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Host-cell apoptosis in Taenia solium-induced brain granulomas in naturally infected pigs

Published online by Cambridge University Press:  14 July 2008

C. S. SIKASUNGE ,
I. K. PHIRI ,
M. V. JOHANSEN ,
A. L. WILLINGHAM III  and
P. S. LEIFSSON
C. S. SIKASUNGE
Affiliation:
School of Veterinary Medicine, University of Zambia, P.O. Box 32379, Lusaka, Zambia
I. K. PHIRI
Affiliation:
School of Veterinary Medicine, University of Zambia, P.O. Box 32379, Lusaka, Zambia
M. V. JOHANSEN*
Affiliation:
DBL – Centre for Health Research and Development, Department of Veterinary Pathobiology, Faculty of Life Sciences, University of Copenhagen, Thorvaldsensvej 57, DK-1870 Frederiksberg C, Denmark
A. L. WILLINGHAM III
Affiliation:
WHO/FAO Collaborating Centre for Parasitic Zoonoses, Faculty of Life Sciences, University of Copenhagen, Dyrlægevej 100, 1870 Frederiksberg C, Denmark
P. S. LEIFSSON
Affiliation:
Department of Veterinary Pathobiology, Faculty of Life Sciences, University of Copenhagen, Ridebanevej 3, 1870 Frederiksberg C, Denmark
*
*Corresponding author: DBL – Centre for Health Research and Development, Department of Veterinary Pathobiology, Faculty of Life Sciences, University of Copenhagen, Thorvaldsensvej 57, DK-1870 Frederiksberg C, Denmark. Tel. +45 35 33 14 38. Fax: +45 35 33 14 33. E-mail: [email protected]
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Summary

To assess whether apoptosis occurs in pig brain granulomas due to Taenia solium cysticerci, brain tissues from 30 pigs naturally infected with T. solium cysticercosis were evaluated by terminal deoxynucleotidyl transferase-end labelling (TUNEL) staining. In addition, tissues were stained with CD3 marker to identify T lymphocytes. Examination of TUNEL-stained tissues showed apoptotic cells in early lesions that contained viable cysticerci. Apoptotic cells were primarily found interspersed with normal cell types, and were mostly located in the inflammatory infiltrate. Late or advanced granulomas with disintegrated scolices did not show TUNEL-positive cells. CD3+ cells were found in both early and advanced lesions and apoptosis mainly co-localized with CD3+ T lymphocytes. This suggests that these cells are constantly undergoing apoptosis and thus die as soon as they arrive at the site of infection. Apoptosis indeed may be one way by which T. solium cysticerci down-regulate the host's cellular immune response in early cysticercosis. Therefore, further research is needed to establish if other cells besides T-lymphocytes are also a target for destruction by cysticerci in early cysticercosis as well as studies to assess if cysteine protease is expressed by viable cysticerci in situ.

Keywords

Taenia soliumcysticercusapoptosisTUNEL stainingCD3 lymphocytesgranulomapig
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 10 , September 2008 , pp. 1237 - 1242
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Behnia, M., Robertson, K. A. and Martin, W. J. (2000). Lung infections: role of apoptosis in host defense and pathogenesis of disease. Chest 117, 1771–1777.Google Scholar
Carpio, A., Escobar, A. and Hauser, W. A. (1998). Cysticercosis and epilepsy: a critical review. Epilepsy 39, 1025–1040.Google Scholar
Chen, L, Rao, K. V., He, Y. X. and Ramaswamy, K. (2002). Skin-stage schistosomula of Schistosoma mansoni produce an apoptosis-inducing factor that can cause apoptosis of T cells. Journal of Biological Chemistry 277, 34329–34335.Google Scholar
De Souza, E. M., Meuser-Batista, M., Batista, D. G., Duarte, B. B., Araújo-Jorge, T. C. and Soeiro, M. N. (2008). Trypanosoma cruzi: Alpha-2-macroglobulin regulates host cell apoptosis induced by the parasite infection in vitro. Experimental Parasitology 118, 331–337.CrossRefGoogle ScholarPubMed
Flisser, A. (1994). Taeniosis and cysticercosis due to Taenia solium. Progress in Clinical Parasitology 4, 77–115.Google ScholarPubMed
Garcia, H. H., Del Brutto, O. H., Nash, T. E., White, A. C., Tsang, V. C. and Gilman, R. H. (2005). New concepts in the diagnosis and management of neurocysticercosis (Taenia solium). American Journal of Tropical Medicine and Hygiene 72, 3–9.Google Scholar
Koffeman, E., Keogh, E., Klein, M., Prakken, B. and Albani, S. (2007). Identification and manipulation of antigen specific T-cells with artificial antigen presenting cells. Methods in Molecular Medicine 136, 69–86.CrossRefGoogle ScholarPubMed
Lee, C. K. and Piedrahita, J. A. (2002). Inhibition of apoptosis in serum starved porcine embryonic fibroblasts. Molecular Reproduction and Development 62, 106–112.Google Scholar
Lenardo, M. J. (1991). Interleukin-2 programs mouse αβ T lymphocytes for apoptosis. Nature, London 353, 858–861.CrossRefGoogle Scholar
Londoño, D. P., Alvarez, J. I, Trujillo, J., Jaramillo, M. M. and Restrepo, B. I. (2002). The inflammatory cell infiltrates in porcine cysticercosis: immunohistochemical analysis during various stages of infection. Veterinary Parasitology 109, 249–259.Google Scholar
Lopes, M. F., Nunes, M. P., Henriques-Pons, A., Giese, N., Morse, H. C. 3rd, Davidson, W. F., Araujo-Jorge, T. C. and DosReis, G. A. (1999). Increased susceptibility of Fas ligand-deficient gld mice to Trypanosoma cruzi infection due to a Th2-biased host immune response. European Journal of Immunology 29, 81–89.Google Scholar
Martins, G. A., Vieira, L. Q., Cunha, F. Q. and Silva, J. S. (1999). Gamma interferon modulates CD95 (Fas) and CD95 ligand (Fas-L) expression and nitric oxide-induced apoptosis during the acute phase of Trypanosoma cruzi infection: A possible role in immune response control. Infection and Immunity 67, 3864–3871.CrossRefGoogle ScholarPubMed
Molinari, J. L., Mejia, H., White, A. C. Jr., Garrido, E., Borgonio, V. M., Baig, S. and Tato, P. (2000). Taenia solium: A cysteine protease secreted by metacestodes depletes human CD4 lymphocytes in vitro. Experimental Parasitology 94, 133–142.CrossRefGoogle ScholarPubMed
Molinari, J. L., Tato, P., Rodriguez, D., Solano, S., Rubio, M. and Sepulveda, J. (1998). Impairment of the inflammatory reaction on implanted Taenia solium metacestodes in mice by a T. solium RNA peptide: a scanning electron microscopy study. Parasitology Research 84, 173–180.CrossRefGoogle Scholar
Murphy, K. M., Heimberger, A. B. and Loh, Y. (1990). Induction by antigen of intrathymic apoptosis of CD4+ CD8+ TCRlo thymocytes in vivo. Science 250, 1720–1723.CrossRefGoogle ScholarPubMed
O'Connell, K. M. and Rogan, M. T. (2000). Apoptosis in human Jurkat T cells after culture with live Taenia crassiceps cysticerci in vitro. Parasitology 120, 649–655.CrossRefGoogle Scholar
Pileri, S. A., Roncador, G., Ceccarelli, C., Piccioli, M., Briskomatis, A., Sabattini, E., Ascani, S., Santini, D., Piccaluga, P. P., Leone, O., Damiani, S., Ercolessi, C., Sandri, F., Pieri, F., Leoncini, L. and Falini, B. (1997). Antigen retrieval techniques in immunohistochemistry: comparison of different methods. Journal of Pathology 183, 116–123.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Presas, A. M., Robert, L., Jiménez, J. A. and Willms, K. (2005). Apoptosis patterns in experimental Taenia solium and Taenia crassiceps strobilae from golden hamsters. Parasitology Research 96, 1–5.Google Scholar
Resendes, A. R., Majó, N., Segalés, J., Espadamala, J., Mateu, E., Chianini, F., Nofrarías, M. and Domingo, M. (2004). Apoptosis in normal lymphoid organs from healthy normal, conventional pigs at different ages detected by TUNEL and cleaved caspase-3 immunohistochemistry in paraffin-embedded tissues. Veterinary Immunology and Immunopathology 99, 203–213.Google Scholar
Sciutto, E., Fragoso, G., Fleury, A., Laclette, J. P., Sotelo, J., Aluja, A., Vargas, L. and Larralde, C. (2000). Review: Taenia solium disease in humans and pigs: an ancient parasitosis disease rooted in developing countries and emerging as a major health problem of global dimensions. Microbes and Infection 2, 1875–1890.Google Scholar
Silva, E. M., Guillermo, L. V., Ribeiro-Gomes, F. L., De Meis, J., Nunes, M. P., Senra, J. F., Soares, M. B., DosReis, G. A. and Lopes, M. F. (2007). Caspase inhibition reduces lymphocyte apoptosis and improves host immune responses to Trypanosoma cruzi infection. European Journal of Immunology 37, 738–746.CrossRefGoogle ScholarPubMed
Silva, R. D., Sotoca, R., Johansson, B., Ludovico, P., Sansonetty, F., Silva, M. T., Peinado, J. M. and Corte-Real, M. (2005). Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Molecular Microbiology 58, 824–834.Google Scholar
Solano, S., Cortés, I. M., Copitin, N. I., Tato, P. and Molinari, J. L. (2006). Lymphocyte apoptosis in the inflammatory reaction around Taenia solium metacestodes in porcine cysticercosis. Veterinary Parasitology 140, 171–176.Google Scholar
Tato, P., Castro, A. M., Rodriguez, D., Soto, R., Arechavaleta, F. and Molinari, J. L. (1995). Suppression of murine lymphocyte proliferation induced by a small RNA-peptide from the Taenia solium metacestode. Parasitology Research 81, 181–187.Google Scholar
Taylor, C. R., Shi, S. R., Chen, C., Young, L., Yang, C. and Cote, R. J. (1996). Comparative study of antigen retrieval heating methods: microwave, microwave and pressure cooker, autoclave, and steamer. Biotechnic and Histochemistry 71, 263–270.Google Scholar
Uddin, J., Gonzalez, A. E., Gilman, R. H., Garcia, H. H., Verastegui, M., Moore, L. J., Evans, C. A. W., Read, R. C. and Friedland, J. S. (2006). Neurocysticercal antigens stimulate chemokine secretion from human monocytes via an NF-[kappa]B-dependent pathway. Microbes and Infection 8, 1732–1740.Google Scholar
Villa, O. F. and Kuhn, R. E. (1996). Mice infected with the larvae of Taenia crassiceps exhibit a Th2-like immune response with concomitant anergy and downregulation of Th1-associated phenomena. Parasitology 112, 561–570.Google Scholar
White, A. C. Jr., Patrick, H. and Diaz, P. (1995). Asymptomatic neurocysticercosis in a patient with AIDS and cryptococcal meningitis. American Journal of Medicine 99, 101–102.CrossRefGoogle Scholar