Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-26T06:34:36.143Z Has data issue: false hasContentIssue false
  • English
  • Français

Distinctive histopathology and modulation of cytokine production during oral and intraperitoneal Trypanosoma cruzi Y strain infection

Published online by Cambridge University Press:  19 February 2014

CHRISTIAN C. KUEHN ,
LUIZ GUSTAVO R. OLIVEIRA ,
MARIZA ABREU MIRANDA  and
JOSÉ CLÓVIS PRADO Jr.
CHRISTIAN C. KUEHN*
Affiliation:
Faculdade de Ciências Farmacêuticas de Ribeirão Preto FCFRP-USP, Universidade de São Paulo, Avenida do Café, s/n, 14040-903, Ribeirão Preto, SP, Brazil
LUIZ GUSTAVO R. OLIVEIRA
Affiliation:
Faculdade de Ciências Farmacêuticas de Ribeirão Preto FCFRP-USP, Universidade de São Paulo, Avenida do Café, s/n, 14040-903, Ribeirão Preto, SP, Brazil
MARIZA ABREU MIRANDA
Affiliation:
Faculdade de Ciências Farmacêuticas de Ribeirão Preto FCFRP-USP, Universidade de São Paulo, Avenida do Café, s/n, 14040-903, Ribeirão Preto, SP, Brazil
JOSÉ CLÓVIS PRADO Jr.
Affiliation:
Faculdade de Ciências Farmacêuticas de Ribeirão Preto FCFRP-USP, Universidade de São Paulo, Avenida do Café, s/n, 14040-903, Ribeirão Preto, SP, Brazil
*
* Corresponding author: Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto FCFRP-USP, Universidade de São Paulo, Avenida do Café s/n°, 14040-903, Ribeirão Preto, SP, Brazil. E-mail: biochris@fcfrp.usp.br
Get access Rights & Permissions [Opens in a new window]

Summary

Acute Chagas disease outbreaks are related to the consumption of food or drink contaminated by triatomine feces, thus making oral infection an important route of transmission. Both vector-borne and oral infections trigger important cardiac manifestations in the host that are related to a dysregulated immune response. The aims of this work were to evaluate possible alterations of lymphocyte CD4+/CD8+ sub-populations, Th1 and Th2 cytokines, nitrite concentrations and cardiac histopathology. One group of male Wistar rats was intraperitoneally infected (I.P.) with 1×105 metacyclic trypomastigotes of the T. cruzi Y strain, and another group of Wistar rats was orally infected (O.I.) with 8×105 metacyclic trypomastigotes of the same strain. The intraperitoneal infection triggered statistically enhanced parasite and peritoneal macrophage numbers, increased concentrations of NO and IL-12 and elevated cardiac inflammatory foci when compared with the oral infection. However, proliferation of CD4+ and CD8+ T cells were not statistically different for oral and intraperitoneal routes.

Keywords

Intraperitoneal and oral infection routeTrypanosoma cruzi (Y strain)parasitaemianitric oxideInterleukin Th-1/Th-2flow cytometryhistopathology
Type
Research Article
Information
Parasitology , Volume 141 , Issue 7 , June 2014 , pp. 904 - 913
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

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

REFERENCES

Aliberti, J. C. S., Cardoso, M. A. A. G., Martins, G. A., Gazzineli, R. T., Vieira, L. Q. and Silva, J. S. (1996). Interleukin-12 mediates resistance to Trypanosoma cruzi in mice and in produced by murine macrophages in response to live trypomastigotes. Infection Immunity 64, 1961–1967.Google Scholar
Aliberti, J. C. S., Machado, F. S. and Souto, J. T. (1999). Beta-chemokines enhance parasite uptake and promote nitric oxide-dependent microbiostatic activity in murine inflammatory macrophages infected with Trypanosoma cruzi . Infection Immunity 67, 4819–4826.Google Scholar
Andrade, S. G. (1985). Morphological and behavioral characterization of Trypanosoma cruzi strains. Revista da Sociedade Brasileira de Medicina Tropical 18, 39–46.Google Scholar
Andrade, S. G. and Magalhães, J. B. (1997). Biodemes and zymodemes of Trypanosoma cruzi strains: correlations with clinical data and experimental pathology. Revista da Sociedade Brasileira de Medicina Tropical 30, 27–35.CrossRefGoogle ScholarPubMed
Andrade, S. G., Carvalho, M. L. and Figueira, R. M. (1970). Caracterização morfobiológica e histopatológica de diferentes cepas do Trypanosoma cruzi . Gazeta Médica da Bahia 70, 32–42.Google Scholar
Brazão, V., Filipin, M. D. V., Santello, F. H., Caetano, L. C., Abrahão, A. A. C., Toldo, M. O. A. and Prado, J. C. (2011). Melatonin and zinc treatment: distinctive modulation of cytokine production in chronic experimental Trypanosoma cruzi infection. Cytokine 56, 627–632. doi: 10.1016/j.cyto.2011.08.037.Google Scholar
Brener, Z. (1969). The behavior of slender and stout forms of Trypanosoma cruzi in the blood-stream of normal and immune mice. Annals of Tropical Medicine and Parasitology 63, 215–220.Google Scholar
Brunet, L. R. (2001). Review – nitric oxide in parasitic infections. International Immunopharmacology 1, 1457–1467. doi: org/10.1016/S1567-5769(01)00090-X.Google Scholar
Camandaroba, P. E. E., Pinheiro Lima, C. M. and Andrade, S. G. (2002). Oral transmission of Chagas disease: importance of Trypanosoma cruzi biodeme in the intragastric experimental infection. Revista do Instituto de Medicina Tropical de São Paulo 44, 97–103. doi: 10.1590/S0036-46652002000200008.Google Scholar
Camargo, E. R. S., Franco, D. J., Garcia, C. M. M. G., Dutra, A. P., Texeira, A. L. Jr., Chiari, E. and Machado, C. R. S. (2000). Infection with different Trypanosoma cruzi populations in rats: myocarditis, cardiac sympathetic denervation and involvement of digestive organs. American Journal of Tropical Medicine and Hygiene 62, 604–612.Google Scholar
Camussi, G., Albano, E., Tetta, C. and Bussolino, F. (1991). The molecular action of tumor-necrosis-factor-alpha. European Journal of Biochemistry 202, 3–14. doi: 10.1111/j.1432-1033.1991.tb16337.x.Google Scholar
Carlier, Y., Dias, J. C. P., Luquetti, A. O., Hontebeyrie, M., Torrico, F. and Truyens, C. (2002). Trypanosomiase americane ou maladie de Chagas. Enciclopédia Médico-Cirúrgico 8, 505–A20.Google Scholar
Clark, I. A. and Rockett, K. A. (1996). Nitric oxide and parasitic disease. Advances in Parasitology 37, 1–56.Google Scholar
Collins, M. H., Craft, J. M., Bustamante, J. M. and Tarleton, R. L. (2011). Oral exposure to Trypanosoma cruzi elicits a systemic CD8+ T cell response and protection against heterotopic challenge. Infection and Immunity 79, 3397–3406. doi: 10.1128/IAI.01080-10.CrossRefGoogle ScholarPubMed
Correa-de-Santana, E., Paez-Pereda, M., Theodoropoulou, M., Kenji Nihei, O., Gruebler, Y., Bozza, M., Arzt, E., Villa-Verde, D. M., Renner, U., Stalla, J., Stalla, G. K. and Savino, W. (2006). Hypothalamus-pituitary-adrenal axis during Trypanosoma cruzi acute infection in mice. Journal of Neuroimmunology 173, 12–22. doi: 10.1016/j.jneuroim.2005.08.015.CrossRefGoogle ScholarPubMed
Cortez, M., Neira, I., Ferreira, D., Luquetti, A. O., Rassi, A., Atayde, V. D. and Yoshida, N. (2003). Infection by Trypanosoma cruzi metacyclic forms deficient in gp82 but expressing a related surface molecule gp30. Infection and Immunity 71, 6184–6191.Google Scholar
Costa, V. M., Torres, K. C., Mendonça, R. Z., Gresser, I., Gollob, K. J. and Abrahamsohn, I. A. (2006). Type I IFNs stimulate nitric oxide production and resistance to Trypanosoma cruzi infection. Journal of Immunology 177, 3193–3200.Google Scholar
Coura, J. R., Junqueira, A. C. V., Fernandes, O., Valente, S. A. S. and Miles, M. A. S. (2002). Emerging Chagas disease in Amazonian Brasil. Trends in Parasitology 18, 171–176. doi: 10.1016/S1471-4922(01)02200-0.Google Scholar
Dias, J. C. P. (1999). Epidemiologia. In Trypanosoma cruzi e Doença de Chagas (org. Brener, Z., Andrade, Z. A. and Barral Netto, M.), pp. 48–74. Editora Guanabara Koogan, Rio de Janeiro, Brasil.Google Scholar
Dujardin, J. P., Garcia-Zapata, M. T., Jurberg, J., Roelants, P., Cardozo, L., Panzera, F., Dias, J. C. P. and Schofield, C. J. (1991). Which species of Rhodnius is invading houses in Brazil? Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 679–680.CrossRefGoogle ScholarPubMed
Eickhoff, C. S., Giddingsa, O. K., Yoshida, N. and Hoft, D. F. (2010). Immune responses to gp82 provide protection against mucosal Trypanosoma cruzi infection. Memórias do Instituto Oswaldo Cruz 105, 687–691.Google Scholar
Elson, C. O. (2007). Perspectives on mucosal vaccines: is mucosal tolerance a barrier? Journal of Immunology 179, 5633–5638.Google Scholar
Fiuza, J. A., Fujiwara, R. T., Gomes, J. A., Rocha, M. O., Chaves, A. T. and de Araújo, F. F. (2009). Profile of central and effector memory T cells in the progression of chronic human chagas disease. PLoS Neglected Tropical Diseases 3, e512. doi: 10.1371/journal.pntd.0000512.Google Scholar
Garcia, S. B., Paula, J. S., Giovanetti, G. S., Zenha, F., Ramalho, E. M., Zucoloto, S., Silva, J. S. and Cuha, F. Q. (1999). Nitric oxide is involved in the lesions of the peripheral autonomic neurons observed in the acute phase of experimental Trypanosoma cruzi infection. Experimental Parasitology 93, 191–197. doi: org/10.1006/expr.1999.4451.Google Scholar
Gazzinelli, R. T., Oswald, I. P., Hieny, S., James, S. L. and Sher, A. (1992). The microbicidal activity of interferon-gamma-treated macrophages against Trypanosoma cruzi involves an L-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by interleukin-10 and transforming growth factor-beta. European Journal of Immunology 22, 2501–2506. doi: 10.1002/eji.1830221006.CrossRefGoogle ScholarPubMed
Goodrich, M. E. and McGee, D. W. (1998). Regulation of mucosal B cell immunoglobulin secretion by intestinal epithelial cell-derived cytokines. Cytokine 10, 948–955. doi: 10.1006/cyto.1998.0385.Google Scholar
Hoft, D. F. (1996). Differential mucosal infectivity of different life stages of Trypanosoma cruzi . American Journal of Tropical Medicine and Hygiene 55, 360–364.Google Scholar
Hoft, D. F. and Eickhoff, C. S. (2005). Type 1 immunity provides both optimal mucosal and systemic protection against a mucosally invasive, intracellular pathogen. Infection and Immunity 70, 4934–4940. doi: 10.1128/IAI.73.8.4934-4940.2005.Google Scholar
Hoft, D. F., Farrar, P. L., Kratz-Owens, K. and Shaffer, D. (1996). Gastric invasion by Trypanosoma cruzi and induction of protective mucosal immune responses. Infection and Immunity 64, 3800–3810.Google Scholar
Hoft, D. F., Schnapp, A. R., Eickhoff, C. S. and Roodman, S. T. (2000). Involvement of CD4_ Th1 cells in systemic immunity protective against primary and secondary challenges with Trypanosoma cruzi . Infection and Immunity 68, 197–204. doi: 10.1128/IAI.68.1.197-204.2000.Google Scholar
Igreja, R. P. (2009). Chagas disease 100 years after its discovery. Lancet 373, 18–24. doi: 10.1016/S0140-6736(09)60775-3.CrossRefGoogle ScholarPubMed
Kuehn, C. C., Oliveira, L. G. R., Santos, C. D., Augusto, M. B., Toldo, M. P. A. and Prado, J. C. Jr. (2011). Prior and concomitant Dehydroepiandrosterone treatment affects immunologic response of cultured macrophages infected with Trypanosoma cruzi in vitro? Veterinary Parasitology 177, 242–246. doi: 10.1016/j.vetpar.2010.12.009.Google Scholar
MacMicking, J., Xie, Q. W. and Nathan, C. (1997). Nitric oxide and macrophage function. Annual Review of Immunology 15, 323–350. doi: 10.1146/annurev.immunol.15.1.323.Google Scholar
Mathers, C. D., Ezzati, M. and Lopez, A. D. (2007). Measuring the burden of neglected tropical diseases: the global burden of disease framework. PLoS Neglected Tropical Disease 1, e114. doi: 10.1371/journal.pntd.0000114.Google Scholar
Mestecky, J., Russell, M. W. and Elson, C. O. (2007). Perspectives on mucosal vaccines: is mucosal tolerance a barrier? Journal of Immunology 179, 5633–5638.Google Scholar
Miles, M. A., Lanham, S. M. and Povoa, M. (1980). Further enzymic characters of Trypanosoma cruzi in their evaluation for strain identification. American Journal of Tropical Medicine and Hygiene 74, 221–237.Google Scholar
Moncada, D., Keeller, K. and Chadee, K. (2003). Entamoeba histolytica cysteine proteinases disrupt the polymeric structure of colonic mucin and alter its protective function. Infection and Immunity 71, 838–844. doi: 10.1128/IAI.71.2.838-844.2003.Google Scholar
Neira, I., Silva, F. A., Cortez, M. and Yoshida, N. (2003). Involvement of Trypanosoma cruzi metacyclic tripomastigote surface molecule gp82 in adhesion to gastric mucin and invasion of epithelial cells. Infection and Immunity 71, 577–561. doi: 10.1128/IAI.71.1.557-561.2003.Google Scholar
Neutra, M. R. and Kozlowski, P. A. (2006). Mucosal vaccines: the promise and the challenge. Nature Reviews Immunology 6, 148–158. doi: 10.1038/nri1777.CrossRefGoogle ScholarPubMed
O'Garra, A. (1998). Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8, 275–283. doi: org/10.1016/S1074-7613(00)80533-6.Google Scholar
Oliveira, M. A., Santiago, H. C. and Lisboa, C. R. (2000). Leishmania sp.: comparative study with Toxoplasma gondii and Trypanosoma cruzi in their ability to initialize IL-12 and IFN-gamma synthesis. Experimental Parasitology 95, 96–105. doi: org/10.1006/expr.2000.4523.Google Scholar
Ozturk, G., Aydinli, B., Celebi, F. and Gursan, N. (2011). Gastric perforation caused by Strongyloides stercoralis: a case report. Turkish Journal of Trauma and Emergency Surgery 17, 90–92. doi: 10.5505/tjtes.2011.51196.Google Scholar
Padilla, A., Xu, D., Martin, D. and Tarleton, R. (2007). Limited role for CD4+ T-cell help in the initial priming of Trypanosoma cruzi-specific CD8+ T cells. Infection and Immunity 75, 231–235. doi: 10.1128/IAI.01245-06.Google Scholar
Perez, A. R., Roggero, E., Nicora, A., Palazzi, J., Besedovsky, H. O., Del Rey, A. and Bottasso, O. A. (2007). Thymus atrophy during Trypanosoma cruzi infection is caused by an immuno-endocrine imbalance. Brain, Behavior, and Immunity 21, 890–900. doi: 10.1016/j.bbi.2007.02.004.CrossRefGoogle ScholarPubMed
Perez, A. R., Morrot, A., Berbert, L. R., Terra-Granado, E. and Savino, W. (2012). Extrathymic CD4+CD8+ lymphocytes in Chagas disease: possible relationship with an immunoendocrine imbalance. Annals of the New York Academy of Sciences 1262, 27–36. doi: 10.1111/j.1749-6632.2012.06627.x.Google Scholar
Pinsky, D. J., Walif, A. J. I., Szabolcs, M., Athan, E. S., Liu, Y., Yang, Y. M., Kline, R. P., Olson, K. E. and Cannon, P. J. (1999). Nitric oxide triggers programmed cell death (apoptosis) of adult rat ventricular myocytes in culture. American Journal of Physiology 277, 1189–1199.Google Scholar
Reed, S. G. (1995). Cytokine control of the macrophage parasites Leishmania and Trypanosoma cruzi . In Molecular Approaches to Parasitology (ed. Boothroyd, J. C. and Richard Komuniecki, R.), 443–445. Wiley Liss, New York, NY, USA.Google Scholar
Reyes, J. L., Terrazas, L. I., Espinoza, B., Cruz-Robles, D., Soto, V. and Rivera-Montoya, I. (2006). Macrophage migration inhibitory factor contributes to host defense against acute Trypanosoma cruzi infection. Infection and Immunity 74, 3170–3179. doi: 10.1128/IAI.01648-05.Google Scholar
Round, J. L. and Mazmanian, S. K. (2009). The gut microbiota shapes intestinal immune responses during health and disease. Nature Reviews Immunology 9, 313–323. doi: 10.1038/nri2515.Google Scholar
Schnapp, A. R., Eickhoff, C. S., Sizemore, D., Curtiss, R. III and Hoft, D. F. (2000). Cruzipain induces both mucosal and systemic protection against Trypanosoma cruzi in mice. Infection and Immunity 70, 5065–5074. doi: 10.1128/IAI.70.9.5065-5074.2002.Google Scholar
Schofield, C. J., Jannin, J. and Salvatella, R. (2006). The future of Chagas’ disease control. Trends in Parasitology 22, 583–588. doi: 10.1016/j.pt.2006.09.011.Google Scholar
Silva, L. H. P. and Nussenzweig, V. (1953). Sobre uma cepa de Trypanosoma cruzi altamente virulenta para o camundongo branco. Folia clinica et biológica 20, 191–201.Google Scholar
Sogayar, R., Kipnis, T. L. and Curi, P. R. (1993). A critical evaluation of the expression of parasitemia in experimental Chagas’ disease. Revista do Instituto de Medicina Tropical 35, 395–398. doi: 10.1590/S0036-46651993000500002.Google Scholar
Souza, M. M., Andrade, S. G., Barbosa, A. A. Jr., Santos, T. T. M., Alves, V. A. F. and Andrade, Z. A. (1996). Trypanosoma cruzi strains and autonomic nervous system pathology in experimental Chagas disease. Memórias do Instituto Oswaldo Cruz 91, 217–224.Google Scholar
Taliaferro, W. H. and Pizzi, T. (1955). Connective tissue reactions in normal and immunized mice to a reticulotropic strain of Trypanosoma cruzi . Journal of Infectious Diseases 96, 199–226.Google Scholar
Tarleton, R. L., Sun, J., Zhang, L. and Postan, M. (1994). Depletion of T-cell subpopulations results in exacerbation of myocarditis and parasitism in experimental Chagas'disease. Infection and Immunity 62, 1820–1829.Google Scholar
Terenzi, F., Diaz-Guerra, M. J. M., Casado, M., Hortelano, S., Leoni, S. and Boscá, L. (1995). Bacterial lipopetides induce nitric oxide synthetase and promote apoptosis through nitric oxide-independent pathways in rat macrophages. Journal of Biological Chemistry 270, 6017–6021. doi: 10.1074/jbc.270.11.6017.Google Scholar
Wang, A. Y. and Peura, D. A. (2011). The prevalence and incidence of Helicobacter pylori-associated peptic ulcer disease and upper gastrointestinal bleeding throughout the world. Gastrointestinal Endoscopy Clinics of North America 21, 613–635. doi: 10.1016/j.giec.2011.07.011.Google Scholar
Yamamoto, M., Vancott, J. L., Okahashi, N., Marinaro, M., Kiyono, H., Fujihashi, K., Jackson, R. J., Chatfield, S. N., Bluethmann, H. and McGhee, J. R. (1996). The role of Th1 and Th2 cells for mucosal IgA responses. Annals of the New York Academy of Sciences 778, 64–71. doi: 10.1111/j.1749-6632.1996.tb21115.x.Google Scholar
Yoshida, N. (2006). Molecular basis of mammalian cell invasion of Trypanosoma cruzi . Anais da Academia Brasileira de Ciências 78, 87–111.Google Scholar
Yoshida, N. (2008). Trypanosoma cruzi infection by oral route: how the interplay between parasite and host components modulates infectivity. Parasitology International 57, 105–109. doi: 10.1016/j.parint.2007.12.008.Google Scholar
Yoshida, N. (2009). Molecular mechanisms of Trypanosoma cruzi infection by oral route. Memórias do Instituto Oswaldo Cruz 104, 101–107.CrossRefGoogle ScholarPubMed
Zhang, L. and Tarleton, R. L. (1999). Parasite persistence correlates with disease severity and localization in chronic Chagas’ disease. Journal of Infectious Diseases 180, 480–486. doi: 10.1086/314889.CrossRefGoogle ScholarPubMed