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Involvement of the β-adrenergic system in the cardiac chronic form of experimental Trypanosoma cruzi infection

Published online by Cambridge University Press:  15 June 2009

M. S. LO PRESTI ,
H. W. RIVAROLA ,
A. R. FERNÁNDEZ ,
J. E. ENDERS ,
G. LEVIN ,
R. FRETES ,
F. M. CERBAN ,
V. V. GARRIDO  and
P. PAGLINI-OLIVA
M. S. LO PRESTI*
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085, PC5000, Córdoba, Argentina Instituto de Investigación en Ciencias de la Salud Humana, Universidad Nacional de La Rioja. Argentina
H. W. RIVAROLA
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085, PC5000, Córdoba, Argentina Instituto de Investigación en Ciencias de la Salud Humana, Universidad Nacional de La Rioja. Argentina
A. R. FERNÁNDEZ
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085, PC5000, Córdoba, Argentina
J. E. ENDERS
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085, PC5000, Córdoba, Argentina
G. LEVIN
Affiliation:
Centro de Investigaciones Endocrinológicas – CONICET, Hospital de Niños Ricardo Gutiérrez, Gallo 1360, Ciudad Autónoma de Buenos Aires, CP1425, Argentina
R. FRETES
Affiliation:
Cátedra de Biología Celular, Histología y Embriología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, 5016Córdoba, Argentina
F. M. CERBAN
Affiliation:
CIBICI-CONICET, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Argentina
V. V. GARRIDO
Affiliation:
CIBICI-CONICET, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Argentina
P. PAGLINI-OLIVA
Affiliation:
Cátedra de Física Biomédica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba. Santa Rosa 1085, PC5000, Córdoba, Argentina Instituto de Investigación en Ciencias de la Salud Humana, Universidad Nacional de La Rioja. Argentina
*
*Corresponding author: Pio Collivadino 4126, Cerro Chico, 5009Córdoba, Argentina. Tel/Fax: +54 351 4332020. E-mail: SilviLoPresti@gmail.com
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Summary

Changes in the cardiac β-adrenergic system in early stages of Trypanosoma cruzi infection have been described. Here, we studied an early (135 days post-infection–p.i.) and a late stage (365 days p.i.) of the cardiac chronic form of the experimental infection (Tulahuen or SGO-Z12 strains), determining plasma epinephrine and norepinephrine levels, β-receptor density, affinity and function, cardiac cAMP concentration and phosphodiesterase activity, cardiac contractility, and the presence of β-receptor autoantibodies. Tulahuen-infected mice presented lower epinephrine and norepinephrine levels; lower β-receptor affinity and density; a diminished norepinephrine response and higher cAMP levels in the early stage, and a basal contractility similar to non-infected controls in the early and augmented in the late stage. The Tulahuen strain induced autoantibodies with weak β-receptor interaction. SGO-Z12-infected mice presented lower norepinephrine levels and epinephrine levels that diminished with the evolution of the infection; lower β-receptor affinity and an increased density; unchanged epinephrine and norepinephrine response in the early and a diminished response in the late stage; higher cAMP levels and unchanged basal contractility. The SGO-Z12 isolate induced β-receptor autoantibodies with strong interaction with the β-receptors. None of the antibodies, however, acted a as β-receptor agonist. The present results demonstrate that this system is seriously compromised in the cardiac chronic stage of T. cruzi infection.

Keywords

chronic Chagas diseasecardiac β-adrenergic systemTrypanosoma cruzi strainscardiac contractilitymyocardiopathy
Type
Research Article
Information
Parasitology , Volume 136 , Issue 8 , July 2009 , pp. 905 - 918
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Aoki, M. P., Cano, R. C., Pallegrini, A. V., Tanos, T., Guiñazú, N. L., Coso, O. A. and Gea, S. (2006). Different signaling pathways are involved in cardiomyocyte survival induced by a Trypanosoma cruzi glycoprotein. Microbes and Infection 8, 1723–1731.CrossRefGoogle ScholarPubMed
Barki-Harrington, L., Perrino, C. and Rockman, H. A. (2004). Network integration of the adrenergic system in cardiac hypertrophy. Cardiovascular Research 63, 391–402.CrossRefGoogle ScholarPubMed
Barrett, M. P., Burchmore, R. J., Stich, A., Lazzari, J. O., Frasch, A. C., Cazzulo, J. J. and Krishna, S. (2003). The trypanosomiases. Lancet 362, 1469–1480.CrossRefGoogle ScholarPubMed
Bestetti, R. B. and Muccillo, G. (1997). Clinical course of Chagas' heart disease: a comparison with dilated cardiomyopathy. International Journal of Cardiology 60, 187–193.CrossRefGoogle ScholarPubMed
Bristow, M. R. (1993). Changes in myocardial and vascular receptors in heart failure. Journal of the American College of Cardiology 22, 61–71.CrossRefGoogle ScholarPubMed
Brodde, O. E. (1991). β1- and β2-adrenoceptors in the human heart: properties, function and alterations in chronic heart failure. Pharmacological Reviews 43, 203–242.Google Scholar
Brodde, O. E. (2008). β1 and β2 adrenoceptor polymorphisms: Functional importance, impact on cardiovascular diseases and drug responses. Pharmacology and Therapeutics 117, 1–29.CrossRefGoogle ScholarPubMed
Bustamante, J. M., Rivarola, H. W., Fernández, A. R., Enders, J., Fretes, R., De Luca D'Oro, G., Palma, J. A. and Paglini-Oliva, P. (2003 a). Trypanosoma cruzi reinfections provoke synergistic effect and cardiac β-adrenergic receptors' dysfunction in the acute phase of experimental Chagas' disease. Experimental Parasitology 103, 136–142.CrossRefGoogle ScholarPubMed
Bustamante, J. M., Rivarola, H. W., Fernandez, A. R., Enders, J., Fretes, R., Palma, J. A. and Paglini-Oliva, P. (2003 b). Indeterminate Chagas disease: Trypanosoma cruzi strain and reinfections are factors involved in the progression of cardiopathy. Clinical Science 104, 415–420.CrossRefGoogle ScholarPubMed
Chakraborti, S., Chakraborti, T. and Shaw, G. (2000). β-adrenergic mechanisms in cardiac diseases. A perspective. Cell Signal 12, 499–513.CrossRefGoogle ScholarPubMed
Correa-Araujo, R., Oliveira, J. S. and Ricciardi Cruzm, A. (1991). Cardiac levels of norepinephrine, dopamine, serotonin and histamine in Chagas' disease. International Journal of Cardiology 31, 329–336.CrossRefGoogle ScholarPubMed
Cossio, P. M., Bustouoabad, O., Paterno, E., Lotti, R., Casanova, M. B., Podesta, M. B., Bolomo, N., Arana, R. M. and de Pasqualini, C. D. (1984). Experimental myocarditis induced in Swiss mice by homologous heart immunization resembles chronic experimental Chagas' heart disease. Clinical Immunology and Immunopathology 33, 165–175.CrossRefGoogle ScholarPubMed
Coura, J. R. (2007). Chagas disease: what is known and what is needed – A background article. Memórias do Instituto Oswaldo Cruz 102, 113–122.CrossRefGoogle ScholarPubMed
Cubillos-Garzón, L. A., Casas, J. P., Morillo, C. A. and Bautista, L. E. (2004). Congestive heart failure in Latin America: the next epidemic. American Heart Journal 147, 412–417.CrossRefGoogle ScholarPubMed
Dzimiri, N. (1999). Regulation of β-Adrenoceptor signalling in cardiac function and disease. Pharmacological Reviews 51, 465–501.Google Scholar
Elizari, M. B. (1999). Chagasic myocardiopathy. Historical prospective. Medicina (Buenos Aires) 59, 25–40.Google Scholar
Esposito, G., Rapacciuolo, A., Naga Prasad, A. V. and Rockman, H. A. (2002). Cardiac hypertrophy: Role of G protein-coupled receptors. Journal of Cardiac Failure 8, S409–S414.CrossRefGoogle ScholarPubMed
Freitas, H. F., Chizzola, P. R., Paes, A. T., Lima, A. C. and Mansur, A. J. (2005). Risk stratification in a Brazilian hospital-based cohort of 1220 outpatients with heart failure: role of Chagas' heart disease. International Journal of Cardiology 102, 239–247.CrossRefGoogle Scholar
George, M. S. and Pitt, G. S. (2006). The real estate of cardiac signaling: Location, location, location. Proceedings of the National Academy of Sciences, USA 103, 7535–7536.CrossRefGoogle ScholarPubMed
Harding, S. E., Brown, L. A., Wynne, D. G., Davies, C. H. and Poole-Wilson, P. A. (1994). Mechanisms of β-adrenoceptor desenzitation in the failing human heart. Cardiovascular Research 28, 1451–1460.CrossRefGoogle Scholar
Higuchi, M. L., De Morais, C. F., Pereira Barreto, A. C., Lopes, E. A., Stolf, N., Bellotti, G. and Pileggi, F. (1987). The role of active myocarditis in the development of heart failure in chronic Chagas' disease: a study based on endomyocardial biopsies. Clinical Cardiology 10, 665–670.CrossRefGoogle ScholarPubMed
Iosa, D., DeQuattro, V., Lee, D. D., Elkayam, U. and Palmero, H. (1989). Plasma norepinephrine in Chagas cardioneuromyopathy: a marker of progressive dysautonomia. American Heart Journal 117, 882–887.CrossRefGoogle ScholarPubMed
Jahns, R., Boivin, V. and Lohse, M. J. (2006). β1-adrenergic receptor function, autoimmunity, and pathogenesis of dilated cardiomyopathy. Trends in Cardiovascular Medicine 16, 20–24.CrossRefGoogle Scholar
Kalil, J. and Cunha-Neto, E. (1996). Autoimmunity in Chagas' cardiomiopathy: fulfilling the criteria at last. Parasitology Today 12, 396–399.CrossRefGoogle Scholar
Keys, J. R. and Koch, W. J. (2004). The adrenergic pathway and heart failure. Recent Progress in Hormone Research 59, 13–30.CrossRefGoogle ScholarPubMed
Kierszenbaum, F. and Hudson, L. (1985). Autoimmunity in Chagas Disease: Cause or Symptom? Parasitology Today 1, 4–9.CrossRefGoogle Scholar
Labovsky, V., Smulski, C. R., Gómez, K., Levy, G. and Levin, M. J. (2007). Anti β1-adrenergic receptor autoantibodies in patients with chronic Chagas heart disease. Clinical and Experimental Immunology 148, 440–449.CrossRefGoogle ScholarPubMed
Laucella, S. A., Rottemberg, M. E. and De Titti, E. H. (1996). Papel de las citoquinas en la resistencia y patología durante la infección con Trypanosoma cruzi. Revista Argentina de Microbiología 28, 99–109.Google Scholar
Leff, P. (1995). The two-state model of receptor activation. Trends in Pharmacological Science 16, 89–97.CrossRefGoogle ScholarPubMed
Lefkowitz, R. J., Cotecchia, S., Samama, P. and Costa, T. (1993). Constitutive activity of receptors coupled to guanine-nucleotide regulatory proteins. Trends in Pharmacological Science 4, 303–308.CrossRefGoogle Scholar
Lenzi, H. L., Oliveira, D. N., Lima, M. T. and Gattass, C. R. (1996). Trypanosoma cruzi: Paninfectivity of CL strain during murine acute infection. Experimental Parasitology 84, 16–27.CrossRefGoogle ScholarPubMed
Levin, M. J. and Hoebeke, J. (2008). Cross-talk between anti-β1-adrenoceptor antibodies in dilated cardiomyopathy and Chagas' heart disease. Autoimmunity 41, 429–33.CrossRefGoogle ScholarPubMed
Lo Presti, M. S., Bustamante, J. M., Rivarola, H. W., Fernández, A. R., Enders, J., Fretes, R., Levin, G. and Paglini-Oliva, P. A. (2006). Changes in the cardiac β-adrenergic system provoked by different T. cruzi strains. International Journal of Cardiology 111, 104–112.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 β-adrenergic system are altered in the chronic indeterminate form of experimental Trypanosoma cruzi infection. International Journal for Parasitology 38, 1481–1492.CrossRefGoogle Scholar
Lohse, M. J., Engelhart, S., Danner, S. and Bohm, M. (1996). Mechanisms of β-adrenergic receptor desenzitation: from molecular biology to heart failure. Basic Research in Cardiology 91, 29–34.CrossRefGoogle Scholar
Lopez Bergami, P., Gómez, K. A., Levy, G. V., Grippo, V., Baldi, A. and Levin, M. J. (2005). The β1 adrenergic effects of antibodies against the C-terminal end of the ribosomal P2β protein of Trypanosoma cruzi associate with a specific pattern of epitope recognition. Clinical and Experimental Immunology 142, 140–147.CrossRefGoogle ScholarPubMed
Machado, C. R., Camargos, E. R., Guerra, L. B. and Moreira, M. C. (2000). Cardiac autonomic denervation in congestive heart failure: comparison of Chagas' heart disease with other dilated cardiomyopathy. Human Pathology 31, 3–10.CrossRefGoogle ScholarPubMed
Manoel-Caetano, F. DA S. and Silva, A. E. (2007). Implications of genetic variability of Trypanosoma cruzi for the pathogenesis of Chagas disease. Cadernos de Saúde Pública 23, 2263–2274.CrossRefGoogle ScholarPubMed
Milligan, G., Bond, R. A. and Lee, M. (1995). Inverse agonism, pharmacological curiosity or potential therapeutic strategy. Trends in Pharmacological Science 16, 10–13.CrossRefGoogle ScholarPubMed
Montamat, E. E., Doro, G. M. D., Gallerano, R. H., Sosa, R. and Blanco, A. (1996). Characterization of Trypanosoma cruzi population by zymodemes: Correlation with clinical picture. American Journal of Tropical Medicine and Hygiene 55, 625–628.CrossRefGoogle ScholarPubMed
Movsesian, M. A. and Bristow, M. R. (2005). Alterations in cAMP-mediated signaling and their role in the pathophysiology of dilated cardiomyopathy. Currents Topics in Developmental Biology 68, 25–48.CrossRefGoogle ScholarPubMed
Nunes, M. P., Sobral, A. C. and Coutinho, S. G. (1992). Quantification of Trypanosoma cruzi in the heart, lymph nodes and liver of experimentally infected mice, using limiting dilution analysis. Memórias do Instituto Oswaldo Cruz 87, 503–509.CrossRefGoogle ScholarPubMed
Rassi, A. Jr., Rassi, W. C. and Little, W. C. (2000). Chagas heart disease. Clinical Cardiology 23, 883–889.Google ScholarPubMed
Rocha, N. N., García, S., Jiménez, L. E. D., Hernández, C. C. Q., Senra, J. F. V., Lina, R. S., Cyrino, F., Bouskela, E., Soares, M. B. P., Ribeiro dos Santos, R. and Campos de Carvalho, A. C. (2006). Characterization of cardiopulmonary function and cardiac muscarinic and adrenergic receptor density adaptatio in C57BL/6 mice with chronic Trypanosoma cruzi infection. Parasitology 133, 729–737.CrossRefGoogle Scholar
Rodríguez, A., Rioult, M. G., Ora, A. and Andrews, N. W. (1995). A trypanosome-soluble factor induces IP3 formation, intracellular Ca2+ mobilization and microfilament rearrangement in host cells. Journal of Cell Biology 129, 1263–1273.CrossRefGoogle ScholarPubMed
Steinberg, S. F. (2004). Beta(2)-Adrenergic receptor signaling complexes in cardiomyocyte caveolae/lipid rafts. Journal of Molecular and Cellular Cardiology 37, 407–415.CrossRefGoogle ScholarPubMed
Sterin-Borda, L. and Borda, E. (1999). Overview of molecular mechanisms in chagasic cardioneuromyopathy and achalasia. Medicina (Buenos Aires) 59, 75–83.Google ScholarPubMed
Sterin-Borda, L. J. and Borda, E. S. (1994). Participation of autonomic nervous system in the pathogenesis of Chagas' disease. Acta Physiologica, Pharmacologica et Therapeutica Latinoamericana 44, 109–123.Google ScholarPubMed
Sterin-Borda, L., Giordanengo, L., Joensen, L. and Gea, S. (2003). Cruzipain induces autoantibodies against cardiac acetylcholine receptors. Functional and pathological implications. European Journal of Immunology 33, 2459–2468.Google Scholar
Taniwaki, N. N., Machado, F. S., Massensini, A. R. and Mortara, R. A. (2006). Trypanosoma cruzi disrupts myofibrillar organization and intracellular calcium levels in mouse neonatal cardiomyocytes. Cell and Tissue Reserach 324, 489–496.CrossRefGoogle ScholarPubMed
Tarleton, R. L. and Zhang, L. (1999). Chagas disease etiology: autoimmunity or parasite persistence? Parasitology Today 5, 94–99.CrossRefGoogle Scholar
Teixeira, A. R. L., Nascimento, R. J. and Sturm, N. R. (2006). Evolution and pathology in Chagas disease – A review. Memórias do Instituto Oswaldo Cruz 101, 463–491.CrossRefGoogle ScholarPubMed
Wallukat, G., Nissen, E., Morvinski, R. and Müller, J. (2000). Autoantibodies against the β and muscarinic receptors in cardiomyopathy. Herz 25, 261–266.CrossRefGoogle ScholarPubMed
World Health Organization (2002). Control of Chagas Disease. Second Report of the WHO Expert Committee. WHO Technical Report Series, No. 905. World Health Organization, Geneva.Google Scholar
World Health Organization (2007). Report on Chagas Disease. World Health Organization on behalf of the Special Programme for Research and Training in Tropical Diseases.Google Scholar
Wood, J. N., Hudson, L., Jessell, T. M. and Yamamoto, M. (1982). A monoclonal antibody defining antigenic determinants on subpopulations of mammalian neurones and Trypanosoma cruzi parasites. Nature, London 296, 34–38.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.CrossRefGoogle ScholarPubMed