Caspase-8 and caspase-9 mediate thymocyte apoptosis in trypanosoma cruzi acutely infected mice

Journal of Leukocyte Biology

Volumn 93, Issue 2, 2013, Pages 227-234

  Farias de Oliveira, Désio Aurélio ^a   Villa Verde, Déa Maria Serra ^a   Panzenhagen, Pedro Henrique Nunes ^a   Santos, Danielle Silva Dos ^a   Berbert, Luiz Ricardo ^a   Savino, Wilson ^a   de Meis, Juliana ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Cell death; Chagas disease; Glucocorticoid; T lymphocytes; Thymus

Indexed keywords

BENZYLOXYCARBONYLISOLEUCYLGLUTAMYLTHREONYLASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLLEUCYLGLUTAMYLHISTIDYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CASPASE 8; CASPASE 8 INHIBITOR; CASPASE 9; CASPASE 9 INHIBITOR;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CHAGAS DISEASE; ENZYME ACTIVATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; THYMOCYTE; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE;

ANIMALS; APOPTOSIS; CASPASE 8; CASPASE 9; CHAGAS DISEASE; FLOW CYTOMETRY; MALE; MICE; MICE, INBRED BALB C; T-LYMPHOCYTES; THYMUS GLAND; TRYPANOSOMA CRUZI;

EID: 84873302789     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1211589     Document Type: Article

References (47)

1. Tarleton, R. L., Reithinger, R., Urbina, J. A., Kitron, U., Gurtler, R. E. (2007) The challenges of Chagas Disease-grim outlook or glimmer of hope. PLoS Med. 4, e332.
2. Coura, J. R., Borges-Pereira, J. (2010) Chagas disease: 100 years after its discovery. A systemic review. Acta Trop. 115, 5-13.
3. Minoprio, P. M., Eisen, H., Forni, L., D'Imperio Lima, M. R., Joskowicz, M., Coutinho, A. (1986) Polyclonal lymphocyte responses to murine Trypanosoma cruzi infection. I. Quantitation of both T- and B-cell responses. Scand. J. Immunol. 24, 661-668.
4. D'Imperio Lima, M. R., Eisen, H., Minoprio, P., Joskowicz, M., Coutinho, A. (1986) Persistence of polyclonal B cell activation with undetectable parasitemia in late stages of experimental Chagas' disease. J. Immunol. 137, 353-356.
5. Minoprio, P. (2001) Parasite polyclonal activators: new targets for vaccination approaches? Int. J. Parasitol. 31, 588-591.
6. De Meis, J., Morrot, A., Farias-de-Oliveira, D. A., Villa-Verde, D. M., Savino, W. (2009) Differential regional immune response in Chagas disease. PLoS Negl. Trop. Dis. 3, e417.
7. Henriques-Pons, A., DeMeis, J., Cotta-De-Almeida, V., Savino, W., Araujo-Jorge, T. C. (2004) Fas and perforin are not required for thymus atrophy induced by Trypanosoma cruzi infection. Exp. Parasitol. 107, 1-4.
8. Cotta-de-Almeida, V., Bonomo, A., Mendes-da-Cruz, D. A., Riederer, I., De Meis, J., Lima-Quaresma, K. R., Vieira-de-Abreu, A., Villa-Verde, D. M., Savino, W. (2003) Trypanosoma cruzi infection modulates intrathymic contents of extracellular matrix ligands and receptors and alters thymocyte migration. Eur. J. Immunol. 33, 2439-2448.
9. Leite de Moraes, M. D., Minoprio, P., Dy, M., Dardenne, M., Savino, W., Hontebeyrie-Joskowicz, M. (1994) Endogenous IL-10 and IFN-γ production controls thymic cell proliferation in mice acutely infected by Trypanosoma cruzi. Scand. J. Immunol. 39, 51-58.
10. Leite de Moraes, M. C., Hontebeyrie-Joskowicz, M., Leboulenger, F., Savino, W., Dardenne, M., Lepault, F. (1991) Studies on the thymus in Chagas' disease. II. Thymocyte subset fluctuations in Trypanosoma cruziinfected mice: relationship to stress. Scand. J. Immunol. 33, 267-275.
11. De Meis, J., Mendes-da-Cruz, D. A., Farias-de-Oliveira, D. A., Correa-de- Santana, E., Pinto-Mariz, F., Cotta-de-Almeida, V., Bonomo, A., Savino, W. (2006) Atrophy of mesenteric lymph nodes in experimental Chagas' disease: differential role of Fas/Fas-L and TNFRI/TNF pathways. Microbes Infect. 8, 221-231.
12. Savino, W., Leite-de-Moraes, M. C., Hontebeyrie-Joskowicz, M., Dardenne, M. (1989) Studies on the thymus in Chagas' disease. I. Changes in the thymic microenvironment in mice acutely infected with Trypanosoma cruzi. Eur. J. Immunol. 19, 1727-1733.
13. Roggero, E., Perez, A. R., Bottasso, O. A., Besedovsky, H. O., Del Rey, A. (2009) Neuroendocrine-immunology of experimental Chagas' disease. Ann. N. Y. Acad. Sci. 1153, 264-271.
14. Perez, A. R., Roggero, E., Nicora, A., Palazzi, J., Besedovsky, H. O., Del Rey, A., Bottasso, O. A. (2007) Thymus atrophy during Trypanosoma cruzi infection is caused by an immuno-endocrine imbalance. Brain Behav. Immun. 21, 890-900.
15. Roggero, E., Perez, A. R., Tamae-Kakazu, M., Piazzon, I., Nepomnaschy, I., Besedovsky, H. O., Bottasso, O. A., del Rey, A. (2006) Endogenous glucocorticoids cause thymus atrophy but are protective during acute Trypanosoma cruzi infection. J. Endocrinol. 190, 495-503.
16. Mantuano-Barradas, M., Henriques-Pons, A., Araujo-Jorge, T. C., Di Virgilio, F., Coutinho-Silva, R., Persechini, P. M. (2003) Extracellular ATP induces cell death in CD4+/CD8+ double-positive thymocytes in mice infected with Trypanosoma cruzi. Microbes Infect. 5, 1363-1371.
17. Mucci, J., Mocetti, E., Leguizamon, M. S., Campetella, O. (2005) A sexual dimorphism in intrathymic sialylation survey is revealed by the transsialidase from Trypanosoma cruzi. J. Immunol. 174, 4545-4550.
18. Mucci, J., Hidalgo, A., Mocetti, E., Argibay, P. F., Leguizamon, M. S., Campetella, O. (2002) Thymocyte depletion in Trypanosoma cruzi infection is mediated by trans-sialidase-induced apoptosis on nurse cells complex. Proc. Natl. Acad. Sci. USA 99, 3896-3901.
19. Silva-Monteiro, E., Reis Lorenzato, L., Kenji Nihei, O., Junqueira, M., Rabinovich, G. A., Hsu, D. K., Liu, F. T., Savino, W., Chammas, R., Villa- Verde, D. M. (2007) Altered expression of galectin-3 induces cortical thymocyte depletion and premature exit of immature thymocytes during Trypanosoma cruzi infection. Am. J. Pathol. 170, 546-556.
20. Leguizamon, M. S., Mocetti, E., Garcia Rivello, H., Argibay, P., Campetella, O. (1999) Trans-sialidase from Trypanosoma cruzi induces apoptosis in cells from the immune system in vivo. J. Infect. Dis. 180, 1398-1402.
21. Pereira, W. O., Amarante-Mendes, G. P. (2011) Apoptosis: a programme of cell death or cell disposal? Scand. J. Immunol. 73, 401-407.
22. Strasser, A., Pellegrini, M. (2004) T-lymphocyte death during shutdown of an immune response. Trends Immunol. 25, 610-615.
23. Chipuk, J. E., Moldoveanu, T., Llambi, F., Parsons, M. J., Green, D. R. (2010) The BCL-2 family reunion. Mol. Cell 37, 299-310.
24. Siegel, R. M. (2006) Caspases at the crossroads of immune-cell life and death. Nat. Rev. Immunol. 6, 308-317.
25. Pinkoski, M. J., Waterhouse, N. J., Green, D. R. (2006) Mitochondria, apoptosis and autoimmunity. Curr. Dir. Autoimmun. 9, 55-73.
26. Lamkanfi, M., Festjens, N., Declercq, W., Vanden Berghe, T., Vandenabeele, P. (2007) Caspases in cell survival, proliferation and differentiation. Cell Death Differ. 14, 44-55.
27. Lopes, M. F., Guillermo, L. V., Silva, E. M. (2007) Decoding caspase signaling in host immunity to the protozoan Trypanosoma cruzi. Trends Immunol. 28, 366-372.
28. Bao, Q., Shi, Y. (2007) Apoptosome: a platform for the activation of initiator caspases. Cell Death Differ. 14, 56-65.
29. Ow, Y. P., Green, D. R., Hao, Z., Mak, T. W. (2008) Cytochrome c: functions beyond respiration. Nat. Rev. Mol. Cell Biol. 9, 532-542.
30. Kierszenbaum, F., Pienkowski, M. M. (1979) Thymus-dependent control of host defense mechanisms against Trypanosoma cruzi infection. Infect. Immun. 24, 117-120.
31. Da Costa, S. C., Calabrese, K. S., Bauer, P. G., Savino, W., Lagrange, P. H. (1991) Studies of the thymus in Chagas' disease: III. Colonization of the thymus and other lymphoid organs of adult and newborn mice by Trypanosoma cruzi. Pathol. Biol. (Paris) 39, 91-97.
32. Parsons, M. J., Green, D. R. (2010) Mitochondria in cell death. Essays Biochem. 47, 99-114.
33. Talaber, G., Boldizsar, F., Bartis, D., Palinkas, L., Szabo, M., Berta, G., Setalo Jr., G., Nemeth, P., Berki, T. (2009) Mitochondrial translocation of the glucocorticoid receptor in double-positive thymocytes correlates with their sensitivity to glucocorticoid-induced apoptosis. Int. Immunol. 21, 1269-1276.
34. Toth, K., Sarang, Z., Scholtz, B., Brazda, P., Ghyselinck, N., Chambon, P., Fesus, L., Szondy, Z. (2011) Retinoids enhance glucocorticoid-induced apoptosis of T cells by facilitating glucocorticoid receptor-mediated transcription. Cell Death Differ. 18, 783-792.
35. Cohen, O., Kfir-Erenfeld, S., Spokoini, R., Zilberman, Y., Yefenof, E., Sionov, R. V. (2009) Nitric oxide cooperates with glucocorticoids in thymic epithelial cell-mediated apoptosis of double positive thymocytes. Int. Immunol. 21, 1113-1123.
36. Stojic-Vukanic, Z., Rauski, A., Kosec, D., Radojevic, K., Pilipovic, I., Leposavic, G. (2009) Dysregulation of T-cell development in adrenal glucocorticoid- deprived rats. Exp. Biol. Med. (Maywood) 234, 1067-1074.
37. Wang, D., Muller, N., McPherson, K. G., Reichardt, H. M. (2006) Glucocorticoids engage different signal transduction pathways to induce apoptosis in thymocytes and mature T cells. J. Immunol. 176, 1695-1702.
38. Herold, M. J., McPherson, K. G., Reichardt, H. M. (2006) Glucocorticoids in T cell apoptosis and function. Cell. Mol. Life Sci. 63, 60-72.
39. Erlacher, M., Knoflach, M., Stec, I. E., Bock, G., Wick, G., Wiegers, G. J. (2005) TCR signaling inhibits glucocorticoid-induced apoptosis in murine thymocytes depending on the stage of development. Eur. J. Immunol. 35, 3287-3296.
40. Wyllie, A. H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555-556.
41. Mangelsdorf, D. J., Thummel, C., Beato, M., Herrlich, P., Schutz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., Evans, R. M. (1995) The nuclear receptor superfamily: the second decade. Cell 83, 835-839.
42. Cifone, M. G., Migliorati, G., Parroni, R., Marchetti, C., Millimaggi, D., Santoni, A., Riccardi, C. (1999) Dexamethasone-induced thymocyte apoptosis: apoptotic signal involves the sequential activation of phosphoinositide- specific phospholipase C, acidic sphingomyelinase, and caspases. Blood 93, 2282-2296.
43. Marchetti, M. C., Di Marco, B., Cifone, G., Migliorati, G., Riccardi, C. (2003) Dexamethasone-induced apoptosis of thymocytes: role of glucocorticoid receptor-associated Src kinase and caspase-8 activation. Blood 101, 585-593.
44. Salmena, L., Lemmers, B., Hakem, A., Matysiak-Zablocki, E., Murakami, K., Au, P. Y., Berry, D. M., Tamblyn, L., Shehabeldin, A., Migon, E., Wakeham, A., Bouchard, D., Yeh, W. C., McGlade, J. C., Ohashi, P. S., Hakem, R. (2003) Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 17, 883-895.
45. Perez, A. R., Silva-Barbosa, S. D., Roggero, E., Calmon-Hamaty, F., Villar, S. R., Gutierrez, F. R., Silva, J. S., Savino, W., Bottasso, O. (2011) Immunoendocrinology of the thymus in Chagas disease. Neuroimmunomodulation 18, 328-338.
46. Lepletier, A., de Frias Carvalho, V., Morrot, A., Savino, W. (2012) Thymic atrophy in acute experimental Chagas disease is associated with an imbalance of stress hormones. Ann. N. Y. Acad. Sci. 1262, 45-50.
47. Hildeman, D. A., Zhu, Y., Mitchell, T. C., Kappler, J., Marrack, P. (2002) Molecular mechanisms of activated T cell death in vivo. Curr. Opin. Immunol. 14, 354-359.