Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T21:25:58.380Z Has data issue: false hasContentIssue false

Chronic indeterminate phase of Chagas’ disease: mitochondrial involvement in infection with two strains

Published online by Cambridge University Press:  09 November 2012

ALEJANDRA LIDIA BÁEZ*
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085. PC 5000. Córdoba, Argentina
MARÍA SILVINA LO PRESTI
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085. PC 5000. Córdoba, Argentina
RICARDO FRETES
Affiliation:
Cátedra de Biología Celular, Histología y Embriología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. 5016 Córdoba, Argentina
CINTIA DÍAZ
Affiliation:
Cátedra de Biología Celular, Histología y Embriología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. 5016 Córdoba, Argentina
PATRICIA PONS
Affiliation:
Centro de Microscopia, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. 5016 Córdoba, Argentina
PAOLA CAROLINA BAZÁN
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085. PC 5000. Córdoba, Argentina
MARIANA STRAUSS
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085. PC 5000. Córdoba, Argentina
HÉCTOR WALTER RIVAROLA
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085. PC 5000. Córdoba, Argentina
PATRICIA PAGLINI-OLIVA
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085. PC 5000. Córdoba, Argentina
*
*Corresponding author: Cátedra de Física Biomédica,Facultad de Ciencias Médicas. Universidad Nacional de Córdoba, Santa Rosa 1085. C.P. 5000, Argentina. Tel: + 51 9 351 4332020. E-mail address: [email protected].

Summary

Chagasic cardiopathy has become one of the most frequent causes of heart failure and sudden death, as well as one of the most common causes of cardio-embolic stroke in Latin America. The myocyte response to oxidative stress involves the progression of cellular changes, primarily targeting the mitochondria and modifying therefore the energy supply. In this paper we analysed the effect of the infection of mice with 2 different strains of Trypanosoma cruzi (Tulahuen and SGO Z12) in the chronic indeterminate stage (75 days post-infection), upon the structure and function of cardiac mitochondria. The structural results showed that 83% of the mitochondria from the Tulahuen-infected mice presented an increase in their matrix and 91% of the mitochondria from the SGO Z12-infected group showed a reduction in their diameter (P < 0·05). When the Krebs cycle and mitochondrial respiratory chain functionality was analysed through the measurement of the citrate synthase and complexes I to IV activity, it showed that their activity was altered in all cases in a similar manner in both infected groups. In this paper we have demonstrated that the chronic indeterminate phase is not ‘silent’ and that cardiac mitochondria are clearly involved in the genesis and progression to the chronic chagasic cardiopathy when different factors alter the host-parasite equilibrium.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Andrade, S. G., Campos, R. F., Sobral, S. C., Magahlanes, J. B., Guedes, R. S. P. and Guerreiro, M. L. (2006). Reinfections with Trypanosoma cruzi strains of different biodems as a factor of aggravation of miocarditis and myosites in mice. Revista da Sociedade Brasileira de Medicina Tropical 39, 18.CrossRefGoogle Scholar
Araujo Jorge, T. C., Waghabi, M. C., Soeiro, M. D. E., Keramidas, M., Bailly, S. and Feige, J. J. (2008). Pivotal role for TGF beta in infectious heart disease: the case of Trypanosoma cruzi infection and consequent chagasic myocardiopathy. Cytokine and Growth Factor Reviews 19, 405413.CrossRefGoogle ScholarPubMed
Báez, A., Lo Presti, M. S., Rivarola, H. W., Guzman Mentesana, G., Pons, P., Fretes, R. and Paglini-Oliva, P. (2011). Mitochondrial involvement in the chronic chagasic cardiomiopathy. Transactions of the Royal Society of Tropical Medicine and Hygiene 105, 239246.CrossRefGoogle Scholar
Báez, A., Lo Presti, S., Rivarola, W., Pons, P., Fretes, R. and Paglini-Oliva, P. (2008). Trypanosoma cruzi: mitochondrial alterations produced by two different strain in the acute phase of the infection. Experimental Parasitology 120, 397402.CrossRefGoogle ScholarPubMed
Bern, C., Montgomery, S. P., Herwaldt, B. L., Rassi, A. Jr., Marin-Neto, J. A., Dantas, R. O., Maguirre, J. H., Acquatella, H., Morillo, C., Kirchhoff, L. V., Gilman, R. H., Reyes, P. A., Salvatella, R. and Moore, A. C. (2007). Evaluation and treatment of Chagas disease in the United States: a systematic review. JAMA: The Journal of the American Medical Association 298, 21712181.CrossRefGoogle ScholarPubMed
Biolo, A., Ribeiro, A. L. and Clausell, N. (2010). Chagas cardiomyopathy–where do we stand after a hundred years? Progress in Cardiovascular Diseases 52, 300316.CrossRefGoogle ScholarPubMed
Bradford, M. A. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein–DNA binding. Analytical Biochemistry 72, 248254.CrossRefGoogle Scholar
Bustamante, J. M., Rivarola, H. W., Fernández, A. R., Enders, J. E., Fretes, R. E. and Paglini Oliva, P. (2003). Indeterminate Chagas' disease: Trypanosoma cruzi strain and reinfection are factors involved in the progression of cardiopathy. Clinical Science 104, 415420.CrossRefGoogle ScholarPubMed
Cardoni, M. I., Antunez, C., Morales, I. and Nantes, R. (1997). Release of reactive oxygen species by phagocytic cells in response to live parasites in mice infected with Trypanosoma cruzi. The American Journal of Tropical Medicine and Hygiene 56, 329334.CrossRefGoogle ScholarPubMed
Coura, J. R. (1988). Determinantes epidemiológicos da doenca do Chagas no Brasil:a infeccao da doenca e sua morbid-mortalidade. Memórias do Instituto Oswaldo Cruz 83, 392402.CrossRefGoogle Scholar
Coura, J. R., Borges-Pereira, J. (2010). Chagas disease: 100 years after its discovery. A systemic review. Acta Tropica 115, 513.CrossRefGoogle ScholarPubMed
De Oliveira, T. B., Pedrosa, R. C. and Filho, D. W. (2007). Oxidative stress in chronic cardiopathy associated with Chagas disease. International Journal of Cardiology 116, 357363.CrossRefGoogle ScholarPubMed
Dhiman, M., Nakayasu, E. S., Madaiah, Y. H., Reynolds, B. K. and Wen, J. J. (2008). Enhanced nitrosative stress during Trypanosoma cruzi infection causes nitrotyrosine modification of host proteins: implications in Chagas’ disease. The American Journal of Pathology 173, 728740.CrossRefGoogle ScholarPubMed
Dhiman, M., Zago, M. P., Nunez, S., Amoroso, A., Rementeria, H., Dousset, P., Nunez Burgos, F. and Garg, N. J. (2012). Cardiac-Oxidized Antigens Are Targets of Immune Recognition by Antibodies and Potential Molecular Determinants in Chagas Disease Pathogenesis. Plos ONE 7, 113.CrossRefGoogle ScholarPubMed
Elizari, M. B. (1999). Chagasic myocardiopathy. Historical prospective. Medicine 59, 2540.Google Scholar
Enders, J. E., Paglini, P., Fernández, A. R., Marco, F. and Palma, J. A. (1995). Cardiac beta-receptors in experimental Chagas’ disease. Revista do Instituto de Medicina Tropical de Sao Paulo 37, 5962.CrossRefGoogle ScholarPubMed
Garg, N., Popov, V. L. and Papaconstantinou, J. (2003). Profiling gene transcription reveals a deficiency of mitochondrial oxidative phosphorylation in Trypanosoma cruzi-infected murine hearts: implication in chagasic myocarditis development. Biochimica et Biophysica Acta 1638, 106120.CrossRefGoogle ScholarPubMed
Gea, S., Gruppi, A., Cerbán, F., Pistoresi-Palencia, M. C. and Vottero-Cima, E. (1992). Immune response in mice immunized with acidic antigenic fractions from Trypanosoma cruzi cytosol. Revista del Instituto de Medicina Tropical de Sao Paulo 34, 389394.CrossRefGoogle ScholarPubMed
Gupta, S., Bhatia, V., Wen, J., Wu, Y., Huang, M. and Garg, N. (2009). Trypanosoma cruzi infection disturbs mitochondrial membrane potential and ROS production rate in cardiomyocytes. Free Radical Biology & Medicine 47, 14141421.CrossRefGoogle ScholarPubMed
Gutierrez, F. R., Mineo, T. W., Pavanelli, W. R., Guedes, P. M. and Silva, J. S. (2009). The effects of nitric oxide on the immune system during Trypanosoma cruzi infection. Memórias do Instituto Oswaldo Cruz 104, 236245.CrossRefGoogle ScholarPubMed
Jarreta, D., Orus, J., Barrientos, A., Miro, O., Roig, E., Heras, M., Moraes, C. T., Cardellach, F. and Casademont, J. (2000). Mitochondrial function in heart muscle from patients with idiopathic dilated cardiomyopathy. Cardiovascular Research 45, 860865.CrossRefGoogle ScholarPubMed
Labriola, C., Sousa, M. and Cazzulo, J. J. (1993). Purifcation of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi by affinity chromatography. Biological Research 26, 101107.Google Scholar
Long, X., Goldenthal, M. J., Wu, G. and Marín-García, J. (2004). Mitochondrial Ca2+ flux and respiratory enzyme activity decline are early events in cardiomyocyte response to H2O2. Journal of Molecular and Cellular Cardiology 37, 6370.CrossRefGoogle ScholarPubMed
Lo Presti, M. S., Rivarola, H. W., Bustamante, J. M., Fernández, A. R., Enders, J. E., Levin, G., Juaneda, E., Fretes, R., Triquell, M. F. and Paglini-Oliva, P. A. (2008). Some components of the cardiac b-adrenergic system are altered in the chronic indeterminate form of experimental Trypanosoma cruzi infection. International Journal for Parasitology 38, 14811492.CrossRefGoogle Scholar
Macedo, V. (1999). Indeterminate form of Chagas disease. Memórias do Instituto Oswaldo Cruz 94, 311316.CrossRefGoogle ScholarPubMed
Marin-García, J. and Goldenthal, M. J. (2008). Mitochondrial centrality in heart failure. Heart Failure Reviews 13, 137150.CrossRefGoogle ScholarPubMed
Maya, J. D., Orellana, M., Ferreira, J., Kemmerling, U., Lopez Muñoz, R. and Morello, A. (2010). Chagas disease: Present status of pathogenic mechanisms and chemotherapy. Biological Research 43, 323331.CrossRefGoogle ScholarPubMed
Moncayo, A. and Silveira, A. C. (2009). Current epidemiological trends for Chagas disease in Latin America and future challenges in epidemiology, surveillance and health policy. Memórias do Instituto Oswaldo Cruz 104, 1730.CrossRefGoogle ScholarPubMed
Pereira Silva, C., Del Carlo, C. H., Tavares de Oliveira, M. Jr., Scipioni, A., Strunz Cassaro, C. and Franchini Ramírez, J. A. (2009). Why do patients with chagasic cardiomyopathy have worse outcomes than those with non chagasic cardiomyopathy? Arquivos Brasileiros de Cardiology 91, 358362.Google Scholar
Polo-Romero, F. J., Beato-Pérez, J. L. and Romero-Portilla, C. (2011). Chagas: an emergent and unknown disease. Revista Clínica Española 211, 165166.CrossRefGoogle ScholarPubMed
Prata, A. (2001). Clinical and epidemiological aspects of Chagas’ disease. The Lancet Infectious Diseases 1, 92100.CrossRefGoogle ScholarPubMed
Reesink, H. W. (2005). European strategies against the parasite transfusion risk. Transfusion Clinique et Biologique 12, 14.CrossRefGoogle ScholarPubMed
Ribeiro, A. L. and Rocha, M. O. (1998). Indeterminate form of Chagas disease: considerations about diagnosis and prognosis. Revista da Sociedade Brasileira de Medicina Tropical 31, 301314.CrossRefGoogle ScholarPubMed
Schummis, G. A. (2007). Epidemiology of Chagas Disease in non endemic countries: the role of international migration. Memórias do Instituto Oswaldo Cruz 102, 7585.Google Scholar
Storino, R. and Milei, J. (1994). Enfermedad de Chagas. Mosby, Doyma Argentina, Buenos Aires, Argentina, South America.Google Scholar
Talvani, A., Rocha, M. O., Barcelos, L. S., Gomes, Y. S., Ribeiro, A. L. and Teixeira, M. M. (2004). Elevated concentrations of CCL2 and tumor necrosis factor-alpha in chagasic cardiomyopathy. Clinical Infectious Diseases 38, 943950.CrossRefGoogle ScholarPubMed
Trounce, I. A., Kim, Y. L., Jun, A. S. and Wallace, D. C. (1996). Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell line. Methods in Enzymology 264, 484509.CrossRefGoogle Scholar
Tsutsi, H. (2006). Oxidative stress in heart failure: the role of mitochondria. Internal Medicine 40, 11771182.CrossRefGoogle Scholar
Ueda, S., Masutani, H., Nakamura, H., Tanaka, T., Ueno, M. and Yodoi, J. (2002). Redox control of cell death. Antioxididants & Redox Signaling 4, 405414.CrossRefGoogle ScholarPubMed
Umezawa, E., Stolf, A. M. S., Corbett, C. E. P. and Shikanai-Yasuda, M. A. (2000). Chagas’ disease. Lancet 357, 797799.CrossRefGoogle Scholar
Vyatkina, G., Bhatia, V., Gerstner, A., Papaconstantinou, J. and Garg, N. (2004). Impaired mitochondrial respiratory chain and bioenergetics during chagasic cardiomyopathy development. Biochimica et Biophysica Acta 1689, 162173.CrossRefGoogle ScholarPubMed
Waghabi, M. C., De Souza, E. M., De Oliveira, J. M., Keramidas, M., Feige, J. J., Araujo Jorge, T. C., Bailly, S. (2009). Pharmacological inhibition of transforming growth factor beta signaling decreases infection and prevents heart damage in acute Chagas disease. Antimicrobial Agents and Chemotherapy 53, 46944701.CrossRefGoogle ScholarPubMed
Wen, J. J. and Garg, N. (2004). Oxidative modifications of mitochondrial respiratory complexes in response to the stress of Trypanosoma cruzi infection. Free Radical Biology & Medicine 37, 20722081.CrossRefGoogle Scholar
Wen, J. J. and Garg, N. J. (2008). Mitochondrial generation of reactive oxygen species is enhanced at the Q(o) site of the complex III in the myocardium of Trypanosoma cruzi-infected mice: beneficial effects of an antioxidant. Journal of Bioenergetics and Biomembranes 40, 587598.CrossRefGoogle Scholar
Wen, J. J., Vyatkina, G. and Garg, N. (2004). Oxidative damage during chagasic cardiomyopathy development: Role of mitochondrial oxidant release and inefficient antioxidant defense. Free Radical Biology &. Medicine 37, 18211833.CrossRefGoogle ScholarPubMed
Wen, J. J., Yachelini, P. C., Sembaj, A., Manzur, R. E. and Garg, N. (2006). Increased oxidative stress is correlated with mitochondrial dysfunction in chagasic patients. Free Radical Biology & Medicine 41, 270276.CrossRefGoogle ScholarPubMed
World Health Organization (2007). Report on Chagas Disease. World Health Organization on behalf of the Special Programme for Research and Training in Tropical Diseases, Geneva, Switzerland.Google Scholar
Zingales, B., Andrade, S. G., Briones, M. R. S., Campell, D. A., Chiari, E. and Fernandez, O. (2009). A new consensus of Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI To TcVI. Memórias do Instituto. Oswaldo Cruz 104, 10511054.CrossRefGoogle ScholarPubMed