixeira VL (2009) Produtos Naturais Marinhos. In: Pereira RC, Soares-Gomes A (eds) Biologia Marinha. Interciência, Rio de Janeiro, pp 443–471

    Google Scholar 

  • Theakston RDG, Reid HA (1983) Development of simple standard assay procedures for the characterization of snake venom. Bull World Health Organ 61:949–956

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ticli FK, Hage LI, Cambraia RS, Pereira PS, Magro AJ, Fontes MR, Stábeli RG, Giglio JR, França SC, Soares AM, Sampaio SV (2005) Rosmarinic acid, a new snake venom phospholipase A2 inhibitor from Cordia verbenacea (Boraginaceae): antiserum action potentiation and molecular interaction. Toxicon 46:318–327

    Article  PubMed  CAS  Google Scholar 

  • Vasconcelos MA, Ferreira WJ, Pereira RC, Cavalcanti DN, Teixeira VL (2010) Chemical constituents from the red alga Plocamium brasiliense (Greville) M. Howe and W.R. Taylor. Biochem Syst Ecol 38:119–121

    Article  CAS  Google Scholar 

  • Veronese EL, Esmeraldino LE, Trombone AP, Santana AE, Bechara GH, Kettelhut I, Cintra AC, Giglio JR, Sampaio SV (2005) Inhibition of the myotoxic activity of Bothrops jararacussu venom and its two major myotoxins, BthTX-I and BthTX-II, by the aqueous extract of Tabernaemontana catharinensis A. DC. (Apocynaceae). Phytomedicine 12:123–130

    Article  PubMed  CAS  Google Scholar 

  • Warrell DA (1992) The global problem of snakebite: its prevention and treatment. In: Gopalakrishnakone P, Tu CK (eds) Recent advances in toxinology research. National University of Singapore, Singapore, pp 1–13

    Google Scholar 

  • Yamakawa M, Nozaki M, Hokama Z (1976) Fractionation of Sakishima habu (Trimeresurus elegans) venom and lethal hemorrhagic and edema forming activities of the fractions. In: Ohsaka A, Hayashi K, Sawai Y (eds) Animal, plant and microbial toxins. Biochemistry, New York, pp 97–109

    Chapter  Google Scholar 

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Acknowledgement

This work was supported by the International Foundation for Science (IFS-Grant F/4571-1), FAPERJ, CNPq, CAPES, and UFF/PROPPi.

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Authors and Affiliations

  1. Department of Cellular and Molecular Biology, Institute of Biology, Federal University Fluminense, Outeiro de São João Batista, s/n, 3º andar, sala 310, Niterói, RJ, 24220-008, Brazil

    Mariana Moreira Claudino, Thaisa Francielle Souza Domingos, Geisiane Alves da Silva & André Lopes Fuly

  2. Department of Marine Biology, Institute of Biology, Federal University Fluminense, Niterói, RJ, 24220-008, Brazil

    Rainiomar Raimundo Fonseca, Diana Negrão Cavalcanti & Valéria Laneuville Teixeira

  3. Department of Organic Chemistry, Institute of Chemistry, Federal University Fluminense, Niterói, RJ, 24220-008, Brazil

    Rainiomar Raimundo Fonseca

  4. Laboratory of Biochemistry of Proteins from Animal Venoms, Research and Development Center, Ezequiel Dias Foundation, Belo Horizonte, MG, 30510-010, Brazil

    Eladio Flores Sanchez

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  1. Mariana Moreira Claudino
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  2. Thaisa Francielle Souza Domingos
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Correspondence to André Lopes Fuly.

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Claudino, M.M., Domingos, T.F.S., da Silva, G.A. et al. Inhibitory effect of the red seaweed Plocamium brasiliense against the toxic effects of Lachesis muta snake venom. J Appl Phycol 26, 2047–2054 (2014). https://doi.org/10.1007/s10811-014-0266-x

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