Abstract
The lectin from the legume Vatairea macrocarpa is a galactose/N-acetylgalactosamine binding protein that induced cellular inflammatory response mediated by resident cells. This study investigated which inflammatory mediators would be released from lectin-activated cells. The intraperitoneal injection in rats of the supernatant from cultured macrophages, but not from mast cells, stimulated with lectin induced a time- and dose-dependent release of a neutrophil chemotactic factor, termed MNCF-VML. Pharmacological modulation with dexamethasone inhibited both the lectin-induced chemotactic activity in vivo and also the lectin-induced release of MNCF-VML into the supernatant of cultured macrophages. Cyclooxygenase and lipoxygenase metabolites are apparently not involved in the action of this factor or its release, since indomethacin or MK886 were unable to affect the lectin response. The molecular weight of MNCF-VML was found to be greater than 5 kDa, which led to the investigation of which cytokine(s) could be involved by the following approaches: (a) treatment of animals with antiserum to tumor necrosis factor alpha (TNF-α), interleukin (IL)-1, or IL-8 before intraperitoneal injection of lectin and (b) addition of antiserum to TNF-α, IL-1, or IL-8 to the supernatant of lectin-stimulated macrophages before intraperitoneal administration. Antiserum to TNF-α, but not IL-1 nor IL-8, inhibited the neutrophil migration induced either by lectin or MNCF-VML. Our data suggest that neutrophil migration induced by V. macrocarpa lectin occurs via the release of cytokines such as TNF-α by macrophages. Thus, this lectin may represent an important tool to better understand pathological situations where an excess of leukocytes at inflammatory sites causes tissue injury.
Similar content being viewed by others
References
Alencar NMN, Assreuy AMS, Alencar VBM, Melo SC, Ramos MV, Cavada BS, Cunha FQ, Ribeiro RA (2003) The galactose-binding lectin from Vatairea macrocarpa seeds induces in vivo neutrophil migration by indirect mechanism. Int J Biochem Cell Biol 35:1674–1681
Alencar NMN, Assreuy AMS, Criddle DN, Souza EP, Soares PMG, Havt A, Aragão KS, Bezerra, DP, Ribeiro RA, Cavada BS (2004) Vatairea macrocarpa lectin induces paw edema with leukocyte infiltration. Protein Pept Lett 11:195–200
Alencar NMN, Cavalcante CF, Vasconcelos MP, Leite KB, Aragão KS, Assreuy AMS, Nogueira NA P, Cavada BS, Vale MR (2005a) Antiinflammatory and antimicrobial effect of lectin from Lonchocarpus sericeus seeds in an experimental model of infectious peritonitis. J Pharm Pharmacol 57:912–922
Alencar VB, Alencar NM, Assreuy AM, Mota ML, Brito GA, Aragão KS, Bittencourt FS, Pinto VP, Debray H, Ribeiro RA, Cavada BS (2005b) Pro-inflammatory effect of Arum maculatum lectin and role of resident cells. Int J Biochem Cell Biol 37:1805–1814
Almkvist J, Dahlgren D, Leffler H, Karlsson A (2002) Activation of the neutrophil nicotinamide adenine dinucleotide phosphate oxidase by galectin-1. J Immunol 168:4034–4041
Andrade JL, Arruda S, Barbosa T, Paim L, Ramos MV, Cavada BS, Barra-Neto M (1999) Lectin-induced nitric oxide production. Cell Immunol 194:98–102
Assreuy AMS, Shibuya MD, Martins GJ, de Souza MLP, Cavada BS, Moreira RA, Oliveira JTA, Ribeiro RA, Flores CA (1997) Anti-inflammatory effect of glucose–mannose binding lectins isolated from Brazilian beans. Mediators Inflamm 6:201–210
Assreuy AMS, Martins GJ, Moreira MEF, Brito GAC, Cavada BS, Ribeiro RA, Flores CA (1999) Prevention of cyclophosphamide-induced hemorrhagic cystitis by glucose–mannose binding plant lectins. J Urol 161:1988–1993
Barbosa T, Arruda S, Cavada BS, Grangeiro TB, Freitas LA, Barral-Neto M (2001) In vivo lymphocyte activation and apoptosis by lectin of the Dioclea subtribe. Mem Inst Oswaldo Cruz 96:673–678
Benjamin CF, Figueiredo RC, Henriques MGMO, Barja-Fidalgo C (1997) Inflammatory and anti-inflammatory effects of soybean agglutinin. Braz J Med Biol Res 30:873–881
Brando-Lima AC, Saldanha-Gama RF, Henriques MO, Monteiro-Moreira, ACO, Moreira RA, Barja-Fidalgo C (2005) Frutalin, a galactose-binding lectin, induces chemotaxis and rearrangement of actin cytoskeleton in human neutrophil: Involvement of tyrosine kinase and phosphoinositide 3-kinase. Toxicol Appl Pharmacol 208:145–154
Calvete JJ,Santos CF, Mann K, Grangeiro TB, Nimtz M, Cavada BS (1998). Primary structure and posttranslational processing of Vatairea macrocarpa seed lectin. J Protein Chem 17:545–547
Crokett-Torabi E, Fantone JC (1995) The selectins: insights into selectin-induced intracellular signaling in leukocytes. Immunol Res 14:237–251
Cunha FQ, Ferreira SH (1986) The release of a neutrophil chemotactic factor from peritoneal macrophage by endotoxin: inhibition by glucocorticoids. Eur J Pharmacol 129:65–76
Dias-Baruffi M, Cunha FQ, Ferreira SH, Roque-Barreira MC (1993) Macrophage-released neutrophil chemotactic factor (MNCF) induces PMN-neutrophil migration through lectin-like activity. Agents Actions 38:54–56
Kilpatrick DC (1991) Lectin interactions with human leukocytes: mitogenicity, cell separation, clinical applications. In: Kilpatrick DC, Van Driessche E, Bog-Hansen TC (eds) Lectin reviews. Sigma Chemical Company, St Louis, pp 69–80
Lis H, Sharon N (1986) Biological properties of lectins. In: Liener LE, Sharon N, Goldstein IJ (eds) The lectins. Properties, functions and application in biology and medicine. Academic, London, pp 26–276
Magnusson KE, Dahlgren C, Sjõlander A (1988) Distinct patters of granulocyte luminal-dependent chemiluminescence response to lectins WGA and RCA-I. Inflammation 12:17–42
Martins AM, Monteiro AM, Havt A, Barbosa PS, Soares TF, Evangelista JS, de Menezes DB, Fonteles, MC, Teixeira EH, Pinto, VP, Nascimento, KS, Alencar NM, Cavada BS (2005) Renal effects induced by the lectin from Vatairea macrocarpa seeds. J Pharm Pharmacol 57:1329–1333
McGreal EP, Martinez-Pomares L, Gordon S (2004) Divergent roles for C-type lectins expressed by cells of the innate immune system. Mol Immunol 41:1109–1121
Mota MRL, Criddle DN, Alencar NMN, Gomes RC, Meireles AVP, Santi-Gadelha T, Gadelha CAA, Oliveira CC, Benevides RG, Cavada BS, Assreuy AMS (2006) Modulation of acute inflammation by a chitin-binding lectin from Araucaria angustifolia seeds via mast cells. Naunyn Schmiedebergs Arch Pharmacol 374(1):1–10
Peumans WJ, Van Damme EJL (1995) Lectins as plant defense proteins. Plant Physiol 109:347–352
Ramos MV, Bomfim LR, Cavada BS, Alencar NMN, Grangeiro TB, Debray H (2000) Further characterization of the glycan-binding specificity of the seed lectin from Vaitarea macrocarpa and its dependence of pH. Protein Pept Lett 7:241–248
Reddy KV, Bhattacharjee G, Schabbauer G, Hollis A, Kempf K, Tencati M, O’Connell M, Guha M, Mackman N (2004) Dexamethasone enhances LPS induction of tissue factor expression in human monocytic cells by increasing tissue factor mRNA stability. J Leukoc Biol 76:145–51
Ribeiro RA, Flores CA, Cunha FQ, Ferreira SH, De Lucca LF (1995) Partial characterization of the RNA from LPS-stimulated macrophages that induces the release of chemotactic cytokines by resident macrophages. Mol Cell Biochem 148:105–113
Roque-Barreira MC, Campos-Neto A (1985) Jacalin: an IgA-binding lectin. J Immunol 134:1740–1743
Santos-de-Oliveira R, Dias-Baruffi M, Thomaz SM, Beltramini LM, Roque-Barreira MC (1994) A neutrophil migration-inducing lectin from Artocarpus integrifolia. J Immunol 153:1798–1807
Sharon N, Lis H (1989) Lectins as cell recognition molecules. Science 246:227–234
Souza GEP, Ferreira SH (1985) Blockade by antimacrophage serum of the migration of PMN neutrophils into the inflamed peritoneal cavity. Agents Actions 17:97–103
Tracey K, Cerami A (1994) Tumor necrosis factor: a pleiotropic cytokine and therapeutic target. Annu Rev Med 45:491–503
Varki A (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3:97–130
Acknowledgements
This research was supported by grants from CNPq, FUNCAP, FINEP and CAPES. Assreuy A.M.S, Cavada B.S., Cunha F.Q., Alencar N.M.N., and Ribeiro R.A. are senior investigators of CNPq—Brazil. A. Leyva provided English language editing.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Alencar, N.M.N., Assreuy, A.M.S., Havt, A. et al. Vatairea macrocarpa (Leguminosae) lectin activates cultured macrophages to release chemotactic mediators. Naunyn-Schmied Arch Pharmacol 374, 275–282 (2007). https://doi.org/10.1007/s00210-006-0124-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00210-006-0124-8