Abstract
Objective and design
This study had investigated the anti-inflammatory activity of a seed lectin (LAL) isolated from Lonchocarpus araripensis.
Material/methods
LAL was purified by affinity chromatography (chitin column) and ion exchange chromatography (DEAE-Sephacel). In vitro LAL was tested for hemagglutinating activity against rabbit erythrocytes. In vivo LAL was assessed for the anti-inflammatory activity via intravenous injection (i.v.) in Swiss mice (25–30 g; n = 6/group) in models of paw edema and peritonitis. Statistical analysis: ANOVA (p < 0.05).
Results
LAL revealed two bands of 30 and 60 kDa (SDS-PAGE) and exhibited hemagglutinating activity. LAL (10 mg/kg) inhibited the paw edema (77 %) and vascular permeability (26 %) induced by carrageenan, and the paw edema induced by serotonin (80 %), bradykinin (49 %), sodium nitroprusside (83 %), TNF-α (75 %) and PGE2 (64 %). LAL also inhibited the neutrophil migration induced by fMLP (70 %) or carrageenan (69 %). The intravital microscopy showed that LAL inhibited rolling (83 %) and adhesion (70 %) of leukocytes. LAL anti-inflammatory effect was reversed by its association with N-acetyl-glucosamine. The nine-daily treatment with LAL (10 mg/kg; i.v.) showed no toxicity.
Conclusion
The novel N-acetyl-d-glucosamine-binding lectin isolated from L. araripensis seeds presents anti-inflammatory effect involving the lectin domain and the inhibition of 5-HT, BK, PGE2, NO, TNF-α and leukocyte rolling and adhesion.
Similar content being viewed by others
References
Peumans WJ, Van Damme EJM. Lectins as plant defense proteins. Plant Physiol. 1995;109(2):347–52.
Ley K. The role of selectins in inflammation and disease. Trends Mol Med. 2003;9(6):263–8.
Assreuy MAS, Shibuya MD, Martins GJ, de Souza MLP, Cavada BS, Moreira RA, Oliveira JTA, Ribeiro RA, Flores CA. Anti-inflammatory effect of glucose-mannose binding lectins isolated from Brazilian beans. Mediators Inflamm. 1997;6(3):201–10.
Rocha BA, Delatorre P, Oliveira TM, Benevides RG, Pires AF, Sousa AA, Assreuy AM, Debray H, Azevedo WFJR, Sampaio AH, Cavada BS. Structural basis for both pro- and anti-inflammatory response induced by mannose-specific legume lectin from Cymbosema roseum. Biochimie. 2011;93(5):806–16.
Simões RC, Rocha BA, Bezerra MJ, Barroso-Neto IL, Pereira-Junior FN, da Mata Moura R, do Nascimento KS, Nagano CS, Delatorre P, de Freitas Pires A, Assreuy AM, Sampaio AH, Cavada BS. Protein crystal content analysis by mass spectrometry and preliminary X-ray diffraction of a lectin from Canavalia grandiflora seeds with modulatory role in inflammation. Rapid Commun Mass Spectrom. 2012;26(7):811–8.
Pinto NV, Cavada BS, Brito LF, Pereira RI, da Silva MT, Castro RR, de Freitas Pires A, Assreuy AM. Effects of Canavalia lectins on acute inflammation in sensitized and non-sensitized rats. Inflammation. 2013;36(3):713–22.
Silva HC, Bari AU, Rocha BA, Nascimento KS, Ponte EL, Pires AF, Delatorre P, Teixeira EH, Debray H, Assreuy AM, Nagano CS, Cavada BS. Purification and primary structure of a mannose/glucose-binding lectin from Parkia biglobosa Jacq. seeds with antinociceptive and anti-inflammatory properties. J Mol Recognit. 2013;26(10):470–8.
Alencar NMN, Teixeira EH, Assreuy MAS, Cavada BS, Flores CA, Ribeiro RA. Leguminous lectins as tools for studying the role of sugar residues in leukocyte recruitment. Mediators Inflamm. 1999;8(2):107–13.
Alencar NM, Cavalcante CF, Vasconcelos MP, Leite KB, Aragão KS, Assreuy AM, Nogueira NA, Cavada BS, Vale MR. Anti-inflammatory and antimicrobial effect of lectin from Lonchocarpus sericeus seeds in an experimental rat model of infectious peritonitis. J Pharm Pharmacol. 2005;57(7):919–22.
Napimoga MH, Cavada BS, Alencar NM, Mota ML, Bitencourt FS, Alves-Filho JC, Grespan R, Gonçalves RB, Clemente-Napimoga JT, de Freitas A, Parada CA, Ferreira SH, Cunha FQ. Lonchocarpus sericeus lectin decreases leukocyte migration and mechanical hypernociception by inhibiting cytokine and chemokines production. Int Immunopharmacol. 2007;7(6):824–35.
Ainouz IL, Sampaio AH, Benevides NMB, Freitas ALP, Costa FHF, Carvalho MC, Pinheiro-Joventino F. Agglutination of enzyme treated erythrocytes by Brazilian marine algae. Bot Mar. 1992;35(6):475–9.
Cirino G, Peers SH, Flower RJ, Browning JL, Pepinsky RB. Human recombinant lipocortin 1 has acute local anti-inflammatory properties in the rat paw edema test. Proc Natl Acad Sci. 1989;86(9):3428–32.
Garcia-Leme J, Wilhelm DL. The effects of adrenalectomy and corticosterone on vascular permeability responses in the skin of the rat. Br J Exp Pathol. 1975;56(5):402–7.
Fortes ZB, Farsky SP, Oliveira MA, Garcia-Leme J. Direct vital microscopic study of defective leukocyte-endothelial interaction in diabetes mellitus. Diabetes. 1991;40(10):1267–73.
Nunes BS, Rensonnet NS, Dal-Secco D, Vieira SM, Cavada BS, Teixeira EH, Moura TR, Teixeira CS, Clemente-Napimoga JT, Cunha FQ, Napimoga MH. Lectin extracted from Canavalia grandiflora seeds presents potential anti-inflammatory and analgesic effects. Naunyn-Schmiedeberg’s Arch Pharmacol. 2009;379(6):609–16.
Assreuy AM, Fontenele SR, Pires AF, Fernandes DC, Rodrigues NV, Bezerra EH, Moura TR, do Nascimento KS, Cavada BS. Vasodilator effects of Diocleinae lectins from the Canavalia genus. Naunyn-Schmiedeberg’s Arch Pharmacol. 2009;380(6):509–21.
Silva HC, Bari AU, Pereira-Júnior FN, Simões RC, Barroso-Neto IL, Nobre CB, Pereira MG, Nascimento KS, Rocha BA, Delatorre P, Nagano CS, Assreuy AM, Cavada BS. Purification and partial characterization of a new pro-inflammatory lectin from Bauhinia bauhinioides Mart (Caesalpinoideae) seeds. Protein Pept Lett. 2011;18(4):396–402.
Alencar NM, Assreuy AM, Havt A, Benevides RG, Moura TR, Sousa RB, Ribeiro RA, Cunha FQ, Cavada BS. Vatairea macrocarpa (Leguminosae) lectin activates cultured macrophages to release chemotactic mediators. Naunyn-Schmiedeberg’s Arch Pharmacol. 2007;374(4):275–82.
Di Rosa M, Giroud JP, Willoughby DA. Studies on the mediators of the acute inflammatory response induced in rats in different sites by carrageenan and turpentine. J Pathol. 1971;104(1):15–29.
Lo TN, Almeida AP, Beaven MA. Dextran and carrageenan evoke different inflammatory responses in rat with respect to composition of infiltrates and effect of indomethacin. J Pharmacol Exp Ther. 1982;221(1):261–7.
Salvemini D, Wang ZQ, Wyatt PS, Bourdon DM, Marino MH, Manning PT, Currie MG. Nitric oxide: a key mediator in the early and late phase of carrageenan-induced rat paw inflammation. Br J Pharmacol. 1996;118(4):829–38.
Vircheva S, Alexandrova A, Georgieva A, Mateeva P, Zamfirova R, Kubera M, Kirkova M. In vivo effects of pentoxifylline on enzyme and non-enzyme antioxidant levels in rat liver after carrageenan-induced paw inflammation. Cell Biochem Funct. 2010;28(8):668–72.
Ribeiro RA, Souza-Filho MVP, Souza MHLP, Oliveira SHP, Costa CHS, Cunha FQ, Ferreira SHP. Role of resident mast cells and macrophages in the neutrophil migration induced by LTB4, fMLP and C5a des arg. Int Arch Allergy Immunol. 1997;112(1):27–35.
Baay M, Brouwer A, Pauwels P, Peeters M, Lardon F. Tumor cells and tumor-associated macrophages: secreted proteins as potential targets for therapy. Clin Dev Immunol. 2011;2011:1–12.
Fukuda M, Hiraoka N, Yeh JC. C-type lectins and sialyl Lewis X oligosaccharides. J Cell Biol. 1999;147(7):467–70.
Al-Mamary ML, Al-Habori M, Al-Aghbari AM, Baker MM. Investigation into the toxicological effects of Catha edulis leaves: a short term study in animal. Phytother Res. 2002;16(2):127–32.
Bitencourt FS, Figueiredo JG, Mota MRL, Bezerra CCR, Silvestre PP, Vale MR, Nascimento KS, Sampaio AH, Nagano CS, Saker-Sampaio S, Farias WRL, Cavada BS, Assreuy AMS, Alencar NMN. Antinociceptive and antiinflammatory effects of a mucin-binding agglutinin isolated from the red marine alga Hypnea cervicornis. Naunyn-Schmiedeberg’s Arch Pharmacol. 2008;377(2):139–48.
Acknowledgments
Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) and technical assistance of Gabriela F.O. Marques-Domingos are acknowledged.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible Editor: Mauro Teixeira.
Deceased: Ronaldo de Albuquerque Ribeiro.
Rights and permissions
About this article
Cite this article
Pires, A.F., Rodrigues, N.V.F.C., Soares, P.M.G. et al. A novel N-acetyl-glucosamine lectin of Lonchocarpus araripensis attenuates acute cellular inflammation in mice. Inflamm. Res. 65, 43–52 (2016). https://doi.org/10.1007/s00011-015-0889-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00011-015-0889-7