Regulatory Lymphoid and Myeloid Cells Determine the Cardiac Immunopathogenesis of Trypanosoma cruzi Infection

Abrahamsohn, 2000, Effects of interleukin-4 deprivation and treatment on resistance to Trypanosoma cruzi, Infect. Immun., 68, 1975, 10.1128/IAI.68.4.1975-1979.2000

Aliberti, 1996, Interleukin-12 mediates resistance to Trypanosoma cruzi in mice and is produced by murine macrophages in response to live trypomastigotes, Infect. Immun., 64, 1961, 10.1128/IAI.64.6.1961-1967.1996

Aliberti, 2001, Modulation of chemokine production and inflammatory responses in interferon-gamma- and tumor necrosis factor-R1-deficient mice during Trypanosoma cruzi infection, Am. J. Pathol., 158, 1433, 10.1016/S0002-9440(10)64094-1

Anderssohn, 2012, The L-Arginine-asymmetric dimethylarginine ratio is an independent predictor of mortality in dilated cardiomyopathy, J. Card. Fail., 18, 904, 10.1016/j.cardfail.2012.10.011

Antúnez, 2000, IL-12 and IFN-gamma production, and NK cell activity, in acute and chronic experimental Trypanosoma cruzi infections, Immunol. Lett., 71, 103, 10.1016/S0165-2478(99)00172-8

Antúnez, 2001, Early IFN-gamma production is related to the presence of interleukin (IL)-18 and the absence of IL-13 in experimental Trypanosoma cruzi infections, Immunol. Lett., 79, 189, 10.1016/S0165-2478(01)00283-8

Araujo, 2007, Potential role of CD4+CD25HIGH regulatory T cells in morbidity in Chagas disease, Front. Biosci., 12, 2797, 10.2741/2273

Argüello, 2014, Presence of antigen-experienced T cells with low grade of differentiation and proliferative potential in chronic Chagas disease myocarditis, PLoS Negl. Trop. Dis., 8, e2989, 10.1371/journal.pntd.0002989

Arocena, 2014, Myeloid-derived suppressor cells are key players in the resolution of inflammation during a model of acute infection, Eur. J. Immunol., 44, 184, 10.1002/eji.201343606

Bergeron, 2006, Trypanosoma cruzi-mediated IFN-gamma-inducible nitric oxide output in macrophages is regulated by iNOS mRNA stability, J. Immunol., 177, 6271, 10.4049/jimmunol.177.9.6271

Bettelli, 2006, Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells, Nature, 441, 235, 10.1038/nature04753

Blackwell, 2010, The biochemistry, measurement and current clinical significance of asymmetric dimethylarginine, Ann. Clin. Biochem., 47, 17, 10.1258/acb.2009.009196

Böhme, 2016, Epstein-Barr virus-induced gene 3 suppresses T helper type 1, type 17 and type 2 immune responses after Trypanosoma cruzi infection and inhibits parasite replication by interfering with alternative macrophage activation, Immunology, 147, 338, 10.1111/imm.12565

Bonney, 2015, Depletion of regulatory T cells decreases cardiac parasitosis and inflammation in experimental Chagas disease, Parasitol. Res., 114, 1167, 10.1007/s00436-014-4300-3

Bronte, 2005, Regulation of immune responses by L-arginine metabolism, Nat. Rev., 5, 641, 10.1038/nri1668

Bronte, 2016, Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards, Nat. Commun., 7, 12150, 10.1038/ncomms12150

Bronte, 2003, L-arginine metabolism in myeloid cells controls T-lymphocyte functions, Trends Immunol., 24, 302, 10.1016/S1471-4906(03)00132-7

Brys, 2005, Reactive oxygen species and 12/15-lipoxygenase contribute to the antiproliferative capacity of alternatively activated myeloid cells elicited during helminth infection, J. Immunol., 174, 6095, 10.4049/jimmunol.174.10.6095

Cabalén, 2016, Chronic Trypanosoma cruzi infection potentiates adipose tissue macrophage polarization toward an anti-inflammatory M2 phenotype and contributes to diabetes progression in a diet-induced obesity model, Oncotarget, 7, 13400, 10.18632/oncotarget.7630

Cabral-Piccin, 2016, Apoptotic CD8 T-lymphocytes disable macrophage-mediated immunity to Trypanosoma cruzi infection, Cell Death Dis., 7, e2232, 10.1038/cddis.2016.135

Cai, 2016, Th17 cells are more protective than Th1 cells against the intracellular parasite Trypanosoma cruzi, PLoS Pathog., 12, e1005902, 10.1371/journal.ppat.1005902

Calderón, 2012, The receptor Slamf1 on the surface of myeloid lineage cells controls susceptibility to infection by Trypanosoma cruzi, PLoS Pathog., 8, e1002799, 10.1371/journal.ppat.1002799

Carbajosa, 2018, L-arginine supplementation reduces mortality and improves disease outcome in mice infected with Trypanosoma cruzi, PLoS Negl. Trop. Dis., 12, e0006179, 10.1371/journal.pntd.0006179

Cardillo, 2015, Immunity and immune modulation in Trypanosoma cruzi infection, Pathog. Dis., 73, ftv082, 10.1093/femspd/ftv082

Chen, 2001, Neutrophil depletion exacerbates experimental Chagas' disease in BALB/c, but protects C57BL/6 mice through modulating the Th1/Th2 dichotomy in different directions, Eur. J. Immunol., 31, 265, 10.1002/1521-4141(200101)31:1<265::AID-IMMU265>3.0.CO;2-L

Choi, 2009, Differential impact of L-arginine deprivation on the activation and effector functions of T cells and macrophages, J. Leukoc. Biol., 85, 268, 10.1189/jlb.0508310

Collison, 2010, IL-35-mediated induction of a potent regulatory T cell population, Nat. Immunol., 11, 1093, 10.1038/ni.1952

Cuervo, 2011, Myeloid-derived suppressor cells infiltrate the heart in acute Trypanosoma cruzi infection, J. Immunol., 187, 2656, 10.4049/jimmunol.1002928

Cuervo, 2008, 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, J. Infect. Dis., 197, 1772, 10.1086/529527

da Costa, 2014, Does L-arginine availability during the early pregnancy alters the immune response of Trypanosoma cruzi infected and pregnant Wistar rats?, Exp. Parasitol., 142, 59, 10.1016/j.exppara.2014.04.012

da Matta Guedes, 2010, IL-17 produced during Trypanosoma cruzi infection plays a central role in regulating parasite-induced myocarditis, PLoS Negl. Trop. Dis., 4, e604, 10.1371/journal.pntd.0000604

de Araújo, 2011, Regulatory T cells phenotype in different clinical forms of Chagas' disease, PLoS Negl. Trop. Dis., 5, e992, 10.1371/journal.pntd.0000992

Esper, 2012, Role of SOCS2 in modulating heart damage and function in a murine model of acute Chagas disease, Am. J. Pathol., 181, 130, 10.1016/j.ajpath.2012.03.042

Flores-García, 2013, CD4+ CD25+ FOXP3+ Treg cells induced by rSSP4 derived from T. cruzi amastigotes increase parasitemia in an experimental Chagas disease model, Biomed. Res. Int., 2013, 632436, 10.1155/2013/632436

Gabrilovich, 2009, Myeloid-derived suppressor cells as regulators of the immune system, Nat. Rev., 9, 162, 10.1038/nri2506

Gallina, 2006, Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells, J. Clin. Invest., 116, 2777, 10.1172/JCI28828

Gao, 2002, Interleukin-6 is required for parasite specific response and host resistance to Trypanosoma cruzi, Int. J. Parasitol., 32, 167, 10.1016/S0020-7519(01)00322-8

Gazzinelli, 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, Eur. J. Immunol., 22, 2501, 10.1002/eji.1830221006

Geissmann, 2010, Unravelling mononuclear phagocyte heterogeneity, Nat. Rev., 10, 453, 10.1038/nri2784

Ghassabeh, 2006, Identification of a common gene signature for type II cytokine-associated myeloid cells elicited in vivo in different pathologic conditions, Blood, 108, 575, 10.1182/blood-2005-04-1485

Gironès, 2014, Global metabolomic profiling of acute myocarditis caused by Trypanosoma cruzi infection, PLoS Negl. Trop. Dis., 8, e3337, 10.1371/journal.pntd.0003337

Golden, 1991, Trypanosoma cruzi: cytokine effects on macrophage trypanocidal activity, Exp. Parasitol., 72, 391, 10.1016/0014-4894(91)90085-B

Gomes, 2003, Evidence that development of severe cardiomyopathy in human Chagas' disease is due to a Th1-specific immune response, Infect. Immun., 71, 1185, 10.1128/IAI.71.3.1185-1193.2003

Goñi, 2002, Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1(+))CD11b(+)immature myeloid suppressor cells, Int. Immunol., 14, 1125, 10.1093/intimm/dxf076

González, 2016, Trypanosoma cruzi experimental infection impacts on the thymic regulatory T cell compartment, PLoS Negl. Trop. Dis., 10, e0004285, 10.1371/journal.pntd.0004285

González, 2015, Immunoendocrine dysbalance during uncontrolled T. cruzi infection is associated with the acquisition of a Th-1-like phenotype by Foxp3(+) T cells, Brain Behav. Immun., 45, 219, 10.1016/j.bbi.2014.11.016

González, 2013, Granulocyte colony-stimulating factor partially repairs the damage provoked by Trypanosoma cruzi in murine myocardium, Int. J. Cardiol., 168, 2567, 10.1016/j.ijcard.2013.03.049

Guedes, 2012, Deficient regulatory T cell activity and low frequency of IL-17-producing T cells correlate with the extent of cardiomyopathy in human Chagas' disease, PLoS Negl. Trop. Dis., 6, e1630, 10.1371/journal.pntd.0001630

Guerrero, 2015, Cyclooxygenase-2 and prostaglandin E2 signaling through prostaglandin receptor EP-2 favor the development of myocarditis during acute Trypanosoma cruzi infection, PLoS Negl. Trop. Dis., 9, e0004025, 10.1371/journal.pntd.0004025

Guilliams, 2014, Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny, Nat. Rev., 14, 571, 10.1038/nri3712

Hall, 2000, Dual role for transforming growth factor beta-dependent signaling in Trypanosoma cruzi infection of mammalian cells, Infect. Immun., 68, 2077, 10.1128/IAI.68.4.2077-2081.2000

Holscher, 1998, Defective nitric oxide effector functions lead to extreme susceptibility of Trypanosoma cruzi-infected mice deficient in gamma interferon receptor or inducible nitric oxide synthase, Infect. Immun., 66, 1208, 10.1128/IAI.66.3.1208-1215.1998

Jäger, 2010, Effector and regulatory T-cell subsets in autoimmunity and tissue inflammation, Scand. J. Immunol., 72, 173, 10.1111/j.1365-3083.2010.02432.x

Kitada, 2017, BATF2 inhibits immunopathological Th17 responses by suppressing Il23a expression during Trypanosoma cruzi infection, J. Exp. Med., 214, 1313, 10.1084/jem.20161076

Konig, 2009, Translational repression of inducible NO synthase in macrophages by l-arginine depletion is not associated with an increased phosphorylation of eIF2alpha, Immunobiology, 214, 822, 10.1016/j.imbio.2009.06.008

Kotner, 2007, Endogenous CD4(+) CD25(+) regulatory T cells have a limited role in the control of Trypanosoma cruzi infection in mice, Infect. Immun., 75, 861, 10.1128/IAI.01500-06

Kralova, 2015, l-arginine attenuates cardiac dysfunction, but further down-regulates alpha-myosin heavy chain expression in isoproterenol-induced cardiomyopathy, Basic Clin. Pharmacol. Toxicol., 117, 251, 10.1111/j.1742-7843.2008.00261.x

Kumar, 1998, The relative contribution of antibody production and CD8+ T cell function to immune control of Trypanosoma cruzi, Parasite Immunol., 20, 207, 10.1046/j.1365-3024.1998.00154.x

Lewis, 2014, Bioluminescence imaging of chronic Trypanosoma cruzi infections reveals tissue-specific parasite dynamics and heart disease in the absence of locally persistent infection, Cell Microbiol., 16, 1285, 10.1111/cmi.12297

Luna-Gomes, 2014, Neutrophils increase or reduce parasite burden in Trypanosoma cruzi-infected macrophages, depending on host strain: role of neutrophil elastase, PLoS ONE, 9, e90582, 10.1371/journal.pone.0090582

Mariano, 2008, The involvement of CD4+CD25+ T cells in the acute phase of Trypanosoma cruzi infection, Microbes Infect., 10, 825, 10.1016/j.micinf.2008.04.009

Martin, 2004, Generation, specificity, and function of CD8+ T cells in Trypanosoma cruzi infection, Immunol. Rev., 201, 304, 10.1111/j.0105-2896.2004.00183.x

Matos, 2017, Immunization with Tc52 or its amino terminal domain adjuvanted with c-di-AMP induces Th17+Th1 specific immune responses and confers protection against Trypanosoma cruzi, PLoS Negl. Trop. Dis., 11, e0005300, 10.1371/journal.pntd.0005300

Medina, 2017, Ebi3 prevents Trypanosoma cruzi-induced myocarditis by dampening IFN-gamma-driven inflammation, Front. Immunol., 8, 1213, 10.3389/fimmu.2017.01213

Mengel, 2016, Chronic Chagas' disease: targeting the interleukin-2 axis and regulatory T cells in a condition for which there is no treatment, Front. Microbiol., 7, 675, 10.3389/fmicb.2016.00675

Ming, 1995, Trypanosome invasion of mammalian cells requires activation of the TGF beta signaling pathway, Cell, 82, 287, 10.1016/0092-8674(95)90316-X

Miyazaki, 2010, IL-17 is necessary for host protection against acute-phase Trypanosoma cruzi infection, J. Immunol., 185, 1150, 10.4049/jimmunol.0900047

Müller, 2003, Concerted action of perforin and granzymes is critical for the elimination of Trypanosoma cruzi from mouse tissues, but prevention of early host death is in addition dependent on the FasL/Fas pathway, Eur. J. Immunol., 33, 70, 10.1002/immu.200390009

Munder, 1999, Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells, J. Immunol., 163, 3771, 10.4049/jimmunol.163.7.3771

Muñoz-Fernández, 1992, Synergism between tumor necrosis factor-alpha and interferon-gamma on macrophage activation for the killing of intracellular Trypanosoma cruzi through a nitric oxide-dependent mechanism, Eur. J. Immunol., 22, 301, 10.1002/eji.1830220203

Nihei, 2014, Administration of a nondepleting anti-CD25 monoclonal antibody reduces disease severity in mice infected with Trypanosoma cruzi, Eur. J. Microbiol. Immunol., 4, 128, 10.1556/EuJMI.4.2014.2.6

Perez-Molina, 2017, Chagas disease, Lancet, 391, 82, 10.1016/S0140-6736(17)31612-4

Ponce, 2016, CD73 Inhibition shifts cardiac macrophage polarization toward a microbicidal phenotype and ameliorates the outcome of experimental Chagas cardiomyopathy, J. Immunol., 197, 814, 10.4049/jimmunol.1600371

Poncini, 2017, Dual role of monocyte-derived dendritic cells in Trypanosoma cruzi infection, Eur. J. Immunol., 47, 1936, 10.1002/eji.201646830

Rassi, 2010, Chagas disease, Lancet, 375, 1388, 10.1016/S0140-6736(10)60061-X

Rodriguez, 2017, Arginine metabolism in myeloid cells shapes innate and adaptive immunity, Front. Immunol., 8, 93, 10.3389/fimmu.2017.00093

Roffê, 2012, IL-10 limits parasite burden and protects against fatal myocarditis in a mouse model of Trypanosoma cruzi infection, J. Immunol., 188, 649, 10.4049/jimmunol.1003845

Sakaguchi, 1995, Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases, J. Immunol., 155, 1151, 10.4049/jimmunol.155.3.1151

Sales, 2008, The regulatory CD4+CD25+ T cells have a limited role on pathogenesis of infection with Trypanosoma cruzi, Microbes Infect., 10, 680, 10.1016/j.micinf.2008.03.008

Sanmarco, 2017, IL-6 promotes M2 macrophage polarization by modulating purinergic signaling and regulates the lethal release of nitric oxide during Trypanosoma cruzi infection, Biochim. Biophys. Acta, 1863, 857, 10.1016/j.bbadis.2017.01.006

Sanoja, 2013, Analysis of the dynamics of infiltrating CD4(+) T cell subsets in the heart during experimental Trypanosoma cruzi infection, PLoS ONE, 8, e65820, 10.1371/journal.pone.0065820

Santamaría, 2013, Osteopontin-dependent regulation of Th1 and Th17 cytokine responses in Trypanosoma cruzi-infected C57BL/6 mice, Cytokine, 61, 491, 10.1016/j.cyto.2012.10.027

Silva, 1992, Interleukin 10 and interferon gamma regulation of experimental Trypanosoma cruzi infection, J. Exp. Med., 175, 169, 10.1084/jem.175.1.169

Silva, 1991, Regulation of Trypanosoma cruzi infections in vitro and in vivo by transforming growth factor beta (TGF-beta), J. Exp. Med., 174, 539, 10.1084/jem.174.3.539

Silverio, 2010, Perforin-expressing cytotoxic cells contribute to chronic cardiomyopathy in Trypanosoma cruzi infection, Int. J. Exp. Pathol., 91, 72, 10.1111/j.1365-2613.2009.00670.x

Stempin, 2004, Arginase induction promotes Trypanosoma cruzi intracellular replication in Cruzipain-treated J774 cells through the activation of multiple signaling pathways, Eur. J. Immunol., 34, 200, 10.1002/eji.200324313

Teerlink, 2005, ADMA metabolism and clearance, Vasc. Med., 10, S73, 10.1177/1358836X0501000111

Telleria, 2017, American Trypanosomiasis. Chagas Disease: One Hundred Years of Research, 844

Tosello Boari, 2012, IL-17RA signaling reduces inflammation and mortality during Trypanosoma cruzi infection by recruiting suppressive IL-10-producing neutrophils, PLoS Pathog., 8, e1002658, 10.1371/journal.ppat.1002658

Vasconcelos, 2013, Administration of granulocyte colony-stimulating factor induces immunomodulation, recruitment of T regulatory cells, reduction of myocarditis and decrease of parasite load in a mouse model of chronic Chagas disease cardiomyopathy, FASEB J., 27, 4691, 10.1096/fj.13-229351

Vincendeau, 2003, Arginases in parasitic diseases, Trends Parasitol., 19, 9, 10.1016/S1471-4922(02)00010-7

Wirth, 1989, Effects of IL-4 on macrophage functions: increased uptake and killing of a protozoan parasite (Trypanosoma cruzi), Immunology, 66, 296

Wynn, 2005, T(H)-17: a giant step from T(H)1 and T(H)2, Nat. Immunol., 6, 1069, 10.1038/ni1105-1069

Zingales, 2009, A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI, Mem. Inst. Oswaldo Cruz, 104, 1051, 10.1590/S0074-02762009000700021

Zingales, 2012, The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications, Infect. Genet. Evol., 12, 240, 10.1016/j.meegid.2011.12.009