The importance of apoptosis for immune regulation in Chagas disease

Memorias do Instituto Oswaldo Cruz

Volumn 104, Issue SUPPL. 1, 2009, Pages 259-262

  DosReis, George A ^a   Lopes, Marcela F ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Apoptosis; Lymphocytes; Phagocytosis cytokines; Trypanosoma cruzi

Indexed keywords

MUS; TRYPANOSOMA CRUZI;

EID: 68949209377     PISSN: 00740276     EISSN: 16788060     Source Type: Journal    
DOI: 10.1590/S0074-02762009000900033     Document Type: Article

References (49)

1. Ameisen JC, Idziorek T, Billaut-Mulot O, Loyens M, Tissier JP, Potentier A, Ouaissi A 1995. Apoptosis in a unicellular eukaryote (Trypanosoma cruzi): implications for the evolutionary origin and role of programmed cell death in the control of cell proliferation, differentiation and survival. Cell Death Differ 2: 285-300.
2. Ariyanayagam MR, Oza SL, Mehlert A, Fairlamb AH 2003. Bis (glutathionyl) spermine and other novel trypanothione analogues in Trypanosoma cruzi. J Biol Chem 278: 27612-27619.
3. Bartholomeu DC, Ropert C, Melo MB, Parroche P, Junqueira CF, Teixeira SM, Sirois C, Kasperkovitz P, Knetter CF, Lien E, Latz E, Golenbock DT, Gazzinelli RT 2008. Recruitment and endolysosomal activation of TLR9 in dendritic cells infected with Trypanosoma cruzi. J Immunol 181: 1333-1344.
4. Celentano AM, Gorelik G, Solana ME, Sterin-Borda L, Borda E, González Cappa SM 1995. PGE2 involvement in experimental infection with Trypanosoma cruzi subpopulations. Prostaglandins 49: 141-153.
5. Damatta RA, Seabra SH, Deolindo P, Arnholdt AC, Manhães L, Goldenberg S, de Souza W 2007. Trypanosoma cruzi exposes phosphatidylserine as an evasion mechanism. FEMS Microbiol Lett 266: 29-33.
6. de Freitas Balanco JM, Moreira ME, Bonomo A, Bozza PT, Amarante-Mendes G, Pirmez C, Barcinski MA 2001. Apoptotic mimicry by an obligate intracellular parasite downregulates macrophage microbicidal activity. Curr Biol 11: 1870-1873.
7. de Meis J, Ferreira LM, Guillermo LV, Silva EM, DosReis GA, Lopes MF 2008. Apoptosis differentially regulates mesenteric and subcutaneous lymph node immune responses to Trypanosoma cruzi. Eur J Immunol 38: 139-146.
8. de Meis J, Mendes-da-Cruz DA, Farias-de-Oliveira DA, Corrêa-deSantana 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.
9. de Oliveira GM, Diniz RL, Batista W, Batista MM, Bani Correa C, de Araújo-Jorge TC, Henriques-Pons A 2007. Fas ligand-dependent inflammatory regulation in acute myocarditis induced by Trypanosoma cruzi infection. Am J Pathol 171: 79-86.
10. de Souza EM, Araújo-Jorge TC, Bailly C, Lansiaux A, Batista MM, Oliveira GM, Soeiro MN 2003. Host and parasite apoptosis following Trypanosoma cruzi infection in in vitro and in vivo models. Cell Tissue Res 314: 223-235.
11. DosReis GA, Freire-de-Lima CG, Nunes MP, Lopes MF 2005. The importance of aberrant T-cell responses in Chagas disease. Trends Parasitol 21: 237-243.
12. DosReis GA, Ribeiro-Gomes FL, Guillermo LV, Lopes MF 2007. Cross-talk between apoptosis and cytokines in the regulation of parasitic infection. Cytokine Growth Factor Rev 18: 97-105.
13. Eriksson U, Ricci R, Hunziker L, Kurrer MO, Oudit GY, Watts TH, Sonderegger I, Bachmaier K, Kopf M, Penninger JM 2003. Dendritic cell-induced autoimmune heart failure requires cooperation between adaptive and innate immunity. Nat Med 9: 1484-1490.
14. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM 1998. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/ paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101: 890-898.
15. Freire-de-Lima CG, Nascimento DO, Soares MB, Bozza PT, CastroFaria-Neto HC, de Mello FG, DosReis GA, Lopes MF 2000. Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 403: 199-203.
16. Guillermo LV, Pereira WF, De Meis J, Ribeiro-Gomes FL, Silva EM, Kroll-Palhares K, Takiya CM, Lopes MF 2009. Targeting caspases in intracellular protozoan infections. Immunopharmacol Immunotoxicol 31: 159-173.
17. Guillermo LV, Silva EM, Ribeiro-Gomes FL, De Meis J, Pereira WF, Yagita H, DosReis GA, Lopes MF 2007. The Fas death pathway controls coordinated expansions of type 1 CD8 and type 2 CD4 T cells in Trypanosoma cruzi infection. J Leukoc Biol 81: 942-951.
18. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature 417: 182-187.
19. Harel-Bellan A, Joskowicz M, Fradelizi D, Eisen H 1983. Modification of T-cell proliferation and interleukin-2 production in mice infected with Trypanosoma cruzi. Proc Natl Acad Sci USA 80: 3466-3469.
20. Hideko Tatakihara VL, Cecchini R, Borges CL, Malvezi AD, Graçade Souza VK, Yamada-Ogatta SF, Rizzo LV, Pinge-Filho P 2008. Effects of cyclooxygenase inhibitors on parasite burden, anemia and oxidative stress in murine Trypanosoma cruzi infection. FEMS Immunol Med Microbiol 52: 47-58.
21. Krammer PH, Arnold R, Lavrik IN 2007. Life and death in peripheral T cells. Nat Rev Immunol 7: 532-542.
22. Leguizamón MS, 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.
23. Lopes MF, Cunha JM, Bezerra FL, Gonzalez MS, Gomes JE, Lapa e Silva JR, Garcia ES, DosReis GA 1995a. Trypanosoma cruzi: both chemically induced and triatomine-derived metacyclic trypomastigotes cause the same immunological disturbances in the infected mammalian host. Exp Parasitol 80: 194-204.
24. Lopes MF, da Veiga VF, Santos AR, Fonseca ME, DosReis GA 1995b. Activation-induced CD4+ T cell death by apoptosis in experimental Chagas' disease. J Immunol 154: 744-752.
25. Lopes MF, DosReis GA 1996. Trypanosoma cruzi-induced immunosuppression: selective triggering of CD4+ T-cell death by the T-cell receptor-CD3 pathway and not by the CD69 or Ly-6 activation pathway. Infect Immun 64: 1559-1564.
26. Lopes MF, Nunes MP, Henriques-Pons A, Giese N, Morse HC 3rd, Davidson WF, Araújo-Jorge TC, DosReis GA 1999. Increased susceptibility of Fas ligand-deficient gld mice to Trypanosoma cruzi infection due to a Th2-biased host immune response. Eur J Immunol 29: 81-89.
27. Lucas M, Stuart LM, Savill J, Lacy-Hulbert A 2003. Apoptotic cells and innate immune stimuli combine to regulate macrophage cytokine secretion. J Immunol 171: 2610-2615.
28. Marañón C, Planelles L, Alonso C, López MC 2000. HSP70 from Trypanosoma cruzi is endowed with specific cell proliferation potential leading to apoptosis. Int Immunol 12: 1685-1693.
29. Martins GA, Cardoso MA, Aliberti JC, Silva JS 1998. Nitric oxideinduced apoptotic cell death in the acute phase of Trypanosoma cruzi infection in mice. Immunol Lett 63: 113-120.
30. Michelin MA, Silva JS, Cunha FQ 2005. Inducible cyclooxygenase released prostaglandin mediates immunosuppression in acute phase of experimental Trypanosoma cruzi infection. Exp Parasitol 111: 71-79.
31. Minoprio P, Itohara S, Heusser C, Tonegawa S, Coutinho A 1989. Immunobiology of murine T. cruzi infection: the predominance of parasite-nonspecific responses and the activation of TCRI T cells. Immunol Rev 112: 183-207.
32. Nunes MP, Andrade RM, Lopes MF, DosReis GA 1998. Activation induced T-cell death exacerbates Trypanosoma cruzi replication in macrophages cocultured with CD4+ T lymphocytes from infected hosts. J Immunol 160: 1313-1319.
33. Pereira NA, Song Z 2008. Some commonly used caspase substrates and inhibitors lack the specificity required to monitor individual caspase activity. Biochem Biophys Res Commun 377: 873-877.
34. Petersen CA, Krumholz KA, Carmen J, Sinai AP, Burleigh BA 2006. Trypanosoma cruzi infection and nuclear factor kappa B activation prevent apoptosis in cardiac cells. Infect Immun 74: 1580-1587.
35. Piacenza L, Peluffo G, Radi R 2001. L-arginine-dependent suppression of apoptosis in Trypanosoma cruzi: contribution of the nitric oxide and polyamine pathways. Proc Natl Acad Sci USA 98: 7301-7306.
36. Ravichandran KS, Lorenz U 2007. Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol 7: 964-974.
37. Rodrigues V Jr, Agrelli GS, Leon SC, Silva Teixeira DN, Tostes S Jr, Rocha-Rodrigues DB 2008. Fas/Fas-L expression, apoptosis and low proliferative response are associated with heart failure in patients with chronic Chagas' disease. Microbes Infect 10: 29-37.
38. Rudin CM, Thompson CB 1997. Apoptosis and disease: regulation and clinical relevance of programmed cell death. Annu Rev Med 48: 267-281.
39. Savill J, Hogg N, Ren Y, Haslett C 1992. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest 90: 1513-1522.
40. Silva EM, Guillermo LV, Ribeiro-Gomes FL, De Meis J, Nunes MP, Senra JF, Soares MB, DosReis GA, Lopes MF 2007. Caspase inhibition reduces lymphocyte apoptosis and improves host immune responses to Trypanosoma cruzi infection. Eur J Immunol 37: 738-746.
41. Silva EM, Guillermo LV, Ribeiro-Gomes FL, De Meis J, Pereira RM, Wu Z, Calegari-Silva TC, Seabra SH, Lopes UG, Siegel RM, Dosreis GA, Lopes MF 2005. Caspase-8 activity prevents type 2 cytokine responses and is required for protective T cell-mediated immunity against Trypanosoma cruzi infection. J Immunol 174: 6314-6321.
42. Tostes S Jr, Bertulucci Rocha-Rodrigues D, de Araujo Pereira G, Rodrigues V Jr 2005. Myocardiocyte apoptosis in heart failure in chronic Chagas' disease. Int J Cardiol 99: 233-237.
43. Tóth B, Garabuczi E, Sarang Z, Vereb G, Vámosi G, Aeschlimann D, Blaskó B, Bécsi B, Erdõdi F, Lacy-Hulbert A, Zhang A, Falasca L, Birge RB, Balajthy Z, Melino G, Fésüs L, Szondy Z 2009. Transglutaminase 2 is needed for the formation of an efficient phagocyte portal in macrophages engulfing apoptotic cells. J Immunol 182: 2084-2092.
44. van Zandbergen G, Bollinger A, Wenzel A, Kamhawi S, Voll R, Klinger M, Müller A, Hölscher C, Herrmann M, Sacks D, Solbach W, Laskay T 2006. Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci USA 103: 13837-13842.
45. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I 1997. Immunosuppressive effects of apoptotic cells. Nature 390: 350-351.
46. Welsh RM, McNally JM 1999. Immune deficiency, immune silencing and clonal exhaustion of T cell responses during viral infections. Curr Opin Microbiol 2: 382-387.
47. Wu Z, Roberts M, Porter M, Walker F, Wherry EJ, Kelly J, Gadina M, Silva EM, DosReis GA, Lopes MF, O'Shea J, Leonard WJ, Ahmed R, Siegel RM 2004. Viral FLIP impairs survival of activated T cells and generation of CD8+T cell memory. J Immunol 172: 6313-6323.
48. Zhang J, Andrade ZA, Yu ZX, Andrade SG, Takeda K, Sadirgursky M, Ferrans VJ 1999. Apoptosis in a canine model of acute Chagasic myocarditis. J Mol Cell Cardiol 31: 581-596.
49. Zuñiga E, Motran CC, Montes CL, Yagita H, Gruppi A 2002. Trypanosoma cruzi infection selectively renders parasite-specific IgG+B lymphocytes susceptible to Fas/Fas ligand-mediated fratricide. J Immunol 168: 3965-3973.