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Effect of the Tc13Tul antigen from Trypanosoma cruzi on splenocytes from naïve mice

Published online by Cambridge University Press:  29 May 2020

Laura Mónica Tasso
Affiliation:
Instituto Nacional de Parasitología (INP) ‘Dr. Mario Fatala Chaben’-ANLIS ‘Dr. Carlos G. Malbrán’, Buenos Aires, Argentina
Andrea Cecilia Bruballa
Affiliation:
Instituto Nacional de Parasitología (INP) ‘Dr. Mario Fatala Chaben’-ANLIS ‘Dr. Carlos G. Malbrán’, Buenos Aires, Argentina
Patricia Andrea Garavaglia
Affiliation:
Instituto Nacional de Parasitología (INP) ‘Dr. Mario Fatala Chaben’-ANLIS ‘Dr. Carlos G. Malbrán’, Buenos Aires, Argentina
Mónica Inés Esteva
Affiliation:
Instituto Nacional de Parasitología (INP) ‘Dr. Mario Fatala Chaben’-ANLIS ‘Dr. Carlos G. Malbrán’, Buenos Aires, Argentina
María Cecilia Albareda
Affiliation:
Instituto Nacional de Parasitología (INP) ‘Dr. Mario Fatala Chaben’-ANLIS ‘Dr. Carlos G. Malbrán’, Buenos Aires, Argentina
Gabriela Andrea García*
Affiliation:
Instituto Nacional de Parasitología (INP) ‘Dr. Mario Fatala Chaben’-ANLIS ‘Dr. Carlos G. Malbrán’, Buenos Aires, Argentina
*
Author for correspondence: Gabriela Andrea García, E-mail: gaandgarcia@yahoo.com

Abstract

Trypanosoma cruzi, the etiological agent of Chagas disease, releases factors, including antigens from the trans-sialidase (TS) superfamily, which modulate the host immune responses. Tc13 antigens belong to group IV of TSs and are characterized by C-terminal EPKSA repeats. Here, we studied the effect of the Tc13 antigen from the Tulahuén strain, Tc13Tul, on primary cultures of splenocytes from naïve BALB/c mice. Recombinant Tc13Tul increased the percentage of viable cells and induced B (CD19+) lymphocyte proliferation. Tc13Tul stimulation also induced secretion of non-specific IgM and interferon-γ (IFN-γ). The same effects were induced by Tc13Tul on splenocytes from naïve C3H/HeJ mice. In vivo administration of Tc13Tul to naïve BALB/c mice increased non-specific IgG in sera. In addition, in vitro cultured splenocytes from Tc13Tul-inoculated mice secreted a higher basal level of non-specific IgM than controls and the in vitro Tc13Tul stimulation of these cells showed an enhanced effect on IgM and IFN-γ secretion. Our results indicate that Tc13Tul may participate in the early immunity in T. cruzi infection by favouring immune system evasion through B-cell activation and non-specific Ig secretion. In contrast, as IFN-γ is an important factor involved in T. cruzi resistance, this may be considered a Tc13Tul effect in favour of the host.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

Present address: Instituto de Medicina Experimental (IMEX)-Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina.

These authors contributed equally to this work.

References

Affranchino, JL, Ibañez, CF, Luquetti, AO, Rassi, A, Reyes, MB, Macina, RA, Aslund, L, Pettersson, U and Frasch, AC (1989) Identification of a Trypanosoma cruzi antigen that is shed during the acute phase of Chagas’ disease. Molecular and Biochemical Parasitology 34, 221228.CrossRefGoogle ScholarPubMed
Akira, S, Uematsu, S and Takeuchi, O (2006) Pathogen recognition and innate immunity. Cell 124, 783801.CrossRefGoogle ScholarPubMed
Alvarez, P, Leguizamón, MS, Buscaglia, CA, Pitcovsky, TA and Campetella, O (2001) Multiple overlapping epitopes in the repetitive unit of the shed acute-phase antigen from Trypanosoma cruzi enhance its immunogenic properties. Infection and Immunity 69, 79467949.CrossRefGoogle ScholarPubMed
Andersson, J, Coutinho, A and Melchers, F (1978) The switch from IgM to IgG secretion in single mitogen-stimulated B-cell clones. The Journal of Experimental Medicine 147, 17441754.10.1084/jem.147.6.1744CrossRefGoogle ScholarPubMed
Aridgides, D, Salvador, R and Pereira Perrin, M (2013) Trypanosoma cruzi coaxes cardiac fibroblasts into preventing cardiomyocyte death by activating nerve growth factor receptor TrkA. PLoS ONE 8, e57450.CrossRefGoogle ScholarPubMed
Bao, Y, Liu, X, Han, C, Xu, S, Xie, B, Zhang, Q, Gu, Y, Hou, J, Qian, L, Qian, C, Han, H and Cao, X (2014) Identification of IFN-γ-producing innate B cells. Cell Research 24, 161176.CrossRefGoogle ScholarPubMed
Bermejo, DA, Amezcua Vesely, MC, Khan, M, Acosta Rodríguez, EV, Montes, CL, Merino, MC, Toellner, KM, Mohr, E, Taylor, D, Cunningham, AF and Gruppi, A (2011) Trypanosoma cruzi infection induces a massive extrafollicular and follicular splenic B-cell response which is a high source of non-parasite-specific antibodies. Immunology 132, 123133.CrossRefGoogle ScholarPubMed
Bermejo, DA, Jackson, SW, Gorosito-Serran, M, Acosta Rodríguez, EV, Amezcua Vesely, MC, Sather, BD, Singh, AK, Khim, S, Mucci, J, Liggitt, D, Campetella, O, Oukka, M, Gruppi, A and Rawlings, DJ (2013) Trypanosoma cruzi trans-sialidase initiates a program independent of the transcription factors RORγt and Ahr that leads to IL-17 production by activated B cells. Nature Immunology 14, 514522.CrossRefGoogle ScholarPubMed
Beucher, M and Norris, KA (2008) Sequence diversity of the Trypanosoma cruzi complement regulatory protein family. Infection and Immunity 76, 750775.CrossRefGoogle ScholarPubMed
Bontempi, EJ, García, GA, Buschiazzo, A, Henriksson, J, Pravia, CA, Ruiz, AM, Pettersson, U and Pszenny, V. (2000) The tyrosine aminotransferase from Trypanosoma rangeli: sequence and genomic characterization. FEMS Microbiology Letters 189, 253257.CrossRefGoogle ScholarPubMed
Bryan, MA, Guyach, SE and Norris, KA (2010) Specific humoral immunity versus polyclonal B cell activation in Trypanosoma cruzi infection of susceptible and resistant mice. PLoS Neglected Tropical Diseases 4, e733.CrossRefGoogle ScholarPubMed
Burgos, JM, Risso, MG, Brenière, SF, Barnabé, C, Campetella, O and Leguizamón, MS (2013) Differential distribution of genes encoding the virulence factor trans-sialidase along Trypanosoma cruzi discrete typing units. PLoS ONE 8, e58967.CrossRefGoogle ScholarPubMed
Burns, JM Jr, Shreffler, WG, Rosman, DE, Sleath, PR, March, CJ and Reed, SG (1992) Identification and synthesis of a major conserved antigenic epitope of Trypanosoma cruzi. Proceedings of the National Academy of Sciences of the USA 89, 1239–1124.CrossRefGoogle Scholar
Buscaglia, CA, Campetella, O, Leguizamón, MS and Frasch, AC (1998) The repetitive domain of Trypanosoma cruzi trans-sialidase enhances the immune response against the catalytic domain. The Journal of Infectious Diseases 177, 431436.CrossRefGoogle ScholarPubMed
Buscaglia, CA, Alfonso, J, Campetella, O and Frasch, AC (1999) Tandem amino acid repeats from Trypanosoma cruzi shed antigens increase the half-life of proteins in blood. Blood 93, 20252032.CrossRefGoogle ScholarPubMed
Buschiazzo, A, Amaya, MF, Cremona, ML, Frasch, AC and Alzari, PM (2002) The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Molecular Cell 10, 757768.CrossRefGoogle ScholarPubMed
Campetella, O, Sánchez, D, Cazzulo, JJ and Frasch, AC (1992) A superfamily of Trypanosoma cruzi surface antigens. Parasitology Today 8, 378380.CrossRefGoogle ScholarPubMed
Cardillo, F, Voltarelli, JC, Reed, SG and Silva, JS (1996) Regulation of Trypanosoma cruzi infection in mice by gamma interferon and interleukin 10: role of NK cells. Infection and Immunity 64, 128134.CrossRefGoogle ScholarPubMed
Cardoso, MS, Reis-Cunha, JL and Bartholomeu, DC (2016) Evasion of the immune response by Trypanosoma cruzi during acute infection. Frontiers in Immunology 6, 659.CrossRefGoogle ScholarPubMed
Cremona, ML, Sánchez, DO, Frasch, AC and Campetella, O (1995) A single tyrosine differentiates active and inactive Trypanosoma cruzi trans-sialidases. Gene 160, 123128.CrossRefGoogle ScholarPubMed
Cremona, ML, Campetella, O, Sanchez, DO and Frasch, AC (1999) Enzymically inactive members of the trans-sialidase family from Trypanosoma cruzi display betagalactose binding activity. Glycobiology 9, 581587.CrossRefGoogle Scholar
Da Silva, AC, Espinoza, AG, Taibi, A, Ouaissi, A and Minoprio, P (1998) A 24 000 MW Trypanosoma cruzi antigen is a B cell activator. Immunology 94, 189196.CrossRefGoogle ScholarPubMed
Duthie, MS, Kahn, M, White, M, Kapur, RP and Kahn, SJ (2005) Critical proinflammatory and anti-inflammatory functions of different subsets of CD1d-restricted natural killer T cells during Trypanosoma cruzi infection. Infection and Immunity 73, 181192.CrossRefGoogle ScholarPubMed
Freitas, LM, dos Santos, SL, Rodrigues-Luiz, GF, Mendes, TA, Rodrigues, TS, Gazzinelli, RT, Teixeira, SM, Fujiwara, RT and Bartholomeu, DC (2011) Genomic analyses, gene expression and antigenic profile of the trans-sialidase superfamily of Trypanosoma cruzi reveal an undetected level of complexity. PLoS ONE 6, e25914.CrossRefGoogle ScholarPubMed
Gao, W, Wortis, HH and Pereira, MA (2002) The Trypanosoma cruzi trans-sialidase is a T cell-independent B cell mitogen and an inducer of non-specific Ig secretion. International Immunology 14, 299308.CrossRefGoogle Scholar
García, GA, Joensen, LG, Bua, J, Ainciart, N, Perry, SJ and Ruiz, AM (2003) Trypanosoma cruzi: molecular identification and characterization of new members of the Tc13 family. Description of the interaction between the Tc13 antigen from Tulahuen strain and the second extracellular loop of the beta(1)-adrenergic receptor. Experimental Parasitology 103, 112119.CrossRefGoogle ScholarPubMed
García, GA, Arnaiz, MR, Laucella, SA, Esteva, MI, Ainciart, N, Riarte, A, Garavaglia, PA, Fichera, LE and Ruiz, AM (2006) Immunological and pathological responses in BALB/c mice induced by genetic administration of Tc13Tul antigen of Trypanosoma cruzi. Parasitology 132, 855866.CrossRefGoogle Scholar
García, GA, Arnaiz, MR, Esteva, MI, Laucella, SA, Garavaglia, PA, Ibarra, SE and Ruiz, AM (2008) Evaluation of immune responses raised against Tc13 antigens of Trypanosoma cruzi in the outcome of murine experimental infection. Parasitology 135, 347357.CrossRefGoogle ScholarPubMed
Gazzinelli, RT, Oswald, IP, Hieny, S, James, SL and Sher, A (1992) The microbicidal activity of interferon-gamma-treated macrophages against Trypanosoma cruzi involves an L-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by interleukin-10 and transforming growth factor-beta. European Journal of Immunology 22, 25012506.CrossRefGoogle ScholarPubMed
Gupta, S, Govil, D, Kakar, PN, Prakash, O, Arora, D, Das, S, Govil, P and Malhotra, A (2009) Colistin and polymyxin B: a re-emergence. Indian Journal of Critical Care Medicine 13, 4953.Google ScholarPubMed
Leguizamón, MS, Mocetti, E, Garcia Rivello, H, Argibay, P and Campetella, O (1999) Trans-sialidase from Trypanosoma cruzi induces apoptosis in cells from the immune system in vivo. The Journal of Infectious Diseases 180, 13981402.CrossRefGoogle ScholarPubMed
Liu, G, Zhang, Y, Zhang, N, Ni, W, Jie, J, Jiang, L and Tai, G (2017) Escherichia coli maltose-binding protein (MBP) activates mouse Th1 through TLR2-mediated MyD88-dependent pathway and TLR4-mediated TRIF-dependent pathway. International Immunopharmacology 50, 338344.CrossRefGoogle ScholarPubMed
Martin, F, Oliver, AM and Kearney, JF (2001) Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14, 617629.CrossRefGoogle ScholarPubMed
Martin, DL, Weatherly, DB, Laucella, SA, Cabinian, MA, Crim, MT, Sullivan, S, Heiges, M, Craven, SH, Rosenberg, CS, Collins, MH, Sette, A, Postan, M and Tarleton, RL (2006) CD8+ T-cell Responses to Trypanosoma cruzi are highly focused on strain-variant trans-sialidase epitopes. PLoS Pathogens 2, e77.CrossRefGoogle ScholarPubMed
Martins, GA, Vieira, LQ, Cunha, FQ and Silva, JS (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, 38643871.CrossRefGoogle ScholarPubMed
Millar, AE, Wleklinski-Lee, M and Kahn, SJ (1999) The surface protein superfamily of Trypanosoma cruzi stimulates a polarized Th1 response that becomes anergic. Journal of Immunology 162, 60926099.Google ScholarPubMed
Minoprio, P, Burlen, O, Pereira, P, Guilbert, B, Andrade, L, Hontebeyrie-Joskowicz, M and Coutinho, A (1998) Most B cells in acute Trypanosoma cruzi infection lack parasite specificity. Scandinavian Journal of Immunology 28, 553561.CrossRefGoogle Scholar
Miyawaki, T, Uehara, T, Nibu, R, Tsuji, T, Yachie, A, Yonehara, S and Taniguchi, N (1992) Differential expression of apoptosis-related Fas antigen on lymphocyte subpopulations in human peripheral blood. Journal of Immunology 149, 37533758.Google ScholarPubMed
Mucci, J, Risso, MG, Leguizamón, MS, Frasch, AC and Campetella, O (2006) The trans-sialidase from Trypanosoma cruzi triggers apoptosis by target cell sialylation. Cellular Microbiology 8, 10861095.CrossRefGoogle ScholarPubMed
Mucci, J, Lantos, AB, Buscaglia, CA, Leguizamón, MS and Campetella, O (2017) The Trypanosoma cruzi surface a nanoscale patch work quilt. Trends in Parasitology 33, 102112.CrossRefGoogle Scholar
Nowell, PC (1960) Phytohemagglutinin: an initiator of mitosis in culture of animal and human leukocytes. Cancer Research 20, 462466.Google Scholar
Oliveira, AC, de Alencar, BC, Tzelepis, F, Klezewsky, W, da Silva, RN, Neves, FS, Cavalcanti, GS, Boscardin, S, Nunes, MP, Santiago, MF, Nóbrega, A, Rodrigues, MM and Bellio, M (2010) 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 6, e1000870.CrossRefGoogle ScholarPubMed
Ouaissi, A, Guilvard, E, Delneste, Y, Caron, G, Magistrelli, G, Herbault, N, Thieblemont, N and Jeannin, P (2002) 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 168, 63666374.CrossRefGoogle ScholarPubMed
Peralta, JM, Teixeira, MG, Shreffler, WG, Pereira, JB, Burns, JM Jr, Sleath, PR and Reed, SG (1994) Serodiagnosis of Chagas disease by enzyme-linked immunosorbent assay using two synthetic peptides as antigens. Journal of Clinical Microbiology 32, 971974.CrossRefGoogle ScholarPubMed
Poltorak, A, He, X, Smirnova, I, Liu, MY, Van Huffel, C, Du, X, Birdwell, D, Alejos, E, Silva, M, Galanos, C, Freudenberg, M, Ricciardi-Castagnoli, P, Layton, B and Beutler, B (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science (New York, N.Y.) 282, 20852088.CrossRefGoogle ScholarPubMed
Rassi, A Jr, Rassi, A and Marin-Neto, JA (2010) Chagas disease. Lancet (London, England) 375, 13881402.CrossRefGoogle ScholarPubMed
Reina-San-Martin, B, Degrave, W, Rougeot, C, Cosson, A, Chamond, N, Cordeiro-Da-Silva, A, Arala-Chaves, M, Coutinho, A and Minoprio, P (2000) A B cell mitogen from a pathogenic trypanosome is a eukaryotic proline racemase. Nature Medicine 6, 890897.CrossRefGoogle Scholar
Romero-Ramírez, S, Navarro-Hernandez, IC, Cervantes-Díaz, R, Sosa-Hernández, VA, Acevedo-Ochoa, E, Kleinberg-Bild, A, Valle-Rios, R, Meza-Sánchez, DE, Hernández-Hernández, JM and Maravillas-Montero, JL (2019) Innate-like B cell subsets during immune responses: beyond antibody production. Journal of Leukocyte Biology 105, 843856.CrossRefGoogle ScholarPubMed
Salvador, R, Aridgides, D and Pereira Perrin, M (2014) Parasite-derived neurotrophic factor/trans-sialidase of Trypanosoma cruzi links neurotrophic signaling to cardiac innate immune response. Infection and Immunity 82, 36873696.CrossRefGoogle ScholarPubMed
Santamaría, AL, De Rissio, AM, Riarte, A, Garavaglia, PA, Bruballa, AC, Rodríguez, MA, Irazu, LE, Ruiz, AM and García, GA (2013) Use of an enzyme-linked immunosorbent assay that utilizes the Tc13Tul antigen of Trypanosoma cruzi to monitor patients after treatment with benznidazole. Diagnostic Microbiology and Infectious Disease 76, 197205.CrossRefGoogle ScholarPubMed
Schmidt, ST, Khadke, S, Korsholm, KS, Perrie, Y, Rades, T, Andersen, P, Foged, C and Christensen, D (2016) The administration route is decisive for the ability of the vaccine adjuvant CAF09 to induce antigen-specific CD8(+) T-cell responses: the immunological consequences of the biodistribution profile. Journal of Controlled Release 239, 107117.CrossRefGoogle ScholarPubMed
Sharon, N and Lis, H (2004) History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14, 53R62R.CrossRefGoogle ScholarPubMed
Todeschini, AR, Girard, MF, Wieruszeski, JM, Nunes, MP, DosReis, GA, Mendonça-Previato, L and Previato, JO (2002a). trans-Sialidase from Trypanosoma cruzi binds host T-lymphocytes in a lectin manner. The Journal of Biological Chemistry 277, 4596245968.10.1074/jbc.M203185200CrossRefGoogle Scholar
Todeschini, AR, Nunes, MP, Pires, RS, Lopes, MF, Previato, JO, Mendonça-Previato, L and DosReis, GA (2002b). Costimulation of host T lymphocytes by a trypanosomal trans-sialidase: involvement of CD43 signaling. Journal of Immunology 168, 51925198.CrossRefGoogle Scholar
Todeschini, AR, Dias, WB, Girard, MF, Wieruszeski, JM, Mendonça-Previato, L and Previato, JO (2004) Enzymatically inactive trans-sialidase from Trypanosoma cruzi binds sialyl and beta-galactopyranosyl residues in a sequential ordered mechanism. The Journal of Biological Chemistry 279, 53235328.CrossRefGoogle Scholar
Tu, W, Cheung, PT and Lau, YL (2000) Insulin-like growth factor 1 promotes cord blood T cell maturation and inhibits its spontaneous and phytohemagglutinin-induced apoptosis through different mechanisms. Journal of Immunology 165, 13311336.CrossRefGoogle ScholarPubMed
WHO-World Health Organization (2015) Chagas Disease in Latin America: An Epidemiological Update Based on 2010 Estimates. Geneva: WHO. http://www.who.int/wer/2015/wer9006.pdf?ua=1 (accessed 3 September 2018).Google Scholar
Wrightsman, RA, Dawson, BD, Fouts, DL and Manning, JE (1994) Identification of immunodominant epitopes in Trypanosoma cruzi trypomastigote surface antigen-1 protein that mask protective epitopes. Journal of Immunology 153, 31483154.Google ScholarPubMed
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