Skip to main content Accessibility help

Trypanosoma cruzi: cell surface dynamics in trypomastigotes of different strains

  • Roberta Ferreira Cura das Neves (a1), Camila Marques Adade (a1), Anne Cristine Silva Fernandes (a1), Angela Hampshire Lopes (a1) and Thaïs Souto-Padrón (a1)...


Capping and shedding of ectodomains in Trypanosoma cruzi may be triggered by different ligands. Here, we analysed the mobility and shedding of cell surface components of living trypomastigotes of the Y strain and the CL Brener clone in the presence of poly-L-lysine, cationized ferritin (CF) and Concanavalin A (Con A). Poly-L-lysine and CF caused intense shedding in Y strain parasites. Shedding was less intense in CL Brener trypomastigotes, and approximately 10% of these parasites did not show any decrease in poly L-lysine or CF labelling. Binding of Con A induced low-intensity shedding in Y strain and redistribution of Con A-binding sites in CL Brener parasites. Trypomastigotes of the Y strain showed intense labelling with anti-〈-galactosyl antibodies, resulting in the lysis of approximately 30% of their population, in contrast with what was observed in CL Brener parasites. Incubation with Con A and CF protected trypomastigotes of the Y strain from lysis by anti-αGal. The last treatment did not interfere with the survival of the CL Brener parasites. This study corroborates with the idea that a ligand can differentially modulate the cell surface of T. cruzi, depending on the strain used, resulting in variable immune system responses and recognition by host cells.


Corresponding author

Author for correspondence: Camila Marques Adade, E-mail:


Hide All

In memorian.



Hide All
Acosta-Serrano, A, Almeida, IC, Freitas-Junior, LH, Yoshida, N and Schenkman, S (2001) The mucin-like glycoprotein super-family of Trypanosoma cruzi: structure and biological roles. Molecular and Biochemical Parasitology 114, 143150.
Adade, CM, Chagas, GS and Souto-Padrón, T (2012) Apis mellifera venom induces different cell death pathways in Trypanosoma cruzi. Parasitology 139, 14441461.
Affranchino, JL, Ibãnez, CF, Luquetti, AO, Rassi, A, Reyes, MB, Macina, RA, Aslund, L, Pettersson, U and Frasch, AC (1989) Identification of a Trypanosoma cruzi antigen that is shed during the acute phase of Chagas’ disease. Molecular and Biochemical Parasitology 34, 221228.
Almeida, IC, Milani, SR, Gorin, PA and Travassos, LR (1991) Complement-mediated lysis of Trypanosoma cruzi trypomastigotes by human anti-alpha-galactosyl antibodies. Journal of Immunology 146, 23942400.
Almeida, IC, Krautz, GM, Krettli, AU and Travassos, LR (1993) Glycoconjugates of Trypanosoma cruzi: a 74 kD antigen of trypomastigotes specifically reacts with lytic anti-α-galactosyl antibodies from patients with chronic Chagas’ disease. Journal Clinical of Laboratory Analysis 7, 307316.
Almeida, IC, Ferguson, MAJ, Schenkman, S and Travassos, LR (1994 a) Lytic anti- α-galactosyl antibodies from patients with chronic Chagas’ disease recognize novel O-linked oligosaccharides on mucin-like glycosylphosphatidylinositol-anchored glycoproteins of Trypansoma cruzi. The Biochemical Journal 304, 793802.
Almeida, IC, Ferguson, MAJ, Schenkman, S and Travassos, LR (1994 b) GPI-anchored glycoconjugates from Trypanosoma cruzi trypomastigotes are recognized by lytic anti- alpha-galactosyl antibodies isolated from patients with chronic Chagas’ disease. Brazilian Journal of Medical and Biological Research 27, 443447.
Alves, MJ and Colli, W (2007) Trypanosoma cruzi: adhesion to the host cell and intracellular survival. IUBMB Life 59, 274279.
Alves, MJM, Kawahara, R, Viner, R, Colli, W, Mattos, EC, Thaysen-Andersen, M, Larsen, MR and Palmisano, G (2017) Comprehensive glycoprofiling of the epimastigote and trypomastigote stages of Trypanosoma cruzi. Journal of Proteomics 151, 182192.
Andrews, NW, Robbins, ES, Ley, V, Hong, KS and Nussenzweig, V (1988) Developmentally regulated, phospholipase C-mediated release of the major surface domains of the major surface glycoproteins of amastigotes of Trypanosoma cruzi. The Journal of Experimental Medicine 167, 300314.
Aparício, IM, Scharfstein, J and Lima, APCA (2004) A new cruzipain-mediated pathway of human cell invasion by Trypanosoma cruzi requires trypomastigote membranes. Infection and Immunity 72, 58925902.
Araújo-Jorge, TC, Barbosa, HS, Moreira, AL, De Souza, W and Meirelles, MN (1986) The interaction of myotropic and macrophagotropic strains of Trypanosoma cruzi with myoblasts and fibres of skeletal muscles. Zeitschrift für Parasitenkunde 72, 577584.
Atwood, JA III, Weatherly, DB, Minning, TA, Bundy, B, Cavola, C, Opperdoes, FR, Orlando, R and Tarleton, RL (2005) The Trypanosoma cruzi proteome. Science 309, 473476.
Barros, HC, Silva, S, Versbick, NV, Araguth, MF, Tedesco, RC, Procópio, DO and Mortara, RA (1996) Release of membrane-bound trails by Trypanosoma cruzi amastigotes onto modified surfaces and mammalian cells. The Journal of Eukaryotic Microbiology 43, 275285.
Bayer-Santos, E, Aguilar-Bonavides, C, Rodrigues, SP, Cordero, EM, Marques, AF, Varela-Ramirez, A, Choi, H, Yoshida, N, da Silveira, JF and Almeida, IC (2013) Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. Journal of Proteome Research 12, 883897.
Bourguignon, SC, De Souza, W and Souto-Padrón, T (1998) Localization of lectin-binding sites on the surface of Trypanosoma cruzi grown in chemically defined conditions. Histochemistry and Cell Biology 110, 527534.
Brener, Z (1965) Comparative studies of different strains of Trypanosoma cruzi. Annals of Tropical Medicine and Parasitology 59, 1926.
Brunoro, GV, Caminha, MA, Ferreira, AT, da Leprevost, FV, Carvalho, PC, Perales, J, Valente, RH and Menna-Barreto, RF (2015) Reevaluating the Trypanosoma cruzi proteomic map: the shotgun description of bloodstream trypomastigotes. Journal of Proteomics 115, 5865.
Butman, BT, Bourguignon, GJ and Bourguignon, LY (1980) Lymphocyte capping induced by polycationized ferritin. Journal of Cellular Physiology 105, 715.
Campo, VL, Riul, TB, Carvalho, I and Baruffi, MD (2014) Antibodies against mucin-based glycopeptides affect Trypanosoma cruzi cell invasion and tumor cell viability. Chembiochem: a European Journal of Chemical Biology 15, 14951507.
Calvet, CM, Melo, TG, Garzoni, LR, Oliveira, FO Jr, Neto, DT, Meirelles, NSLM and Pereira, MCL (2012) Current understanding of the Trypanosoma cruzi-cardiomyocyte interaction. Frontiers in Immunology 3, 327.
Castro, ACCL and Ribeiro dos Santos, R (1977) Imunopatologia do rim na forma crônica da moléstia de Chagas experimental. Revista Goiana de Medicina 23, 113.
Cestari, IS, Krarup, A, Sim, RB, Inal, JM and Ramirez, MI (2009) Role of early lectin pathway activation in the complement-mediated killing of Trypanosoma cruzi. Molecular Immunology 47, 426437.
Danon, D, Goldstein, L, Marikovsky, H and Skutelsky, E (1972) Use of cationized ferritin as a label of negative charges on cell surfaces. Journal of Ultrastructure Research 38, 500510.
De Carvalho, L, Souto-Padrón, T and de Souza, W (1991) Localization of lectin-binding sites and sugar-binding proteins in tachyzoites of Toxoplasma gondii. The Journal of Parasitology 77, 156161.
De Godoy, LM, Marchini, FK, Pavoni, DP, de Rampazzo, RC, Probst, CM, Goldenberg, S and Krieger, MA (2012) Quantitative proteomics of Trypanosoma cruzi during metacyclogenesis. Proteomics 12, 26942703.
Dello Sbarba, P and Rovida, E (2002) Transmodulation of cell surface regulatory molecules via ectodomain shedding. Biological Chemistry 383, 6983.
Doyle, JJ, Behin, R, Mauel, J and Rowe, DS (1972) Antibody-induced movement of membrane components of Leishmania enriettii. The Journal of Experimental Medicine 139, 10611069.
Fonseca, LM, da Costa, KM, Chaves, VS, Freire-de-Lima, CG, Morrot, A, Mendonça-Previato, L, Previato, JO and Freire-de-Lima, L (2019) Theft and reception of host cell's sialic acid: dynamics of Trypanosoma cruzi Trans-sialidases and mucin-like molecules on Chagas’ disease immunomodulation. Frontiers in Immunology 10, 164.
Frevert, U and Reinwald, E (1988) Formation of filopodia in Trypanosoma congolense by crosslinking the variant surface antigen. Journal of Ultrastructure and Molecular Structure Research 99, 124136.
Garcia-Silva, MR, das Neves, RF, Cabrera-Cabrera, F, Sanguinetti, J, Medeiros, LC, Robello, C, Naya, H, Fernandez-Calero, T, Souto-Padron, T, de Souza, W and Cayota, A (2014) Extracellular vesicles shed by Trypanosoma cruzi are linked to small RNA pathways, life cycle regulation, and susceptibility to infection of mammalian cells. Parasitology Research 113, 285304.
Gazzinelli, RT, Pereira, ME, Romanha, A, Gazzinelli, G and Brener, Z (1991) Direct lysis of Trypanosoma cruzi: a novel effector mechanism of protection mediated by human anti-gal antibodies. Parasite Immunology 13, 345355.
Giannini, MS and D'Alessandro, PA (1978) Unusual antibody-induced modulation of surface antigens in the cell coat of bloodstream trypanosome. Science 201, 916918.
Giorgi, ME and de Lederkremer, RM (2011) Trans-sialidase and mucins of Trypanosoma cruzi: an important interplay for the parasite. Carbohydrate Research 346, 13891393.
Gonçalves, MF, Umezawa, ES, Katzin, AM, de Souza, W, Alves, MJ, Zingales, B and Colli, W (1991) Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Experimental Parasitology 72, 4353.
Joiner, KA, Dias da Silva, W, Rimoldi, MT, Hammer, CH, Sher, A and Kipnis, TL (1988) Biochemical characterization of a factor produced by trypomastigotes of Trypanosoma cruzi that accelerates the decay of complement C3 convertases. The Journal of Biological Chemistry 263, 1132711335.
Kahn, S, Wleklinski, M, Aruffo, A, Farr, A, Coder, D and Kahn, M (1995) Trypanosoma cruzi amastigotes adhesion to macrophages is facilitated by the mannose receptor. The Journal of Experimental Medicine 182, 12431258.
Kahn, SJ, Wleklinski, M, Ezekowitz, RAB, Coder, D, Aruffo, A and Farr, A (1996) The major surface glycoprotein of Trypanosoma cruzi amastigotes are ligands of the human serum mannose-binding protein. Infection and Immunity 64, 26492656.
Kipnis, TL, David, JR, Alper, PA, Sher, A and da Silva, WD (1981) Enzymatic treatment transforms trypomastigotes of Trypanosoma cruzi into activators of alternative complement pathway and potentiates their uptake by macrophages. Proceedings of the National Academy of Sciences of the USA 78, 602605.
Kloetzel, J and Deane, MP (1977) Presence of immunoglobulins on the surface of bloodstream Trypanosoma cruzi. Capping during differentiation in culture. Revista do Instituto de Medicina Tropical de São Paulo 19, 397402.
Krettli, AU and Brener, Z (1976) Protective effects of specific antibodies in Trypanosoma cruzi infections. The Journal of Immunology 116, 755760.
Krettli, AU, Weiss-Carrington, P and Nussenzweig, RS (1979) Membrane-bound antibodies to bloodstream Trypanosoma cruzi in mice: strain differences in susceptibility to complement-mediated lysis. Clinical and Experimental Immunology 37, 416423.
Leon, W, Villalta, F, Queiroz, T and Szarfman, A (1979) Antibody-induced capping in the intracellular stage of Trypanosoma cruzi. Infection and Immunity 26, 12181220.
Madison, MN, Kleshchenko, YY, Nde, PN, Simmons, KJ, Lima, MF and Villalta, F (2007) Human defensins α-1 causes Trypanosoma cruzi membrane pore formation and induces DNA fragmentation which leads to trypanosome destruction. Infection and Immunity 75, 47804791.
Meirelles, MNL, Martinez-Palomo, A, Souto-Padrón, T and De Souza, W (1983) Participation of Concanavalin A binding sites in the interaction between Trypanosoma cruzi and macrophages. Journal of Cell Science 62, 287299.
Meirelles, MNL, Souto-Padrón, T and De Souza, W (1984) Participation of cell surface anionic sites in the interaction between Trypanosoma cruzi and macrophages. Journal of Submicroscopic Cytology 16, 533545.
Melo, RC and Brener, Z (1978) Tissue tropism of different Trypanosoma cruzi strains. Journal of Parasitology 64, 475482.
Norris, KA (1996) Ligand-binding renders the 160 KDa Trypanosoma cruzi complement regulatory protein susceptible to proteolytic cleavage. Microbial Pathogenesis 21, 235248.
Norris, KA and Schrimpf, JE (1994) Biochemical analysis of the membrane and soluble forms of the complement regulatory protein of Trypanosoma cruzi. Infection and Immunity 62, 236243.
Pereira-Chioccola, VL, Acosta-Serrano, A, Almeida, IC, Ferguson, MA, Souto-Padrón, T, Rodrigues, MM, Travassos, LR and Schenkman, S (2000) Mucin-like molecules from a negatively charged coat that protects Trypanosoma cruzi trypomastigotes from killing by human anti-α-galactosyl antibodies. Journal of Cell Science 113, 12991307.
Pinto da Silva, P, Martínez-Palomo, A and Gonzalez-Robles, A (1975) Membrane structure and surface coat of Entamoeba histolytica. Topochemistry and dynamics of the cell surface: cap formation and microexudate. The Journal of Cell Biology 64, 538550.
Portillo, S, Zepeda, BG, Iniguez, E, Olivas, JJ, Karimi, NH, Moreira, OC, Marques, AF, Michael, K, Maldonado, RA and Almeida, IC (2019) A prophylactic α-Gal-based glycovaccine effectively protects against murine acute Chagas disease. Nature Partner Journals Vaccines 4, 13.
Rothfuchs, AG, Roffê, E, Gibson, A, Cheever, AW, Ezekowitz, RA, Takahashi, K, Steindel, M, Sher, A and Báfica, A (2012) Mannose-binding lectin regulates host resistance and pathology during experimental infection with Trypanosoma cruzi. PLoS ONE 7, e47835.
Saraiva, EM, Vannier-Santos, MA, Silva-Filho, FC and de Souza, W (1989) Anionic site behavior in Leishmania and its role in the parasite-macrophage interaction. Journal of Cell Science 93, 481489.
Schmuñis, GA, Szarfman, A, Langembach, T and de Souza, W (1978) Induction of capping in blood-stage trypomastigotes of Trypanosoma cruzi by human anti-Trypanosoma cruzi antibodies. Infection and Immunity 20, 567569.
Schmuñis, GA, Szarfman, A, De Souza, W and Langembach, T (1980) Trypanosoma cruzi: antibody-induced mobility of surface antigens. Experimental Parasitology 50, 90102.
Soeiro, MNC, Paiva, MM, Barbosa, HS, Meirelles, MN and Araújo-Jorge, TC (1999) A cardiomyocyte mannose receptor system is involved in Trypanosoma cruzi invasion and is down-modulated after infection. Cell Structure and Function 24, 139149.
Souto-Padrón, T (2002) The surface charge of trypanosomatids. Anais da Academia Brasileira de Ciências 74, 649675.
Souto-Padrón, T and De Souza, W (1986) The surface charge of Trypanosoma cruzi: analysis using cell electrophoresis, lectins and ultrastructural cytochemistry. Journal of Submicroscopic Cytology 18, 701709.
Souto-Padrón, T, De Carvalho, TU, Chiari, E and de Souza, W (1984) Further studies on the cell surface charge of Trypanosoma cruzi. Acta Tropica 41, 215225.
Souto-Padrón, T, Harth, G and de Souza, W (1990) Immunocytochemical localization of neuraminidase in Trypanosoma cruzi. Infection and Immunity 58, 586592.
Serna, C, Lara, JA, Rodrigues, SP, Marques, AF, Almeida, IC and Maldonado, RA (2014) A synthetic peptide from Trypanosoma cruzi mucin-like associated surface protein as candidate for a vaccine against Chagas disease. Vaccine 32, 35253532.
Szarfman, A, Queiroz, T and De Souza, W (1980) Mobility of Concanavalin A receptors in Trypanosoma cruzi. Journal of Parasitology 66, 10551057.
Taverna, S, Ghersi, G, Ginestra, A, Rigogliuso, S, Pecorella, S, Alaimo, G, Saladino, F, Dolo, V, Dell'Era, P, Pavan, A, Pizzolanti, G, Mignatti, P, Presta, M and Vittorelli, ML (2003) Shedding of membrane vesicles mediates Fibroblast Growth Factor-2 release from cell. The Journal of Biological Chemistry 51, 5191151919.
Trocoli-Torrecilhas, AC, Tonelli, RR, Pavanelli, WR, da Silva, JS, Schumacher, RI, de Souza, W, E Silva, NC, de Almeida Abrahamsohn, I, Colli, W and Manso Alves, MJ (2009) Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes and Infection 11, 2939.
Waniek, PJ, Jansen, AM and Araújo, CAC (2011) Trypanosoma cruzi infection modulates the expression of Triatoma brasiliensis def1 in the midgut. Vector Borne and Zoonotic Diseases 11, 845847.
Werb, Z and Yan, Y (1998) A cellular striptease act. Science 282, 12791280.
Yokoyama-Yasunaka, JKU, Pral, EMF, Oliveira, OC Jr, Alfieri, SC and Stolf, AM (1994) Trypanosoma cruzi: identification of proteinases in shed components of trypomastigote forms. Acta Tropica 57, 307315.
Zingales, B, Andrade, SG, Briones, MR, Campbell, DA, Chiari, E, Fernandes, O, Guhl, F, Lages-Silva, E, Macedo, AM, Machado, CR, Miles, MA, Romanha, AJ, Sturm, NR, Tibayrenc, M, Schijman, AG and Second Satellite Meeting (2009) A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memórias do Instituto Oswaldo Cruz 104, 10511054.


Trypanosoma cruzi: cell surface dynamics in trypomastigotes of different strains

  • Roberta Ferreira Cura das Neves (a1), Camila Marques Adade (a1), Anne Cristine Silva Fernandes (a1), Angela Hampshire Lopes (a1) and Thaïs Souto-Padrón (a1)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed