Abstract
Neutrophil migration is responsible for tissue damage observed in inflammatory diseases and is also implicated in inflammatory nociception. The use of lectins has been demonstrated to be effective in different activities including anti-inflammatory, antimicrobial, and in cancer therapy. In this study, we addressed the potential use of a lectin from Canavalia grandiflora seeds (ConGF) to control neutrophil migration and inflammatory hypernociception. Pretreatment of the animals intravenously (15 min before) with ConGF inhibited neutrophil migration to the peritoneal cavity in a dose-dependent fashion confirmed by an inhibition of rolling and adhesion of leukocytes by intravital microscopy. Another set of experiments showed that pretreatment of the animals with ConGF inhibited the mechanical hypernociception in mice induced by the i.pl. injection of carrageenan or formalin. This anti-nociceptive effect correlated with an effective blockade of neutrophil influx, as assessed by the hind paw tissue myeloperoxidase levels. Furthermore, ConGF had important inhibitory effects on the mouse carrageenan-induced paw edema. In addition, animals treated with ConGF showed inhibition of cytokines release. In conclusion, we demonstrated that the lectin ConGF inhibits neutrophil migration and mechanical inflammatory hypernociception.
Similar content being viewed by others
References
Aiello RJ, Bourassa PA, Lindsey S, Weng W, Freeman A, Showell HJ (2002) Leukotriene B4 receptor antagonism reduces monocytic foam cells in mice. Arterioscler Thromb Vasc Biol 22:443–449
Ben-Chetrit E, Bergmann S, Sood R (2006) Mechanism of the anti-inflammatory effect of colchicine in rheumatic diseases: a possible new outlook through microarray analysis. Rheumatology 45:274–282
Bitencourt Fda S, Figueiredo JG, Mota MR, Bezerra CC, Silvestre PP, Vale MR, Nascimento KS, Sampaio AH, Nagano CS, Saker-Sampaio S, Farias WR, Cavada BS, Assreuy AM, de Alencar NM (2008) Antinociceptive and anti-inflammatory effects of a mucin-binding agglutinin isolated from the red marine alga Hypnea cervicornis. Naunyn-Schmiedeberg’s Arch Pharmacol 377:139–148
Ceccatto VM, Cavada BS, Nunes EP, Nogueira NA, Grangeiro MB, Moreno FB, Teixeira EH, Sampaio AH, Alves MA, Ramos MV, Calvete JJ, Grangeiro TB (2002) Purification and partial characterization of a lectin from Canavalia grandiflora benth. seeds. Protein Peptide Lett 9:67–73
Conti P, Reale M, Fiore S, Cancelli A, Angeletti PU, Dinarello CA (1988) Recombinant interleukin 1 and tumor necrosis factor acting in synergy to release thromboxane, 6-KETO-PGF1α and PGE2 by human neutrophils. Scand J Rheumatol Suppl 75:318–324
Cunha FQ, Poole S, Lorenzetti BB, Ferreira SH (1992) The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br J Pharmacol 107:660–664
Cunha TM, Verri WA Jr, Silva JS, Poole S, Cunha FQ, Ferreira SH (2005) A cascade of cytokines mediates mechanical inflammatory hypernociception in mice. Proc Natl Acad Sci U S A. 102:1755–1760
Cunha TM, Verri WA Jr, Schivo IR, Napimoga MH, Parada CA, Poole S, Teixeira MM, Ferreira SH, Cunha FQ (2008) Crucial role of neutrophils in the development of mechanical inflammatory hypernociception. J Leukoc Biol 83:824–832
Dal Secco D, Paron JA, de Oliveira SH, Ferreira SH, Silva JS, Cunha Fde Q (2003) Neutrophil migration in inflammation: nitric oxide inhibits rolling, adhesion and induces apoptosis. Nitric Oxide 9:153–164
Di Rosa M, Giroud JP, Willoughby DA (1971) Studies on the mediators of the acute inflammatory response induced in rats in different sites by carrageenan and turpentine. J Pathol 104:15–29
Dube DH, Bertozzi CR (2005) Glycans in cancer and inflammation–potential for therapeutics and diagnostics. Nat Rev 4:477–488
Edamatsu T, Xiao YQ, Tanabe J, Mue S, Ohuchi K (1997) Induction of neutrophil chemotactic factor production by staurosporine in rat peritoneal neutrophils. Br J Pharmacol 121:1651–1658
Fortes ZB, Farsk YSP, Oliveira MA, Garcia-Leme J (1991) Direct vital microscopic study of defective leukocyte–endothelial interaction in diabetes mellitus. Diabetes 40:1267–1273
Friedl P, Weigelin B (2008) Interstitial leukocyte migration and immune function. Nat Immunol 9:960–969
Granger DN, Benoit JN, Suzuki M, Grisham MB (1989) Leukocyte adherence to venular endothelium during ischemia-reperfusion. Am J Physiol 257:G683–G688
Grespan R, Fukada SY, Lemos HP, Vieira SM, Napimoga MH, Teixeira MM, Fraser AR, Liew FY, McInnes IB, Cunha FQ (2008) CXCR2-specific chemokines mediate leukotriene B4-dependent recruitment of neutrophils to inflamed joints in mice with antigen-induced arthritis. Arthritis Rheum 58:2030–2040
Hébert E (2000) Endogenous lectins as cell surface transducers. Biosci Rep 20:213–237
Hogg JC, Walker BA (1995) Polymorphonuclear leucocyte traffic in lung inflammation. Thorax 50:819–820
Jones AK, al-Janabi MA, Solanki K, Sobnack R, Greenwood A, Doyle DV, Britton KE, Huskisson EC (1991) In vivo leukocyte migration in arthritis. Arthritis Rheum 34:270–275
Jourdan D, Ardid D, Bardin L, Bardin M, Neuzeret D, Lanphouthacoul L, Eschalier A (1997) A new automated method of pain scoring in the formalin test in rats. Pain 71:265–270
Kasama T, Miwa Y, Isozaki T, Odai T, Adachi M, Kunkel SL (2005) Neutrophil-derived cytokines: potential therapeutic targets in inflammation. Curr Drug Targets Inflamm Allergy 4:273–279
Le Bars D, Gozariu M, Cadden SW (2001) Animal models of nociception. Pharmacol Rev 53:597–652
Machuka J, Van Damme JEJM, Peumans WJ, Jackai LEN (1999) Effect of plant lectins on larval development of the legume pod borer; Maruca vitrata. Entomol Exp Appl 93:179–187
Mackay CR (2008) Moving targets: cell migration inhibitors as new anti-inflammatory therapies. Nat Immunol 9:988–998
Mathis S, Jala VR, Haribabu B (2007) Role of leukotriene B4 receptors in rheumatoid arthritis. Autoimmun Rev 7:12–17
Mayadas TN, Cullere X (2005) Neutrophil beta2 integrins: moderators of life or death decisions. Trends Immunol 26:388–395
Morris CJ (2003) Carrageenan-induced paw edema in the rat and mouse. Methods Mol Biol 225:115–121
Mota MR, Criddle DN, Alencar NM, Gomes RC, Meireles AV, Santi-Gadelha T, Gadelha CA, Oliveira CC, Benevides RG, Cavada BS, Assreuy AM (2006) Modulation of acute inflammation by a chitin-binding lectin from Araucaria angustifolia seeds via mast cells. Naunyn-Schmiedeberg’s Arch Pharmacol 374:1–10
Napimoga MH, Cavada BS, Alencar NM, Mota ML, Bittencourt FS, Alves-Filho JC, Grespan R, Gonçalves RB, Clemente-Napimoga JT, de Freitas A, Parada CA, Ferreira SH, Cunha FQ (2007) Lonchocarpus sericeus lectin decreases leukocyte migration and mechanical hypernociception by inhibiting cytokine and chemokines production. Int Immunopharmacol 7:824–835
Napimoga MH, Vieira SM, Dal-Secco D, Freitas A, Souto FO, Mestriner FL, Alves-Filho JC, Grespan R, Kawai T, Ferreira SH, Cunha FQ (2008) Peroxisome proliferator-activated receptor-gamma ligand, 15-deoxy-Delta12,14-prostaglandin J2, reduces neutrophil migration via a nitric oxide pathway. J Immunol 180:609–617
Ozaki Y (1990) Anti-inflammatory effects of Curcuma xanthorrhiza Roxb, and its active principle. Chem Pharm Bull 38:1045–1048
Pusztai A, Bardocz S, Ewen SW (2008) Uses of plant lectins in bioscience and biomedicine. Front Biosci 13:1130–1140
Rhodes JM, Campbell BJ (2002) Inflammation and colorectal cancer: IBD-associated and sporadic cancer compared. Trends Mol Med 8:10–16
Safieh-Garabedian B, Poole S, Allchorne A, Winter J, Woolf CJ (1995) Contribution of interleukin-1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br J Pharmacol 115:1265–1275
Sharon N, Lis H (2004) History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14:53R–62R
Smith CW (1993) Endothelial adhesion molecules and their role in inflammation. Can J Physiol Pharmacol 71:76–87
Teixeira EH, Napimoga MH, Carneiro VA, de Oliveira TM, Cunha RM, Havt A, Martins JL, Pinto VP, Gonçalves RB, Cavada BS (2006) In vitro inhibition of Streptococci binding to enamel acquired pellicle by plant lectins. J Appl Microbiol 101:111–116
Teixeira EH, Napimoga MH, Carneiro VA, de Oliveira TM, Nascimento KS, Nagano CS, Souza JB, Havt A, Pinto VP, Gonçalves RB, Farias WR, Saker-Sampaio S, Sampaio AH, Cavada BS (2007) In vitro inhibition of oral streptococci binding to the acquired pellicle by algal lectins. J Appl Microbiol 103:1001–1006
Thurston G, Rudge JS, Ioffe E, Zhou H, Ross L, Croll SD, Glazer N, Holash J, McDonald DM, Yancopoulos GD (2000) Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 6:460–463
Tjolsen A, Berge OG, Hunskaar S, Rosland JH, Hole K (1992) The formalin test: an evaluation of the method. Pain 51:5–17
Van Damme EJM, Peumans WJ, Barre A, Rouge P (1988) Plant lectins: a composite of several distinct families of structurally and evolutionarily related proteins with diverse biological roles. Crit Rev Plant Sci 17:575–692
Verri WA Jr, Cunha TM, Parada CA, Poole S, Cunha FQ, Ferreira SH (2006) Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol Ther 112:116–138
Acknowledgments
This work was supported by grants from Programa de Apoio a Pesquisa–Universidade de Uberaba (PAPE-UNIUBE 2007/005) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nunes, B.S., Rensonnet, N.S., Dal-Secco, D. et al. Lectin extracted from Canavalia grandiflora seeds presents potential anti-inflammatory and analgesic effects. Naunyn-Schmied Arch Pharmacol 379, 609–616 (2009). https://doi.org/10.1007/s00210-009-0397-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00210-009-0397-9