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Potential utilization of a lambda carrageenan polysaccharide, derived from a cultivated, clonal strain of the red seaweed Chondrus crispus (Irish moss) against toxic actions of venom of Bothrops jararaca and B. jararacussu snakes

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Abstract

Snakebites are a serious occupational problem affecting rural populations of tropical and sub-tropical, developing countries. Envenomation caused by the snakes Bothrops jararaca and B. jararacussu is characterized by local pain, edema, hemorrhage, tissue necrosis, and death. Despite the fact that antivenom may prevent the death of bite victims, treatment does not prevent tissue necrosis, often leading to amputation or deformity of the victim’s affected limb.Therefore, more efficient therapies need to be investigated. In this work, we tested the ability of a carrageenan galactan polysaccharide, isolated from a clonal strain of the red alga, Chondrus crispus (commonly known as Irish moss) to inhibit toxic, in vitro (coagulation, hemolytic and proteolytic) or in vivo (hemorrhagic, edematogenic, myotoxic and lethal) activities of B. jararaca or B. jararacussu venom. When the polysaccharide was mixed together with the venoms, inhibition of their toxic activities was achieved, but with different potencies. Moreover, inhibition of hemorrhage, edema, lethality, or myotoxicity was observed, even if the polysaccharide was injected before or after the injection of venoms, regardless of the route of administration (i.e., intravenous, subcutaneous, and intraperitoneal). A gel formulation containing the polysaccharide of C. crispus also protected mice from hemorrhage after administration of the venoms. Thus, the lambda carrageenan polysaccharide, as produced by a strain of C. crispus, may aid antivenom to block the toxic activities of B. jararaca and B. jararacussu venom, as well as to aid in the development of a more efficient therapy for envenomation by these venomous snakes.

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References

  • Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335

  • Brasil (2010) Farmacopeia Brasileira. Anvisa, Brasília

    Google Scholar 

  • Cabrita MT, Vale C, Rauter AP (2010) Halogenated compounds from marine algae. Molecules 8:2301–2317

    CAS  Google Scholar 

  • Cao S, He X, Qin L, He M, Yang Y, Liu Z, Mao W (2019) Anticoagulant and antithrombotic properties in vitro and in vivo of a novel sulfated polysaccharide from marine green alga Monostroma nitidum. Mar Drugs 17:247–268

    CAS  PubMed Central  Google Scholar 

  • Cardoso MA, Noseda MD, Fujii MT, Zibetti RGM, Duarte MER (2007) Sulfated xylomannans isolated from red seaweeds Chondrophycus papillosus and C. flagelliferus (Ceramiales) from Brazil. Carbohydr Res 342:2766–2775

    CAS  PubMed  Google Scholar 

  • Craigie JS, Cornish ML, Deveau LE (2019) Commercialization of Irish moss aquaculture: the Canadian experience. Bot Mar 62:411–432

    Google Scholar 

  • da Silva AC, Ferreira LG, Duarte ME, Noseda MD, Sanchez EF, Fuly AL (2015) Sulfated galactan from Palisada flagellifera inhibits toxic effects of Lachesis muta snake venom. Mar Drugs 13:3761–3775

    PubMed  PubMed Central  Google Scholar 

  • da Silva AC, Ferreira LG, Duarte ME, Fujii MT, Sanchez EF, Noseda M, Fuly AL (2016) Protective effect of the sulfated agaran isolated from the red seaweed Laurencia aldingensis against toxic effects of the venom of the snake, Lachesis muta. Mar Biotechnol 18:619–629

    Google Scholar 

  • Duarte MER, Cauduro JP, Noseda DG, Noseda MD, Gonçalves AG, Pujol CA, Damonte EB, Cerezo AS (2004) The structure of the agaran sulfate from Acanthophora spicifera (Rhodomelaceae, Ceramiales) and its antiviral activity. Relation between structure and antiviral activity in agarans. Carbohydr Res 339:335–347

    CAS  PubMed  Google Scholar 

  • Fry BG (2018) Snakebite: when the human touch becomes a bad touch. Toxins 10:170–194

    PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Ganesan P, Noda K, Manabe Y, Ohkubo T, Tanaka Y, Maoka T, Sugawara T, Hirata T (2011) Siphonaxanthin, a marine carotenoid from green algae, effectively induces apoptosis in human leucemia (HL-60) cells. Biochim Biophys Acta 1810:497–503

    CAS  PubMed  Google Scholar 

  • Garcia ES, Guimarães JA, Prado JL (1978) Purification and characterization of a sulfhydryl-dependent protease from Rhodnius prolixus midgut. Arch Biochem Biophys 188:315–322

    CAS  PubMed  Google Scholar 

  • Gutiérrez JM, Rucavado A, Escalante T, Díaz C (2005) Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage. Toxicon 45:997–1011

    PubMed  Google Scholar 

  • Gutiérrez JM, Fan HW, Silvera CL, Ângulo Y (2009) Stability, distribution and use of antivenoms for snakebite envenomation in Latin America: report of a workshop. Toxicon 53:625–630

    PubMed  Google Scholar 

  • Gutiérrez JM, Leon G, Burnouf T (2011) Antivenoms for the treatment of snakebite envenomings: the road ahead. Biologicals 39:129–142

    PubMed  Google Scholar 

  • Hafting JT, Critchley AT, Cornish ML, Hubley SA, Archibald AF (2012) On-land cultivation of functional seaweed products for human usage. J Appl Phycol 24:385–392

    Google Scholar 

  • Hafting JT, Craigie JS, Stengel DBD, Loureiro RR, Buschmann AH, Yarish C, Edwards MD, Critchley AT (2015) Prospects and challenges for industrial production of seaweed bioactives. J Phycol 51:821–837

    CAS  PubMed  Google Scholar 

  • Halling C, Wikstrom SA, Lillieskold-Sjoo G, Mork E, Lundsor E, Zuccarello GC (2013) Introduction of Asian strains and low genetic variation in farmed seaweeds: indications for new management practices. J Appl Phycol 25:89–95

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kulshreshtha G, Burlot SA, Marty C, Critchley A, Hafting J, Bedoux G, Bourgougnon N, Prithiviraj B (2015) Enzyme-assisted extraction of bioactive material from Chondrus crispus and Codium fragile and its effect on Herpes simplex virus (HSV-1). Mar Drugs 13:558–580

    PubMed  PubMed Central  Google Scholar 

  • Liu Y, Liu C, Tan H, Zhao T, Cao J, Wang F (2009) Sulfation of a polysaccharide obtained from Phellinus ribis and potential biological activities of the sulfated derivatives. Carbohydr Polym 77:370–375

    CAS  Google Scholar 

  • Luna KPO, da Silva MB, Pereira VRA (2011) Clinical and immunological aspects of envenomations by Bothrops snakes. J Venom Anim Toxins Incl Trop Dis 17:130–141

    Google Scholar 

  • Melo PA, Suarez-Kurtz G (1988) Release of sarcoplasmic enzymes from skeletal muscle by Bothrops jararacussu venom: antagonism by heparin and by the serum of South American marsupials. Toxicon 26:87–95

    CAS  PubMed  Google Scholar 

  • Mourão PA (2015) Perspective on the use of sulfated polysaccharides from marine organisms as a source of new antithrombotic drugs. Mar Drugs 13:2770–2784

    PubMed  PubMed Central  Google Scholar 

  • Otero R, Gutiérrez JM, Beatriz MM, Duque E, Rodríguez O, Luis Arango J, Gómez F, Toro A, Cano F, María Rodríguez L, Caro E, Martínez J, Cornejo W, Mariano Gómez L, Luis Uribe F, Cárdenas S, Núñez V, Díaz A (2002) Complications of Bothrops, Porthidium, and Bothriechis snakebites in Colombia. A clinical and epidemiological study of 39 cases attended in a university hospital. Toxicon 40:1107–1114

    CAS  PubMed  Google Scholar 

  • Pengzhan Y, Ning L, Xiguang L, Gefei Z, Quanbin Z, Pengcheng L (2003) Antihyperlipidemic effects of different molecular weight sulfated polysaccharides from Ulva pertusa (Chlorophyta). Pharmacol Res 48:543–549

    PubMed  Google Scholar 

  • Pereira L, Critchley AT, Amado AM, Ribeiro-Claro PJA (2009) A comparative analysis of phycocolloids produced by underutilized versus industrially utilized carrageenophytes (Gigartinales, Rhodophyta). J Appl Phycol 21:599–605

    CAS  Google Scholar 

  • Pereira L, Gheda SF, Ribeiro-Claro PJA (2013) Analysis by vibrational spectroscopy of seaweed polysaccharides with potential use in food, pharmaceutical, and cosmetic industries. Int J Carbohydr Chem 537202:1–7

    Google Scholar 

  • Queiroz GP, Pessoa LA, Portaro FC, de Furtado F, Tambourgi DV (2008) Interspecific variation in venom composition and toxicity of Brazilian snakes from Bothrops genus. Toxicon 52:842–851

    CAS  PubMed  Google Scholar 

  • Roriz KRPS, Zaqueo KD, Setubal SS, Katsuragawa TH, Silva RRD, Fernandes CFC, Cardoso LAP, Rodrigues MMS, Soares AM, Stábeli RG, Zuliani JP (2018) Epidemiological study of snakebite cases in Brazilian Western Amazonia. Rev Soc Bras Med Trop 51:338–346

  • Salehi B, Sharifi-Rad J, Seca AML, Pinto DCGA, Michalak I, Trincone A, Mishra AP, Nigam M, Zam W, Martins N (2019) Current trends on seaweeds: looking at chemical composition, phytopharmacology, and cosmetic applications. Molecules 24:4182–4232

    CAS  PubMed Central  Google Scholar 

  • Sangha SJ, Kandasamy S, Khan W, Bahia NS, Singh PR, Critchley AT, Balakrishnan Prithiviraj B (2015) λ-carrageenan suppresses tomato chlorotic dwarf viroid (TCDVd) replication and symptom expression in tomatoes. Mar Drugs 13:2875–2889

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stevan FR, Oliveira MBM, Bucchi DF, Noseda MD, LacominI M, Duarte MER (2001) Cytotoxic effects against HeLa cells of polysaccharides from seaweeds. J Submicrosc Cytol Pathol 33:477–484

    CAS  PubMed  Google Scholar 

  • Theakston RDG, Laing G (2014) Diagnosis of snakebite and the importance of immunological tests in venom research. Toxins 6:1667–1695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Usov AI (2011) Polysaccharides of the red algae. Adv Carbohydr Chem Biochem 65:115–217

    CAS  PubMed  Google Scholar 

  • Warrel DA (2010) Snake bite. Lancet 375:77–88

  • Wijesekara I, Pangestuti R, Kim SK (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84:14–21

    CAS  Google Scholar 

  • Xue CH, Fang Y, Lin H, Chen L, Li ZJ, Deng D, Lu CX (2001) Chemical characters and antioxidative properties of sulfated polysaccharides from Laminaria japonica. J Appl Phycol 13:67–70

    CAS  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. Plenum Press, New York, pp 97–109

    Google Scholar 

  • Zamunér SR, da Cruz-Höfling MA, Corrado AP, Hyslop S, Rodrigues-Simioni L (2004) Comparison of the neurotoxic and myotoxic effects of Brazilian Bothrops venoms and their neutralization by commercial antivenom. Toxicon 44:259–271

    PubMed  Google Scholar 

Download references

Acknowledgments

The clonal strain of C. crispus was cultivated on-land by Acadian in Nova Scotia, Canada. The lambda carrageenan extract was a kind gift from Cargill Texturants (Normandie) to Dr. B. Prithiviraj Dalhousie University, which was then provided to this study.

Funding

This research was supported by Brazilian funding agencies: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Universidade Federal Fluminense/Pró-reitoria de Pós-graduação, Pesquisa e Inovação (UFF/PROPPI).

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da Silva, A.C.R., Pereira, K.K.G., Critchley, A.T. et al. Potential utilization of a lambda carrageenan polysaccharide, derived from a cultivated, clonal strain of the red seaweed Chondrus crispus (Irish moss) against toxic actions of venom of Bothrops jararaca and B. jararacussu snakes. J Appl Phycol 32, 4309–4320 (2020). https://doi.org/10.1007/s10811-020-02229-7

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