Abstract
Murine peritoneal macrophages (MPM) can be subdivided into two subpopulations of mature and immature macrophages. In contrast to mature macrophages, immature ones were highly susceptible toTrypanosoma cruzi infection. This high susceptibility was associated with a low production of α2-macroglobulin. Interferon-γ (IFN-γ)-activated immature macrophages also exhibited a higher infection rate than did IFN-γ-activated mature ones. This higher rate of infection was associated with a low production of both nitric oxide (N=O) and tumor necrosis factor-a (TFN-α). In contrast, mature MPM showed a lower rate of infection and produced higher levels of N=O and TFN-α. Taken together, these results show a clear-cut difference in the course ofT. cruzi infection in relation to the macrophage maturation state.
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Alcina A, Fresno M (1987) Activation by synergism between endotoxin and lymphokines of the mouse macrophage cell line J774 against infection byTrypanosoma cruzi. Parasite Immunol 9:175–186
Araujo-Jorge TC (1989) The biology ofTrypanosoma cruzi-macrophage interaction. Mem Inst Oswaldo Cruz 84:441–462
Araujo-Jorge TC, De Meirelles MNL, Isaac S (1990)Trypanosoma cruzi: killing and enhanced uptake by resident peritoneal macrophages treated with alpha-2-macroglobulin. Parasitol Res 76:545–552
Araujo-Jorge TC, Lage MJF, Rivera MT, Carlier Y, Van Leuven F (1992)Trypanosoma cruzi: enhanced alpha-macroglobulin levels correlate with the resistance of BALB/cj mice to acute infection. Parasitol Res 78:215–221
Carlier Y, Rivera MT, Truyens C, Goldman M, Lambert P, Flament J, Bauwens D, Vray B (1987) Pregnancy and humoral immune response in mice chronically infected byTrypanosoma cruzi. Infect Immun 55:2496–2501
Coquette A, Boeynaems JM, Saint-Guillain M, Vray B (1988) Macrophage heterogeneity in prostaglandins and thromboxane synthesis: differential activation by Fc- and C3b-dependent bacterial phagocytosis. Prostaglandins 36:491–505
Eilers A, Seegert D, Schindler C, Baccarini M, Decker T (1993) The response of gamma interferon activation factor is under developmental control in cells of the macrophage lineage. Mol Cell Biol 13:3245–3254
Gazzinelli RT, Oswald IP, Hieny S, James SL, Sher A (1992) Microbicidal activity of IFN-γ treated macrophages againstTrypanosoma cruzi involved anl-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by IL-10 and TGF-β. Eur J Immunol 22:2501–2506
Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and (15N) nitrate in biological fluids. Anal Biochem 126:131–138
Green LM, Reade JL, Ware CF (1984) Rapid colorimetric assay for cell viability: application to the quantitation of cytotoxic and growth inhibitory lymphokines. J Immunol Methods 70:257–268
Green SJ, Crawford M, Hockmeyer JT, Meltzer MS, Nacy CA (1990)Leishmania major amastigotes initiate thel-arginine-dependent killing mechanism in IFN-γ-stimulated macrophages by induction of tumor necrosis factor-α. J Immunol 145:4290–4297
Griess P (1879) Bemerkungen zu der Abhandlung des HH. Weselsky und Benedikt “ueber einige Azoverbindung”. Ber Dtsch Chem Ges 12:426–434
Gutteridge WE, Cover B, Gaborak M (1978) Isolation of blood and intracellular forms ofTrypanosoma cruzi from rats and other rodents and preliminary studies of their metabolism. Parasitology 76:159–176
Isaac L, Pereira M, Santos M, Sampaio EP, Lima NR, Lage MJF, De Meirelles MNL, Araujo-Jorge TC (1990)Trypanosoma cruzi: plasma levels of alpha-2-macroglobulin during experimental murine infections with reticulotropic and myotropic strains. Parasitol Res 76:726–728
Kreutz M, Krause SW, Henneman A, Rehm A, Andreesen R (1992) Macrophage heterogeneity and differentiation: defined serum-free culture conditions induce different types of macrophages in vitro. Res Immunol 143:107–115
Lages-Silva E, Ramirez LE, Krettli AU, Brener Z (1986) Effect of protective and non protective antibodies in the phagocytosis rate ofTrypanosoma cruzi blood forms by mouse peritoneal macrophages. Parasite Immunol 9:21–30
Lanham SM, Godfrey DG (1970) Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp Parasitol 28:521–534
Lucas R, Heirweigh K, Neirynck A, Remels L, Van Heuverswyn H, De Baetselier P (1990) Generation and characterization of a neutralizing rat anti-rm TNF-α monoclonal antibody. Immunology 71:218–223
Metz G, Carlier Y, Vray B (1993)Trypanosoma cruzi infection upregulates nitric oxide production by IFN-γ-preactivated macrophages limiting cell infection, independently of the respiratory burst. Parasite Immunol 15:693–699
Michishita M, Yoshida Y, Uchino H, Nagata K (1990) Induction of tumor necrosis factor-α and its receptors during differentiation in myeloid leukemic cells along the monocytic pathway. J Biol Chem 265:8751–8759
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63
Munoz-Fernandez MA, Fernandez MA, Fresno M (1992) Synergism between tumor necrosis factora and IFN-γ on macrophage activation against intracellularTrypanosoma cruzi through a nitric oxide-dependent mechanism. Eur J Immunol 22:301–307
Nedwin GE, Svedersky LP, Bringman TS, Palladino MA, Goeddel DV (1985) Effect of interleukin 2, interferon gamma, and mitogens on the production of tumor necrosis factors alpha and beta. J Immunol 135:2492–2497
Nelson JAS, Parhar RS, Scordras JM, Lala PK (1990) Characterization of macrophage subsets regulating murine natural killer cell activity. J Leukocyte Biol 48:382–393
Nogueira N (1986) American trypanosomiasis: antigens and host parasite interaction. In: Pearson TW (ed) Parasite antigens. Marcel Dekker, New York, pp 97–110
Pecora IL, Reis GA dos, Barcinski MA, Dorigo DD (1980) Frequency distribution ofTrypanosoma cruzi in macrophages from resistant and susceptible strains of mice. Experientia 36:942–944
Plasma N, Vray B (1993) Mouse peritoneal macrophages: characterization of function l subsets following Percoll density gradients. Res Immunol 144:151–163
Plata F, Wietzerbin J, Pons FG, Falcoff E, Eisen H (1984) Synergistic protection by specific antibodies and interferon against infection byTrypanosoma cruzi in vitro. Eur J Immunol 14:930–935
Saksela O, Hovi T, Vaheri A (1985) Urokinase-type plasminogen activator and its inhibitor secreted by cultured human monocyte-macrophages. J Cell Physiol 122:125–132
Sunderkötter C, Kunz M, Steinbrink K, Meinardus-Hager G, Goebeler M, Bildau H, Sorg C (1993) Resistance of mice to experimental leishmaniasis is associated with more rapid appearance of mature macrophages in vitro and in vivo. J Immunol 151:4891–4901
Tarleton R (1988) Tumor necrosis factor (cachectin) production during experimental Chagas' Disease. Clin Exp Immunol 73:186–190
Van Furth R (1989) Origin and turnover of monocytes and macrophages. In: Ilmar Iversen O (ed) Cell kinetics of the inflammatory reaction. (Current topics in pathology series). Springer, Berlin Heidelberg New York, pp 125–150
Villalta F, Oda LM, Angluster J, Alviano CS, Leon W (1980) Phagocytosis of three developmental forms ofTrypanosoma cruzi: effect of specific sera. Acta Trop (Basel) 38:375–381
Vray B, De Baetselier P, Ouaissi A, Carlier Y (1991)Trypanosoma cruzi but notTrypanosoma brucei fails to induce a chemiluminescent signal in a macrophage hybridoma cell line. Infect Immun 59:3303–3308
Wirth JJ, Kierszenbaum F, Sonnenfeld G, Zlotnik A (1985) Enhancing effects of gamma interferon on phagocytic cell association with and killing ofTrypanosoma cruzi. Infect Immun 49:61–66
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Plasman, N., Metz, G. & Vray, B. Interferon-γ-activated immature macrophages exhibit a highTrypanosoma cruzi infection rate associated with a low production of both nitric oxide and tumor necrosis factor-α. Parasitol Res 80, 554–558 (1994). https://doi.org/10.1007/BF00933002
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DOI: https://doi.org/10.1007/BF00933002