In vitro challenge of human dendritic cells with Paracoccidioides brasiliensis induces preferential generation of Treg cells
Main Article Content
Abstract
Paracoccidioidomycosis (PCM) is a systemic mycosis, endemic to most Latin American countries (especially Brazil) whose etiologic agent is the thermodimorphic fungus Paracoccidioides brasiliensis (Pb). Host resistance/susceptibility to PCM has been explained by the involvement of different subpopulations of CD4+ cells. However, the mechanisms leading to preferential induction of any subpopulation are still unclear, and the participation of dendritic cells (DCs) must be highlighted. These cells bind, capture, kill, process microorganisms and migrate to peripheral lymphoid tissue where they maturate, efficiently trigger, and drive CD4+ T cell-mediated immune responses. The nature of the interaction of these cells with each microorganism defines CD4+ cell differentiation. Few studies have evaluated which subsets of CD4+ cells are preferentially induced after the interaction of human DCs/Pb. Here, we show that in vitro challenge of DCs with Pb results in the preferential induction of Treg cells.
Keywords:
Paracoccidioides brasiliensis, Human Dendritic Cells;, Treg Cells
Article Details
How to Cite
FERNANDES, Reginaldo K et al.
In vitro challenge of human dendritic cells with Paracoccidioides brasiliensis induces preferential generation of Treg cells.
Medical Research Archives, [S.l.], v. 5, n. 12, dec. 2017.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/1664>. Date accessed: 22 dec. 2024.
doi: https://doi.org/10.18103/mra.v5i12.1664.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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[22] KS Ferreira, KR Bastos, M Russo, SR. Almeida. Interaction between Paracoccidioides brasiliensis and pulmonary dendritic cells induces interleukin-10 production and toll-like receptor-2 expression: possible mechanisms of susceptibility. J Infect Dis 2007;196:1108-15.
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[24] AH Tavares, LS Derengowski, K.S. Ferreira, et al. Murine dendritic cells transcriptional modulation upon Paracoccidioides brasiliensis infection. PLoS Negl Trop Dis 2012;6:1459.
[25] AM Soares, S Calvi, MT Peraçoli, AC Fernandez, LA Dias, AR Dos Anjos. Modulatory effect of prostaglandins on human monocyte activation for killing of high- and low-virulence strains of Paracoccidioides brasiliensis. Immunology 2001;102:480-5.
[26] RK Fernandes, TF Bachiega, DR Rodrigues, et al. Paracoccidioides brasiliensis interferes on dendritic cells maturation by inhibiting PGE2 production. PLoS One 2015;10:e0120948.
[27] C Audiger, MJ Rahman, T Yun, KV Tarbell, S Lesage. The Importance of Dendritic Cells in Maintaining Immune Tolerance. J Immunol 2017;198:2223-2231.
[28] RM Steinman, MC Nussenzweig. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc Natl Acad Sci USA 2002;99:351-8 Review.
[29] LJ Carreño, PA González, SM. Bueno, CA Riedel, AM Kalergis. Modulation of the dendritic cell-T-cell synapse to promote pathogen immunity and prevent autoimmunity. Immunotherapy 2011;3:6-11 Review.
[30] PA Morel, MS Turner. Dendritic cells and the maintenance of self-tolerance. Immunol Res 2011;50:124-9 Review.
[31] M Hara, CI Kingsley, M Niimi, et al. IL-10 is required for regulatory T cells to mediate tolerance to alloantigenin vivo. J Immunol 2001;166:3789-3796.
[32] S Yamagiwa, J Gray, S Hashimoto, DA Horwitz. A role for TGF-β in the generation and expansion of CD4+CD25+regulatory T cells from human peripheral blood. J Immunol 2001;166:7282-7289.
[33] KA Cavassani, AP Campanelli, AP Moreira, et al. Systemic and local characterization of regulatory T cells in a chronic fungal infection in humans. J Immunol 2006;177:5811-8.
[34] AA Silva, MN Sotto, MI Duarte, C Pagliari. Regulatory T cells in cutaneous lesions of patients with Paracoccidioidomycosis. Microb Pathog 2013;65:36-40.
[35] MC Ferreira, RT de Oliveira, RM da Silva, MH Blotta, RL Mamoni. Involvement of regulatory T cells in the immunosuppression characteristic of patients with paracoccidioidomycosis. Infect Immun 2010;78:4392–4401.
[36] FV Loures, EF Araújo, C Feriotti, et al. Dectin-1 induces M1 macrophages and prominent expansion of CD8+IL-17+ cells in pulmonary Paracoccidioidomycosis. J Infect Dis 2014;210:762-73.
[37] AP Moreira, KA Cavassani, FS Massafera Tristão, et al. CCR5-dependent regulatory T cell migration mediates fungal survival and severe immunosuppression. J Immunol 2008;180:3049-56.
[38] M Felonato, A Pina, EF de Araujo, et al. Anti-CD25 treatment depletes Treg cells and decreases disease severity in susceptible and resistant mice infected with Paracoccidioides brasiliensis. PLoS One 2012;7:e51071.
[39] C Montagnoli, A Bacci, S Bozza, et al. B7/CD28-dependent CD4+CD25+ regulatory T cells are essential components of the memory-protective immunity to Candida albicans. J Immunol 2002;169:6298–6308.
[40] S Hori, TL Carvalho, J Demengeot. CD25+CD4+ regulatory suppress CD4+ T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur J Immunol 2002;32:1282–1291.
[41] C Montagnoli, F Fallarino, R Gaziano, et al. Immunity and tolerance to Aspergillus involve functionally distinct regulatory T cells and tryptophan catabolism. J Immunol 2006;176:1712–1723.
[42] A Rivera, TM Hohl, N Collins, et al. Dectin-1 diversifies Aspergillus fumigatus-specific T cell responses by inhibiting T helper type 1 CD4 T cell differentiation. J Exp Med 2011;208:369-81.
[43] A Pina, EF de Araujo, M Felonato, et al. Myeloid dendritic cells (DCs) of mice susceptible to paracoccidioidomycosis suppress T cell responses whereas myeloid and plasmacytoid DCs from resistant mice induce effector and regulatory T cells. Infect Immun 2013;81:1064-77.
[44] FV Loures, A Pina, M Felonato, EF Araújo, KR Leite, VL Calich. Toll-like receptor 4 signaling leads to severe fungal infection associated with enhanced proinflammatory immunity and impaired expansion of regulatory T cells. Infect Immun 2010;78:1078-88.
[45] SB Bazan, TA Costa, EF de Araújo, et al. Loss- and Gain-of-Function Approaches Indicate a Dual Role Exerted by Regulatory T Cells in Pulmonary Paracoccidioidomycosis. PLoS Negl Trop Dis 2015;9:e0004189.
[46] EF Araújo, DH Medeiros, NA Galdino, A Condino-Neto, VL Calich, FV Loures. Tolerogenic Plasmacytoid Dendritic Cells Control Paracoccidioides brasiliensis Infection by Inducting Regulatory T Cells in an IDO-Dependent Manner. PLoS Pathog 2016;12:e1006115.
[2] DR Matute, JG McEwen, R Puccia, et al. Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Mol Biol Evol 2006;23:65-73.
[3] MM Teixeira, RC Theodoro, MJ de Carvalho, et al. Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus. Mol Phylogenet Evol 2009;52: 273-283.
[4] MA Shikanai-Yasuda, Fde Q Telles Filho, RP Mendes, AL Colombo, ML Moretti. Guidelines in paracoccidioidomycosis. Ver Soc Bras Med Trop 2006;39:297-310.
[5] G Benard. An overview of the immunopathology of human paracoccidioidomycosis. Mycopathologia 2008;16:209-21.
[6] VLG Calich, M Russo, CAC Vaz, E Burger, LM Singer-Vermes. Resistance mechanism to experimental Paracoccidioides brasiliensis infection. Cienc Cult 1994;46:455-61.
[7] SR de Almeida, JZ de Moraes, ZP de Camargo, JL Gesztesi, M Mariano, JD Lopes. Pattern of immune response to GP43 from Paracoccidioides brasiliensis in susceptible and resistant mice is influenced by antigen-presenting cells. Cell Immunol 1998;190:68-76.
[8] VLG Calich, SS Kashino. Cytokines produced by susceptible and resistant mice in the course of Paracoccidioides brasiliensis infection. Braz J Med Biol Res 1998;3:615-23.
[9] SS Kashino, RA Fazioli, C Cafalli-Favati, et al. Resistance to Paracoccidioides brasiliensis infection is linked to a preferential Th1 immune response, whereas susceptibility is associated with absence of IFN-gamma production. J Interferon Cytokine Res 2000;20:89-97.
[10] SJ Oliveira, RL Mamoni, CC Musatti, PMO Papaiordanou, MHSL Blotta. Cytokines and lymphocyte proliferation in juvenile and adult forms of paracoccidioidomycosis: comparisons with infected and non-infected controls. Microbes Infected 2002;4:139-44.
[11] RL Mamoni, MHSL Blotta. Kinetics of cytokines and chemokines gene expression distinguishes Paracoccidioides brasiliensis infection from disease. Cytokine 2005;32:20-29.
[12] MC Livonesi, JT Souto, AP Campanelli, et al. Deficiency of IL-12p40 subunit determines severe paracoccidioidomycosis in mice. Med Mycol 2008;46:637-46.
[13] SA Calvi, MT Peracoli, RP Mendes, et al. Effect of cytokines on the in vitro fungicidal activity of monocytes from paracoccidioidomycosis patients. Microbes Infect 2003;5:107-13.
[14] G Benard, CC Romano, CR Cacere, M Juvenale, MJ Mendes-Giannini, AJ Duarte. Imbalance of IL-2, IFN-gamma and IL-10 secretion in the immunosuppression associated with human paracoccidioidomycosis. Cytokine 2001;13:248-52.
[15] RL Mamoni, SA Nouér, SJ Oliveira, et al. Enhanced production of specific IgG4, IgE, IgA and TGF-beta in sera from patients with the juvenile form of paracoccidioidomycosis. Med Mycol 2002;40:153-9.
[16] LF de Castro, MC Ferreira, RM da Silva, MH Blotta, LN Longhi, RL Mamoni. Characterization of the immune response in human paracoccidioidomycosis. J Infect 2013;67:470-85.
[17] M Cella, F Sallusto, A Lanzavecchia. Origen, maturation and antigen presenting function of dendritic cells. Curr Opin Immunol 1997;9:10-6.
[18] RM Steinman. The dendritic cell system and its role in immunogenicity. Annu Ver Immunol 1991;9:271-96.
[19] J Banchereau, RM Steinman. Dendritic cells and the control of immunity. Nature 1998;392:245-52 Review.
[20] SR Almeida, JD Lopes. The low efficiency of dendritic cells and macrophages from mice susceptible to Paracoccidioides brasiliensis in inducing a Th1 response. Braz J Med Biol Res 2001;34:529-37.
[21] KS Ferreira, JD Lopes, SR Almeida. Down-regulation of dendritic cell activation induced by Paracoccidioides brasiliensis. Immunol Lett 2004;94:107-14.
[22] KS Ferreira, KR Bastos, M Russo, SR. Almeida. Interaction between Paracoccidioides brasiliensis and pulmonary dendritic cells induces interleukin-10 production and toll-like receptor-2 expression: possible mechanisms of susceptibility. J Infect Dis 2007;196:1108-15.
[23] MC Fornazim, RL Mamoni, MHSL Blotta. Human dendritic cells pulsed with low virulence strain of Paracoccidioides brasiliensis (Pb265) induce the proliferation of IFN-γ and IL-17 producing cells. XXXIII Congress of the Brazilian Society for Immunology 2008;1:1-3.
[24] AH Tavares, LS Derengowski, K.S. Ferreira, et al. Murine dendritic cells transcriptional modulation upon Paracoccidioides brasiliensis infection. PLoS Negl Trop Dis 2012;6:1459.
[25] AM Soares, S Calvi, MT Peraçoli, AC Fernandez, LA Dias, AR Dos Anjos. Modulatory effect of prostaglandins on human monocyte activation for killing of high- and low-virulence strains of Paracoccidioides brasiliensis. Immunology 2001;102:480-5.
[26] RK Fernandes, TF Bachiega, DR Rodrigues, et al. Paracoccidioides brasiliensis interferes on dendritic cells maturation by inhibiting PGE2 production. PLoS One 2015;10:e0120948.
[27] C Audiger, MJ Rahman, T Yun, KV Tarbell, S Lesage. The Importance of Dendritic Cells in Maintaining Immune Tolerance. J Immunol 2017;198:2223-2231.
[28] RM Steinman, MC Nussenzweig. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc Natl Acad Sci USA 2002;99:351-8 Review.
[29] LJ Carreño, PA González, SM. Bueno, CA Riedel, AM Kalergis. Modulation of the dendritic cell-T-cell synapse to promote pathogen immunity and prevent autoimmunity. Immunotherapy 2011;3:6-11 Review.
[30] PA Morel, MS Turner. Dendritic cells and the maintenance of self-tolerance. Immunol Res 2011;50:124-9 Review.
[31] M Hara, CI Kingsley, M Niimi, et al. IL-10 is required for regulatory T cells to mediate tolerance to alloantigenin vivo. J Immunol 2001;166:3789-3796.
[32] S Yamagiwa, J Gray, S Hashimoto, DA Horwitz. A role for TGF-β in the generation and expansion of CD4+CD25+regulatory T cells from human peripheral blood. J Immunol 2001;166:7282-7289.
[33] KA Cavassani, AP Campanelli, AP Moreira, et al. Systemic and local characterization of regulatory T cells in a chronic fungal infection in humans. J Immunol 2006;177:5811-8.
[34] AA Silva, MN Sotto, MI Duarte, C Pagliari. Regulatory T cells in cutaneous lesions of patients with Paracoccidioidomycosis. Microb Pathog 2013;65:36-40.
[35] MC Ferreira, RT de Oliveira, RM da Silva, MH Blotta, RL Mamoni. Involvement of regulatory T cells in the immunosuppression characteristic of patients with paracoccidioidomycosis. Infect Immun 2010;78:4392–4401.
[36] FV Loures, EF Araújo, C Feriotti, et al. Dectin-1 induces M1 macrophages and prominent expansion of CD8+IL-17+ cells in pulmonary Paracoccidioidomycosis. J Infect Dis 2014;210:762-73.
[37] AP Moreira, KA Cavassani, FS Massafera Tristão, et al. CCR5-dependent regulatory T cell migration mediates fungal survival and severe immunosuppression. J Immunol 2008;180:3049-56.
[38] M Felonato, A Pina, EF de Araujo, et al. Anti-CD25 treatment depletes Treg cells and decreases disease severity in susceptible and resistant mice infected with Paracoccidioides brasiliensis. PLoS One 2012;7:e51071.
[39] C Montagnoli, A Bacci, S Bozza, et al. B7/CD28-dependent CD4+CD25+ regulatory T cells are essential components of the memory-protective immunity to Candida albicans. J Immunol 2002;169:6298–6308.
[40] S Hori, TL Carvalho, J Demengeot. CD25+CD4+ regulatory suppress CD4+ T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur J Immunol 2002;32:1282–1291.
[41] C Montagnoli, F Fallarino, R Gaziano, et al. Immunity and tolerance to Aspergillus involve functionally distinct regulatory T cells and tryptophan catabolism. J Immunol 2006;176:1712–1723.
[42] A Rivera, TM Hohl, N Collins, et al. Dectin-1 diversifies Aspergillus fumigatus-specific T cell responses by inhibiting T helper type 1 CD4 T cell differentiation. J Exp Med 2011;208:369-81.
[43] A Pina, EF de Araujo, M Felonato, et al. Myeloid dendritic cells (DCs) of mice susceptible to paracoccidioidomycosis suppress T cell responses whereas myeloid and plasmacytoid DCs from resistant mice induce effector and regulatory T cells. Infect Immun 2013;81:1064-77.
[44] FV Loures, A Pina, M Felonato, EF Araújo, KR Leite, VL Calich. Toll-like receptor 4 signaling leads to severe fungal infection associated with enhanced proinflammatory immunity and impaired expansion of regulatory T cells. Infect Immun 2010;78:1078-88.
[45] SB Bazan, TA Costa, EF de Araújo, et al. Loss- and Gain-of-Function Approaches Indicate a Dual Role Exerted by Regulatory T Cells in Pulmonary Paracoccidioidomycosis. PLoS Negl Trop Dis 2015;9:e0004189.
[46] EF Araújo, DH Medeiros, NA Galdino, A Condino-Neto, VL Calich, FV Loures. Tolerogenic Plasmacytoid Dendritic Cells Control Paracoccidioides brasiliensis Infection by Inducting Regulatory T Cells in an IDO-Dependent Manner. PLoS Pathog 2016;12:e1006115.