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Journal of Parasitology Research
Volume 2012, Article ID 737324, 13 pages
http://dx.doi.org/10.1155/2012/737324
Review Article

Nonimmune Cells Contribute to Crosstalk between Immune Cells and Inflammatory Mediators in the Innate Response to Trypanosoma cruzi Infection

1Departamento de Bioquímica Clínica, Centro de Investigaciones en Bioquímica Clínica e Inmunología (CIBICI), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Córdoba 5000, Argentina
2Department of Immunobiology, School of Medicine, Yale University, New Haven, CT 06520, USA
3Centro de Biología Molecular Severo Ochoa, Consejo Superior de Investigaciones Científicas (CSIC), Universidad Autónoma de Madrid (UAM), Cantoblanco, Madrid 28049, Spain

Received 6 May 2011; Accepted 19 June 2011

Academic Editor: Mauricio M. Rodrigues

Copyright © 2012 Maria Pilar Aoki et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. WHO, “Chagas disease (American trypanosomiasis),” Fact sheet, no 340, 2010.
  2. G. A. Schmunis and Z. E. Yadon, “Chagas disease: a Latin American health problem becoming a world health problem,” Acta Tropica, vol. 115, no. 1-2, pp. 14–21, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. N. U. Gironès and M. Fresno, “Etiology of Chagas disease myocarditis: autoimmunity, parasite persistence, or both?” Trends in Parasitology, vol. 19, no. 1, pp. 19–22, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. J. S. Leon and D. M. Engman, “The significance of autoimmunity in the pathogenesis of chagas heart disease,” Frontiers in Bioscience, vol. 8, pp. e316–e323, 2003. View at Google Scholar · View at Scopus
  5. J. A. Marin-Neto, E. Cunha-Neto, B. C. Maciel, and M. V. Simões, “Pathogenesis of chronic Chagas heart disease,” Circulation, vol. 115, no. 9, pp. 1109–1123, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Junqueira, B. Caetano, D. C. Bartholomeu et al., “The endless race between Trypanosoma cruzi and host immunity: lessons for and beyond Chagas disease,” Expert Reviews in Molecular Medicine, vol. 12, p. e29, 2010. View at Google Scholar
  7. K. M. Bonney and D. M. Engman, “Chagas heart disease pathogenesis: one mechanism or many?” Current Molecular Medicine, vol. 8, no. 6, pp. 510–518, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. W. Savino, D. M. S. Villa-Verde, D. A. Mendes-da-Cruz et al., “Cytokines and cell adhesion receptors in the regulation of immunity to Trypanosoma cruzi,” Cytokine and Growth Factor Reviews, vol. 18, no. 1-2, pp. 107–124, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. F. R. S. Gutierrez, P. M. M. Guedes, R. T. Gazzinelli, and J. S. Silva, “The role of parasite persistence in pathogenesis of Chagas heart disease,” Parasite Immunology, vol. 31, no. 11, pp. 673–685, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Uematsu and S. Akira, “Toll-like receptors and innate immunity,” Journal of Molecular Medicine, vol. 84, no. 9, pp. 712–725, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Trinchieri and A. Sher, “Cooperation of Toll-like receptor signals in innate immune defence,” Nature Reviews Immunology, vol. 7, no. 3, pp. 179–190, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Akira, S. Uematsu, and O. Takeuchi, “Pathogen recognition and innate immunity,” Cell, vol. 124, no. 4, pp. 783–801, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Akira, “TLR signaling,” Current Topics in Microbiology and Immunology, vol. 311, pp. 1–16, 2006. View at Google Scholar
  14. R. Ramasawmy, E. Cunha-Neto, K. C. Fae et al., “Heterozygosity for the S180L variant of MAL/TIRAP, a gene expressing an adaptor protein in the toll-like receptor pathway, is associated with lower risk of developing chronic chagas cardiomyopathy,” Journal of Infectious Diseases, vol. 199, no. 12, pp. 1838–1845, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. M. A. S. Campos, I. C. Almeida, O. Takeuchi et al., “Activation of toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite,” Journal of Immunology, vol. 167, no. 1, pp. 416–423, 2001. View at Google Scholar · View at Scopus
  16. E. Maganto-Garcia, C. Punzon, C. Terhorst, and M. Fresno, “Rab5 activation by toll-like receptor 2 is required for Trypanosoma cruzi internalization and replication in macrophages,” Traffic, vol. 9, no. 8, pp. 1299–1315, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Ouaissi, E. Guilvard, Y. Delneste et al., “The Trypanosoma cruzi Tc52-released protein induces human dendritic cell maturation, signals via Toll-like receptor 2, and confers protection against lethal infection,” Journal of Immunology, vol. 168, no. 12, pp. 6366–6374, 2002. View at Google Scholar · View at Scopus
  18. P. S. Coelho, A. Klein, A. Talvani et al., “Glycosylphosphatidylinositol-anchored mucin-like glycoproteins isolated from Trypanosoma cruzi trypomastigotes induce in vivo leukocyte recruitment dependent on MCP-1 production by IFN-gamma-primed-macrophages,” Journal of Leukocyte Biology, vol. 71, no. 5, pp. 837–844, 2002. View at Google Scholar · View at Scopus
  19. E. A. Carrera-Silv, N. Guiñazu, A. Pellegrini et al., “Importance of TLR2 on hepatic immune and non-immune cells to attenuate the strong inflammatory liver response during Trypanosoma cruzi acute infection,” PLoS Neglected Tropical Diseases, vol. 4, no. 11, article e863, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Bafica, H. C. Santiago, R. Goldszmid, C. Ropert, R. T. Gazzinelli, and A. Sher, “Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection,” Journal of Immunology, vol. 177, no. 6, pp. 3515–3519, 2006. View at Google Scholar · View at Scopus
  21. M. A. Campos, M. Closel, E. P. Valente et al., “Impaired production of proinflammatory cytokines and host resistance to acute infection with Trypanosoma cruzi in mice lacking functional myeloid differentiation factor 88,” Journal of Immunology, vol. 172, no. 3, pp. 1711–1718, 2004. View at Google Scholar · View at Scopus
  22. L. K. M. Shoda, K. A. Kegerreis, C. E. Suarez et al., “DNA from protozoan parasites Babesia bovis, Trypanosoma cruzi, and T. brucei is mitogenic for B lymphocytes and stimulates macrophage expression of interleukin-12, tumor necrosis factor alpha, and nitric oxide,” Infection and Immunity, vol. 69, no. 4, pp. 2162–2171, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. E. A. Carrera-Silva, R. C. Cano, N. Guiñazu, M. P. Aoki, A. Pellegrini, and S. Gea, “TLR2, TLR4 and TLR9 are differentially modulated in liver lethally injured from BALB/c and C57BL/6 mice during Trypanosoma cruzi acute infection,” Molecular Immunology, vol. 45, no. 13, pp. 3580–3588, 2008. View at Google Scholar
  24. A. M. Padilla, L. J. Simpson, and R. L. Tarleton, “Insufficient TLR activation contributes to the slow development of CD8 + T cell responses in Trypanosoma cruzi infection,” Journal of Immunology, vol. 183, no. 2, pp. 1245–1252, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. A. C. Oliveira, B. C. de Alencar, F. Tzelepis et al., “Impaired innate immunity in Tlr4(-/-) mice but preserved CD8+ T cell responses against Trypanosoma cruzi in Tlr4-, Tlr2-, Tlr9- or Myd88-deficient mice,” PLoS Pathogens, vol. 6, no. 4, Article ID e1000870, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. F. S. Mariano, F. R. S. Gutierrez, W. R. Pavanelli et al., “The involvement of CD4+CD25+ T cells in the acute phase of Trypanosoma cruzi infection,” Microbes and Infection, vol. 10, no. 7, pp. 825–833, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. F. F. Araujo, J. A. Gomes, M. O. Rocha et al., “Potential role of CD4+CD25HIGH regulatory T cells in morbidity in Chagas disease,” Frontiers in Bioscience, vol. 12, pp. 2797–2806, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. M. P. Bell, P. A. Svingen, M. K. Rahman, Y. Xiong, and W. A. Faubion Jr., “FOXP3 regulates TLR10 expression in human T regulatory cells,” Journal of Immunology, vol. 179, no. 3, pp. 1893–1900, 2007. View at Google Scholar · View at Scopus
  29. N. K. Crellin, R. V. Garcia, O. Hadisfar, S. E. Allan, T. S. Steiner, and M. K. Levings, “Human CD4+ T cells express TLR5 and its ligand flagellin enhances the suppressive capacity and expression of FOXP3 in CD4 +CD25+ T regulatory cells,” Journal of Immunology, vol. 175, no. 12, pp. 8051–8059, 2005. View at Google Scholar · View at Scopus
  30. P. Lewkowicz, N. Lewkowicz, A. Sasiak, and H. Tchorzewski, “Lipopolysaccharide-activated CD4+CD25+ T regulatory cells inhibit neutrophil function and promote their apoptosis and death,” Journal of Immunology, vol. 177, no. 10, pp. 7155–7163, 2006. View at Google Scholar · View at Scopus
  31. H. Liu, M. Komai-Koma, D. Xu, and F. Y. Liew, “Toll-like receptor 2 signaling modulates the functions of CD4 +CD25+ regulatory T cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 18, pp. 7048–7053, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. R. P. M. Sutmuller, M. H. M. G. M. Den Brok, M. Kramer et al., “Toll-like receptor 2 controls expansion and function of regulatory T cells,” Journal of Clinical Investigation, vol. 116, no. 2, pp. 485–494, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Ropert and R. T. Gazzinelli, “Regulatory role of toll-like receptor 2 during infection with Trypanosoma cruzi,” Journal of Endotoxin Research, vol. 10, no. 6, pp. 425–430, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. A. C. Oliveira, J. R. Peixoto, L. B. De Arrada et al., “Expression of functional TLR4 confers proinflammatory responsiveness to Trypanosoma cruzi glycoinositolphospholipids and higher resistance to infection with T. cruzi,” Journal of Immunology, vol. 173, no. 9, pp. 5688–5696, 2004. View at Google Scholar · View at Scopus
  35. D. C. Bartholomeu, C. Ropert, M. B. Melo et al., “Recruitment and endo-lysosomal activation of TLR9 in dendritic cells infected with Trypanosoma cruzi,” Journal of Immunology, vol. 181, no. 2, pp. 1333–1344, 2008. View at Google Scholar · View at Scopus
  36. M. H. Shaw, T. Reimer, Y. G. Kim, and G. Nuñez, “NOD-like receptors (NLRs): bona fide intracellular microbial sensors,” Current Opinion in Immunology, vol. 20, no. 4, pp. 377–382, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. S. E. Girardin, R. Tournebize, M. Mavris et al., “CARD4/Nod1 mediates NF-kappaB and JNK activation by invasive Shigella flexneri,” EMBO Reports, vol. 2, no. 8, pp. 736–742, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. N. Inohara, T. Koseki, L. Del Peso et al., “Nod1, an Apaf-1-like activator of caspase-9 and nuclear factor-κB,” Journal of Biological Chemistry, vol. 274, no. 21, pp. 14560–14567, 1999. View at Publisher · View at Google Scholar · View at Scopus
  39. G. K. Silva, F. R. S. Gutierrez, P. M. M. Guedes et al., “Cutting edge: nucleotide-binding oligomerization domain 1-dependent responses account for murine resistance against Trypanosoma cruzi infection,” Journal of Immunology, vol. 184, no. 3, pp. 1148–1152, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. A. D. Chessler, L. R. Ferreira, T. H. Chang, K. A. Fitzgerald, and B. A. Burleigh, “A novel IFN regulatory factor 3-dependent pathway activated by trypanosomes triggers IFN-beta in macrophages and fibroblasts,” Journal of Immunology, vol. 181, no. 11, pp. 7917–7924, 2008. View at Google Scholar · View at Scopus
  41. C. Une, J. Andersson, and A. Örn, “Role of IFN-α/β and IL-12 in the activation of natural killer cells and interferon-γ production during experimental infection with Trypanosoma cruzi,” Clinical and Experimental Immunology, vol. 134, no. 2, pp. 195–201, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Bogdan, J. Mattner, and U. Schleicher, “The role of type I interferons in non-viral infections,” Immunological Reviews, vol. 202, pp. 33–48, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Koga, S. Hamano, H. Kuwata et al., “TLR-dependent induction of IFN-β mediates host defense against Trypanosoma cruzi,” Journal of Immunology, vol. 177, no. 10, pp. 7059–7066, 2006. View at Google Scholar · View at Scopus
  44. H. Kayama, R. Koga, K. Atarashi et al., “NFATc1 mediates toll-like receptor-independent innate immune responses during Trypanosoma cruzi infection,” PLoS Pathogens, vol. 5, no. 7, Article ID e1000514, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. A. C. Monteiro, V. Schmitz, E. Svensjo et al., “Cooperative activation of TLR2 and bradykinin B2 receptor is required for induction of type 1 immunity in a mouse model of subcutaneous infection by Trypanosoma cruzi,” Journal of Immunology, vol. 177, no. 9, pp. 6325–6335, 2006. View at Google Scholar · View at Scopus
  46. V. Schmitz, E. Svensjö, R. R. Serra, M. M. Teixeira, and J. Scharfstein, “Proteolytic generation of kinins in tissues infected by Trypanosoma cruzi depends on CXC chemokine secretion by macrophages activated via Toll-like 2 receptors,” Journal of Leukocyte Biology, vol. 85, no. 6, pp. 1005–1014, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. A. C. Monteiro, V. Schmitz, A. Morrot et al., “Bradykinin B2 receptors of dendritic cells, acting as sensors of kinins proteolytically released by Trypanosoma cruzi, are critical for the development of protective type-1 responses,” PLoS Pathogens, vol. 3, no. 11, p. e185, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Aliberti, J. P. B. Viola, A. Vieira-de-Abreu, P. T. Bozza, A. Sher, and J. Scharfstein, “Cutting edge: bradykinin induces IL-12 production by dendritic cells: a danger signal that drives Th1 polarization,” Journal of Immunology, vol. 170, no. 11, pp. 5349–5353, 2003. View at Google Scholar · View at Scopus
  49. O. Takeuchi and S. Akira, “Pattern recognition receptors and inflammation,” Cell, vol. 140, no. 6, pp. 805–820, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Jiang, J. Liang, J. Fan et al., “Regulation of lung injury and repair by Toll-like receptors and hyaluronan,” Nature Medicine, vol. 11, no. 11, pp. 1173–1179, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Medzhitov, “Innate immunity: quo vadis?” Nature Immunology, vol. 11, no. 7, pp. 551–553, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Seki and D. A. Brenner, “Toll-like receptors and adaptor molecules in liver disease: update,” Hepatology, vol. 48, no. 1, pp. 322–335, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. B. Gao, W. I. Jeong, and Z. Tian, “Liver: an organ with predominant innate immunity,” Hepatology, vol. 47, no. 2, pp. 729–736, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. I. N. Crispe, “The liver as a lymphoid organ,” Annual Review of Immunology, vol. 27, pp. 147–163, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. R. F. Schwabe, E. Seki, and D. A. Brenner, “Toll-Like receptor signaling in the liver,” Gastroenterology, vol. 130, no. 6, pp. 1886–1900, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. M. S. Duthie, M. Kahn, M. White, R. P. Kapur, and S. J. Kahn, “Critical proinflammatory and anti-inflammatory functions of different subsets of CD1d-restricted natural killer T cells during Trypanosoma cruzi infection,” Infection and Immunity, vol. 73, no. 1, pp. 181–192, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. G. A. García, M. R. Arnaiz, S. A. Laucella et al., “Immunological and pathological responses in BALB/c mice induced by genetic administration of Tc13 Tul antigen of Trypanosoma cruzi,” Parasitology, vol. 132, no. 6, pp. 855–866, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Singh and M. J. Czaja, “Regulation of hepatocyte apoptosis by oxidative stress,” Journal of Gastroenterology and Hepatology, vol. 22, supplement 1, pp. S45–S48, 2007. View at Publisher · View at Google Scholar
  59. L. Conde de la Rosa, M. H. Schoemaker, T. E. Vrenken et al., “Superoxide anions and hydrogen peroxide induce hepatocyte death by different mechanisms: involvement of JNK and ERK MAP kinases,” Journal of Hepatology, vol. 44, no. 5, pp. 918–929, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Preiss, A. Thompson, X. Chen et al., “Characterization of the innate immune signalling pathways in hepatocyte cell lines,” Journal of Viral Hepatitis, vol. 15, no. 12, pp. 888–900, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Wu, Z. Meng, M. Jiang et al., “Hepatitis B virus suppresses toll-like receptor-mediated innate immune responses in murine parenchymal and nonparenchymal liver cells,” Hepatology, vol. 49, no. 4, pp. 1132–1140, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Postan, M. R. Arnaiz, and L. E. Fichera, “Myocardial cell response to Trypanosoma cruzl infection,” Medicina, vol. 59, supplement 2, pp. 57–62, 1999. View at Google Scholar · View at Scopus
  63. L. Zhang and R. L. Tarleton, “Characterization of cytokine production in m urine Trypanosoma cruzi infection by in situ immunocytochemistry: lack of association between susceptibility and type 2 cytokine production,” European Journal of Immunology, vol. 26, no. 1, pp. 102–109, 1996. View at Google Scholar · View at Scopus
  64. B. Chandrasekar, P. C. Melby, D. A. Troyer, J. T. Colston, and G. L. Freeman, “Temporal expression of pro-inflammatory cytokines and inducible nitric oxide synthase in experimental acute Chagasic cardiomyopathy,” American Journal of Pathology, vol. 152, no. 4, pp. 925–934, 1998. View at Google Scholar · View at Scopus
  65. F. S. Machado, G. A. Martins, J. C. S. Aliberti, F. L. A. C. Mestriner, F. Q. Cunha, and J. S. Silva, “Trypanosoma cruzi-infected cardiomyocytes produce chemokines and cytokines that trigger potent nitric oxide-dependent trypanocidal activity,” Circulation, vol. 102, no. 24, pp. 3003–3008, 2000. View at Google Scholar · View at Scopus
  66. E. Hovsepian, G. A. Mirkin, F. Penas, A. Manzano, R. Bartrons, and N. B. Goren, “Modulation of inflammatory response and parasitism by 15-Deoxy-Delta(12,14) prostaglandin J(2) in Trypanosoma cruzi-infected cardiomyocytes,” International Journal for Parasitology, vol. 41, no. 5, pp. 553–562, 2011. View at Publisher · View at Google Scholar
  67. P. A. Manque, C. Probst, M. C. Pereira et al., “Trypanosoma cruzi infection induces a global host cell response in cardiomyocytes,” Infection and Immunity, vol. 79, no. 5, pp. 1855–1862, 2011. View at Publisher · View at Google Scholar
  68. R. M. Smith, S. Lecour, and M. N. Sack, “Innate immunity and cardiac preconditioning: a putative intrinsic cardioprotective program,” Cardiovascular Research, vol. 55, no. 3, pp. 474–482, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. M. P. Aoki, N. L. Guiñazú, A. V. Pellegrini, T. Gotoh, D. T. Masih, and S. Gea, “Cruzipain, a major Trypanosoma cruzi antigen, promotes arginase-2 expression and survival of neonatal mouse cardiomyocytes,” American Journal of Physiology, vol. 286, no. 2, pp. C206–C212, 2004. View at Google Scholar · View at Scopus
  70. M. P. Aoki, R. C. Cano, A. V. Pellegrini et al., “Different signaling pathways are involved in cardiomyocyte survival induced by a Trypanosoma cruzi glycoprotein,” Microbes and Infection, vol. 8, no. 7, pp. 1723–1731, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. C. A. Petersen, K. A. Krumholz, and B. A. Burleigh, “Toll-like receptor 2 regulates interleukin-1β-dependent cardioinyocyte hypertrophy triggered by Trypanosoma cruzi,” Infection and Immunity, vol. 73, no. 10, pp. 6974–6980, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. T. P. Combs, Nagajyothi, S. Mukherjee et al., “The adipocyte as an important target cell for Trypanosoma cruzi infection,” Journal of Biological Chemistry, vol. 280, no. 25, pp. 24085–24094, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. F. Nagajyothi, M. S. Desruisseaux, N. Thiruvur et al., “Trypanosoma cruzi Infection of cultured adipocytes results in an inflammatory phenotype,” Obesity, vol. 16, no. 9, pp. 1992–1997, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. C. D. Mills, K. Kincaid, J. M. Alt, M. J. Heilman, and A. M. Hill, “M-1/M-2 macrophages and the Th1/Th2 paradigm,” Journal of Immunology, vol. 164, no. 12, pp. 6166–6173, 2000. View at Google Scholar · View at Scopus
  75. C. P. Jenkinson, W. W. Grody, and S. D. Cederbaum, “Comparative properties of arginases,” Comparative Biochemistry and Physiology B, vol. 114, no. 1, pp. 107–132, 1996. View at Publisher · View at Google Scholar · View at Scopus
  76. I. M. Corraliza, G. Soler, K. Eichmann, and M. Modolell, “Arginase induction by suppressors of nitric oxide synthesis (IL-4, IL-10 and PGE2) in murine bone-marrow-derived macrophages,” Biochemical and Biophysical Research Communications, vol. 206, no. 2, pp. 667–673, 1995. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Munder, K. Eichmann, and M. Modolell, “Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype,” Journal of Immunology, vol. 160, no. 11, pp. 5347–5354, 1998. View at Google Scholar · View at Scopus
  78. V. Boutard, B. Fouqueray, C. Philippe, J. Perez, and L. Baud, “Fish oil supplementation and essential fatty acid deficiency reduce nitric oxide synthesis by rat macrophages,” Kidney International, vol. 46, no. 5, pp. 1280–1286, 1994. View at Google Scholar · View at Scopus
  79. M. M. Jost, E. Ninci, B. Meder et al., “Divergent effects of GM-CSF and TGFβ1 on bone marrow-derived macrophage arginase-1 activity, MCP-1 expression, and matrix metalloproteinase-12: a potential role during arteriogenesis,” FASEB Journal, vol. 17, no. 15, pp. 2281–2283, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. O. Levillain, S. Balvay, and S. Peyrol, “Mitochondrial expression of arginase II in male and female rat inner medullary collecting ducts,” Journal of Histochemistry and Cytochemistry, vol. 53, no. 4, pp. 533–541, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. T. Gotoh, T. Sonoki, A. Nagasaki, K. Terada, M. Takiguchi, and M. Mori, “Molecular cloning of cDNA for nonhepatic mitochondrial arginase (arginase II) and comparison of its induction with nitric oxide synthase in a murine macrophage-like cell line,” FEBS Letters, vol. 395, no. 2-3, pp. 119–122, 1996. View at Publisher · View at Google Scholar · View at Scopus
  82. G. Wu and S. M. Morris Jr., “Arginine metabolism: nitric oxide and beyond,” Biochemical Journal, vol. 336, no. 1, pp. 1–17, 1998. View at Google Scholar · View at Scopus
  83. M. Tsujino, Y. Hirata, T. Imai et al., “Induction of nitric oxide synthase gene by interleukin-1β in cultured rat cardiocytes,” Circulation, vol. 90, no. 1, pp. 375–383, 1994. View at Google Scholar · View at Scopus
  84. M. Bergeron and M. Olivier, “Trypanosoma cruzi-mediated IFN-γ-inducible nitric oxide output in macrophages is regulated by iNOS mRNA stability,” Journal of Immunology, vol. 177, no. 9, pp. 6271–6280, 2006. View at Google Scholar · View at Scopus
  85. R. T. Gazzinelli, I. P. Oswald, S. Hieny, S. L. James, and A. Sher, “The microbicidal activity of interferon-γ-treated macrophages against Trypanosoma cruzi involves an L-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by interleukin-10 and transforming growth factor-β,” European Journal of Immunology, vol. 22, no. 10, pp. 2501–2506, 1992. View at Publisher · View at Google Scholar · View at Scopus
  86. G. Metz, Y. Carlier, and B. Vray, “Trypanosoma cruzi upregulates nitric oxide release by IFN-γ-preactivated macrophages, limiting cell infection independently of the respiratory burst,” Parasite Immunology, vol. 15, no. 12, pp. 693–699, 1993. View at Google Scholar · View at Scopus
  87. M. A. Munoz-Fernandez, M. A. Fernandez, and M. Fresno, “Synergism between tumor necrosis factor-α and interferon-γ on macrophage activation for the killing of intracellular Trypanosoma cruzi through a nitric oxide-dependent mechanism,” European Journal of Immunology, vol. 22, no. 2, pp. 301–307, 1992. View at Google Scholar · View at Scopus
  88. D. R. Pakianathan and R. E. Kuhn, “Trypanosoma cruzi affects nitric oxide production by murine peritoneal macrophages,” Journal of Parasitology, vol. 80, no. 3, pp. 432–437, 1994. View at Publisher · View at Google Scholar · View at Scopus
  89. N. Plasman, G. Metz, and B. Vray, “Interferon-γ-activated immature macrophages exhibit a high Trypanosoma cruzi infection rate associated with a low production of both nitric oxide and tumor necrosis factor-α,” Parasitology Research, vol. 80, no. 7, pp. 554–558, 1994. View at Google Scholar · View at Scopus
  90. C. G. Freire-De-Lima, D. O. Nascimento, M. B. P. Soares et al., “Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages,” Nature, vol. 403, no. 6766, pp. 199–203, 2000. View at Publisher · View at Google Scholar · View at Scopus
  91. K. L. Cummings and R. L. Tarleton, “Inducible nitric oxide synthase is not essential for control of Trypanosoma cruzi infection in mice,” Infection and Immunity, vol. 72, no. 7, pp. 4081–4089, 2004. View at Publisher · View at Google Scholar · View at Scopus
  92. N. Gironés, J. L. Bueno, J. Carrión, M. Fresno, and E. Castro, “The efficacy of photochemical treatment with methylene blue and light for the reduction of Trypanosoma cruzi in infected plasma,” Vox Sanguinis, vol. 91, no. 4, pp. 285–291, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. C. Hölscher, G. Köhler, U. Müller, H. Mossmann, G. A. Schaub, and F. Brombacher, “Defective nitric oxide effector functions lead to extreme susceptibility of Trypanosoma cruzi-infected mice deficient in gamma interferon receptor or inducible nitric oxide synthase,” Infection and Immunity, vol. 66, no. 3, pp. 1208–1215, 1998. View at Google Scholar
  94. A. D. Malvezi, R. Cecchini, F. De Souza, C. E. Tadokoro, L. V. Rizzo, and P. Pinge-Filho, “Involvement of nitric oxide (NO) and TNF-α in the oxidative stress associated with anemia in experimental Trypanosoma cruzi infection,” FEMS Immunology and Medical Microbiology, vol. 41, no. 1, pp. 69–77, 2004. View at Publisher · View at Google Scholar · View at Scopus
  95. O. Goño, P. Alcaide, and M. Fresno, “Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1+)CD11b+ immature myeloid suppressor cells,” International Immunology, vol. 14, no. 10, pp. 1125–1134, 2002. View at Google Scholar · View at Scopus
  96. H. Cuervo, M. A. Pineda, M. P. Aoki, S. Gea, M. Fresno, and N. Gironès, “Inducible nitric oxide synthase and arginase expression in heart tissue during acute Trypanosoma cruzi infection in mice: arginase I is expressed in infiltrating CD68+ macrophages,” Journal of Infectious Diseases, vol. 197, no. 12, pp. 1772–1782, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. L. Giordanengo, N. Guiñazú, C. Stempin, R. Fretes, F. Cerbán, and S. Gea, “Cruzipain, a major Trypanosoma cruzi antigen, conditions the host immune response in favor of parasite,” European Journal of Immunology, vol. 32, no. 4, pp. 1003–1011, 2002. View at Publisher · View at Google Scholar
  98. C. Stempin, L. Giordanengo, S. Gea, and F. Cerbán, “Alternative activation and increase of Trypanosoma cruzi survival in murine macrophages stimulated by cruzipain, a parasite antigen,” Journal of Leukocyte Biology, vol. 72, no. 4, pp. 727–734, 2002. View at Google Scholar · View at Scopus
  99. C. C. Stempin, T. B. Tanos, O. A. Coso, and F. M. Cerbán, “Arginase induction promotes Trypanosoma cruzi intracellular replication of Cruzipain-treated J774 cells through the activation of multiple signaling pathways,” European Journal of Immunology, vol. 34, no. 1, pp. 200–209, 2004. View at Publisher · View at Google Scholar · View at Scopus
  100. N. Guiñazú, A. Pellegrini, E. A. Carrera-Silva et al., “Immunisation with a major Trypanosoma cruzi antigen promotes pro-inflammatory cytokines, nitric oxide production and increases TLR2 expression,” International Journal for Parasitology, vol. 37, no. 11, pp. 1243–1254, 2007. View at Publisher · View at Google Scholar
  101. M. M. Rodrigues, M. Ribeirão, V. Pereira-Chioccola, L. Renia, and F. Costa, “Predominance of CD4 Th1 and CD8 Tc1 cells revealed by characterization of the cellular immune response generated by immunization with a DNA vaccine containing a Trypanosoma cruzi gene,” Infection and Immunity, vol. 67, no. 8, pp. 3855–3863, 1999. View at Google Scholar · View at Scopus
  102. A. E. Fujimura, S. S. Kinoshita, V. L. Pereira-Chioccola, and M. M. Rodrigues, “DNA sequences encoding CD4+ and CD8+ T-cell epitopes are important for efficient protective immunity induced by DNA vaccination with a Trypanosoma cruzi gene,” Infection and Immunity, vol. 69, no. 9, pp. 5477–5486, 2001. View at Publisher · View at Google Scholar · View at Scopus
  103. C. P. Knubel, F. F. Martínez, R. E. Fretes et al., “Indoleamine 2,3-dioxigenase (IDO) is critical for host resistance against Trypanosoma cruzi,” FASEB Journal, vol. 24, no. 8, pp. 2689–2701, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. S. Gupta, J. J. Wen, and N. J. Garg, “Oxidative stress in chagas disease,” Interdisciplinary Perspectives on Infectious Diseases, vol. 2009, Article ID 190354, 8 pages, 2009. View at Publisher · View at Google Scholar
  105. F. R. DeLeo and M. T. Quinn, “Assembly of the phagocyte NADPH oxidase: molecular interaction of oxidase proteins,” Journal of Leukocyte Biology, vol. 60, no. 6, pp. 677–691, 1996. View at Google Scholar · View at Scopus
  106. F. Villalta and F. Kierszenbaum, “Role of polymorphonuclear cells in Chagas' disease. I. Uptake and mechanisms of destruction of intracellular (amastigote) forms of Trypanosoma cruzi by human neutrophils,” Journal of Immunology, vol. 131, no. 3, pp. 1504–1510, 1983. View at Google Scholar · View at Scopus
  107. R. L. Cardoni, M. I. Antunez, C. Morales, and I. Rodriguez Nantes, “Release of reactive oxygen species by phagocytic cells in response to live parasites in mice infected with Trypanosoma cruzi,” American Journal of Tropical Medicine and Hygiene, vol. 56, no. 3, pp. 329–334, 1997. View at Google Scholar · View at Scopus
  108. A. M. Celentano and S. M. Gonzalez Cappa, “Induction of macrophage activation and opsonizing antibodies by Trypanosoma cruzi subpopulations,” Parasite Immunology, vol. 14, no. 2, pp. 155–167, 1992. View at Google Scholar · View at Scopus
  109. R. C. N. Melo, D. L. Fabrino, H. D'Ávila, H. C. Teixeira, and A. P. Ferreira, “Production of hydrogen peroxide by peripheral blood monocytes and specific macrophages during experimental infection with Trypanosoma cruzi in vivo,” Cell Biology International, vol. 27, no. 10, pp. 853–861, 2003. View at Publisher · View at Google Scholar · View at Scopus
  110. X. Ba, S. Gupta, M. Davidson, and N. J. Garg, “Trypanosoma cruzi induces the reactive oxygen species-PARP-1-RelA pathway for up-regulation of cytokine expression in cardiomyocytes,” Journal of Biological Chemistry, vol. 285, no. 15, pp. 11596–11606, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. N. Guiñazú, E. A. Carrera-Silva, M. C. Becerra, A. Pellegrini, I. Albesa, and S. Gea, “Induction of NADPH oxidase activity and reactive oxygen species production by a single Trypanosoma cruzi antigen,” International Journal for Parasitology, vol. 40, no. 13, pp. 1531–1538, 2010. View at Publisher · View at Google Scholar
  112. M. N. Alvarez, G. Peluffo, L. Piacenza, and R. Radi, “Intraphagosomal peroxynitrite as a macrophage-derived cytotoxin against internalized Trypanosoma cruzi: consequences for oxidative killing and role of microbial peroxiredoxins in infectivity,” Journal of Biological Chemistry, vol. 286, no. 8, pp. 6627–6640, 2011. View at Publisher · View at Google Scholar
  113. S. Kusmartsev, Y. Nefedova, D. Yoder, and D. I. Gabrilovich, “Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer Is mediated by reactive oxygen species,” Journal of Immunology, vol. 172, no. 2, pp. 989–999, 2004. View at Google Scholar · View at Scopus
  114. Y. Xia and J. L. Zweier, “Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 13, pp. 6954–6958, 1997. View at Publisher · View at Google Scholar · View at Scopus