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DTU I isolates of Trypanosoma cruzi induce upregulation of Galectin-3 in murine myocarditis and fibrosis

Published online by Cambridge University Press:  13 February 2014

MARÍA F. FERRER ,
CARLA A. PASCUALE ,
RICARDO M. GOMEZ  and
MARÍA S. LEGUIZAMÓN
MARÍA F. FERRER
Affiliation:
Instituto de Biotecnología y Biología Molecular, Universidad Nacional de La Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
CARLA A. PASCUALE
Affiliation:
Instituto de Microbiología y Parasitología Médica, Universidad de Buenos Aires-CONICET, Argentina Instituto de Investigaciones Biotecnológicas, Instituto Tecnológico de Chascomús, Universidad Nacional de San Martin-CONICET, Argentina
RICARDO M. GOMEZ*
Affiliation:
Instituto de Biotecnología y Biología Molecular, Universidad Nacional de La Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
MARÍA S. LEGUIZAMÓN*
Affiliation:
Instituto de Microbiología y Parasitología Médica, Universidad de Buenos Aires-CONICET, Argentina Instituto de Investigaciones Biotecnológicas, Instituto Tecnológico de Chascomús, Universidad Nacional de San Martin-CONICET, Argentina
*
*Corresponding authors. Ricardo M. Gómez, Instituto de Biotecnología y Biología Molecular, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Calle 49 y 115, 1900 La Plata, Argentina. E-mail: rmg@biol.unlp.edu.ar
*María Susana Leguizamón, Instituto de Microbiología y Parasitología Médica, Facultad de Medicina, Universidad de Buenos Aires, Paraguay 2155, Piso 13, 1121, Buenos Aires, Argentina. E-mail: sleguiza@fmed.uba.ar
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Summary

Chagas heart disease is a major public concern since 30% of infected patients develop cardiac alterations. The relationship between Trypanosoma cruzi discrete typing units (DTUs) and the biological properties exhibited by the parasite population has yet to be elucidated. In this study, we analysed the expression of α-smooth muscle actin (α-SMA) and galectin-3 (Gal-3) associated with cardiac extracellular matrix (ECM) remodelling a murine chronic cardiomyopathy induced by Tc I genotypes. We found the induction of myocarditis was associated with the upregulation of Col I, α-SMA, Gal-3, IFN-γ and IL-13, as analysed by q-PCR. In myocardial areas of fibrosis, the intensity of myocarditis and significant ECM remodelling correlated with the presence of Col I-, Gal-3- and α-SMA-positive cells. These results are promising for the further efforts to evaluate the relevance of Gal-3 in Chagas heart disease, since this galectin was proposed as a prognosis marker in heart failure patients.

Keywords

Chagas diseasegalectin-3fibrosissmooth muscle actinDTU
Type
Research Article
Information
Parasitology , Volume 141 , Issue 6 , May 2014 , pp. 849 - 858
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Copyright © Cambridge University Press 2014 

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References

REFERENCES

Acosta-Rodriguez, E. V., Montes, C. L., Motran, C. C., Zuniga, E. I., Liu, F. T., Rabinovich, G. A. and Gruppi, A. (2004). Galectin-3 mediates IL-4-induced survival and differentiation of B cells: functional cross-talk and implications during Trypanosoma cruzi infection. Journal of Immunology 172, 493–502. doi: 10.1007/s00430-011-0192-3.CrossRefGoogle ScholarPubMed
Andrade, S. G. and Grimaud, J. A. (1986). Chronic murine myocarditis due to Trypanosoma cruzi – an ultrastructural study and immunochemical characterization of cardiac interstitial matrix. Memórias do Instituto Oswaldo Cruz 81, 29–41. doi: 10.1590/S0074-02761986000100004.CrossRefGoogle ScholarPubMed
Araujo-Jorge, T. C., Waghabi, M. C., Bailly, S. and Feige, J. J. (2012). The TGF-beta pathway as an emerging target for Chagas disease therapy. Clinical Pharmacology and Therapeutics 92, 613–621. doi: 10.1038/clpt2012102 [pii].CrossRefGoogle ScholarPubMed
Bahia-Oliveira, L. M., Gomes, J. A., Rocha, M. O., Moreira, M. C., Lemos, E. M., Luz, Z. M., Pereira, M. E., Coffman, R. L., Dias, J. C., Cancado, J. R., Gazzinelli, G. and Correa-Oliveira, R. (1998). IFN-gamma in human Chagas’ disease: protection or pathology? Brazilian Journal of Medical and Biological Research 31, 127–131. doi: 10.1590/S0100-879X1998000100017.Google Scholar
Bonney, K. M. and Engman, D. M. (2008). Chagas heart disease pathogenesis: one mechanism or many? Current Molecular Medicine 8, 510–518. doi: 10.2174/156652408785748004.CrossRefGoogle ScholarPubMed
Brandariz, S., Schijman, A., Vigliano, C., Arteman, P., Viotti, R., Beldjord, C. and Levin, M. J. (1995). Detection of parasite DNA in Chagas’ heart disease. Lancet 346, 1370–1371. doi: 10.1016/S0140-6736(95)92388-8.CrossRefGoogle ScholarPubMed
Burgos, J. M., Diez, M., Vigliano, C., Bisio, M., Risso, M., Duffy, T., Cura, C., Brusses, B., Favaloro, L., Leguizamon, M. S., Lucero, R. H., Laguens, R., Levin, M. J., Favaloro, R. and Schijman, A. G. (2010). Molecular identification of Trypanosoma cruzi discrete typing units in end-stage chronic Chagas heart disease and reactivation after heart transplantation. Clinical Infectious Disease 51, 485–495. doi: 10.1086/655680.CrossRefGoogle ScholarPubMed
Burgos, J. M., Risso, M. G., Breniere, S. F., Barnabe, C., Campetella, O. and Leguizamon, M. S. (2013). Differential distribution of genes encoding the virulence factor trans-sialidase along Trypanosoma cruzi discrete typing units. PLoS ONE 8, e58967. doi: 10.1371/journal.pone.0058967 PONE-D-12-38981 [pii].Google Scholar
Cain, B. S., Meldrum, D. R., Dinarello, C. A., Meng, X., Joo, K. S., Banerjee, A. and Harken, A. H. (1999). Tumor necrosis factor-alpha and interleukin-1beta synergistically depress human myocardial function. Critical Care Medicine 27, 1309–1318. doi: 10.1097/00003246-199907000- 00018.Google Scholar
Calvet, C. M., Melo, T. G., Garzoni, L. R., Oliveira, F. O., Neto, D. T., , N. S. L.M., Meirelles, L. and Pereira, M. C. (2012). Current understanding of the Trypanosoma cruzi-cardiomyocyte interaction. Frontiers in Immunology 3, 327. doi: 10.3389/fimmu.2012.00327.Google Scholar
Campbell, D. A., Westenberger, S. J. and Sturm, N. R. (2004). The determinants of Chagas disease: connecting parasite and host genetics. Current Molecular Medicine 4, 549–562. doi: 10.2174/1566524043360249.Google Scholar
Carranza, J. C., Valadares, H. M., D'Avila, D. A., Baptista, R. P., Moreno, M., Galvao, L. M., Chiari, E., Sturm, N. R., Gontijo, E. D., Macedo, A. M. and Zingales, B. (2009). Trypanosoma cruzi maxicircle heterogeneity in Chagas disease patients from Brazil. International Journal for Parasitology 39, 963–973. doi: S0020-7519(09)00095-2 [pii] 10.1016/j.ijpara.2009.01.009.Google Scholar
Cunha-Neto, E., Rizzo, L. V., Albuquerque, F., Abel, L., Guilherme, L., Bocchi, E., Bacal, F., Carrara, D., Ianni, B., Mady, C. and Kalil, J. (1998). Cytokine production profile of heart-infiltrating T cells in Chagas’ disease cardiomyopathy. Brazilian Journal of Medical and Biological Research 31, 133–137. doi: 10.1590/S0100-879X1998000100018.Google Scholar
Cunha-Neto, E., Dzau, V. J., Allen, P. D., Stamatiou, D., Benvenutti, L., Higuchi, M. L., Koyama, N. S., Silva, J. S., Kalil, J. and Liew, C. C. (2005). Cardiac gene expression profiling provides evidence for cytokinopathy as a molecular mechanism in Chagas’ disease cardiomyopathy. American Journal of Pathology 167, 305–313. doi: S0002-9440(10)62976-8 [pii]10.1016/S0002-9440(10)62976-8.Google Scholar
de Boer, R. A., Yu, L. and van Veldhuisen, D. J. (2010). Galectin-3 in cardiac remodeling and heart failure. Current Heart Failure Reports 7, 1–8. doi: 10.1007/s11897-010-0004-x.Google Scholar
Desmouliere, A., Redard, M., Darby, I. and Gabbiani, G. (1995). Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. American Journal of Pathology 146, 56–66. doi: PMC1870783.Google Scholar
Di Noia, J. M., Buscaglia, C. A., De Marchi, C. R., Almeida, I. C. and Frasch, A. C. (2002). A Trypanosoma cruzi small surface molecule provides the first immunological evidence that Chagas' disease is due to a single parasite lineage. Journal of Experimental Medicine 195, 401–413. doi: 10.1084/jem.20011433.CrossRefGoogle ScholarPubMed
Dutra, W. O., Menezes, C. A., Villani, F. N., da Costa, G. C., da Silveira, A. B., Reis, D. and Gollob, K. J. (2009). Cellular and genetic mechanisms involved in the generation of protective and pathogenic immune responses in human Chagas disease. Memórias do Instituto Oswaldo Cruz 104 (Suppl. 1), 208–218. doi: S0074-02762009000900027 [pii].Google Scholar
Feldman, A. M. and McNamara, D. (2000). Myocarditis. New England Journal of Medicine 343, 1388–1398. doi: 10.1056/NEJM200011093431908.Google Scholar
Feliciangeli, M. D., Dujardin, J. P., Bastrenta, B., Mazzarri, M., Villegas, J., Flores, M. and Munoz, M. (2002). Is Rhodnius robustus (Hemiptera: Reduviidae) responsible for Chagas disease transmission in Western Venezuela? Tropical Medicine and International Health 7, 280–287. doi: 853 [pii].Google Scholar
Frangogiannis, N. G. (2006). Targeting the inflammatory response in healing myocardial infarcts. Current Medicinal Chemistry 13, 1877–1893. doi: 10.2174/092986706777585086.Google Scholar
Frangogiannis, N. G. (2008). The immune system and cardiac repair. Pharmacology Research 58, 88–111. doi: 10.1016/j.phrs.2008.06.007 S1043-6618(08)00108-4 [pii].Google Scholar
Freitas, J. M., Lages-Silva, E., Crema, E., Pena, S. D. and Macedo, A. M. (2005). Real time PCR strategy for the identification of major lineages of Trypanosoma cruzi directly in chronically infected human tissues. International Journal of Parasitology 35, 411–417. doi: S0020-7519(04)00260-7 [pii] 10.1016/j.ijpara.2004.10.023.Google Scholar
Gomez, R. M., Castagnino, C. G. and Berria, M. I. (1992). Extracellular matrix remodelling after coxsackievirus B3-induced murine myocarditis. International Journal of Experimental Pathology 73, 643–653. doi: PMC2002023.Google Scholar
Gomez, R. M., Vieira, M. L., Schattner, M., Malaver, E., Watanabe, M. M., Barbosa, A. S., Abreu, P. A., de Morais, Z. M., Cifuente, J. O., Atzingen, M. V., Oliveira, T. R., Vasconcellos, S. A. and Nascimento, A. L. (2008). Putative outer membrane proteins of Leptospira interrogans stimulate human umbilical vein endothelial cells (HUVECS) and express during infection. Microbial Pathogenesis 45, 315–322. doi: S0882-4010(08)00107-1 [pii] 10.1016/j.micpath.2008.08.004.CrossRefGoogle ScholarPubMed
Guhl, F. and Ramirez, J. D. (2011). Trypanosoma cruzi I diversity: towards the need of genetic subdivision? Acta Tropica 119, 1–4. doi: 10.1016/j.actatropica.2011.04.002 S0001-706X(11)00072-6 [pii].Google Scholar
Gurtner, G. C., Werner, S., Barrandon, Y. and Longaker, M. T. (2008). Wound repair and regeneration. Nature 453, 314–321. doi: 10.1038/nature07039 nature07039 [pii].CrossRefGoogle ScholarPubMed
Hardison, J. L., Wrightsman, R. A., Carpenter, P. M., Lane, T. E. and Manning, J. E. (2006). The chemokines CXCL9 and CXCL10 promote a protective immune response but do not contribute to cardiac inflammation following infection with Trypanosoma cruzi . Infection and Immunity 74, 125–134. doi: 74/1/125 [pii] 10.1128/IAI.74.1.125-134.2006.Google Scholar
Haudek, S. B., Taffet, G. E., Schneider, M. D. and Mann, D. L. (2007). TNF provokes cardiomyocyte apoptosis and cardiac remodeling through activation of multiple cell death pathways. Journal of Clinical Investigation 117, 2692–2701. doi: 10.1172/JCI29134.CrossRefGoogle ScholarPubMed
Henderson, N. C., Mackinnon, A. C., Farnworth, S. L., Poirier, F., Russo, F. P., Iredale, J. P., Haslett, C., Simpson, K. J. and Sethi, T. (2006). Galectin-3 regulates myofibroblast activation and hepatic fibrosis. Proceedings of the National Academy of Sciences USA 103, 5060–5065. doi: 0511167103 [pii] 10.1073/pnas.0511167103.Google Scholar
Henderson, N. C., Mackinnon, A. C., Farnworth, S. L., Kipari, T., Haslett, C., Iredale, J. P., Liu, F. T., Hughes, J. and Sethi, T. (2008). Galectin-3 expression and secretion links macrophages to the promotion of renal fibrosis. American Journal of Pathology 172, 288–298. doi: 10.2353/ajpath.2008.070726 S0002-9440(10)61796-8 [pii].Google Scholar
Jaquenod De Giusti, C., Alberdi, L., Frik, J., Ferrer, M. F., Scharrig, E., Schattner, M. and Gomez, R. M. (2011). Galectin-3 is upregulated in activated glia during Junin virus-induced murine encephalitis. Neuroscience Letters 501, 163–166. doi: 10.1016/j.neulet.2011.07.007 S0304-3940(11)01040-8 [pii].Google Scholar
Junqueira, L. C., Bignolas, G. and Brentani, R. R. (1979). Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochemistry Journal 11, 447–455. doi: 10.1007/BF01002772.Google Scholar
Kaviratne, M., Hesse, M., Leusink, M., Cheever, A. W., Davies, S. J., McKerrow, J. H., Wakefield, L. M., Letterio, J. J. and Wynn, T. A. (2004). IL-13 activates a mechanism of tissue fibrosis that is completely TGF-beta independent. Journal of Immunology 173, 4020–4029. doi: 173/6/4020 [pii].CrossRefGoogle ScholarPubMed
Kleshchenko, Y. Y., Moody, T. N., Furtak, V. A., Ochieng, J., Lima, M. F. and Villalta, F. (2004). Human galectin-3 promotes Trypanosoma cruzi adhesion to human coronary artery smooth muscle cells. Infection and Immunity 72, 6717–6721.Google Scholar
Kubota, T., McTiernan, C. F., Frye, C. S., Slawson, S. E., Lemster, B. H., Koretsky, A. P., Demetris, A. J. and Feldman, A. M. (1997). Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-alpha. Circulation Research 81, 627–635. doi: 10.1161/01.RES.81.4.627.Google Scholar
Lee, C. G., Homer, R. J., Zhu, Z., Lanone, S., Wang, X., Koteliansky, V., Shipley, J. M., Gotwals, P., Noble, P., Chen, Q., Senior, R. M. and Elias, J. A. (2001). Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor beta(1). Journal of Experimental Medicine 194, 809–821. doi: 10.1084/jem.194.6.809.Google Scholar
Liu, F. T. and Rabinovich, G. A. (2010). Galectins: regulators of acute and chronic inflammation. Annals of the New York Academy of Sciences 1183, 158–182. doi: 10.1111/j.1749-6632.2009.05131.x.CrossRefGoogle ScholarPubMed
Lok, D. J., Van Der Meer, P., de la Porte, P. W., Lipsic, E., Van Wijngaarden, J., Hillege, H. L. and van Veldhuisen, D. J. (2010). Prognostic value of galectin-3, a novel marker of fibrosis, in patients with chronic heart failure: data from the DEAL-HF study. Clinical Research in Cardiology 99, 323–328. doi: 10.1007/s00392-010-0125-y.Google Scholar
Macedo, A. M., Machado, C. R., Oliveira, R. P. and Pena, S. D. (2004). Trypanosoma cruzi: genetic structure of populations and relevance of genetic variability to the pathogenesis of Chagas disease. Memórias do Instituto Oswaldo Cruz 99, 1–12. doi: S0074-02762004000100001 [pii].CrossRefGoogle Scholar
Machado, F. S., Dutra, W. O., Esper, L., Gollob, K. J., Teixeira, M. M., Factor, S. M., Weiss, L. M., Nagajyothi, F., Tanowitz, H. B. and Garg, N. J. (2012). Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease. Seminars in Immunopathology 34, 753–770. doi: 10.1007/s00281-012-0351-7.CrossRefGoogle ScholarPubMed
Marin-Neto, J. A., Cunha-Neto, E., Maciel, B. C. and Simoes, M. V. (2007). Pathogenesis of chronic Chagas heart disease. Circulation 115, 1109–1123. doi: 115/9/1109 [pii] 10.1161/CIRCULATIONAHA.106.624296.CrossRefGoogle ScholarPubMed
Miles, M. A., Feliciangeli, M. D. and de Arias, A. R. (2003). American trypanosomiasis (Chagas’ disease) and the role of molecular epidemiology in guiding control strategies. British Medical Journal 326, 1444–1448. doi: 10.1136/bmj.326.7404.1444 326/7404/1444 [pii].Google Scholar
Moody, T. N., Ochieng, J. and Villalta, F. (2000). Novel mechanism that Trypanosoma cruzi uses to adhere to the extracellular matrix mediated by human galectin-3. FEBS Letters 470, 305–308.CrossRefGoogle Scholar
PAHO (2007). Health conditions and trends. In Health in the Americas, Vol. 1, pp. 58–207. Pan American Health Organization, Washington, DC, USA.Google Scholar
Paiva, C. N., Figueiredo, R. T., Kroll-Palhares, K., Silva, A. A., Silverio, J. C., Gibaldi, D., Pyrrho Ados, S., Benjamim, C. F., Lannes-Vieira, J. and Bozza, M. T. (2009). CCL2/MCP-1 controls parasite burden, cell infiltration, and mononuclear activation during acute Trypanosoma cruzi infection. Journal of Leukocyte Biology 86, 1239–1246. doi: 10.1189/jlb.0309187 jlb.0309187 [pii].CrossRefGoogle ScholarPubMed
Pilling, D., Fan, T., Huang, D., Kaul, B. and Gomer, R. H. (2009). Identification of markers that distinguish monocyte-derived fibrocytes from monocytes, macrophages, and fibroblasts. PLoS ONE 4, e7475. doi: 10.1371/journal.pone.0007475.Google Scholar
Ramirez, J. D., Guhl, F., Rendon, L. M., Rosas, F., Marin-Neto, J. A. and Morillo, C. A. (2010). Chagas cardiomyopathy manifestations and Trypanosoma cruzi genotypes circulating in chronic Chagasic patients. PLoS Neglected Tropical Diseases 4, e899. doi: 10.1371/journal.pntd.0000899.Google Scholar
Rassi, A. Jr., Rassi, A. and Marin-Neto, J. A. (2010). Chagas disease. Lancet 375, 1388–1402. doi: S0140-6736(10)60061-X [pii] 10.1016/S0140-6736(10)60061-X.Google Scholar
Risso, M. G., Garbarino, G. B., Mocetti, E., Campetella, O., Gonzalez Cappa, S. M., Buscaglia, C. A. and Leguizamon, M. S. (2004). Differential expression of a virulence factor, the trans-sialidase, by the main Trypanosoma cruzi phylogenetic lineages. Journal of Infectious Disease 189, 2250–2259. doi: 10.1086/420831 JID31720 [pii].Google Scholar
Rocha Rodrigues, D. B., dos Reis, M. A., Romano, A., Pereira, S. A., Teixeira Vde, P., Tostes, S. Jr. and Rodrigues, V. Jr. (2012). In situ expression of regulatory cytokines by heart inflammatory cells in Chagas’ disease patients with heart failure. Clinical and Developmental Immunology 2012, 361730. doi: 10.1155/2012/361730.Google Scholar
Roffe, E., Rothfuchs, A. G., Santiago, H. C., Marino, A. P., Ribeiro-Gomes, F. L., Eckhaus, M., Antonelli, L. R. and Murphy, P. M. (2012). IL-10 limits parasite burden and protects against fatal myocarditis in a mouse model of Trypanosoma cruzi infection. Journal of Immunology 188, 649–660. doi: 10.4049/jimmunol.1003845 jimmunol.1003845 [pii].Google Scholar
Sato, S. and Hughes, R. C. (1994). Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. Journal of Biological Chemistry 269, 4424–4430. doi: 10.2353/ajpath.2008.070726.Google Scholar
Shi, Q., Liu, X., Bai, Y., Cui, C., Li, J., Li, Y., Hu, S. and Wei, Y. (2011). In vitro effects of pirfenidone on cardiac fibroblasts: proliferation, myofibroblast differentiation, migration and cytokine secretion. PLoS ONE 6, e28134. doi: 10.1371/journal.pone.0028134 PONE-D-11-15265 [pii].CrossRefGoogle ScholarPubMed
Soares, M. B., de Lima, R. S., Rocha, L. L., Vasconcelos, J. F., Rogatto, S. R., dos Santos, R. R., Iacobas, S., Goldenberg, R. C., Iacobas, D. A., Tanowitz, H. B., de Carvalho, A. C. and Spray, D. C. (2010). Gene expression changes associated with myocarditis and fibrosis in hearts of mice with chronic chagasic cardiomyopathy. Journal of Infectious Disease 202, 416–426. doi: 10.1086/653481.CrossRefGoogle ScholarPubMed
Solana, M. E., Ferrer, M. F., Novoa, M. M., Song, W. C. and Gomez, R. M. (2012). Decay-accelerating factor 1 deficiency exacerbates Trypanosoma cruzi-induced murine chronic myositis. Muscle and Nerve 46, 582–587. doi: 10.1002/mus.23347.Google Scholar
Sun, Y. and Weber, K. T. (2000). Infarct scar: a dynamic tissue. Cardiovascular Research 46, 250–256. doi: S0008-6363(00)00032-8 [pii].Google Scholar
Tanowitz, H. B., Machado, F. S., Jelicks, L. A., Shirani, J., de Carvalho, A. C., Spray, D. C., Factor, S. M., Kirchhoff, L. V. and Weiss, L. M. (2009). Perspectives on Trypanosoma cruzi-induced heart disease (Chagas disease). Progress in Cardiovascular Disease 51, 524–539. doi: 10.1016/j.pcad.2009.02.001 S0033-0620(09)00012-7 [pii].CrossRefGoogle ScholarPubMed
Tarleton, R. L. (2001). Parasite persistence in the aetiology of Chagas disease. International Journal of Parasitology 31, 550–554. doi: S0020-7519(01)00158-8 [pii].Google Scholar
Tarleton, R. L. (2003). Chagas disease: a role for autoimmunity? Trends in Parasitology 19, 447–451. doi: S1471492203002228 [pii].Google Scholar
Teixeira, M. M., da Silva, F. M., Marcili, A., Umezawa, E. S., Shikanai-Yasuda, M. A., Cunha-Neto, E., Kalil, J., Stolf, N. and Stolf, A. M. (2006). Short communication: Trypanosoma cruzi lineage I in endomyocardial biopsy from a north-eastern Brazilian patient at end-stage chronic Chagasic cardiomyopathy. Tropical Medicine and International Health 11, 294–298. doi: 10.1111/j.1365-3156.2006.01575.x.Google Scholar
Turner, C. W., Lima, M. F. and Villalta, F. (2002). Trypanosoma cruzi uses a 45-kDa mucin for adhesion to mammalian cells. Biochemical and Biophysical Research Communications 290, 29–34. doi: 10.1006/bbrc.2001.6189.CrossRefGoogle ScholarPubMed
Villalta, F., Scharfstein, J., Ashton, A. W., Tyler, K. M., Guan, F., Mukherjee, S., Lima, M. F., Alvarez, S., Weiss, L. M., Huang, H., Machado, F. S. and Tanowitz, H. B. (2009). Perspectives on the Trypanosoma cruzi-host cell receptor interactions. Parasitology Research 104, 1251–1260. doi: 10.1007/s00436-009-1383-3.Google Scholar
Vray, B., Camby, I., Vercruysse, V., Mijatovic, T., Bovin, N. V., Ricciardi-Castagnoli, P., Kaltner, H., Salmon, I., Gabius, H. J. and Kiss, R. (2004). Up-regulation of galectin-3 and its ligands by Trypanosoma cruzi infection with modulation of adhesion and migration of murine dendritic cells. Glycobiology 14, 647–657. doi: 10.1093/glycob/cwh068.Google Scholar
WHO (2002). Control of Chagas disease. Report of a WHO Expert Committee. World Health Organization Technical Report Series 905, 1–109.Google Scholar
Zhu, Z., Homer, R. J., Wang, Z., Chen, Q., Geba, G. P., Wang, J., Zhang, Y. and Elias, J. A. (1999). Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. Journal of Clinical Investigation 103, 779–788. doi: 10.1172/JCI5909.Google Scholar
Zingales, B., Andrade, S. G., Briones, M. R., Campbell, D. A., Chiari, E., Fernandes, O., Guhl, F., Lages-Silva, E., Macedo, A. M., Machado, C. R., Miles, M. A., Romanha, A. J., Sturm, N. R., Tibayrenc, M., Schijman, A. G. and Second Satellite, M. (2009). A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memórias do Instituto Oswaldo Cruz 104, 1051–1054. doi: S0074-02762009000700021 [pii].Google Scholar
Zlochiver, S., Munoz, V., Vikstrom, K. L., Taffet, S. M., Berenfeld, O. and Jalife, J. (2008). Electrotonic myofibroblast-to-myocyte coupling increases propensity to reentrant arrhythmias in two-dimensional cardiac monolayers. Biophysical Journal 95, 4469–4480. doi: 10.1529/biophysj.108.136473.Google Scholar