Abstract
The effect of incubation with lectins of the macrophages or two evolutive stages ofTrypanosoma cruzi (noninfective epimastigotes and infective trypomastigotes) on the ingestion of the parasites by mouse peritoneal macrophages was studied. Lectins which bind to residues of mannose (Lens culinaris, LCA),n-acetyl-d-glucosamine orn-acetylneur-aminic acid (Triticum vulgaris, WGA), β-d-galactose (Ricinus communis, RCA),n-acetyl-d-galactosamine (Phaseolus vulgaris, PHA;Dolichos biflorus, DBA; andWistaria floribunda, WFA), fucose (Lotus tetragonolobus, LTA), andn-acetylneuraminic acid (Limulus polyphemus, LPA) were used. By lectin blockage we concluded that, α-d-mannose-like, β-d-galactose andn-acetyl-d-galactosamine (PHA, reagent) residues, located on the macrophage's surface are required for both epi- and trypomastigote uptake, whilen-acetylneuraminic acid and fucose residues, impede trypomastigote ingestion but do not interfere with epimastigote interiorization. Macrophages'n-acetyl-d-glucosamine residues are required for epimastigote uptake. On the other hand, from theT. cruzi surface, mannose residues prevent ingestion of epi- and trypomastigotes. Galactose residues participate in endocytosis of trypomastigotes, but hinder epimastigote interiorization. Exposedn-acetyl-d-glucosamine residues are required for uptake of the two evolutive forms.n-acetylneuraminic acid residues on the trypomastigote membrane prevent their endocytosis by macrophages. These results together with those reported previously showing the effect of monosaccharides on theT. cruzi-macrophage interaction, indicate that (a) sugar residues located on the parasite and on macrophage surface play some role in the process of recognition ofT. cruzi, (b) different macrophage carbohydrate-containing receptors are involved in the recognition of epimastigotes and trypomastigotes forms ofT. cruzi, (c)n-acetylneuraminic acid residues located on the surface of trypomastigotes or macrophages impede the interaction of the parasite with these host cells, and suggest that (d) sugar-binding proteins located on the macrophage surface participate in the recognition of β-d-galactose andn-acetyl-d-galactosamine residues located on the surface of trypomastigotes and exposed after blockage or splitting off ofn-acetylneuraminic acid residues. Some lectins which bind to macrophages and block the ingestion of parasites did not interfere with their adhesion.
Similar content being viewed by others
References
Adams DO, Hamilton TA (1984) The biology of macrophage activation. Ann Rev Immunol 2: 283–318
Alcantara A, Brener Z (1980)Trypanosoma cruzi: role of macrophage membrane components in the phagocytosis of bloodstream forms. Exp Parasitol 50: 1–6
Andrews NW, Colli W (1981) Interiorization ofTrypanosoma cruzi in cultured mammalian cells. Inhibition byn-acetyl-d-glucosamine. Proc Eight Annual Meeting on Chagas' disease. Caxambú, Brazil Abstr 104
Araújo-Jorge TC, De Souza W (1984) Effect of carbohydrates, periodate and enzymes in the process of endocytosis ofTrypanosoma cruzi by macrophages. Acta Trop (Basel) 41: 17–28
Aswell G, Morell AG (1974) The role of surface carbohydrates in the hepatic recognition and transport of circulating glycoproteins. Adv Enzymol 41: 99–128
Bar-Shavit Z, Goldman R (1976) Concanavalin A-mediated attachment and ingestion of yeast cells by macrophages. Exp Cell Res 99: 221–236
Bianco C, Griffin FM, Silverstein SC (1975) Studies of macrophage complement receptor. J Exp Med 141: 1278–1290
Bongertz V, Dvorak JA, Crane MSJ, Galvão-Castro B (1983) Preliminary report:Trypanosoma cruzi: Altempts to inhibit penetration into non-phagocytic host cells. Proc Tenth Annual Meeting on Chagas' disease. Caxambú, Brazil Abstr I 11
Brown JC, Hunt RC (1978) Lectins. Int Rev Cytol 52: 277–349
Clarcke AC, Hoggart RM (1982) The use of lectins in the study of glycoproteins. In: Antibody as a tool. Marchalones JJ, War GW (eds) pp 347–401
Crane MJ, Dvorak JD (1982) Influence of monosaccharides on the infection of vertebrate cells byTrypanosoma cruzi andToxoplasma gondii. Mol Biochem Parasitol 5: 333–341
De Souza W (1984) Cell biology ofTrypanosoma cruzi. Int Rev Cytol 86: 197–283
Goldman R, Sharon N, Lotan R (1976) A differential response elicited in macrophages on interaction with lectins. Exp Cell Res 99: 408–422
Goldstein JJ, Hayes CE (1978) The lectins: carbohydrate binding proteins of plant and animals. Adv Carbohydrate Chem Biochem 35: 127–340
Hakamori SI (1981) Glycosphingolipids in cellular interaction, differentition and oncogenesis. Ann Rev Biochem 50: 733–764
Jancik JM, Schauer R, Andrews KH, Düring M (1978) Sequestration of neuraminidase-treated erythrocytes. Studies on its topographic, morphologic and immunologic aspects. Cell Tissue Res 186: 209–226
Katzin AM, Colli W (1983) Lectin receptors inTrypanosoma cruzi. Ann-acetyl-d-glucosamine-containing surface glycoprotein specific for the trypomastigote stage. Biochim Biophys Acta 727: 403–411
Kelmet S, Shukle A, Schauer R (1984) Binding of glutaraldehyde-fixed erythrocytes after partial removal on reduction of sialic acid by macrophages. Hoppe-Seyler's Z Physiol Chem 365: 1011–1884
Kipnis TL, David JR, Alper CA, Sher A, Da Silva W (1981) Enzymatic transforms trypomastigotes ofTrypanosoma cruzi into activators of alternative complement pathway and potentiates their uptake by macrophages. Proc Nat Acad Sci (USA) 78: 602–605
Kolb H, Kolb-Bachofen V (1978) A lectin-like receptor on mammalian macrophages. Biochim Biophys Res Commun 85: 678–683
Kolb H, Kolb-Bachofen V, Schlepper-Schafer J (1979) Cell contacts mediated byd-galactose specific lectins on liver cells. Biol Cellulaire 36: 301–308
Kolb-Bachofen V, Ross PH, Kempke G, Schlepper-Schafer J, Kolb H (1984) Isolation of the galactose-specific receptors on rat liver macrophages. Hoppe-Seyler's Z Physiol Chem 365: 1017–1018
Loures MA, Pimenta PF, De Souza W (1980) Isolation of bloodstream trypomastigotes ofTrypanosoma cruzi by a gradient of metrizamide. J Parasitol 66: 1058–1059
Meirelles MNL, Araújo-Jorge TC, De Souza W (1980) Interaction of epimastigote and trypomastigote forms ofTrypanosoma cruzi with chicken macrophages “in vitro”. Parasitology 31: 373–381
Meirelles MNL, Araújo-Jorge TC, De Souza W (1982) Interaction ofTrypanosoma cruzi with macrophages in vitro: Dissociation of the attachment and internalization phases by low temperature and cytochalasin B. Z Parasitenkd 68: 7–14
Meirelles MNL, Martinez-Palomo A, Souto-Padrón T, De Souza W (1983) Participation of concanavalin A binding sites in the interaction betweenTrypanosoma cruzi and macrophages. J Cell Sci 62: 287–299
Meirelles MNL, Souto-Padrón T, De Souza W (1984) Participation of cell surface anionic sites in the interaction betweenTrypanosoma cruzi and macrophages. J Submicrosc Cytol 16: 533–545
Müller ME (1974) Neuraminidases of bacteria and protozoa and their pathogenic role. In: Belgium Institute Research Commun. Symposium on neuraminidases, 55: 34–56
Müller E, Franco MW, Schauer R (1981) Involvement of membrane galactose in the “in vivo” and “in vitro” sequestration of desialylated erythrocytes. Hoppe-Seyler's Z Physiol Chem 362: 1615–1620
Müller E, Schröder C, Franco MW, Shukla AK, Schauer R (1983) Involvement of a galactose-specific macrophage lectin in binding and phagocytosis of erythrocytes. In: Lectins; biology, biochemistry and clinical biochemistry. Bog-Hansen TC, Spengler GA (eds) Vol 3 Walter de Gruyter, Berlin New York, p 435
Nagamura Y, Kolb M (1980) Presence of a lectin-like receptor ford-galactose on rat peritoneal macrophages. FEBS Lett 115: 59–62
Nicolson GL (1974) The interaction of lectins with animal cell surface. Int Rev Cytol 39: 89–190
Nogueira N, Cohn Z (1976)Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. J Exp Med 143: 1402–1420
Nogueira N, Chaplan S, Cohn Z (1980)Trypanosoma cruzi: Factors modifying ingestion and fate of blood form trypomastigotes. J Exp Med 152: 447–451
Pereira MEA (1983) A developmentally regulated neuraminidase activity inTrypanosoma cruzi. Science 219: 1444–1446
Pereira MEA, Loures MA, Villalta F, Andrade AFB (1980) Lectin receptors as markers forTrypanosoma cruzi. J Exp Med 152: 1375–1392
Santos ABS, De Souza W (1983) Surface charge and ultrastructure of the cell surface of resident and thioglycollate elicited mouse peritoneal macrophages. J Submicroscop Cytol 15: 897–911
Schottelius J, Uhlenbruck G (1983) Comparative studies ofTrypanosoma cruzi andTrypanosoma cruzi-like stocks from different South American countries using lectins-Z Parasitenkd 69: 727–736
Souto-Padrón T, Carvalho TU, Chiari E, De Souza W (1984) Further studies on the cell surface charge ofTrypanosoma cruzi. Acta Trop 41: 215–225
Uhlenbruck G, Mil A van, Overbeck K, Koch O (1982) Makrophagen und phagocytose —Fendekouvesti. Immun Infekt 10: 122–129
Villalta F, Kierzenbaum F (1983) Role of cell surface mannose residues in host cell invasion byTrypanosoma cruzi. Biochem Biophys Acta 736: 39–44
Villalta F, Kierzenbaum F (1984) Host cell invasion byTrypanosoma cruzi: role of cell surface galactose residues. Biochem Biophys Res Comm 119: 228–235
Warren L (1960) Metabolism ofTrypanosoma cruzi, Chagas. I. Effect of culture age and substrate concentration on respiratory rate. J Parasitol 46: 529–530
Zenian A, Kierzenbaum F (1982) Inhibition of macrophage-Trypanosoma cruzi interaction by concanavalin A and differential binding of bloodstream and culture forms to the macrophage surface. J Parasitol 68: 408–415
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
de Araújo-Jorge, T.C., de Souza, W. Interaction ofTrypanosoma cruzi with macrophages: effect of previous incubation of the parasites or the host cells with lectins. Z. Parasitenkd. 72, 153–171 (1986). https://doi.org/10.1007/BF00931143
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00931143