Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-31T08:41:54.067Z Has data issue: false hasContentIssue false

Could angiotensin-modulating drugs be relevant for the treatment of Trypanosoma cruzi infection? A systematic review of preclinical and clinical evidence

Published online by Cambridge University Press:  20 February 2019

Thaiany G. Souza-Silva
Affiliation:
Department of Structural Biology, Institute of Biomedical Sciences, Federal University of Alfenas, Alfenas, 37130-001, Minas Gerais, Brazil
Lívia F. Diniz
Affiliation:
Department of Pathology and Parasitology, Institute of Biomedical Sciences, Federal University of Alfenas, Alfenas, 37130-001, Minas Gerais, Brazil
Ana Lia Mazzeti
Affiliation:
Department of Pathology and Parasitology, Institute of Biomedical Sciences, Federal University of Alfenas, Alfenas, 37130-001, Minas Gerais, Brazil
Andrea A. S. Mendonça
Affiliation:
Department of Structural Biology, Institute of Biomedical Sciences, Federal University of Alfenas, Alfenas, 37130-001, Minas Gerais, Brazil
Reggiani V. Gonçalves
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, 36570-000, Minas Gerais, Brazil
Rômulo D. Novaes*
Affiliation:
Department of Structural Biology, Institute of Biomedical Sciences, Federal University of Alfenas, Alfenas, 37130-001, Minas Gerais, Brazil
*
Author for correspondence: Rômulo D. Novaes, E-mail: romuonovaes@yahoo.com.br; romulo.novaes@unifal-mg.edu.br

Abstract

Although leucocytes are targets of renin-angiotensin system (RAS) effector molecules and RAS-modulating drugs exert immunomodulatory effects, their impact on Trypanosoma cruzi infection remains poorly understood. By using the framework of a systematic review, we integrated the preclinical and clinical evidence to investigate the relevance of angiotensin-inhibiting drugs on T. cruzi infections. From a comprehensive and structured search in biomedical databases, only original studies were analysed. In preclinical and clinical studies, captopril, enalapril and losartan were RAS-modulating drugs used. The main in vitro findings indicated that these drugs increased parasite uptake per host cells, IL-12 expression by infected dendritic cells and IFN-γ by T lymphocytes, in addition to attenuating IL-10 and IL-17 production by CD8 + T cells. In animal models, reduced parasitaemia, tissue parasitism, leucocytes infiltration and mortality were often observed in T. cruzi-infected animals receiving RAS-modulating drugs. In patients with Chagas’ disease, these drugs exerted a controversial impact on cytokine and hormone levels, and a limited effect on cardiovascular function. Considering a detailed evaluation of reporting and methodological quality, the current preclinical and clinical evidence is at high risk of bias, and we hope that our critical analysis will be useful in mitigating the risk of bias in further studies.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akat, PB, Bapat, TR, Murthy, MB, Karande, VB and Burute, SR (2010) Comparison of the efficacy and tolerability of telmisartan and enalapril in patients of mild to moderate essential hypertension. Indian Journal of Pharmacology 42, 153156.Google Scholar
Andrade, JP, Marin Neto, JA, Paola, AA, Vilas-Boas, F, Oliveira, GM, Bacal, F, Bocchi, EA, Almeida, DR, Fragata Filho, AA, da Moreira, MC, Xavier, SS, Oliveira Junior, WA and Dias, JC (2011) I Latin American Guideline for the diagnosis and treatment of Chagas’ heart disease: executive summary. Brazilian Cardiology Archives 96, 434442.Google Scholar
Angheben, A, Boix, L, Buonfrate, D, Gobbi, F, Bisoffi, Z, Pupella, S, Gandini, G and Aprili, G (2015) Chagas disease and transfusion medicine: a perspective from non-endemic countries. Blood Transfusion 13, 540550.Google Scholar
Balouz, V, Aguero, F and Buscaglia, CA (2017) Chagas disease diagnostic applications: present knowledge and future steps. Advances in parasitology 97, 145.Google Scholar
Barrias, ES, de Carvalho, TMU and Couza, W (2013) Trypanosoma cruzi: entry into mammalian host cells and parasitophorous vacuole formation. Frontiers in Immunology 4, 110.Google Scholar
Barroso, LC, Magalhaes, GS, Galvão, I, Reis, AC, Souza, DG, Sousa, LP, Santos, RAS, Campagnole-Santos, MJ, Pinho, V and Teixeira, MM (2017) Angiotensin-(1-7) promotes resolution of neutrophilic inflammation in a model of antigen-induced arthritis in mice. Frontiers in Immunology 8, 111.Google Scholar
Biolo, A, Ribeiro, AL and Clausell, N (2010) Chagas cardiomyopathy-where do we stand after a hundred years? Progress in Cardiolovascular Diseases 52, 300316.Google Scholar
Botoni, FA, Poole-Wilson, PA, Ribeiro, AL, Okonko, DO, Oliveira, BM, Pinto, AS, Teixeira, MM, Teixeira, AL Jr, Reis, AM, Dantas, JB, Ferreira, CS, Tavares, WC Jr and Rocha, MO (2007) A randomized trial of carvedilol after renin-angiotensin system inhibition in chronic Chagas cardiomyopathy. American Heart Journal 153, 18.Google Scholar
Botoni, FA, Ribeiro, ALP, Marinho, CC, Lima, MMO, Nunes, MCP and Rocha, MOC (2013) Treatment of Chagas cardiomyopathy. BioMed Research International 2013, 19.Google Scholar
Brener, Z (1973) Biology of Trypanosoma Cruzi. Annual Review of Microbiology 27, 347382.Google Scholar
Cabral-Piccin, MP, Guillermo, LV, Vellozo, NS, Filardy, AA, Pereira-Marques, ST, Rigoni, TS, Pereira-Manfro, WF, Dos Reis, GA and Lopes, MF (2016) Apoptotic CD8 T-lymphocytes disable macrophage-mediated immunity to Trypanosoma cruzi infection. Cell Death and Disease 7, 22322232.Google Scholar
Campos, MC, Leon, LL, Taylor, MC and Kelly, JM (2014) Benznidazole-resistance in Trypanosoma cruzi: evidence that distinct mechanisms can act in concert. Molecular and Biochemical Parasitology 193, 1719.Google Scholar
Cardillo, F, de Pinho, RT, Antas, PR and Mengel, J (2015) Immunity and immune modulation in Trypanosoma cruzi infection. Pathogens and Disease 73, 118.Google Scholar
Chatelain, E and Konar, N (2015) Translational challenges of animal models in Chagas disease drug development: a review. Drug design, development and therapy 9, 48074823.Google Scholar
Chumbinho, LC, Pizzini, CC, Oliveira, FS, Batista, W and Oliveira, GM (2012) Cardiorenal interaction during the acute phase of experimental Tripanosoma cruzi infection: the influence of aldosterone and the AT1 receptor on mortality. Journal of Experimental and Integrative Medicine 2, 199206.Google Scholar
Contreras, VT, Araujo-Jorge, TC, Bonaldo, MC, Thomaz, N, Barbosa, HS, Meirelles, Mde, N and Goldenberg, S (1988) Biological aspects of the Dm28c clone of Trypanosoma cruzi after metacyclogenesis in chemically defined media. Memories of the Oswaldo Cruz Institute 83, 123133.Google Scholar
Costerousse, O, Allegrini, J, Lopez, M and Alhenc-Gelas, F (1993) Angiotensin I-converting enzyme in human circulating mononuclear cells: genetic polymorphism of expression in T-lymphocytes. The Biochem Journal 290, 3340.Google Scholar
Cunha-Neto, E and Chevillard, C (2014) Chagas disease cardiomyopathy: immunopathology and genetics. Mediators of Inflammations 2014, 111.Google Scholar
da Costa, TA, Silva, MV, Mendes, MT, Carvalho-Costa, TM, Batista, LR, Lages-Silva, E, Rodrigues, V, Oliveira, CJ and Ramirez, LE (2014) Immunomodulation by Trypanosoma cruzi: toward understanding the association of dendritic cells with infecting TcI and TcII populations. Journal of Immunology Research 2014, 112.Google Scholar
de Paula Costa, G, Silva, RR, Pedrosa, MC, Pinho, V, de Lima, WG, Teixeira, MM, Bahia, MT and Talvani, A (2010) Enalapril prevents cardiac immune-mediated damage and exerts anti-Trypanosoma cruzi activity during acute phase of experimental Chagas disease. Parasite Immunology 32, 202208.Google Scholar
Dias, JC, Ramos, AN Jr, Gontijo, ED, Luquetti, A, Shikanai-Yasuda, MA, Coura, JR, Torres, RM, Melo, JR, Almeida, EA, Oliveira, W Jr, Silveira, AC, Rezende, JM, Pinto, FS, Ferreira, AW, Rassi, A, Fragata, AA Filho, Sousa, AS, Correia, D Filho, Jansen, AM, Andrade, GM, Britto, CF, Pinto, AY, Rassi, A Jr, Campos, DE, Abad-Franch, F, Santos, SE, Chiari, E, Hasslocher-Moreno, AM, Moreira, EF, Marques, DS, Silva, EL, Marin-Neto, JA, Galvão, LM, Xavier, SS, Valente, SA, Carvalho, NB, Cardoso, AV, Silva, RA, Costa, VM, Vivaldini, SM, Oliveira, SM, Valente, VD, Lima, MM and Alves, RV (2016) Brazilian consensus on Chagas disease, 2015. Epidemiology and Health Services: A Review of the Brazilian Unified Health System 25, 786.Google Scholar
Downs, SH and Black, N (1998) The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. Journal of Epidemiol and Community Health 52, 377384.Google Scholar
Eickhoff, CS, Lawrence, CT, Sagartz, JE, Bryant, LA, Labovitz, AJ, Gala, SS and Hoft, DF (2010) ECG detection of murine Chagasic cardiomyopathy. The Journal of Parasitology 96, 758764.Google Scholar
Felizardo, AA, Marques, DVB, Caldas, IS, Gonçalves, RV and Novaes, RD (2018) Could age and aging change the host response to systemic parasitic infections? A systematic review of preclinical evidence. Experimental Gerontology 104, 1727.Google Scholar
Fernandes, MC and Andrews, NW (2012) Host cell invasion by Trypanosoma cruzi: a unique strategy that promotes persistence. FEMS Microbiology Reviews 36, 734747.Google Scholar
Ferraz, ML, Gazzinelli, RT, Alves, RO, Urbina, JA and Romanha, AJ (2009) Absence of CD4 + T lymphocytes, CD8 + T lymphocytes, or B lymphocytes has different effects on the efficacy of posaconazole and benznidazole in treatment of experimental acute Trypanosoma cruzi infection. Antimicrobial Agents and Chemotherapy 53, 174179.Google Scholar
Fresno, M and Gironès, N (2018) Regulatory lymphoid and myeloid cells determine the cardiac immunopathogenesis of Trypanosoma cruzi infection. Frontiers in Microbiology 9, 110.Google Scholar
Garcia-Alvarez, A, Sitges, M, Pinazo, MJ, Regueiro-Cueva, A, Psada, E, Poyatos, S, Ortiz-Pérez, JT, Heras, M, Azqueta, M, Gascon, J and Sanz, G (2010) Chagas cardiomyopathy: The potential of diastolic dysfunction and brain natriuretic peptide in the early identification of cardiac damage. PLos neglected tropical diseases 4, e-826.Google Scholar
Goes, GR, Rocha, PS, Diniz, ARS, Aguiar, PHN, Machado, CR and Vieira, LQ (2016) Trypanosoma cruzi needs a signal provided by reactive oxygen species to infect macrophages. PLoS Negligence Tropical Disease 10, 125.Google Scholar
Gulin, JEN, Bisio, M, Rocco, DM, Altcheh, J, Solana, ME and García-Bournissen, F (2018) Molecular and biological characterization of a highly pathogenic Trypanosoma cruzi strain isolated from a patient with congenital infection. Experimental Parasitology 186, 5058.Google Scholar
Guo, YJ, Li, WH, Wu, R, Xie, Q and Cui, Q (2008) ACE2 overexpression inhibits angiotensin ii-induced monocyte chemoattractant protein-1 expression in macrophages. Archives of Medical Research 39, 149154.Google Scholar
Hernández-Fonseca, JP, Duran, A, Valero, N and Mosquera, J (2015) Losartan and enalapril decrease viral absorption and interleukin 1 beta production by macrophages in an experimental dengue virus infection. Archives of virology 160, 28622865.Google Scholar
Hoch, NE, Guzik, TJ, Chen, W, Deans, T, Maalouf, SA, Gratze, P, Weyand, C and Harrison, DG (2009) Regulation of T-cell function by endogenously produced angiotensin II. American Jornal of Physiology Regulatory, Integrative and Comparative Physiology 296, 208216.Google Scholar
Hodsman, GP, Isles, CG, Murray, GD, Usherwood, TP, Webb, DJ and Robertson, JI (1983) Factors related to first dose hypotensive effect of captopril: prediction and treatment. British Medical Journal 286, 832834.Google Scholar
Hooijmans, CR, Rovers, MM, de Vries, RB, Leenaars, M, Ritskes-Hoitinga, M and Langendam, MW (2014) SYRCLE's risk of bias tool for animal studies. BMC Medical Research Methodology 14, 19.Google Scholar
Hunter, CA, Ellis-Neyes, LA, Slifer, T, Kanaly, S, Grünig, G, Fort, M, Rennick, D and Araujo, FG (1997) IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. Journal of Immunology 158, 33113316.Google Scholar
Ikeda, LS, Harm, SC, Arcuri, KE, Goldberg, AI and Sweet, CS (1997) Comparative antihypertensive effects of losartan 50 mg and losartan 50 mg titrated to 100 mg in patients with essential hypertension. Blood Pressure 6, 3543.Google Scholar
Jackson, Y, Pinto, A and Pett, S (2014) Chagas disease in Australia and New Zealand: risks and needs for public health interventions. Troical Medicine International Health 19, 212218.Google Scholar
Jenkins, M (2004) Evaluation of methodological search filters-a review. Health Information and Libraries Journal 21, 148163.Google Scholar
Jurewicz, M, McDermott, DH, Sechler, JM, Tinckam, K, Takakura, A, Carpenter, CB, Milford, E and Abdi, R (2007) Human T and natural killer cells possess a functional renin-angiotensin system: further mechanisms of angiotensin ii-induced inflammation. Journal of the American Society of Nephrology 18, 10931102.Google Scholar
Kao, W, Gheorghiade, M, Hall, V and Goldstein, S (1989) Relation between plasma norepinephrine and response to medical therapy in men with congestive heart failure secondary to coronary artery disease or idiopathic dilated cardiomyopathy. The American Journal of Cardiology 64, 609613.Google Scholar
Khoury, AM, Davila, DF, Bellabarba, G, Donis, JH, Torres, A, Lemorvan, C, Hernandez, L and Bishop, W (1996) Acute effects of digitalis and enalapril on the neurohormonal profile of Chagasic patients with severe congestive heart failure. International Journal of Cardiology 57, 2129.Google Scholar
Kranzhofer, R, Browatzki, M, Schmidt, J and Kübler, W (1999) Angiotensin II activates the proinflammatory transcription factor nuclear factor-κB in human monocytes. Biochemical and Biophysical Research Communications 257, 826828.Google Scholar
Lana, M (2017) Experimental studies of Chagas disease in animal. In Telleria, J and Tibayrenc, M (eds). American Trypanosomiasis - Chagas Disease. Elsevier, pp. 299320.Google Scholar
Lara, LS, Andrade-Lima, L, Magalhães Calvet, C, Borsoi, J, Lopes Alberto Duque, T, Henriques-Pons, A, Souza Pereira, MC and Veiga, PL (2018) Trypanosoma cruzi infection of human induced pluripotent stem cell-derived cardiomyocytes: an in vitro model for drug screening for Chagas disease. Microbes and Infection 18, 112.Google Scholar
Lawrence, T (2009) The nuclear factor NF-kappa B pathway in inflammation. Cold Spring Harbor perspectives in biology 1, 110.Google Scholar
Leite, ALJ, Paula Costa, G, Lopes, LR, Mota, LWDR, Vieira, PMA and Talvani, A (2017) The immunomodulatory effects of the enalapril in combination with benznidazole during acute and chronic phases of the experimental infection with Trypanosoma cruzi. Acta Tropica 174, 136145.Google Scholar
Leon, JS, Wang, K and Engman, DM (2003) Captopril ameliorates myocarditis in acute experimental Chagas disease. Circulation 107, 22642269.Google Scholar
Liu, YH, Liu, LY, Wu, JX, Chen, SX and Sun, YX (2006) Comparison of captopril and enalapril to study the role of the sulfhydryl-group in improvement of endothelial dysfunction with ACE inhibitors in high dieted methionine mice. Journal of Cardiovascular Pharmacology 47, 8288.Google Scholar
Magalhães, GS, Barroso, LC, Reis, AC, Rodrigues-Machado, MG, Gregório, JF, Motta-Santos, D, Oliveira, AC, Perez, DA, Barcelos, LS, Teixeira, MM, Santos, RAS, Pinho, V and Campagnole-Santos, MJ (2018) Angiotensin-(1-7) promotes resolution of eosinophilic inflammation in an experimental model of asthma. Frontiers in Immunology 9, 110.Google Scholar
Malik, LH, Singh, GD and Amsterdam, EA (2015) The epidemiology, clinical manifestations, and management of Chagas heart disease. Clinical Cardiology 38, 565569.Google Scholar
Marinho, CR, D'Império Lima, MR, Grisotto, MG and Alvarez, JM (1999) Influence of acute-phase parasite load on pathology, parasitism, and activation of the immune system at the late chronic phase of Chagas’ disease. Infection and Immunity 67, 308318.Google Scholar
Martin, D and Tarleton, R (2004) Generation, specificity, and function of CD8+ T cells in Trypanosoma cruzi infection. Immunological Reviews 201, 304317.Google Scholar
McGrath, JC and Lilley, E (2015) Implementing guidelines on reporting research using animals (ARRIVE etc.): new requirements for publication in BJP. British Journal of Pharmacology 172, 31893193.Google Scholar
Medei, EH, Nascimento, JHM, Pedrosa, RC and de Carvalho, ACC (2008) Role of autoantibodies in the physiopathology of Chagas’ disease. Brazilian Cardiology Archives 91, 110.Google Scholar
Medeiros, GA, Silvério, JC, Marino, AP, Roffê, E, Vieira, V, Kroll-Palhares, K, Carvalho, CE, Silva, AA, Teixeira, MM and Lannes-Vieira, J (2009) Treatment of chronically Trypanosoma cruzi-infected mice with a CCR1/CCR5 antagonist (Met-RANTES) results in amelioration of cardiac tissue damage. Microbes and Infection 11, 264273.Google Scholar
Melo, RC and Brener, Z (1978) Tissue tropism of different Trypanosoma cruzi strains. The Journal of parasitology 64, 475482.Google Scholar
Melo, RC and Machado, CR (2001) Trypanosoma cruzi: Peripheral Blood monocytes and heart macrophages in the resistance to acute experimental infection in rats. Experimental Parasitology 97, 1523.Google Scholar
Messenger, LA, Miles, MA and Bern, C (2015) Between a bug and a hard place: Trypanosoma cruzi genetic diversity and the clinical outcomes of Chagas disease. Expert Review of Anti-Infective Therapy 13, 9951029.Google Scholar
Mion, D Jr, Gomes, MAM, Nobre, F, Amodeo, C, Kohlmann, O Jr, Praxedes, JN and Machado, CA (2004) IV Brazilian guidelines for hypertension. Brazilian Cardiology Archives 82, 114.Google Scholar
Miranda, MB, Melo, AS, Almeida, MS, Marinho, SM, Oliveira, W Jr and Gomes, YM (2017) Ex vivo T-lymphocyte chemokine receptor phenotypes in patients with chronic Chagas disease. Journal of the Brazilian Society of Tropical Medicine 50, 689692.Google Scholar
Moher, D, Liberati, A, Tetzlaff, J and Altman, DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine 6, 16.Google Scholar
Monteiro, AC, Schmitz, V, Svensjo, E, Gazzinelli, RT, Almeida, IC, Todorov, A, de Arruda, LB, Torrecilhas, AC, Pesquero, JB, Morrot, A, Bouskela, E, Bonomo, A, Lima, AP, Müller-Esterl, W and Scharfstein, J (2006) Cooperative activation of TLR2 and bradykinin B2 receptor is required for induction of type 1 immunity in a mouse model of subcutaneous infection by Trypanosoma cruzi. The Journal of Immunology 177, 63256335.Google Scholar
Nataraj, C, Oliverio, MI, Mannon, RB, Mannon, PJ, Audoly, LP, Amuchastegui, CS, Ruiz, P, Smithies, O and Coffman, TM (1999) Angiotensin II regulates cellular immune responses through a calcineurin-dependent pathway. The Journal of clinical investigation 104, 16931701.Google Scholar
Nogueira, SS, Felizardo, AA, Caldas, IS, Gonçalves, RV and Novaes, RD (2018) Challenges of immunosuppressive and antitrypanosomal drug therapy after heart transplantation in patients with chronic Chagas disease: a systematic review of clinical recommendations. Transplantation Reviews 32, 157167.Google Scholar
Noireau, F, Diosque, P and Jansen, AM (2009) Trypanosoma cruzi: adaptation to its vectors and its hosts. Veterinary Research 40, 26.Google Scholar
Okamura, A, Rakugi, H, Ohishi, M, Yanagitani, Y, Takiuchi, S, Moriguchi, K, Fennessy, PA, Higaki, J and Ogihara, T (1999) Upregulation of renin-angiotensin system during differentiation of monocytes to macrophages. Journal of Hypertension 17, 537545.Google Scholar
Oliveira, LRC, Picka, MCM, Nicolete, VC, Calvi, SA and Marcondes-Machado, J (2012) Organ tropism during the acute and chronic phases of Trypanosoma cruzi infection in BALB/c mice. The Journal of venomous animals and toxins including tropical diseases 18, 3443.Google Scholar
Paiva, CN, Medei, E and Bozza, MT (2018) ROS and Trypanosoma cruzi: fuel to infection, poison to the heart. PLoS Pathogens 14, 119.Google Scholar
Patten, RD, Aronovitz, MJ, Einstein, M, Lambert, M, Pandian, NG, Mendelsohn, ME and Konstam, MA (2003) Effects of angiotensin II receptor blockade versus angiotensin-converting-enzyme inhibition on ventricular remodelling following myocardial infarction in the mouse. Clinical Science 104, 109118.Google Scholar
Peeters, AC, Netea, MG, Kullberg, BJ, Thien, T and Meer, JW (1998) The effect of renin-angiotensin system inhibitors on pro-and anti-inflammatory cytokine production. Immunology 94, 376379.Google Scholar
Penitente, AR, Leite, AL, de Paula Costa, G, Shrestha, D, Horta, AL, Natali, AJ, Neves, CA and Talvani, A (2015) Enalapril in combination with Benznidazole reduces cardiac inflammation and creatine kinases in mice chronically infected with Trypanosoma cruzi. The American Journal of Tropical Medicine and Hygiene 93, 976982.Google Scholar
Pereira, RM, Greco, GMZ, Moreira, AM, Chagas, PF, Caldas, IS, Gonçalves, RV and Novaes, RD (2017) Applicability of plant-based products in the treatment of Trypanosoma cruzi and Trypanosoma brucei infections: a systematic review of preclinical in vivo evidence. Parasitology 144, 12751287.Google Scholar
Pérez-Mazliah, DE, Eiro, MDC, Álvarez, G, Lococo, B, Bertocchi, G, César, G, Natale, MA, Alberda, MC, Viotti, R and Laucella, SA (2018) Distinct monocyte subset phenotypes in patients with different clinical forms of chronic Chagas disease and seronegative dilated cardiomyopathy. PLoS Neglected Tropical Diseases 12, 116.Google Scholar
Pérez-Molina, JA, Sojo-Dorado, J, Norman, F, Monge-Maillo, B, Díaz-Menéndez, M, Albajar-Viñas, P and López-Vélez, R (2013) Nifurtimox therapy for Chagas disease does not cause hypersensitivity reactions in patients with such previous adverse reactions during benznidazole treatment. Acta Tropica 127, 101104.Google Scholar
Pinto, AYN, Valente, SA, Valente, VC, Ferreira, AG Jr and Coura, JR (2008) Acute phase of Chagas disease in the Brazilian Amazon: study of 233 cases of Pará, Amapá and Maranhão observed between 1988 and 2005. Journal of the Brazilian Society of Tropical Medicine 41, 602614.Google Scholar
Poveda, C, Fresno, M, Girones, N, Martins-Filho, OA, Ramírez, JD, Santi-Rocca, J, Marin-Neto, JA, Morillo, CA, Rosas, F and Guhl, F (2014) Cytokine profiling in Chagas disease: towards understanding the association with infecting Trypanosoma cruzi discrete typing units (A BENEFIT TRIAL Sub-Study). PLoS ONE 9, 18.Google Scholar
Qu, C, Brinck-Jensen, NS, Zang, M and Chen, K (2014) Monocyte-derived dendritic cells: targets as potent antigen-presenting cells for the design of vaccines against infectious diseases. International Journal of Infectious Diseases 19, 15.Google Scholar
Rassi, A Jr, Rassi, A and Marin-Neto, JA (2009) Chagas heart disease: pathophysiologic mechanisms, prognostic factors and risk stratification. Memories of the Oswaldo Cruz Institute 104, 152158.Google Scholar
Rassi, A Jr, Rassi, A and Rezende, JM (2012) American trypanosomiasis (Chagas disease). Infectious Disease Clinics of North America 26, 275291.Google Scholar
Rassi, A Jr, Marin-Neto, JA and Rassi, A (2017) Chronic Chagas cardiomyopathy: a review of the main pathogenic mechanisms and the efficacy of aetiological treatment following the Benznidazole Evaluation for Interrupting Trypanosomiasis (BENEFIT) trial. Memories of the Oswaldo Cruz Institute 112, 224235.Google Scholar
Reed, SG, Brownell, CE, Russo, DM, Silva, JS, Grabstein, KH and Morrissey, PJ (1994) IL-10 mediates susceptibility to Trypanosoma cruzi infection. Journal Immunology 153, 31353140.Google Scholar
Reilly, CF, Tewksbury, DA, Schechter, NM and Travis, J (1982) Rapid conversion of angiotensin I to angiotensin II by neutrophil and mast cell proteinases. The Journal of Biological Chemistry 257, 86198622.Google Scholar
Resende, MM and Mill, JG (2002) Alternative routes of angiotensin II production and their importance under physiological or pathophysiological conditions. Brazilian Cardiology Archives 78, 425431.Google Scholar
Ribeiro, ALP (2018) Functional capacity in Chagas disease. Journal of the Brazilian Society of Tropical Medicine 51, 413414.Google Scholar
Roberti, RR, Martinez, EE, Andrade, JL, Araujo, VL, Brito, FS, Portugal, OP and Horowitz, SF (1992) Chagas cardiomyopathy and captopril. European Heart Journal 13, 966970.Google Scholar
Roffê, E, Rothfuchs, AG, Santiago, HC, Marino, AP, Ribeiro-Gomes, FL, Eckhaus, M, Antonelli, LR and Murphy, PM (2012) IL-10 limits parasite burden and protects against fatal myocarditis in a mouse model of Trypanosoma cruzi infection. The Journal of Immunology 188, 649660.Google Scholar
Rodea, GB, Cuevas, TIM, Ramos, BJ and Campos, AA (2018) Chagas disease: an overview of diagnosis. Journal of Microbiology e Experimentation 6, 151157.Google Scholar
Roman-Campos, D, Duarte, HL, Sales, PA, Natali, AJ, Ropert, C, Gazzinelli, RT and Cruz, JS (2009) Changes in cellular contractility and cytokines profile during Trypanosoma cruzi infection in mice. Basic Research in Cardiology 104, 238246.Google Scholar
Romano, PS, Cueto, JA, Casassa, AF, Vanrell, MC, Gottlieb, RA and Colombo, MI (2012) Molecular and cellular mechanisms involved in the Trypanosoma cruzi/host cell interplay. IUBMB life 64, 387396.Google Scholar
Santiago, HC, Feng, CG, Bafica, A, Roffe, E, Arantes, RM, Cheever, A, Taylor, G, Vierira, LQ, Aliberti, J, Gazzinelli, RT and Sher, A (2005) Mice deficient in LRG-47 display enhanced susceptibility to Trypanosoma cruzi infection associated with defective hemopoiesis and intracellular control of parasite growth. The Journal of immunology 175, 81658172.Google Scholar
Santos, JSC, Mnezes, CAS, Villani, FNA, Magalhães, LMD, Scharfstein, J, Gollob, KJ and Dutra, WO (2010) Captopril increases the intensity of monocyte infection by Trypanosoma cruzi and induces human T helper type 17 cells. Clinical and Experimental Immunology 162, 528536.Google Scholar
Santos, PF, Moreira, DS, Baba, EH, Volpe, CMO, Ruiz, JC, Romanha, AJ and Murta, SMF (2016) Molecular characterization of lipoamide dehydrogenase gene in Trypanosoma cruzi populations susceptible and resistant to benznidazole. Experimental Parasitology 170, 19.Google Scholar
Scharfstein, J, Schmitz, V, Morandi, V, Capella, MM, Lima, AP, Morrot, A, Juliano, L and Müller-Esterl, W (2000) Host cell invasion by Trypanosoma cruzi is potentiated by activation of bradykinin B(2) receptors. The Journal of Experimental Medicine 192, 12891300.Google Scholar
Schindler, R, Dinarello, CA and Koch, KM (1995) Angiotensin-converting enzyme inhibitors suppress synthesis of tumor necrosis factor and interleukin 1 by human peripheral blood mononuclear cells. Cytokine 7, 526533.Google Scholar
Shen, XZ, Billet, S, Lin, C, Okwan-Duodu, D, Chen, X, Lukacher, AE and Bernstein, KE (2011) The carboxypeptidase ACE shapes the MHC class I peptide repertoire. Nature Immunology 12, 10781085.Google Scholar
Silva, GK, Cunha, LD, Horta, CV, Silva, ALN, Gutierrez, FRS, Silva, JS and Zamboni, DS (2013) A parent-of-origin effect determines the susceptibility of a non-informative F1 population to Trypanosoma cruzi infection in vivo. PLoS ONE 8, 110.Google Scholar
Simic, M, Hinman, RS, Wrigley, TV, Bennell, KL and Hunt, MA (2011) Gait modification strategies for altering medial knee joint load: a systematic review. Arthritis Care and Research 63, 122.Google Scholar
Simões, MV, Romano, MMD, Schamidt, A, Martins, KSM and Marin-neto, JA (2018) Chagas disease cardiomyopathy. International Journal of Cardiovascular Sciences 31, 173189.Google Scholar
Soares, MBP, Silva-Mota, KN, Lima, RS, Bellintani, MC, Carvalho, LP and Santos, RR (2001) Modulation of Chagasic cardiomyopathy by interleukin-4 dissociation between inflammation and tissue parasitism. American Journal Pathology 159, 703709.Google Scholar
Soares, RCO, Soares, CS, Moraes, SMF, Batista, MR, Kwabara, HN, Sousa, AMR, Moreira, NM, Gomes, ML and Araújo, SM (2012) Trypanosoma cruzi experimental infection in mice: influence of physical exercise versus lineages and sexes. Brazilian Journal of Sports Medicine 18, 5157.Google Scholar
Sousa, MA and Alencar, AA (1984) On the tissular parasitism of Trypanosoma cruzi Y strain in swiss mice. Journal of the Institute of Tropical Medicine of São Paulo 26, 316321.Google Scholar
Souza, LL and Costa-Neto, CM (2012) Angiotensin-(1-7) decreases LPS-induced inflammatory response in macrophages. Journal of Cellular Physiology 227, 21172122.Google Scholar
Szajnbok, FE, Barretto, AC, Mady, C, Parga Filho, J, Gruppi, C, Alfieri, RG, da Luz, PL and Pileggi, F (1993) Enalapril beneficial action on ventricular diastolic function in Chagas disease myocardiopathy. Brazilian Archives of Cardiology 60, 273278.Google Scholar
Talvani, A, Rocha, MO, Barcelos, LS, Gomes, YM, Ribeiro, AL and Teixeira, MM (2004) Elevated concentrations of CCL2 and tumor necrosis factor–α in Chagasic cardiomyopathy. Clinical Infectious Diseases 38, 943950.Google Scholar
Teixeira, AR, Hecht, MM, Guimaro, MC, Sousa, AO and Nitz, N (2011) Pathogenesis of Chagas’ disease: parasite persistence and autoimmunity. Clinical Microbiology Reviews 24, 592630.Google Scholar
Thomas, MC, Pickering, RJ, Tsorotes, D, Koitka, A, Sheehy, K, Bernardi, S, Toffoli, B, Nguyen-Huu, TP, Head, GA, Fu, Y, Chin-Dusting, J, Cooper, ME and Tikellis, C (2010) Genetic Ace2 deficiency accentuates vascular inflammation and atherosclerosis in the ApoE knockout mouse. Circulation Research 107, 888897.Google Scholar
Trischmann, T, Tanowitz, H, Wittner, M and Bloom, B (1978) Trypanosoma cruzi: role of the immune response in the natural resistance of inbred strains of mice. Experimental Parasitology 45, 160168.Google Scholar
Vazques, BP, Vazquez, TP, Miguel, CB, Rodrigues, WF, Mendes, MT, Oliveira, CJF and Chica, JEL (2015) Inflammatory responses and intestinal injury development during acute Trypanosoma cruzi infection are associated with the parasite load. Parasites and Vectors 8, 112.Google Scholar
Vorraro, F, Cabrera, WHK, Ribeiro, OG, Jensen, JR, Franco, M, Ibãnez, OM and Starobinas, N (2014) Trypanosoma cruzi infection in genetically selected mouse lines: genetic linkage with quantitative trait locus controlling antibody response. Mediators of Inflammation 2014, 115.Google Scholar
World Health Organization (2018) Chagas disease (American trypanosomiasis). WHO Technical Report Series. Geneva, Switzerland. World Health Organization.Google Scholar
Yamauchi, LM 1, Aliberti, JC, Baruffi, MD, Portela, RW, Rossi, MA, Gazzinelli, RT, Mineo, JR and Silva, JS (2007) The binding of CCL2 to the surface of Trypanosoma cruzi induces chemo-attraction and morphogenesis. Microbes and Infection 9, 111118.Google Scholar
Zhang, YY, Li, JN, Xia, HHX, Zhang, SL, Zhong, J, Wu, YY, Miao, SK and Zhou, LM (2013) Protective effects of losartan in mice with chronic viral myocarditis induced by coxsackievirus B3. Life Sciences 92, 11861194.Google Scholar
Supplementary material: File

Souza-Silva et al. supplementary material

Souza-Silva et al. supplementary material 1

Download Souza-Silva et al. supplementary material(File)
File 94.4 KB