[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Springer Nature Link
Log in

Dual effects of a lectin from the green seaweed Caulerpa cupressoides var. lycopodium on inflammatory mediators in classical models of inflammation

  • Original Research Paper
  • Published:
Inflammation Research Aims and scope Submit manuscript

Abstract

Objective

Wide biotechnological investigations of only a limited number of seaweed lectins have been performed. We previously demonstrated the anti-nociceptive and anti-inflammatory effects of a lectin isolated from the green seaweed Caulerpa cupressoides var. lycopodium (CcL). Herein, we further studied the mechanisms of action of CcL.

Methods

Classical acute inflammation models induced by different flogistic agents were used to evaluate the anti-inflammatory action of CcL. CcL was injected locally into the rat paw to verify a possible pro-inflammatory outcome.

Results

CcL (0.1, 1 or 10 mg/kg; i.v.) reduced the carrageenan-induced rat paw edema and neutrophilic infiltration, which was not altered by either mucin (inhibitor of CcL carbohydrate-binding site) or ZnPP-IX (specific HO-1 inhibitor). Immunohistochemical analyses showed that CcL (1 mg/kg) reduced the expression of the cytokines IL-1β, TNF-α, IL-6 and COX-2. CcL (0.1, 1 or 10 mg/kg) inhibited dextran, and CcL (1 mg/kg) inhibited histamine-induced rat paw edema. Both effects were reversed by mucin inhibition. CcL (1 mg/kg) was ineffective for the treatment of serotonin- and bradykinin-induced rat paw edema. When injected via the i.pl. route, CcL (10 mg/kg) elicited rat paw edema involving a wide range of mediators.

Conclusions

The anti-inflammatory action of CcL involves the inhibition of IL-1β, TNF-α, IL-6 and COX-2 expression and histamine H1 receptors. When locally administered, CcL exerts pro-inflammatory actions.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Knowles RG. Development of anti-inflammatory drugs—the research and development process. Basic Clin Pharmacol Toxicol. 2014;114:7–12.

    Article  CAS  PubMed  Google Scholar 

  2. Bruno A, Tacconelli S, Patrignani P. Variability in the response to non-steroidal anti-inflammatory drugs: mechanisms and perspectives. Basic Clin Pharmacol Toxicol. 2014;114:56–63.

    Article  CAS  PubMed  Google Scholar 

  3. Quindere AL, Fontes BP, Vanderlei EdSO, Queiroz INLd, Rodrigues JAG, de Araújo IWFd, et al. Peripheral antinociception and anti-edematogenic effect of a sulfated polysaccharide from Acanthophora muscoides. Pharmacol Rep. 2013;65:600–13.

    Article  PubMed  Google Scholar 

  4. Grangeiro NMG, Aguiar JA, Chaves HV, Brito GAC, Graça JRV, Bezerra MM. Heme oxygenase/carbon monoxide-biliverdin pathway may be involved in the antinociceptive activity of etoricoxib, a selective COX-2 inhibitor. Pharmacol Rep. 2011;63:112–9.

    Article  CAS  PubMed  Google Scholar 

  5. do Val DR, Bezerra MM, Silva AAR, Pereira KMA, Rios LC, Lemos JC, et al. Tephrosia toxicaria Pers. reduces temporomandibular joint inflammatory hypernociception: the involvement of the HO-1 pathway. Eur J Pain. 2014;18(9):1280–9.

    Article  CAS  PubMed  Google Scholar 

  6. Peumans WJ, Van Damme EJM. Lectins as plant defense proteins. Plant Physiol. 1995;109(347–52):347–52.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Arnaud J, Audfray A, Imberty A. Binding sugars: from natural lectins to synthetic receptors and engineered neolectins. Chem Soc Rev. 2013;42(11):4798–813.

    Article  CAS  PubMed  Google Scholar 

  8. Teixeira EH, Arruda FVS, Nascimento KS, Carneiro VA, Nagano CS, Silva BR, et al. Biological applications of plants and algae lectins: an overview. InTech 2012:533–58.

  9. Bitencourt FS, Figueiredo JL, Mota MRL, Bezerra CCR, Silvestre PP, Vale MR, et al. Antinociceptive and anti-inflammatory effects of a mucin-binding agglutinin isolated from the red marine alga Hypnea cervicornis. Naunyn Schmiedebergs Arch Pharmacol. 2008;377:139–48.

    Article  CAS  Google Scholar 

  10. Vanderlei ES, Patoilo KK, Lima NA, Lima AP, Rodrigues JA, Silva LM, et al. Antinociceptive and anti-inflammatory activities of lectin from the marine green alga Caulerpa cupressoides. Int Immunopharmacol. 2010;10(9):1113–8.

    Article  CAS  PubMed  Google Scholar 

  11. Silva LMCM, Lima V, Holanda ML, Pinheiro PG, Rodrigues JAG, Lima MEP, et al. Antinociceptive and anti-inflammatory activities of lectin from marine red alga Pterocladiella capillacea. Biol Pharm Bull. 2008;33(5):830–5.

    Article  Google Scholar 

  12. Neves SA, Dias-Baruffi M, Freitas ALP, Roque-Barreira MC. Neutrophil migration induced in vivo and in vitro by marine algal lectins. Inflammat Res. 2001;50:486–90.

    Article  CAS  Google Scholar 

  13. Abreu TM, Silva LMCM, Vanderlei ESO, Melo CML, Pereira VRA, Benevides NMB. Cytokine production induced by marine algae lectins in BALB/c mice splenocytes. Protein Pept Lett. 2012;19:975–81.

    Article  Google Scholar 

  14. Benevides NMB, Holanda ML, Melo FR, Pereira MG, Monteiro ACO, Freitas ALP. Purification and partial characterization of the lectin from the marine green alga Caulerpa cupressoides (Vahl) C. Agardh. Bot Mar. 2001;44:17–22.

    Article  CAS  Google Scholar 

  15. da Conceição Rivanor RL, Chaves HV, do Val DR, de Freitas AR, Lemos JC, Rodrigues JAG, et al. A lectin from the green seaweed Caulerpa cupressoides reduces mechanical hyper-nociception and inflammation in the rat temporomandibular joint during zymosan-induced arthritis. Int Immunopharmacol. 2014;21(1):34–43.

    Article  PubMed  Google Scholar 

  16. Assreuy AM, Gomes DM, Silva MSJ, Torres VM, Siqueira RCL, Pires AF, et al. Biological effects of a sulfated-polysaccharide isolated from the marine red algae Champia feldmannii. Biol Pharm Bull. 2008;31(4):691–5.

    Article  CAS  PubMed  Google Scholar 

  17. Winter CA, Risley EA, Nuss GW. Carrageenin induced oedema in hind paw of rats as an assay for anti-inflammatory drugs. Proc Soc Exp Biol Med. 1962;111:544–7.

    Article  CAS  PubMed  Google Scholar 

  18. Bradley PP, Christensen RD, Rothstein G. Cellular and extracellular myeloperoxidase in pyogenic inflammation. Blood. 1982;60:618–22.

    CAS  PubMed  Google Scholar 

  19. Freitas A, Alves-Filho JC, Secco DD, Neto AF, Ferriera SH, Barja-Fidalgo C, et al. Heme oxygenase/carbon monoxide-biliverdin pathway down regulates neutrophil rolling, adhesion and migration in acute inflammation. Br J Pharmacol. 2006;149(345–54):345–54.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Lo TN, Almeida AP, Beaven MA. Dextran and carrageenan evoke different inflammatory response in rat with respect to composition of infiltrates and effect of indomethacin. J Pharmacol Exp Ther. 1982;221:261–7.

    CAS  PubMed  Google Scholar 

  21. Assreuy AM, Fontenele SR, Pires AF, Fernandes DC, Rodrigues NVFC, Bezerra EHS, et al. Vasodilator effects of diocleinae lectins from the Canavalia genus. Naunyn Schmied Arch Pharmacol. 2009;380:509–21.

    Article  CAS  Google Scholar 

  22. Cunha GMA, Bezarra PJP, Saldanha MDD, Cavalcante MC, De Brun VMS, Viana GSB. Pentoxifylline improves learning and memory in glutamate-lesioned rats. Pharmacol Biochem Behav. 2000;66:687–94.

    Article  CAS  PubMed  Google Scholar 

  23. Figueiredo JG, Bitencourt FS, Mota MRL, Silvestre PP, Aguiar CN, Benevides RG, et al. Pharmacological analysis of the neutrophil migration induced by D. rostrata lectin: involvement of cytokines and nitric oxide. Toxicon. 2009;54:736–44.

    Article  CAS  PubMed  Google Scholar 

  24. Mota MRL, Criddle DN, Alencar NM, Gomes RC, Meireles AVP, Santi-Gadelha T, et al. Modulation of acute inflammation by a chitin-binding lectin from Araucaria angustifolia seeds via mast cells. Naunyn Schmiedeberg’s Arch Pharmacol. 2006;374:1–10.

    Article  CAS  Google Scholar 

  25. Alencar NMN, Mota MRL, Rodrigues NVFC, Martins JL, Nascimento KS, Assreuy AM, et al. Neutrophil-infiltrated paw edema induced by mannose-binding Dioclea violacea lectin. Pharmacol Rep. 2013;65:220–5.

    Article  PubMed  Google Scholar 

  26. Turner MD, Nedjai B, Hurst T, Pennington DJ. Cytokines and chemokines: at the crossroads of cell signalling and inflammatory disease. Biochim Biophys Acta (BBA) Mol Cell Res. 2014;1843(11):2563–82.

    Article  CAS  Google Scholar 

  27. Haddad JJ. Cytokines and related receptor-mediated signaling pathways. Biochem Biophys Res Commun. 2002;297:700–13.

    Article  CAS  PubMed  Google Scholar 

  28. Kumar V, Sharma N. Neutrophils: cinderella of innate immune system. Int Immunopharmacol. 2010;10:1325–34.

    Article  CAS  PubMed  Google Scholar 

  29. Stables MJ, Gilroy DW. Old and new generation lipid mediators in acute inflammation and resolution. Prog Lipid Res. 2011;50(1):35–51.

    Article  CAS  PubMed  Google Scholar 

  30. Parada CA, Tambeli CH, Cunha FQ, Ferrera SH. The major role of peripheral release of histamine and 5-hydroxytryptamine in formalin-induced nociception. Neuroscience. 2001;102(4):937–44.

    Article  CAS  PubMed  Google Scholar 

  31. Alencar NM, Cavalcante CF, Vasconcelos MP, Leite KB, Aragão KS, Assreuy AM, et al. Anti-inflammatory and antimicrobial effect of lectin from Lonchocarpus sericeus seeds in an experimental rat model of infectious peritonitis. J Pharm Pharmacol. 2005;57:919–22.

    Article  CAS  PubMed  Google Scholar 

  32. Alencar NMN, Assreuy AMS, Alencar VBM, Melo SC, Ramos MV, Cavada BS, et al. The galactose-binding lectin from Vatairea macrocarpa seeds induces in vivo neutrophil migration by indirect mechanism. Int J Biochem Cell Biol. 2003;35:1674–81.

    Article  CAS  PubMed  Google Scholar 

  33. Santi-Gadelha T, de Almeida Gadelha CA, Aragão KS, de Oliveira ClC, Lima Mota MR, Gomes RC, et al. Purification and biological effects of Araucaria angustifolia (Araucariaceae) seed lectin. Biochem Biophys Res Commun. 2006;350(4):1050–5.

    Article  CAS  PubMed  Google Scholar 

  34. Assreuy AM, Shibuya MD, Martins GJ, Souza MLP, Cavada BS, Ribeiro RA, et al. Anti-inflammatory effect of glucose–mannose binding lectins isolated from Brazilian beans. Mediators Inflamm. 1997;6:201–10.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Brazilian grants from Conselho Nacional de Pesquisa (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Instituto de Biomedicina do Semi-Árido Brasileiro (INCT), and Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP). The authors thank Professor Ana Cecília Menezes Fortes Xavier for identifying the seaweed species and Adalberto Nascimento de Lima Júnior for the technical assistance provided. BENEVIDES, N. M. B. and BEZERRA, M. M. are senior investigators of CNPq/Brazil.

Author information

Authors and Affiliations

  1. Institute of Medical Biochemistry, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil

    Ismael Nilo Lino de Queiroz & José Ariévilo Gurgel Rodrigues

  2. Department of Biochemistry and Molecular Biology, Federal University of Ceará, Bloco 907 Campus do Pici, Fortaleza, CEP: 60440-900, Brazil

    Ismael Nilo Lino de Queiroz, Ana Luíza Gomes Quinderé, Edfranck de Sousa Oliveira Vanderlei, Natássia Albuquerque Ribeiro, Renata Line da Conceição Rivanor, Chistiane Oliveira Coura & Norma Maria Barros Benevides

  3. Faculty of Medicine, Department of Physiology and Pharmacology, Federal University of Ceará, Campus do Porangabuçu, Fortaleza, Brazil

    Ana Luíza Gomes Quinderé

  4. Faculty of Medicine, Federal University of Ceará, Sobral, Brazil

    Kátia Alves Ribeiro & Mirna Marques Bezerra

  5. Faculty of Dentistry, Federal University of Ceará, Sobral, Brazil

    Karuza Maria Alves Pereira & Hellíada Vasconcelos Chaves

  6. Department of Fisheries Engineering, Federal University of Ceará, Bloco 840 Campus do Pici, Fortaleza, Brazil

    Ianna Wivianne Fernandes de Araújo

Authors
  1. Ismael Nilo Lino de Queiroz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Luíza Gomes Quinderé
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Ariévilo Gurgel Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edfranck de Sousa Oliveira Vanderlei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Natássia Albuquerque Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Renata Line da Conceição Rivanor
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kátia Alves Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chistiane Oliveira Coura
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Karuza Maria Alves Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hellíada Vasconcelos Chaves
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mirna Marques Bezerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ianna Wivianne Fernandes de Araújo
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Norma Maria Barros Benevides
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Norma Maria Barros Benevides.

Additional information

Responsible Editor: Mauro Teixeira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Queiroz, I.N.L., Quinderé, A.L.G., Rodrigues, J.A.G. et al. Dual effects of a lectin from the green seaweed Caulerpa cupressoides var. lycopodium on inflammatory mediators in classical models of inflammation. Inflamm. Res. 64, 971–982 (2015). https://doi.org/10.1007/s00011-015-0880-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00011-015-0880-3

Keywords