Artículo

Benatar, A.F.; García, G.A.; Bua, J.; Cerliani, J.P.; Postan, M.; Tasso, L.M.; Scaglione, J.; Stupirski, J.C.; Toscano, M.A.; Rabinovich, G.A.; Gómez, K.A. "Galectin-1 Prevents Infection and Damage Induced by Trypanosoma cruzi on Cardiac Cells" (2015) PLoS Neglected Tropical Diseases. 9(10)
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Abstract:

Background: Chronic Chagas cardiomyopathy caused by Trypanosoma cruzi is the result of a pathologic process starting during the acute phase of parasite infection. Among different factors, the specific recognition of glycan structures by glycan-binding proteins from the parasite or from the mammalian host cells may play a critical role in the evolution of the infection. Methodology and Principal Findings: Here we investigated the contribution of galectin–1 (Gal–1), an endogenous glycan-binding protein abundantly expressed in human and mouse heart, to the pathophysiology of T. cruzi infection, particularly in the context of cardiac pathology. We found that exposure of HL–1 cardiac cells to Gal–1 reduced the percentage of infection by two different T. cruzi strains, Tulahuén (TcVI) and Brazil (TcI). In addition, Gal–1 prevented exposure of phosphatidylserine and early events in the apoptotic program by parasite infection on HL–1 cells. These effects were not mediated by direct interaction with the parasite surface, suggesting that Gal–1 may act through binding to host cells. Moreover, we also observed that T. cruzi infection altered the glycophenotype of cardiac cells, reducing binding of exogenous Gal–1 to the cell surface. Consistent with these data, Gal–1 deficient (Lgals1-/-) mice showed increased parasitemia, reduced signs of inflammation in heart and skeletal muscle tissues, and lower survival rates as compared to wild-type (WT) mice in response to intraperitoneal infection with T. cruzi Tulahuén strain. Conclusion/Significance: Our results indicate that Gal–1 modulates T. cruzi infection of cardiac cells, highlighting the relevance of galectins and their ligands as regulators of host-parasite interactions. © 2015 Benatar et al.

Registro:

Documento: Artículo
Título:Galectin-1 Prevents Infection and Damage Induced by Trypanosoma cruzi on Cardiac Cells
Autor:Benatar, A.F.; García, G.A.; Bua, J.; Cerliani, J.P.; Postan, M.; Tasso, L.M.; Scaglione, J.; Stupirski, J.C.; Toscano, M.A.; Rabinovich, G.A.; Gómez, K.A.
Filiación:Laboratorio de Biología Molecular de la Enfermedad de Chagas (LabMECh), Instituto de Investigaciones en Ingeniería Genética y Biología Molecular (INGEBI-CONICET), Buenos Aires, Argentina
Instituto Nacional de Parasitología “Dr. Mario Fatala Chaben”, Administración Nacional de Laboratorios e Institutos de Salud “Dr. Carlos G. Malbrán”, Buenos Aires, Argentina
Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental (IBYME-CONICET), Buenos Aires, Argentina
Hospital Pedro de Elizalde, Servicio de Cardiología, Sección Electrofisiología, Buenos Aires, Argentina
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:agglutinin; galectin 1; lipocortin 5; phytohemagglutinin; galectin 1; adult; aged; animal cell; Article; cell invasion assay; Chagas disease; clinical article; clinical assessment; controlled study; Doppler echocardiography; electrocardiography; enzyme linked immunosorbent assay; flow cytometry; gene deletion; genetic transfection; glycosylation; heart transplantation; histopathology; host parasite interaction; human; image analysis; immunoblotting; mouse; nonhuman; protein expression; reverse transcription polymerase chain reaction; RNA extraction; survival; thorax radiography; Trypanosoma cruzi; trypomastigote; animal; Brazil; cardiac muscle cell; cell culture; Chagas disease; disease model; female; host parasite interaction; immunology; knockout mouse; male; metabolism; middle aged; parasitemia; parasitology; pathology; physiology; survival analysis; Adult; Aged; Animals; Brazil; Cells, Cultured; Chagas Disease; Disease Models, Animal; Female; Galectin 1; Host-Parasite Interactions; Humans; Male; Mice; Mice, Knockout; Middle Aged; Myocytes, Cardiac; Parasitemia; Survival Analysis; Trypanosoma cruzi
Año:2015
Volumen:9
Número:10
DOI: http://dx.doi.org/10.1371/journal.pntd.0004148
Título revista:PLoS Neglected Tropical Diseases
Título revista abreviado:PLoS. Negl. Trop. Dis.
ISSN:19352727
CAS:galectin 1, 258495-34-0; lipocortin 5, 111237-10-6; phytohemagglutinin, 9008-97-3; Galectin 1
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19352727_v9_n10_p_Benatar

Referencias:

  • Moncayo, A., Silveira, A.C., Current epidemiological trends for Chagas disease in Latin America and future challenges in epidemiology, surveillance and health policy (2009) Mem Inst Oswaldo Cruz, 104, pp. 17-30. , 19753454, .;:–
  • http://apps.who.int/gb/ebwha/pdf_files/WHA63/A63_17-en.pdf, World Health Organization. Chagas disease: control and elimination. UNDP/World Bank/WHO. (Accessed 2011 Nov 9); 2010; Schumis, G.A., Yadon, Z.E., Chagas disease: a Latin American health problem becoming a world health problem (2010) Acta Trop, 115, pp. 14-21. , 10.1016/j.actatropica.2009.11.003, 19932071, .;:–
  • Coura, J.R., Viñas, P.A., Chagas disease: a new worldwide challenge (2010) Nature, 465, pp. 56-57. , .;:–
  • Alves, M.J., Colli, W., Trypanosoma cruzi: adhesion to the host cell and intracellular survival (2007) IUBMB Life, 59, pp. 274-279. , 17505965, .;:–
  • Rassi, A., Jr., Rassi, A., Marin-Neto, J.A., Chagas disease (2010) Lancet, 375, pp. 1388-1402. , 10.1016/S0140-6736(10)60061-X, 20399979, .;:–
  • Machado, F.S., Jelicks, L.A., Kirchhoff, L.V., Shirani, J., Nagajyothi, F., Mukherjee, S., Chagas heart disease: report on recent developments (2012) Cardiol Rev, 20, pp. 53-65. , 22293860, ..;:–
  • Parada, H., Carrasco, H.A., Añez, N., Fuenmayor, C., Inglessis, I., Cardiac involvement is a constant finding in acute Chagas' disease: a clinical, parasitological and histopathological study (1997) Int J Cardiol, 60, pp. 49-54. , 9209939, .;:–
  • Elizari, M.V., Chiale, P.A., Cardiac arrhythmias in Chagas' heart disease (1993) J Cardiovasc Electrophysiol, 4, pp. 596-608. , 8269325, .;:–
  • Chiale, P.A., Ferrari, I., Autoantibodies in Chagas' cardiomyopathy and arrhythmias (2001) Autoimmunity, 34, pp. 205-210. , 11908779, .;:–
  • Zacks, M.A., Wen, J.J., Vyatkina, G., Bhatia, V., Garg, N., An overview of chagasic cardiomyopathy: pathogenic importance of oxidative stress (2005) An Acad Bras Cienc, 77, pp. 695-715. , 16341444, .;:–
  • Tanowitz, H.B., Machado, F.S., Jelicks, L.A., Shirani, J., de Carvalho, A.C., Spray, D.C., Perspectives on Trypanosoma cruzi-induced heart disease (Chagas disease) (2009) Prog Cardiovasc Dis, 51, pp. 524-539. , 10.1016/j.pcad.2009.02.001, 19410685, ..;:–
  • Bonney, K.M., Engman, D.M., Chagas Heart Disease Pathogenesis: One Mechanism or Many? (2008) Clin Mol Med, 8, pp. 510-518. , .;:–
  • Machado, F.S., Dutra, W.O., Esper, L., Gollob, K.J., Teixeira, M.M., Factor, S.M., Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease (2012) Semin Immunopathol, 34, pp. 753-770. , 10.1007/s00281-012-0351-7, 23076807, ..;:–
  • Cunha-Neto, E., Teixeira, P.C., Nogueira, L.G., Kalil, J., Autoimmunity (2011) Adv Parasitol, 76, pp. 129-152. , 10.1016/B978-0-12-385895-5.00006-2, 21884890, .;:–
  • Teixeira, A.R.L., Hecht, M.M., Guimaro, M.C., Sousa, A.O., Nitz, N., Pathogenesis of Chagas’ Disease: Parasite Persistence and Autoimmunity (2011) Clin Microbio Rev, 24, pp. 592-630. , .;:–
  • Nagajyothi, F., Machado, F.S., Burleigh, B.A., Jelicks, L.A., Scherer, P.E., Mukherjee, S., Mechanism of Trypanosoma cruzi persistence in Chagas disease (2012) Cell Microbiol, 14, pp. 634-643. , 10.1111/j.1462-5822.2012.01764.x, 22309180, ..;:–
  • Di Lella, S., Sundblad, V., Cerliani, J.P., Guardia, C.M., Estrin, D.A., Vasta, G.R., When galectins recognize glycans: from biochemistry to physiology and back again (2011) Biochemistry, 50, pp. 7842-7857. , 10.1021/bi201121m, 21848324, ..;:–
  • Rabinovich, G.A., Croci, D.O., Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer (2012) Immunity, 36, pp. 322-335. , 10.1016/j.immuni.2012.03.004, 22444630, .;:–
  • Pace, K.E., Lee, C., Stewart, P.L., Baum, L.G., Restricted receptor segregation into membrane microdomains occurs on human T cells during apoptosis induced by galectin–1 (1999) J Immunol, 163, pp. 3801-3811. , 10490978, .;:–
  • Rabinovich, G.A., Daly, G., Dreja, H., Tailor, H., Riera, C.M., Hirabayashi, J., Recombinant galectin–1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis (1999) J Exp Med, 190, pp. 385-398. , 10430627, ..;:–
  • Thijssen, V.L., Postel, R., Brandwijk, R.J., Dings, R.P., Nesmelova, I., Satijn, S., Galectin–1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy (2006) Proc Natl Acad Sci USA, 103, pp. 15975-15980. , 17043243, ..;:–
  • Toscano, M.A., Bianco, G.A., Ilarregui, J.M., Croci, D.O., Correale, J., Hernandez, J.D., Differential glycosylation of TH1, TH2 and TH–17 effector cells selectively regulates susceptibility to cell death (2007) Nat Immunol, 8, pp. 825-834. , 17589510, ..;:–
  • Liu, F.T., Rabinovich, G.A., Galectins: regulators of acute and chronic inflammation (2010) Ann NY Acad Sci, 1183, pp. 158-182. , 10.1111/j.1749-6632.2009.05131.x, 20146714, .;:–
  • Croci, D.O., Cerliani, J.P., Dalotto-Moreno, T., Méndez-Huergo, S.P., Mascanfroni, I.D., Dergan-Dylon, S., Glycosylation-dependent lectin-receptor interactions preserve angiogenesis in anti-VEGF refractory tumors (2014) Cell, 156, pp. 744-758. , 10.1016/j.cell.2014.01.043, 24529377, ..;:–
  • Seropian, I.M., Cerliani, J.P., Toldo, S., Van Tassell, B.W., Ilarregui, J.M., González, G.E., Galectin–1 controls cardiac inflammation and ventricular remodeling during acute myocardial infarction (2013) Am J Pathol, 182, pp. 29-40. , 10.1016/j.ajpath.2012.09.022, 23142379, ..;:–
  • Giordanengo, L., Gea, S., Barbieri, G., Rabinovich, G.A., Anti-galectin–1 autoantibodies in human Trypanosoma cruzi infection: differential expression of this beta-galactoside-binding protein in cardiac Chagas' disease (2001) Clin Exp Immunol, 124, pp. 266-273. , 11422204, .;:–
  • Zúñiga, E., Gruppi, A., Hirabayashi, J., Kasai, K.I., Rabinovich, G.A., Regulated expression and effect of galectin–1 on Trypanosoma cruzi-infected macrophages: modulation of microbicidal activity and survival (2001) Infect Immun, 69, pp. 6804-6812. , 11598053, .;:–
  • Barrionuevo, P., Beigier-Bompadre, M., Ilarregui, J.M., Toscano, M.A., Bianco, G.A., Isturiz, M.A., A novel function for galectin–1 at the crossroad of innate and adaptive immunity: galectin–1 regulates monocyte/macrophage physiology through a non apoptotic ERK-dependent pathway (2007) J Immunol, 178, pp. 436-445. , 17182582, ..;:–
  • Trischmann, T.M., Bloom, B.R., Trypanosoma cruzi: ability of T-cell-enriched and -depleted lymphocyte populations to passively protect mice (1980) Exp Parasitol, 49, pp. 225-232. , 6767621, .;:–
  • Wynne de Martini, G.J., Abramo Orrego, L., de Rissio, A.M., Alvarez, M., Mujica, L.P., Culture of Trypanosoma cruzi in a monophasic medium. Application to large-scale cultures in fermentation processes (1980) Medicina (B Aires), 40, pp. 109-114. , .;:–
  • Claycomb, W.C., Lanson, N.A., Jr., Stallworth, B.S., Egeland, D.B., Delcarpio, J.B., Bahinski, A., HL–1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte (1998) Proc Natl Acad Sci USA, 95, pp. 2979-2984. , 9501201, ..;:–
  • Rabinovich, G.A., Daly, G., Dreja, H., Tailor, H., Riera, C.M., Hirabayashi, J., Recombinant galectin–1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis (1999) J Exp Med, 190, pp. 385-398. , 10430627, ..;:–
  • Aretz, H.G., Billingham, M.E., Edwards, W.D., Factor, S.M., Fallon, J.T., Fenoglio, J.J., Myocarditis, a histopathological definition and classification (1987) Am J Cardiovasc Pathol, 1, pp. 3-14. , 3455232, ..;:–
  • Tarleton, R.L., Sun, J., Zhang, L., Postan, M., Depletion of T-cell subpopulations results in exacerbation of myocarditis and parasitism in experimental Chagas' disease (1994) Infect Immun, 62, pp. 1820-1829. , 8168945, .;:–
  • Castro-Sesquen, Y.E., Gilman, R.H., Paico, H., Yauri, V., Angulo, N., Ccopa, F., Cell death and serum markers of collagen metabolism during cardiac remodeling in Cavia porcellus experimentally infected with Trypanosoma cruzi (2013) PLoS Negl Trop Dis, 7, p. e1996. , 10.1371/journal.pntd.0001996, 23409197, ..;:
  • Stahl, P., Ruppert, V., Meyer, T., Schmidt, J., Campos, M.A., Gazzinelli, R.T., Trypomastigotes and amastigotes of Trypanosoma cruzi induce apoptosis and STAT3 activation in cardiomyocytes in vitro (2013) Apoptosis, 18, pp. 653-663. , 10.1007/s10495-013-0822-x, 23435997, ..;:–
  • Epting, C.L., Coates, B.M., Engman, D.M., Molecular mechanisms of host cell invasion by Trypanosoma cruzi (2010) Exp Parasitol, 126, pp. 283-291. , 10.1016/j.exppara.2010.06.023, 20599990, .;:–
  • Caradonna, K.L., Burleigh, B.A., Mechanisms of host cell invasion by Trypanosoma cruzi (2011) Adv. Parasitol, 76, pp. 33-61. , 10.1016/B978-0-12-385895-5.00002-5, 21884886, .;:–
  • Nagajyothi, F., Machado, F.S., Burleigh, B.A., Jelicks, L.A., Scherer, P.E., Mukherjee, S., Mechanisms of Trypanosoma cruzi persistence in Chagas disease (2012) Cell Microbiol, 14, pp. 634-643. , 10.1111/j.1462-5822.2012.01764.x, 22309180, ..;:–
  • Calvet, C.M., Melo, T.G., Garzoni, L.R., Oliveira, F.O., Jr., Neto, D.T., Current understanding of the Trypanosoma cruzi-cardiomyocyte interaction (2012) Front Immunol, 30, p. 327. , ..;:
  • Vasta, G.R., Roles of galectins in infection (2009) Nat Rev Microbiol, 7, pp. 424-438. , 10.1038/nrmicro2146, 19444247, .;:–
  • Sato, S., Bhaumik, P., St-Pierre, G., Pelletier, I., Role of galectin–3 in the initial control of Leishmania infection (2014) Crit Rev Immunol, 34, pp. 147-175. , 24940913, .;:–
  • Pineda, M.A., Corvo, L., Soto, M., Fresno, M., Bonay, P., Interactions of human galectins with Trypanosoma cruzi: binding profile correlate with genetic clustering of lineages (2015) Glycobiology, 25, pp. 197-210. , 10.1093/glycob/cwu103, 25267603, .;:–
  • Machado, F.C., Cruz, L., da Silva, A.A., Cruz, M.C., Mortara, R.A., Roque-Barreira, M.C., Recruitment of galectin–3 during cell invasion and intracellular trafficking of Trypanosoma cruzi extracellular amastigotes (2014) Glycobiology, 24, pp. 179-184. , 10.1093/glycob/cwt097, 24225883, ..;:–
  • Silva-Monteiro, E., Reis Lorenzato, L., Kenji Nihei, O., Junqueira, M., Rabinovich, G.A., Hsu, D.K., Altered expression of galectin–3 induces cortical thymocyte depletion and premature exit of immature thymocytes during Trypanosoma cruzi infection (2007) Am J Pathol, 170, pp. 546-556. , 17255323, ..;:–
  • Moody, T.N., Ochieng, J., Villalta, F., Novel mechanism that Trypanosoma cruzi uses to adhere to the extracellular matrix mediated by human galectin–3 (2000) FEBS Lett, 470, pp. 305-308. , 10745086, .;:–
  • Kleshchenko, Y.Y., Moody, T.N., Furtak, V.A., Ochieng, J., Lima, M.F., Villalta, F., Human galectin–3 promotes Trypanosoma cruzi adhesion to human coronary artery smooth muscle cells (2004) Infect Immun, 72, pp. 6717-6721. , 15501810, .;:–
  • Acosta-Rodríguez, E.V., Montes, C.L., Motrán, C.C., Zuniga, E.I., Liu, F.T., Rabinovich, G.A., Galectin–3 mediates IL-4-induced survival and differentiation of B cells: functional cross-talk and implications during Trypanosoma cruzi infection (2004) J Immunol, 172, pp. 493-502. , 14688359, .;:–
  • Pineda, M.A., Cuervo, H., Fresno, M., Soto, M., Bonay, P., Lack of galectin–3 prevents cardiac fibrosis and effective immune responses in a murine model of Trypanosoma cruzi infection (2015) J Infect Dis, , .. pii: jiv185
  • Starossom, S.C., Mascanfroni, I.D., Imitola, J., Cao, L., Raddassi, K., Hernandez, S.F., Galectin–1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration (2012) Immunity, 37, pp. 249-263. , 10.1016/j.immuni.2012.05.023, 22884314, ..;:–
  • Zuñiga, E., Rabinovich, G.A., Iglesias, M.M., Gruppi, A., Regulated expression of galectin–1 during B-cell activation and implications for T-cell apoptosis (2001) J Leukoc Biol, 70, pp. 73-79. , 11435488, .;:–
  • Tarleton, R.L., Zhang, L., Chagas disease etiology: autoimmunity or parasite persistence? (1999) Parasitol Today, 15, pp. 94-99. , 10322321, .;:–
  • Tarleton, R.L., Koller, B.H., Latour, A., Postan, M., Susceptibility of beta 2-microglobulin-deficient mice to Trypanosoma cruzi infection (1992) Nature, 356, pp. 338-340. , 1549177, .;:–
  • Tarleton, R.L., Grusby, M.J., Postan, M., Glimcher, L.H., Trypanosoma cruzi infection in MHC-deficient mice: further evidence for the role of both class I- and class II-restricted T cells in immune resistance and disease (1996) Int Immunol, 8, pp. 13-22. , 8671585, .;:–
  • Styrt, B., Sugarman, B., Estrogens and infection (1991) Rev Infect Dis, 13, pp. 1139-1150. , 1775847, .;:–
  • Grossman, C., Possible underlying mechanisms of sexual dimorphism in the immune response, fact and hypothesis (1989) J Steroid Biochem, 34, pp. 241-251. , 2696846, .;:–
  • de Souza, E.M., Rivera, M.T., Araújo-Jorge, T.C., de Castro, S.L., Modulation induced by estradiol in the acute phase of Trypanosoma cruzi infection in mice (2001) Parasitol Res, 87, pp. 513-520. , 11484845, .;:–
  • Micucci, L.R., Bazán, P.C., Fauro, R., Baez, A., Lo Presti, M.S., Triquel, M.F., Importance of hostsex in the development of Trypanosoma cruzi infection (2010) Rev Fac Cien Med Univ Nac Cordoba, 67, pp. 73-76. , 21450143, ..;:–
  • Poncini, C.V., Ilarregui, J.M., Batalla, E.I., Engels, S., Cerliani, J.P., Cucher, M.A., Trypanosoma cruzi infection imparts a regulatory program in dendritic cells and T cells via galectin-1-dependent mechanisms (2015) J. Immunol, , ..; in press
  • Murfin, D.J., Choromanski, L., Kuhn, R.E., Relationship of route of infection to susceptibility and immune response of inbred mice to Y strain Trypanosoma cruzi (1989) Am J Trop Med Hyg, 41, pp. 41-49. , 2504068, .;:–
  • Martin, D.L., Weatherly, D.B., Laucella, S.A., Cabinian, M.A., Crim, M.T., Sullivan, S., CD8+ T-Cell responses to Trypanosoma cruzi are highly focused on strain-variant trans-sialidase epitopes (2006) PLoS Pathog, 2 (8), p. e77. , 16879036, ..;():
  • Alba Soto, C.D., Mirkin, G.A., Solana, M.E., González Cappa, S.M., Trypanosoma cruzi infection modulates in vivo expression of major histocompatibility complex class II molecules on antigen-presenting cells and T-cell stimulatory activity of dendritic cells in a strain-dependent manner (2003) Infect Immun, 71, pp. 1194-1199. , 12595432, .;:–
  • Toscano, M.A., Tongren, J.E., de Souza, J.B., Liu, F.T., Riley, E.M., Rabinovich, G.A., Endogenous galectin–3 controls experimental malaria in a species-specific manner (2012) Parasite Immunol, 34, pp. 383-387. , 10.1111/j.1365-3024.2012.01366.x, 22486577, .;:–
  • Vray, B., Camby, I., Vercruysse, V., Mijatovic, T., Bovin, N.V., Ricciardi-Castagnoli, P., Up-regulation of galectin–3 and its ligands by Trypanosoma cruzi infection with modulation of adhesion and migration of murine dendritic cells (2004) Glycobiology, 14, pp. 647-657. , 15044384, ..;:–
  • Kranz, C., Basinger, A.A., Güçsavaş-Calikoğlu, M., Sun, L., Powell, C.M., Henderson, F.W., Expanding spectrum of congenital disorder of glycosylation Ig (CDG-Ig): sibs with a unique skeletal dysplasia, hypogammaglobulinemia, cardiomyopathy, genital malformations, and early lethality (2007) Am J Med Genet A, 143A, pp. 1371-1378. , 17506107, ..;:–
  • Montpetit, M.L., Stocker, P.J., Schwetz, T.A., Harper, J.M., Norring, S.A., Schaffer, L., Regulated and aberrant glycosylation modulate cardiac electrical signaling (2009) Proc Natl Acad Sci USA, 106, pp. 16517-16522. , 10.1073/pnas.0905414106, 19666501, ..;:–
  • Watanabe, I., Zhu, J., Sutachan, J.J., Gottschalk, A., Recio-Pinto, E., Thornhill, W.B., The glycosylation state of Kv1.2 potassium channels affects trafficking, gating, and simulated action potentials (2007) Brain Res, 1144, pp. 1-18. , 17324383, .;:–

Citas:

---------- APA ----------
Benatar, A.F., García, G.A., Bua, J., Cerliani, J.P., Postan, M., Tasso, L.M., Scaglione, J.,..., Gómez, K.A. (2015) . Galectin-1 Prevents Infection and Damage Induced by Trypanosoma cruzi on Cardiac Cells. PLoS Neglected Tropical Diseases, 9(10).
http://dx.doi.org/10.1371/journal.pntd.0004148
---------- CHICAGO ----------
Benatar, A.F., García, G.A., Bua, J., Cerliani, J.P., Postan, M., Tasso, L.M., et al. "Galectin-1 Prevents Infection and Damage Induced by Trypanosoma cruzi on Cardiac Cells" . PLoS Neglected Tropical Diseases 9, no. 10 (2015).
http://dx.doi.org/10.1371/journal.pntd.0004148
---------- MLA ----------
Benatar, A.F., García, G.A., Bua, J., Cerliani, J.P., Postan, M., Tasso, L.M., et al. "Galectin-1 Prevents Infection and Damage Induced by Trypanosoma cruzi on Cardiac Cells" . PLoS Neglected Tropical Diseases, vol. 9, no. 10, 2015.
http://dx.doi.org/10.1371/journal.pntd.0004148
---------- VANCOUVER ----------
Benatar, A.F., García, G.A., Bua, J., Cerliani, J.P., Postan, M., Tasso, L.M., et al. Galectin-1 Prevents Infection and Damage Induced by Trypanosoma cruzi on Cardiac Cells. PLoS. Negl. Trop. Dis. 2015;9(10).
http://dx.doi.org/10.1371/journal.pntd.0004148