1,331
Views
76
CrossRef citations to date
0
Altmetric
Original Research Articles

Vesicles from different Trypanosoma cruzi strains trigger differential innate and chronic immune responses

, , , , , , , , , , & show all
Article: 28734 | Received 06 Jan 2015, Accepted 11 Jan 2015, Published online: 26 Nov 2015

References

  • Coura JR, Vinas PA. Chagas disease: a new worldwide challenge. Nature. 2010; 465: S6–7.
  • Tyler KM, Engman DM. The life cycle of Trypanosoma cruzi revisited. Int J Parasitol. 2001; 31: 472–81.
  • Burleigh BA, Woolsey AM. Cell signalling and Trypanosoma cruzi invasion. Cell Microbiol. 2002; 4: 701–11.
  • Burleigh BA. Host cell signaling and Trypanosoma cruzi invasion: do all roads lead to lysosomes?. Sci STKE. 2005; 2005: pe36.
  • Caradonna KL, Burleigh BA. Mechanisms of host cell invasion by Trypanosoma cruzi. Adv Parasitol. 2011; 76: 33–61.
  • Mott A, Lenormand G, Costales J, Fredberg JJ, Burleigh BA. Modulation of host cell mechanics by Trypanosoma cruzi. J Cell Physiol. 2009; 218: 315–22.
  • Ouaissi A, Ouaissi M. Molecular basis of Trypanosoma cruzi and Leishmania interaction with their host(s): exploitation of immune and defense mechanisms by the parasite leading to persistence and chronicity, features reminiscent of immune system evasion strategies in cancer diseases. Arch Immunol Ther Exp (Warsz). 2005; 53: 102–14.
  • Campos MA, Almeida IC, Takeuchi O, Akira S, Valente EP, Procopio DO et al. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J Immunol. 2001; 167: 416–23.
  • Dutra WO, Menezes CA, Magalhaes LM, Gollob KJ. Immunoregulatory networks in human Chagas disease. Parasite Immunol. 2014; 36: 377–87.
  • Basso B, Marini V. Experimental Chagas disease. Innate immune response in Balb/c mice previously vaccinated with Trypanosoma rangeli. I. The macrophage shows immunological memory: reality or fiction?. Immunobiology. 2014; 219: 275–84.
  • Basso B. Modulation of immune response in experimental Chagas disease. World J Exp Med. 2013; 3: 1–10.
  • Dc-Rubin SS, Schenkman S. Trypanosoma cruzi trans-sialidase as a multifunctional enzyme in Chagas’ disease. Cell Microbiol. 2012; 14: 1522–30.
  • Mattos EC, Tonelli RR, Colli W, Alves MJ. The Gp85 surface glycoproteins from Trypanosoma cruzi. Subcell Biochem. 2014; 74: 151–80.
  • Alves MJ, Colli W. Trypanosoma cruzi: adhesion to the host cell and intracellular survival. IUBMB Life. 2007; 59: 274–9.
  • Magdesian MH, Tonelli RR, Fessel MR, Silveira MS, Schumacher RI, Linden R et al. A conserved domain of the gp85/trans-sialidase family activates host cell extracellular signal-regulated kinase and facilitates Trypanosoma cruzi infection. Exp Cell Res. 2007; 313: 210–18.
  • Soares RP, Torrecilhas AC, Assis RR, Rocha MN, Moura e Castro FA, Freitas GF et al. Intraspecies variation in Trypanosoma cruzi GPI-mucins: biological activities and differential expression of alpha-galactosyl residues. Am J Trop Med Hyg. 2012; 87: 87–96.
  • Acosta-Serrano A, Almeida IC, Freitas-Junior LH, Yoshida N, Schenkman S. The mucin-like glycoprotein super-family of Trypanosoma cruzi: structure and biological roles. Mol Biochem Parasitol. 2001; 114: 143–50.
  • Goncalves MF, Umezawa ES, Katzin AM, de Souza W, Alves MJ, Zingales B et al. Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Exp Parasitol. 1991; 72: 43–53.
  • Trocoli Torrecilhas AC, Tonelli RR, Pavanelli WR, da Silva JS, Schumacher RI, de Souza W et al. Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes Infect. 2009; 11: 29–39.
  • Torrecilhas AC, Schumacher RI, Alves MJ, Colli W. Vesicles as carriers of virulence factors in parasitic protozoan diseases. Microbes Infect. 2012; 14: 1465–74.
  • Hong SW, Choi EB, Min TK, Kim JH, Kim MH, Jeon SG et al. An important role of alpha-hemolysin in extracellular vesicles on the development of atopic dermatitis induced by Staphylococcus aureus. PLoS One. 2014; 9: e100499.
  • Marcilla A, Martin-Jaular L, Trelis M, de Menezes-Neto A, Osuna A, Bernal D et al. Extracellular vesicles in parasitic diseases. J Extracell Vesicles. 2014; 3: 25040.
  • Campos JH, Soares RP, Ribeiro K, Cronemberger Andrade A, Batista WL, Torrecilhas AC. Extracellular vesicles: role in inflammatory responses and potential uses in vaccination in cancer and infectious diseases. J Immunol Res. 2015; 2015: 832057.
  • Geiger A, Hirtz C, Becue T, Bellard E, Centeno D, Gargani D et al. Exocytosis and protein secretion in Trypanosoma. BMC Microbiol. 2010; 10: 20.
  • Silverman JM, Clos J, de'Oliveira CC, Shirvani O, Fang Y, Wang C et al. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci. 2010; 123: 842–52.
  • Silverman JM, Reiner NE. Leishmania exosomes deliver preemptive strikes to create an environment permissive for early infection. Front Cell Infect Microbiol. 2011; 1: 26.
  • Silverman JM, Clos J, Horakova E, Wang AY, Wiesgigl M, Kelly I et al. Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells. J Immunol. 2010; 185: 5011–22.
  • Zingales B, Andrade SG, Briones MR, Campbell DA, Chiari E, Fernandes O et al. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz. 2009; 104: 1051–4.
  • Andrews NW, Colli W. Adhesion and interiorization of Trypanosoma cruzi in mammalian cells. J Protozool. 1982; 29: 264–9.
  • Uphoff CC, Drexler HG. Detection of mycoplasma contaminations. Methods Mol Biol. 2005; 290: 13–23.
  • Soares RP, Cardoso TL, Barron T, Araujo MS, Pimenta PF, Turco SJ. Leishmania braziliensis: a novel mechanism in the lipophosphoglycan regulation during metacyclogenesis. Int J Parasitol. 2005; 35: 245–53.
  • Paranaiba L, de Assis R, Nogueira P, Torrecilhas A, Campos J, Silveira A et al. Leishmania enriettii: biochemical characterisation of lipophosphoglycans (LPGs) and glycoinositolphospholipids (GIPLs) and infectivity to Cavia porcellus. Parasit Vectors. 2015; 8: 31.
  • Assis RR, Ibraim IC, Noronha FS, Turco SJ, Soares RP. Glycoinositolphospholipids from Leishmania braziliensis and L. infantum: modulation of innate immune system and variations in carbohydrate structure. PLoS Negl Trop Dis. 2012; 6: e1543.
  • Torrecilhas AC, Faquim-Mauro E, Da Silva AV, Abrahamsohn IA. Interference of natural mouse hepatitis virus infection with cytokine production and susceptibility to Trypanosoma cruzi. Immunology. 1999; 96: 381–8.
  • Sathler-Avelar R, Vitelli-Avelar DM, Massara RL, Borges JD, Lana M, Teixeira-Carvalho A et al. Benznidazole treatment during early-indeterminate Chagas’ disease shifted the cytokine expression by innate and adaptive immunity cells toward a type 1-modulated immune profile. Scand J Immunol. 2006; 64: 554–63.
  • Dutra WO, Colley DG, Pinto-Dias JC, Gazzinelli G, Brener Z, Pereira ME et al. Self and nonself stimulatory molecules induce preferential expansion of CD5+ B cells or activated T cells of chagasic patients, respectively. Scand J Immunol. 2000; 51: 91–7.
  • Almeida IC, Camargo MM, Procopio DO, Silva LS, Mehlert A, Travassos LR et al. Highly purified glycosylphosphatidylinositols from Trypanosoma cruzi are potent proinflammatory agents. EMBO J. 2000; 19: 1476–85.
  • Galili U. The alpha-gal epitope and the anti-Gal antibody in xenotransplantation and in cancer immunotherapy. Immunol Cell Biol. 2005; 83: 674–86.
  • Almeida IC, Milani SR, Gorin PA, Travassos LR. Complement-mediated lysis of Trypanosoma cruzi trypomastigotes by human anti-alpha-galactosyl antibodies. J Immunol. 1991; 146: 2394–400.
  • Gazzinelli RT, Pereira ME, Romanha A, Gazzinelli G, Brener Z. Direct lysis of Trypanosoma cruzi: a novel effector mechanism of protection mediated by human anti-gal antibodies. Parasite Immunol. 1991; 13: 345–56.
  • Almeida IC, Ferguson MA, Schenkman S, Travassos LR. Lytic anti-alpha-galactosyl antibodies from patients with chronic Chagas’ disease recognize novel O-linked oligosaccharides on mucin-like glycosyl-phosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi. Biochem J. 304: 793–802.
  • Talvani A, Ribeiro CS, Aliberti JC, Michailowsky V, Santos PV, Murta SM et al. Kinetics of cytokine gene expression in experimental chagasic cardiomyopathy: tissue parasitism and endogenous IFN-gamma as important determinants of chemokine mRNA expression during infection with Trypanosoma cruzi. Microbes Infect. 2000; 2: 851–66.
  • Di Girolamo F, Raggi C, Birago C, Pizzi E, Lalle M, Picci L et al. Plasmodium lipid rafts contain proteins implicated in vesicular trafficking and signalling as well as members of the PIR superfamily, potentially implicated in host immune system interactions. Proteomics. 2008; 8: 2500–13.
  • Hassani K, Olivier M. Immunomodulatory impact of Leishmania-induced macrophage exosomes: a comparative proteomic and functional analysis. PLoS Negl Trop Dis. 2013; 7: e2185.
  • Marcilla A, Trelis M, Cortes A, Sotillo J, Cantalapiedra F, Minguez MT et al. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One. 2012; 7: e45974.
  • Ferguson MA. The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J Cell Sci. 1999; 112: 2799–809.
  • Gazzinelli RT, Denkers EY. Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nat Rev Immunol. 2006; 6: 895–906.
  • Oliveira AC, Peixoto JR, de Arruda LB, Campos MA, Gazzinelli RT, Golenbock DT et al. Expression of functional TLR4 confers proinflammatory responsiveness to Trypanosoma cruzi glycoinositolphospholipids and higher resistance to infection with T. cruzi. J Immunol. 2004; 173: 5688–96.
  • Giordanengo L, Guinazu N, Stempin C, Fretes R, Cerban F, Gea S. Cruzipain, a major Trypanosoma cruzi antigen, conditions the host immune response in favor of parasite. Eur J Immunol. 2002; 32: 1003–11.
  • Pineda MA, Corvo L, Soto M, Fresno M, Bonay P. Interactions of human galectins with Trypanosoma cruzi: binding profile correlate with genetic clustering of lineages. Glycobiology. 2015; 25: 197–210.
  • Arthur JS, Ley SC. Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol. 2013; 13: 679–92.
  • Ropert C, Almeida IC, Closel M, Travassos LR, Ferguson MA, Cohen P et al. Requirement of mitogen-activated protein kinases and I kappa B phosphorylation for induction of proinflammatory cytokines synthesis by macrophages indicates functional similarity of receptors triggered by glycosylphosphatidylinositol anchors from parasitic protozoa and bacterial lipopolysaccharide. J Immunol. 2001; 166: 3423–31.
  • Ropert C, Gazzinelli RT. Regulatory role of toll-like receptor 2 during infection with Trypanosoma cruzi. J Endotoxin Res. 2004; 10: 425–30.
  • Ibraim IC, de Assis RR, Pessoa NL, Campos MA, Melo MN, Turco SJ et al. Two biochemically distinct lipophosphoglycans from Leishmania braziliensis and Leishmania infantum trigger different innate immune responses in murine macrophages. Parasit Vectors. 2013; 6: 54.
  • Rassi A Jr., Rassi A, Marin-Neto JA. Chagas disease. Lancet. 2010; 375: 1388–402.
  • Gazzinelli RT, Ropert C, Campos MA. Role of the toll/interleukin-1 receptor signaling pathway in host resistance and pathogenesis during infection with protozoan parasites. Immunol Rev. 2004; 201: 9–25.
  • Lima MT, Lenzi HL, Gattass CR. Negative tissue parasitism in mice injected with a noninfective clone of Trypanosoma cruzi. Parasitol Res. 1995; 81: 6–12.
  • Souza PE, Rocha MO, Rocha-Vieira E, Menezes CA, Chaves AC, Gollob KJ et al. Monocytes from patients with indeterminate and cardiac forms of Chagas’ disease display distinct phenotypic and functional characteristics associated with morbidity. Infect Immun. 2004; 72: 5283–91.
  • Vitelli-Avelar DM, Sathler-Avelar R, Teixeira-Carvalho A, Pinto Dias JC, Gontijo ED, Faria AM et al. Strategy to assess the overall cytokine profile of circulating leukocytes and its association with distinct clinical forms of human Chagas disease. Scand J Immunol. 2008; 68: 516–25.
  • Sathler-Avelar R, Vitelli-Avelar DM, Teixeira-Carvalho A, Martins-Filho OA. Innate immunity and regulatory T-cells in human Chagas disease: what must be understood?. Mem Inst Oswaldo Cruz. 2009; 104(Suppl 1): 246–51.
  • Sathler-Avelar R, Vitelli-Avelar DM, Eloi-Santos SM, Gontijo ED, Teixeira-Carvalho A, Martins-Filho OA. Blood leukocytes from benznidazole-treated indeterminate chagas disease patients display an overall type-1-modulated cytokine profile upon short-term in vitro stimulation with Trypanosoma cruzi antigens. BMC Infect Dis. 2012; 12: 123.
  • Costa GC, da Costa Rocha MO, Moreira PR, Menezes CA, Silva MR, Gollob KJ et al. Functional IL-10 gene polymorphism is associated with Chagas disease cardiomyopathy. J Infect Dis. 2009; 199: 451–4.
  • Dutra WO, Martins-Filho OA, Cancado JR, Pinto-Dias JC, Brener Z, Freeman Junior GL et al. Activated T and B lymphocytes in peripheral blood of patients with Chagas’ disease. Int Immunol. 1994; 6: 499–506.
  • Bryan MA, Guyach SE, Norris KA. Specific humoral immunity versus polyclonal B cell activation in Trypanosoma cruzi infection of susceptible and resistant mice. PLoS Negl Trop Dis. 2010; 4: e733.
  • Bermejo DA, Amezcua-Vesely MC, Montes CL, Merino MC, Gehrau RC, Cejas H et al. BAFF mediates splenic B cell response and antibody production in experimental Chagas disease. PLoS Negl Trop Dis. 2010; 4: e679.
  • Fares RC, Correa-Oliveira R, de Araujo FF, Keesen TS, Chaves AT, Fiuza JA et al. Identification of phenotypic markers of B cells from patients with Chagas disease. Parasite Immunol. 2013; 35: 214–23.
  • Duddy ME, Alter A, Bar-Or A. Distinct profiles of human B cell effector cytokines: a role in immune regulation?. J Immunol. 2004; 172: 3422–7.
  • Souza PE, Rocha MO, Menezes CA, Coelho JS, Chaves AC, Gollob KJ et al. Trypanosoma cruzi infection induces differential modulation of costimulatory molecules and cytokines by monocytes and T cells from patients with indeterminate and cardiac Chagas’ disease. Infect Immun. 2007; 75: 1886–94.
  • Gravina HD, Antonelli L, Gazzinelli RT, Ropert C. Differential use of TLR2 and TLR9 in the regulation of immune responses during the infection with Trypanosoma cruzi. PLoS One. 2013; 8: e63100.