Skip to main content Accessibility help

Enzymatic activities linked to cardiac energy metabolism of Trypanosoma evansi-infected rats and their possible functional correlations to disease pathogenesis



The aim of this study was to investigate the activities of important enzymes involved in the phosphoryl transfer network (adenylate kinase and creatine kinase (CK)), lactate dehydrogenase (LDH), respiratory chain complexes and biomarkers of cardiac function in rat experimentally infected by Trypanosoma evansi. Rat heart samples were evaluated at 5 and 15 days post-infection (PI). At 5 day PI, there was an increase in LDH and CK activities, and a decrease in respiratory chain complexes II, IV and succinate dehydrogenase activities. In addition, on day 15 PI, a decrease in the respiratory chain complex IV activity was observed. Biomarkers of cardiac function were higher in infected animals on days 5 and 15 PI. Considering the importance of the energy metabolism for heart function, it is possible that the changes in the enzymatic activities involved in the cardiac phosphotransfer network and the decrease in respiratory chain might be involved partially in the role of biomarkers of cardiac function of T. evansi-infected rats.


Corresponding author

* Corresponding author. Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil; Department of Animal Science, Universidade do Estado de Santa Catarina (UDESC), Chapecó, SC, Brazil. E-mail: and


Hide All
Arnold, S. (2012). The power of life – cytochrome c oxidase takes center stage in metabolic control, cell signalling and survival. Mitochondrion 12, 4656.
Baéz, A. L., Lopresti, M. S., Fretes, R., Díaz, C., Pons, P., Bazán, P. C., Strauss, M., Rivarola, H. W. and Paglini-Oliva, P. (2013). Chronic indeterminate phase of Chaga's disease: mitochondrial involvement in infection with two strains. Parasitology 143, 414421.
Baldisseraa*, M. D., Oliveira, C. B., Rech, V. C., Rezer, J. F. P., Sagrillo, M. R., Alves, M. P., Silva, A. P. T., da, Leal, D. B. R., Boligon, A. A., Athayde, M. L., Da Silva, A. S., Mendes, R. E., and Monteiro, S. G., (2014). Treatment with essential oil of Achyrocline satureioides in rats infected with Trypanosoma evansi: Relationship between protective effect and tissue damage. Pathology, research and practice 210, 10681074.
Bal, M. S., Singla, L. D., Kumar, H., Vasudev, A., Gupta, K. and Juyal, P. D. (2012). Pathological studies on experimental Trypanosoma evansi infection in Swiss albino mice. Journal Parasitic Diseases 36, 260264.
Bottomley, P. A., Wu, K. C., Gerstenblith, G., Schulman, S. P., Steinberg, A. and Weiss, R. G. (2009). Reduced myocardial creatine kinase flux in human myocardial infarction: an in vivo phosphorus magnetic resonance spectroscopy study. Circulation 119, 19181924.
Brdiczca, D., Kaldis, P. and Wallimann, T. (1994). In vitro complex formation between the octamer of mitochondrial creatine kinase and porin. Journal of Biological Chemistry 269, 2764027644.
Carvajal, K. and Moreno-Sanchez, R. (2003). Heart metabolic disturbances in cardiovascular diseases. Archives of Medical Research 34, 8999.
Chen, Y. R. and Zweier, J. L. (2014). Cardiac mitochondria and reactive oxygen species generation. CirculationResearch 114, 524537.
Colpo, C. B., Monteiro, S. G., Stainki, D. R., Colpo, E. T. B. and Henriques, G. B. (2005). Natural infectionbyTrypanosoma evansi in dogs. Ciência Rural 35, 717719.
Da Silva, A. S., Doyle, R. L. and Monteiro, S. G. (2006). Métodos de contenção e confecção de esfregaço sanguíneo para pesquisa de hemoparasitas em ratos e camundongos. Faculdade de Medicina Veterinária, Zootecnia e Agronomia 13, 8387.
Da Silva, A. S., Wolkmer, P., Gressler, L. T., Otto, M. A., Bess, F., Tavares, K. S., Zanette, R. A. and Monteiro, S. G. (2009). Trypanosoma evansipathogenicitystrain in ratsinoculatedwith parasite in fresh and cryopreserved blood. Ciência Rural 39, 18421846.
Da Silva, A. S., Pierezan, F., Wolkmer, P., Costa, M. M., Oliveira, C. B., Tonin, A. A., Santurio, J. M., Lopes, S. T. A. and Monteiro, S. G. (2010). Pathological findings associated with experimental infection by Trypanosoma evansi in cats. Journal of Comparative Pathology 142, 170176.
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.
Dolci, A. and Panteghini, M. (2006). The exciting story of cardiac biomarkers: from retrospective detection to gold standard for acute myocardial infarction and more. Clinica Chimica Acta 369, 179187.
Dzeja, P. and Terzic, A. (2009). Adenylate kinase and AMP signaling networks: metabolic monitoring, signal communication and body energy sensing. International Journal of Molecular Science 10, 17291772.
Dzeja, P. P., Vitkevicius, K. T., Redfield, M. M., Burnettm, J. C. and Terzic, A. (1999). Adenylate kinase-catalyzed phosphotransfer in the myocardium: increased contribution in heart failure. Circulation Research 84, 11371143.
Finol, H. J., Roschman-González, A. (2014). Ultrastructural Study on Tissue Alterations Caused by Trypanosomatids in Experimental Murine Infections. Frontier public health 2, 16.
Fischer, J. C., Ruitenbeek, W., Berden, J. A., Trijbels, J. M., Veerkamp, J. H., Stadhouders, A. M., Sengersa, R. C. A., and Janssena, A. J. M. (1985). Differential investigation of the capacity of succinate oxidation in human skeletal muscle.. Clinica Chimica Acta 153, 2326.
Gao, L., Laude, K. and Cai, H. (2008). Mitochondrial pathophysiology, Reactive oxygen species, and cardiovascular diseases. Veterinary Clinical North America Small Animal Practice 38, 137155.
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: implications in chagasic myocarditis development. Biochimica Biophysica Acta 1638, 106120.
Halliwell, B., and Gutteridge, J. M. C. (2007). Free Radicals in Biology and Medicine. 4th edn, Clarendon Press, Oxford.
Herrera, H. M., Davila, A. M. R., Norek, A., Abreu, U. G., Souza, S. S., Da Andrea, P. S. and Jansen, A. M. (2004). Enzootiology of Trypanosoma evansi in Pantanal, Brazil. Veterinary Parasitology 25, 263275.
Hoare, C. A. (1972). The Trypanosomes of Mammals a Zoological Monograph. Blackwell, Oxford, UK, 546 p.
Hughes, B. P. (1962). A method for estimation of serum creatine kinase and its use in comparing creatine kinase and aldolase activity in normal and pathological sera. Clinica Chimica Acta 7, 597603.
Ingwall, J. S. (2004). Transgenic and cardiac energetics: new insights into cardiac metabolism. Journal of Molecular and Cellular Cardiology 37, 613623.
Jacobson, J. and Duchen, M. R. (2004). Interplay between mitochondria and cellular calcium signalling. Molecular and Cellular Biochemistry 256–257, 209218.
Jaffe, A. S., Babuin, L. and Apple, F. S. (2006). Biomarkers in acute cardiac disease: the present and the future. Journal of the American College of Cardiology 48, 111.
Joshi, P. P., Shegokar, V. R., Powar, R. M., Herder, S., Katti, R., Salkar, H. R., Dani, V. S., Bhargava, A., Jannin, J. and Truc, P. (2005). Human Trypanosomosis caused by Trypanosoma evansi in India: the first case report. American Journal of Tropical Medicine and Hygiene 73, 491495.
Kaplan, A., Szabo, L. L. and Opheim, K. E. (1998). Clinical Chemistry: Interpretation and Techniques. Lea e Febiger, Philadelphia.
Leong, S. F., Lai, J. F. K., Lim, L. and Clark, J. B. (1981). Energy-metabolising enzymes in brain regions of adult and aging rats. Journal of Neurochemistry 37, 15481556.
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265267.
Lucas, D. T. and Szweda, L. I. (1999). Declines in mitochondrial respiration during cardiac reperfusion: age-dependent inactivation of alpha-ketoglutarate dehydrogenase. Proceedings of the National Academy of Sciences of the United States of America 96, 66896693.
Meyer, D. E., Basha, H. I. and Koenig, M. K. (2013). Mitochondrial cardiomyopathy: pathophysiology, diagnosis, and management. Texas Heart Institute Journal 40, 385394.
Neubauer, S. (2007). The failing heart - an engine out of fuel. New England Journal of Medicine 356, 11401151.
Nickel, A., Loffler, J. and Maack, C. (2013). Myocardial energetic in heart failure. Basic Research in Cardiology 108, 358378.
Park, H. S. and Hourani, S. M. (1999). Differential effects of adenine nucleotide analogueson shape change and aggregation induced by adnosine 5-diphosphate (ADP) inhuman platelets. British Journal of Pharmacology 127, 13591366.
Ranjithkumar, M., Kamili, N. M., Saxena, A., Dan, A., Dey, S., and Raut, S. S. (2011). Disturbance of oxidant/antioxidant equilibrium in horses naturally infected with Trypanosoma evansi . Veterinary Parasitology 180, 349353.
Rodrigues, A., Fighera, R. A., Souza, T. M., Schild, A. L., Soares, M. P., Milano, J. and Barros, C. S. L. (2005). Outbreaks of trypanosomiasis in horses by Trypanosoma evansi in the state of Rio Grande do Sul, Brazil: epidemiological, clinical, hematological and pathological aspects. Pesquisa Veterinária Brasileira 25, 239249.
Rustin, P., Chretien, D., Bourgeron, T., Gérard, B., Rotig, A., Saudubray, J. M., and Munnick, A. (1994). Biochemical and molecular investigations in respiratory chain deficiencies. Clinica Chimica Acta 228, 3551.
Sadek, H. A., Humphries, K. M., Szweda, P. A. and Szweda, L. I. (2002). Selective inactivation of redox-sensitive mitochondrial enzymes during cardiac reperfusion. Archives of Biochemistry and Biophysics 406, 222228.
Saks, V., Dzeja, P., Schlattner, U., Vendelin, M., Terzic, A. and Wallimann, T. (2006). Cardiac system bioenergetics: metabolic basis of the Frank–Starling law. Journal of Physiology 571, 253273.
Saks, V. A., Tiivel, T., Kay, L., Novel-Chate, V., Daneshrad, Z., Rossi, A., Fontaine, E., Keriel, C., Leverve, X., Ventura-Clapier, R., Anflous, K., Samuel, J. L. and Rappaport, L. (1996). On the regulation of cellular energetics in health and disease. Molecular and Cellular Biochemistry 160–161, 195208.
Saks, V. A., Dossantos, P., Gellerich, F. N. and Diolez, P. (1998). Quantitative studies of enzyme-substrate compartmentation, functional coupling and metabolic channeling in muscle cells. Molecular and Cellular Biochemistry 184, 291307.
Schapira, A. H. (2012). Mitochondrial diseases. Lancet 379, 18251834.
Scorrano, L. (2013). Keeping mitochondria in shape: a matter of life and death. European Journal of Clinical Investigation 43, 886893.
Silva, R. A. M. S., Seidl, A., Ramirez, L. and Dávila, A. M. R. (2002). Trypanosoma evansi e Trypanosoma vivax: Biologia, Diagnóstico e Controle. Embrapa Pantanal, Corumbá, p. 162.
Teixeira, P. C., Iwai, L. K., Kumaroto, A. C. K., Honorato, R., Fiorelli, A., Stolf, N., Kalil, J. and Cunha-Neto, E. (2006). Proteomic inventory of myocardial proteins from patients with chronic Chaga's cardiomyopathy. Brazilian Journal of Medical and Biological Research 39, 15491562.
Tejero, F., Arias-Mota, L. L., Roschman-González, A., Aso, P. M. and Finol, H. J. (2010). Trypanosoma evansi: ultrastructural cardiac muscle and cardiac microvasculature changes in experimental murine infections. Acta Scientiae Veterinariae 38, 279285.
Ventura-Clapier, R., Garnier, A., Veksler, V. and Joubert, F. (2010). Bioenergetics of the failing heart. Biochimica et Biophysica Acta 1813, 13601372.
Vyatkina, G., Bhatia, V., Gerstner, A., Papaconstantinou, J. and Garg, N. (2004). Impaired mitochondrial respiratory chain and bioenergetics during cardiomyopathy development. Biochimica et Biophysica Acta 1689, 162173.
Wallace, D. C. (1999). Mitochondrial diseases in man and mouse. Science 283, 14821487.
Wolkmer, P., Da Silva, A. S., Traesel, C. K., Paim, F. C., Cargnelutti, J. F., Pagnoncelli, M., Picada, M. E., Monteiro, S. G. and Lopes, S. T. (2009). Lipid peroxidation associated with anemia in rats experimentally infected with Trypanosoma evansi . Veterinary Parasitology 28, 4146.
Zheng, X. X., Shoffner, J. M., Voljavec, A. S. and Wallace, D. C. (1990). Evaluation of procedures for assaying oxidative phosphorylation enzyme activities in mitochondrial myophaty muscle biopsies. Biochimica Biophysica Acta 1019, 110.



Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed