Skip to main content
×
Home

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

  • ALEJANDRA LIDIA BÁEZ (a1), MARÍA SILVINA LO PRESTI (a1), RICARDO FRETES (a2), CINTIA DÍAZ (a2), PATRICIA PONS (a3), PAOLA CAROLINA BAZÁN (a1), MARIANA STRAUSS (a1), HÉCTOR WALTER RIVAROLA (a1) and PATRICIA PAGLINI-OLIVA (a1)...
Summary
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.

Copyright
Corresponding author
*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: alejandralidiab@hotmail.com.
References
Hide All
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Coura J. R., Borges-Pereira J. (2010). Chagas disease: 100 years after its discovery. A systemic review. Acta Tropica 115, 513.
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.
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.
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.
Elizari M. B. (1999). Chagasic myocardiopathy. Historical prospective. Medicine 59, 2540.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Macedo V. (1999). Indeterminate form of Chagas disease. Memórias do Instituto Oswaldo Cruz 94, 311316.
Marin-García J. and Goldenthal M. J. (2008). Mitochondrial centrality in heart failure. Heart Failure Reviews 13, 137150.
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.
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.
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.
Polo-Romero F. J., Beato-Pérez J. L. and Romero-Portilla C. (2011). Chagas: an emergent and unknown disease. Revista Clínica Española 211, 165166.
Prata A. (2001). Clinical and epidemiological aspects of Chagas’ disease. The Lancet Infectious Diseases 1, 92100.
Reesink H. W. (2005). European strategies against the parasite transfusion risk. Transfusion Clinique et Biologique 12, 14.
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.
Schummis G. A. (2007). Epidemiology of Chagas Disease in non endemic countries: the role of international migration. Memórias do Instituto Oswaldo Cruz 102, 7585.
Storino R. and Milei J. (1994). Enfermedad de Chagas. Mosby, Doyma Argentina, Buenos Aires, Argentina, South America.
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.
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.
Tsutsi H. (2006). Oxidative stress in heart failure: the role of mitochondria. Internal Medicine 40, 11771182.
Ueda S., Masutani H., Nakamura H., Tanaka T., Ueno M. and Yodoi J. (2002). Redox control of cell death. Antioxididants & Redox Signaling 4, 405414.
Umezawa E., Stolf A. M. S., Corbett C. E. P. and Shikanai-Yasuda M. A. (2000). Chagas’ disease. Lancet 357, 797799.
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.
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.
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.
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.
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.
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.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 1
Total number of PDF views: 18 *
Loading metrics...

Abstract views

Total abstract views: 224 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th November 2017. This data will be updated every 24 hours.