Tumor necrosis factor- alpha synergizes with IFN- gamma in mediating killing of Leishmania major through the induction of nitric oxide.

Liew, F Y; Li, Y; Millott, S

doi:10.4049/jimmunol.145.12.4306

Cited by 523Research on Leishmaniasis StudiesLeprosy Research and TreatmentImmune cells in cancer

Tumor necrosis factor- alpha synergizes with IFN- gamma in mediating killing of Leishmania major through the induction of nitric oxide.

Liew, F Y, Li, Y, Millott, S·1990·The Journal of Immunology

DOI 10.4049/jimmunol.145.12.4306

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Abstract

CBA mice develop cutaneous lesions when infected with Leishmania major. The disease development was significantly reduced by injecting into the lesion a combination of rIFN-gamma and rTNF-alpha. The doses of IFN-gamma and TNF-alpha used were suboptimal in that either cytokine alone did not have any effect. The therapeutic effect of IFN-gamma and TNF-alpha in vivo is reflected in their ability to activate macrophages to kill the intracellular parasites in vitro. The macrophage leishmanicidal activity induced by TNF-alpha and IFN-gamma can be completely inhibited by a specific inhibitor (l-NG monomethyl arginine) of nitric oxide synthesis. There was a direct correlation between the intracellular killing of the parasites and the production of nitric oxide by the macrophages. In contrast, there was no correlation between leishmanicidal activity and superoxide production by macrophages.

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IFNγ co-operates with other TH1 cell cytokines and acts synergistically to enhance their ability to eliminate pathogens.
“It is worth noting that IFNγ co-operates with other TH1 cell cytokines and acts synergistically to enhance their ability to eliminate pathogens31,32.”
From An Omicron-specific, self-amplifying mRNA booster vaccine for COVID-19: a phase 2/3 randomized trial (2024) · cites this paper as [32]

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Sher, A., & Coffman, R. L. (1992) · Annual Review of Immunology · doi:10.1146/annurev.iy.10.040192.002125 · Cited by 841 · see citing works
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Background
Leishmaniasis: Current Status of Vaccine Development
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Background
Leishmaniases of the New World: current concepts and implications for future research
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Role of oxidants in microbial pathophysiology
Miller, R. A., & Britigan, B. E. (1997) · Clinical Microbiology Reviews · doi:10.1128/cmr.10.1.1 · Cited by 577 · see citing works
“By treating murine-activated macrophages in vitro with N-monomethyl-L-arginine, a competitive inhibitor of nitrate and nitrite synthesis from L-arginine, a number of investigators have implicated NO as having microbiostatic and/or microbicidal activity against pathogens such as Cryptococcus neoformans (117), Toxoplasm…”
Background
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Background
Leishmania species: models of intracellular parasitism
Alexander, J. K., Satoskar, A. R., & Russell, D. G. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.18.2993 · Cited by 348 · see citing works
The Importance of Th2 Cytokines in Protective Immunity to Nematodes
Urban, J. F., Madden, K. B., Svetica, A., Cheever, A. W., Trotta, P. P., Gause, W. C., Katona, I. M., & Finkelman, F. D. (1992) · Immunological Reviews · doi:10.1111/j.1600-065x.1992.tb01415.x · Cited by 345 · see citing works
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Background
Immunology of Leishmaniasis
Liew, F. Y., & O’Donnell, C. A. (1993) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(08)60208-0 · Cited by 334 · see citing works
Self-citation
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James, S. L. (1995) · Microbiological Reviews · doi:10.1128/mr.59.4.533-547.1995 · Cited by 357 · see citing works
The Interaction of Leishmania Species with Macrophages
Alexander, J. K., & Russell, D. G. (1992) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(08)60022-6 · Cited by 323 · see citing works
Immunology of tuberculosis and implications in vaccine development
Flynn, J. L. (2003) · Tuberculosis · doi:10.1016/j.tube.2003.08.010 · Cited by 304 · see citing works
Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major.
Stenger, S., Thüring, H., Röllinghoff, M., & Bogdan, C. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.180.3.783 · Cited by 302 · see citing works
The Hamster as a Model of Human Visceral Leishmaniasis: Progressive Disease and Impaired Generation of Nitric Oxide in the Face of a Prominent Th1-Like Cytokine Response
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Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection
Nauciel, C., & Espinasse-Maes, F. (1992) · Infection and Immunity · doi:10.1128/iai.60.2.450-454.1992 · Cited by 283 · see citing works
“A synergistic interaction between IFN--y and TNF-a has been reported in several other studies (14, 22, 26).”
Result
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Flesch, I. E. A., & Kaufmann, S. H. E. (1991) · Infection and Immunity · doi:10.1128/iai.59.9.3213-3218.1991 · Cited by 280 · see citing works
Oxidative Responses of Human and Murine Macrophages During Phagocytosis of Leishmania chagasi
Gantt, K. R., Goldman, T. L., McCormick, M. L., Miller, M. A., Jerônimo, S. M. B., Nascimento, E. T., Britigan, B. E., & Wilson, M. E. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.2.893 · Cited by 278 · see citing works
Parasitic Adaptive Mechanisms in Infection by Leishmania
Cunningham, A. C. (2002) · Experimental and Molecular Pathology · doi:10.1006/exmp.2002.2418 · Cited by 267 · see citing works
Concepts of Fever
Mackowiak, P. A. (1998) · Archives of Internal Medicine · doi:10.1001/archinte.158.17.1870 · Cited by 254 · see citing works
Role of Poly-ADP Ribosyltransferase Activation in the Vascular Contractile and Energetic Failure Elicited by Exogenous and Endogenous Nitric Oxide and Peroxynitrite
Szabó, C., Zingarelli, B., & Salzman, A. L. (1996) · Circulation Research · doi:10.1161/01.res.78.6.1051 · Cited by 247 · see citing works
Kinetoplastid Membrane Protein-11 DNA Vaccination Induces Complete Protection against Both Pentavalent Antimonial-Sensitive and -Resistant Strains of Leishmania donovani That Correlates with Inducible Nitric Oxide Synthase Activity and IL-4 Generation: Evidence for Mixed Th1- and Th2-Like Responses in Visceral Leishmaniasis
Basu, R., Bhaumik, S., Basu, J. M., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.11.7160 · Cited by 244 · see citing works
A possible novel pathway of regulation by murine T helper type‐2 (Th2) cells of a Th1 cell activity via the modulation of the induction of nitric oxide synthase on macrophages
Liew, F. Y., Li, Y., Severn, A., Millott, S. M., Schmidt, J., Salter, M., & Moncada, S. (1991) · European Journal of Immunology · doi:10.1002/eji.1830211027 · Cited by 222 · see citing works
Self-citation
Effects of cytokines on intracellular growth of Brucella abortus
Jiang, X., & Baldwin, C. L. (1993) · Infection and Immunity · doi:10.1128/iai.61.1.124-134.1993 · Cited by 224 · see citing works
Pro- and anti-inflammatory cytokines in cutaneous leishmaniasis: a review
Maspi, N., Abdoli, A., & Ghaffarifar, F. (2016) · Pathogens and Global Health · doi:10.1080/20477724.2016.1232042 · Cited by 225 · see citing works
Cytokine profile and pathology in human leishmaniasis
Ribeiro-de-Jesus, A., de Almeida, R. P., Lessa, H. A., et al. (1998) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x1998000100020 · Cited by 219 · see citing works
Inducible nitric oxide synthase activity of cloned murine microglial cells
Corradin, S. B., Mauël, J., Donini, S. D., Quattrocchi, E., & Ricciardi‐Castagnoli, P. (1993) · Glia · doi:10.1002/glia.440070309 · Cited by 216 · see citing works
The arginine‐nitric oxide pathway: A target for new drugs
Kerwin, J. F., & Heller, M. (1994) · Medicinal Research Reviews · doi:10.1002/med.2610140103 · Cited by 204 · see citing works
Resistance to Leishmania major infection correlates with the induction of nitric oxide synthase in murine macrophages
Liew, F. Y., Li, Y., Moss, D., Parkinson, C., Rogers, M. V., & Moncada, S. (1991) · European Journal of Immunology · doi:10.1002/eji.1830211216 · Cited by 197 · see citing works
Self-citation
Differential induction of nitric oxide synthase in various organs of the mouse during endotoxaemia: role of TNF-alpha and IL-1-beta.
Cunha, F. Q., Assreuy, J., Moss, D. W., Rees, D. D., Leal, L. M. C. C., Moncada, S., CARRIER, M. J., O'Donnell, C. A., & Liew, F. Y. (1994) · PubMed Central · Cited by 192 · see citing works
Self-citation
Rapidly Fatal Leishmaniasis in Resistant C57BL/6 Mice Lacking TNF
Wilhelm, P., Ritter, U., Labbow, S., Donhauser, N., Röllinghoff, M., Bogdan, C., & Körner, H. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.6.4012 · Cited by 184 · see citing works
Decreased In Situ Expression of Interleukin-10 Receptor Is Correlated with the Exacerbated Inflammatory and Cytotoxic Responses Observed in Mucosal Leishmaniasis
de Faria, D. R., Gollob, K. J., Barbosa, J., et al. (2005) · Infection and Immunity · doi:10.1128/iai.73.12.7853-7859.2005 · Cited by 186 · see citing works
Polyfunctional CD4+ T Cells As Targets for Tuberculosis Vaccination
Lewinsohn, D. A., Lewinsohn, D. M., & Scriba, T. J. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01262 · Cited by 176 · see citing works
“major infection (19, 20), which in turn is associated with enhanced control of disease by the combination of IFN-γ and TNF-α in the murine model (20).”
Background
The Role of Nitric Oxide and Reactive Oxygen Species in the Killing of Leishmania braziliensis by Monocytes from Patients with Cutaneous Leishmaniasis
Carneiro, P. P., Conceição, J., Macedo, M. N., Magalhães, V., Carvalho, E. M., & Bacellar, O. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148084 · Cited by 179 · see citing works
“In murine systems, IFN-γ has been shown to synergize with TNF, to activate inducible nitric oxide synthase (iNOS or NOS2) to produce nitric oxide (NO) resulting in eradication of intracellular parasites [11, 12].”
Background
Peroxynitrite: A two-faced metabolite of nitric oxide
Muijsers, R. B. R., Folkerts, G., Henricks, P. A. J., Sadeghi-Hashjin, G., & Nijkamp, F. P. (1997) · Life Sciences · doi:10.1016/s0024-3205(96)00651-0 · Cited by 176 · see citing works
Induction of Inducible Nitric Oxide Synthase-NO· by Lipoarabinomannan ofMycobacterium tuberculosisIs Mediated by MEK1-ERK, MKK7-JNK, and NF-κB Signaling Pathways
Chan, E. D., Morris, K. R., Belisle, J. T., Hill, P. J., Remigio, L. K., Brennan, P. J., & Riches, D. W. H. (2001) · Infection and Immunity · doi:10.1128/iai.69.4.2001-2010.2001 · Cited by 171 · see citing works
Treatment with Albendazole for Intestinal Disease Due to Enterocytozoon bieneusi in Patients with AIDS
Dieterich, D. T., Lew, E. A., Kotler, D. P., Poles, M. A., & Orenstein, J. M. (1994) · Journal of Infectious Diseases · doi:10.1093/infdis/169.1.178 · Cited by 170 · see citing works
The Role of Nitric Oxide in Inflammation
Lyons, C. R. (1995) · Advances in immunology · doi:10.1016/s0065-2776(08)60589-1 · Cited by 169 · see citing works
Convergence of TNF and IFN signalling pathways through synergistic induction of IRF-1/ISGF-2 is mediated by a composite GAS/ B promoter element
Pine, R. I. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.21.4346 · Cited by 164 · see citing works
Blockade of endogenous TNF-alpha exacerbates primary and secondary pulmonary histoplasmosis by differential mechanisms.
Allendoerfer, R., & Deepe, G. S. (1998) · PubMed · Cited by 164 · see citing works
From mouse to man: safety, immunogenicity and efficacy of a candidate leishmaniasis vaccine LEISH‐F3+GLA‐SE
Coler, R. N., Duthie, M. S., Hofmeyer, K. A., Guderian, J., Jayashankar, L., Vergara, J., Rolf, T., Misquith, A., Laurance, J. D., Raman, V. S., et al. (2015) · Clinical & Translational Immunology · doi:10.1038/cti.2015.6 · Cited by 163 · see citing works
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Saio, M., Radoja, S., Marino, M., & Frey, A. B. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.10.5583 · Cited by 157 · see citing works
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Allendoerfer, R., & Deepe, G. S. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.12.6072 · Cited by 156 · see citing works
Nitric oxide: An overview
Rodeberg, D. A., Chaet, M. S., Bass, R. C., Arkovitz, M. S., & Garcia, V. F. (1995) · The American Journal of Surgery · doi:10.1016/s0002-9610(05)80017-0 · Cited by 154 · see citing works
Type 2 Diabetes Mellitus and Altered Immune System Leading to Susceptibility to Pathogens, Especially Mycobacterium tuberculosis
Ferlita, S., Yegiazaryan, A., Noori, N., Lal, G., Nguyen, T. K., To, K., & Venketaraman, V. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8122219 · Cited by 151 · see citing works
“TNF-α also works in synergy with IFN-γ to induce nitric oxide production [33].”
Background
Recruitment of CD8+ T cells expressing granzyme A is associated with lesion progression in human cutaneous leishmaniasis
de Faria, D. R., Souza, P. E. A., Durães, F. V., Carvalho, E. M., Gollob, K. J., Machado, P. R. L., & Dutra, W. O. (2009) · Parasite Immunology · doi:10.1111/j.1365-3024.2009.01125.x · Cited by 142 · see citing works
Evaluation of Immunomodulatory Effects of Lactic Acid Bacteria in Turbot (Scophthalmus maximus)
Villamil, L., Tafalla, C., Figueras, A. J., & Novoa, B. (2002) · Clinical and Vaccine Immunology · doi:10.1128/cdli.9.6.1318-1323.2002 · Cited by 142 · see citing works
Evaluation of the role of mitogen-activated protein kinases in the expression of inducible nitric oxide synthase by IFN-gamma and TNF-alpha in mouse macrophages.
Chan, E. D., Winston, B. W., Uh, S., Wynes, M. W., Rose, D. M., & Riches, D. W. H. (1999) · PubMed · Cited by 139 · see citing works
Role of inorganic nitrogen oxides and tumor necrosis factor alpha in killing Leishmania donovani amastigotes in gamma interferon-lipopolysaccharide-activated macrophages from Lshs and Lshr congenic mouse strains
Roach, T. I. A., Kiderlen, A. F., & Blackwell, J. M. (1991) · Infection and Immunity · doi:10.1128/iai.59.11.3935-3944.1991 · Cited by 138 · see citing works
TNF-Mediated Restriction of Arginase 1 Expression in Myeloid Cells Triggers Type 2 NO Synthase Activity at the Site of Infection
Schleicher, U., Paduch, K., Debus, A., Obermeyer, S., König, T., Kling, J. C., Ribechini, E., Dudziak, D., Mougiakakos, D., Murray, P. J., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.001 · Cited by 136 · see citing works
“…1 T helper (Th1) cells and the expression of NOS2, which are strictly required for the resolution of Leishmania infections (Diefenbach et al., 1998; Liew et al., 1990), were preserved in Tnf / mice (Wilhelm et al., 2001), leading to interest in identifying the mechanism that underlies the…”
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Gilles, P. N., Guerrette, D. L., Ulevitch, R. J., Schreiber, R. D., & Chisari, F. V. (1992) · Hepatology · doi:10.1002/hep.1840160308 · Cited by 133 · see citing works
Immune privilege in sites of chronic infection: Leishmania and regulatory T cells
Peters, N. C., & Sacks, D. L. (2006) · Immunological Reviews · doi:10.1111/j.1600-065x.2006.00432.x · Cited by 132 · see citing works
Matrix-M adjuvant enhances antibody, cellular and protective immune responses of a Zaire Ebola/Makona virus glycoprotein (GP) nanoparticle vaccine in mice
Bengtsson, K. L., Song, H., Stertman, L., et al. (2016) · Vaccine · doi:10.1016/j.vaccine.2016.02.033 · Cited by 131 · see citing works
Induction of cystine transport activity in mouse peritoneal macrophages by bacterial lipopolysaccharide
Sato, H., Fujiwara, K., Sagara, J., & Bannai, S. (1995) · Biochemical Journal · doi:10.1042/bj3100547 · Cited by 128 · see citing works
Attenuation of Lung Inflammation and Fibrosis in Interferon-γ –Deficient Mice after Intratracheal Bleomycin
Chen, E. S., Greenlee, B. M., Wills-Karp, M. A., & Möller, D. R. (2001) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.24.5.4064 · Cited by 125 · see citing works
Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates.
Naotunne, T. D. S., Karunaweera, N. D., Mendis, K., & Carter, R. (1993) · PubMed Central · Cited by 125 · see citing works
Evaluation of the Role of Mitogen-Activated Protein Kinases in the Expression of Inducible Nitric Oxide Synthase by IFN-γ and TNF-α in Mouse Macrophages
Chan, E. D., Winston, B. W., Uh, S., Wynes, M. W., Rose, D. M., & Riches, D. W. H. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.1.415 · Cited by 125 · see citing works
Successful Therapy of Lethal Murine Visceral Leishmaniasis with Cystatin Involves Up-Regulation of Nitric Oxide and a Favorable T Cell Response
Das, L., Datta, N., Bandyopadhyay, S. K., & Das, P. K. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.6.4020 · Cited by 123 · see citing works
Tumor Necrosis Factor and Lymphotoxin
Beyaert, R., & Fiers, W. (1998) · Elsevier eBooks · doi:10.1016/b978-012498340-3/50025-7 · Cited by 119 · see citing works
Anti-TGF-beta treatment promotes rapid healing of Leishmania major infection in mice by enhancing in vivo nitric oxide production.
Li, J., Hunter, C. A., & Farrell, J. P. (1999) · PubMed · Cited by 120 · see citing works
Expression and Bactericidal Activity of Nitric Oxide Synthase inBrucella suis-Infected Murine Macrophages
Gross, A., Spiesser, S., Terraza, A., Rouot, B., Caron, E., & Dornand, J. (1998) · Infection and Immunity · doi:10.1128/iai.66.4.1309-1316.1998 · Cited by 119 · see citing works
Macrophages as host, effector and immunoregulatory cells in leishmaniasis: Impact of tissue micro-environment and metabolism
Bogdan, C. (2020) · Cytokine X · doi:10.1016/j.cytox.2020.100041 · Cited by 113 · see citing works
Differential mechanisms of intracellular killing ofMycobacterium aviumandListeria monocytogenesby activated human and murine macrophages. The role of nitric oxide
Bermudez, L. E. (1993) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.1993.tb05895.x · Cited by 118 · see citing works
Low dose TGF-beta attenuates IL-12 responsiveness in murine Th cells.
Gorham, J. D., Guler, M. L., Fenoglio, D., Gubler, U., & MURPHY, K. M. M. (1998) · PubMed · Cited by 116 · see citing works
Identification of a Novel GTPase, the Inducibly Expressed GTPase, That Accumulates in Response to Interferon γ
Taylor, G. A., Jeffers, M., Largaespada, D. A., Jenkins, N. A., Copeland, N. G., & Woude, G. F. V. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.34.20399 · Cited by 116 · see citing works
Th1 CD4+ lymphocytes delete activated macrophages through the Fas/APO-1 antigen pathway.
Ashany, D., Song, X., Lacy, E., et al. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.24.11225 · Cited by 115 · see citing works
In Vivo Blockage of Nitric Oxide with Aminoguanidine Inhibits Immunosuppression Induced by an Attenuated Strain ofSalmonella typhimurium, PotentiatesSalmonellaInfection, and Inhibits Macrophage and Polymorphonuclear Leukocyte Influx into the Spleen
MacFarlane, A. S., Schwacha, M. G., & Eisenstein, T. K. (1999) · Infection and Immunity · doi:10.1128/iai.67.2.891-898.1999 · Cited by 114 · see citing works
Neutralization of gamma interferon and tumor necrosis factor alpha blocks in vivo synthesis of nitrogen oxides from L-arginine and protection against Francisella tularensis infection in Mycobacterium bovis BCG-treated mice
Green, S. J., Nacy, C. A., Schreiber, R. D., Granger, D. L., Crawford, R. M., Meltzer, M. S., & Fortier, A. H. (1993) · Infection and Immunity · doi:10.1128/iai.61.2.689-698.1993 · Cited by 109 · see citing works
SIR2-Deficient Leishmania infantum Induces a Defined IFN-γ/IL-10 Pattern That Correlates with Protection
Silvestre, R., Cordeiro‐da‐Silva, A., Santarém, N., Vergnes, B., Séréno, D., & Ouaissi, A. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.5.3161 · Cited by 110 · see citing works
Visceral Leishmaniasis in Mice Devoid of Tumor Necrosis Factor and Response to Treatment
Murray, H. W., Jungbluth, A., Ritter, E., et al. (2000) · Infection and Immunity · doi:10.1128/iai.68.11.6289-6293.2000 · Cited by 110 · see citing works
The role of protein kinase C in the induction of nitric oxide synthesis by murine macrophages
Severn, A., Wakelam, M. J. O., & Liew, F. Y. (1992) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(92)91330-s · Cited by 109 · see citing works
Self-citation
Defective localization of the NADPH phagocyte oxidase to Salmonella -containing phagosomes in tumor necrosis factor p55 receptor-deficient macrophages
Vázquez‐Torres, A., Fantuzzi, G., Edwards, C. K., Dinarello, C. A., & Fang, F. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.041618998 · Cited by 107 · see citing works
Salivary gland material from the sand fly Lutzomyia longipalpis has an inhibitory effect on macrophage function in vitro
Theodos, C. M., & Titus, R. G. (1993) · Parasite Immunology · doi:10.1111/j.1365-3024.1993.tb00634.x · Cited by 108 · see citing works
Collective nitric oxide production provides tissue-wide immunity during Leishmania infection
Olekhnovitch, R., Ryffel, B., Müller, A. J., & Bousso, P. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72058 · Cited by 102 · see citing works
Chlamydia muridarumT-Cell Antigens Formulated with the Adjuvant DDA/TDB Induce Immunity against Infection That Correlates with a High Frequency of Gamma Interferon (IFN-γ)/Tumor Necrosis Factor Alpha and IFN-γ/Interleukin-17 Double-Positive CD4+T Cells
Yu, H. B., Jiang, X., Shen, C., Karunakaran, K. P., Jiang, J., Rosin, N. L., & Brunham, R. C. (2010) · Infection and Immunity · doi:10.1128/iai.01374-09 · Cited by 100 · see citing works
“TNF is another effector cytokine produced by Th1 cells that can mediate control of intracellular infection, including that due to Chlamydia (23, 30, 35).”
Background
Cloning, characterization and overexpression of two iron superoxide dismutase cDNAs from Leishmania chagasi: role in pathogenesis1Note: L.c.FeSODA and L.c.SODB cDNA sequences have been assigned EMBL/GenBank™ data base accession numbers AF003964 and AF003963, respectively.1,2Note: A previous article on this same topic entitled `Molecular cloning, characterization and expression in Escherichia coli of iron superoxide dismutase cDNA from Leishmania donovani chagasi' by Ismail et al. which was published in Infect Immun 1994;62:657–664 has been retracted.2
Paramchuk, W. J., Ismail, S. O., Bhatia, A., & Gedamu, L. (1997) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(97)00141-2 · Cited by 100 · see citing works
Further Evidence of the Presence of Constitutive and Inducible Nitric Oxide Synthase Isoforms in Human Platelets
Chen, L., & Mehta, J. L. (1996) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199601000-00024 · Cited by 100 · see citing works
Anti-TGF-β Treatment Promotes Rapid Healing of Leishmania major Infection in Mice by Enhancing In Vivo Nitric Oxide Production
Li, J., Hunter, C. A., & Farrell, J. P. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.2.974 · Cited by 99 · see citing works
Role of the NF-κB Signaling Pathway and κBcis-Regulatory Elements on theIRF-1andiNOSPromoter Regions in Mycobacterial Lipoarabinomannan Induction of Nitric Oxide
Morris, K. R., Lutz, R. D., Choi, H.-S., Kamitani, T., Chmura, K., & Chan, E. D. (2003) · Infection and Immunity · doi:10.1128/iai.71.3.1442-1452.2003 · Cited by 98 · see citing works
Role of nitric oxide in Sjögren's syndrome
Konttinen, Y. T., Platts, L. A. M., Tuominen, S., Eklund, K. K., Santavirta, N., Törnwall, J., Sorsa, T. A., Hukkanen, M., & Polak, J. M. (1997) · Arthritis & Rheumatism · doi:10.1002/art.1780400515 · Cited by 98 · see citing works
Low Dose TGF-β Attenuates IL-12 Responsiveness in Murine Th Cells
Gorham, J. D., Guler, M. L., Fenoglio, D., Gubler, U., & MURPHY, K. M. M. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.4.1664 · Cited by 98 · see citing works
Analgesic and anti-inflammatory effects ofMangifera indica L. extract (Vimang)
Garrido, G., Gonz�lez, D., Delporte, C. L., Backhouse, N., Quintero, G., Sellés, A. J. N., & Morales, M. A. (2001) · Phytotherapy Research · doi:10.1002/1099-1573(200102)15:1 · Cited by 167 · see citing works
Cytokines: Making the right choice
Finkelman, F. D., & Urban, J. F. (1992) · Parasitology Today · doi:10.1016/0169-4758(92)90105-b · Cited by 97 · see citing works
Mycolactone-Mediated Inhibition of Tumor Necrosis Factor Production by Macrophages Infected with<i>Mycobacterium ulcerans</i>Has Implications for the Control of Infection
Torrado, E., Adusumilli, S., Fraga, A. G., Small, P. L. C., Castro, A. G., & Pedrosa, J. (2007) · Infection and Immunity · doi:10.1128/iai.00290-07 · Cited by 95 · see citing works
“From studies in the mouse model, it is known that TNF is required to upregulate the macrophage bactericidal mechanisms, particularly in concert with IFN- (7, 24, 52).”
Background
Tumor necrosis factor alpha augments nitric oxide-dependent macrophage cytotoxicity against Entamoeba histolytica by enhanced expression of the nitric oxide synthase gene
Lin, J., Seguin, R. M., Keller, K., et al. (1994) · Infection and Immunity · doi:10.1128/iai.62.5.1534-1541.1994 · Cited by 95 · see citing works
“vated macrophages, has been shown to be a potent mediator of the immune response against parasitic infection (15), such as those caused by Plasmodium yoelii (30), Leishmania major (18-20, 31), Toxoplasma gondii (2), Trypanosoma cruzi (33), and Schistosoma mansoni (16).”
Background
Targeted Delivery of IFNγ to Tumor Vessels Uncouples Antitumor from Counterregulatory Mechanisms
Curnis, F., Gasparri, A. M., Sacchi, A., Cattaneo, A., Magni, F., & Corti, A. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4282 · Cited by 94 · see citing works
Potentiality of Interleukin-18 as a Useful Reagent for Treatment and Prevention ofLeishmania majorInfection
Ohkusu, K., Yoshimoto, T., Takeda, K., et al. (2000) · Infection and Immunity · doi:10.1128/iai.68.5.2449-2456.2000 · Cited by 94 · see citing works

Nitric oxide :principles and actions
Lancaster, J. R. (1996) · Cited by 283 · see citing works
Selective Fluorescent Activation for Bioimaging the Expression of Nitric Oxide in Cellular and In Vivo Systems
Zhang, J., & Hong, H. (2010) · Methods in molecular biology · doi:10.1007/978-1-61737-964-2_5 · Cited by 2 · see citing works
Multifunctional role of nitric oxide in inflammation
Laskin, J. D., Heck, D. E., & Laskin, D. L. (1994) · Trends in Endocrinology and Metabolism · doi:10.1016/1043-2760(94)90105-8 · Cited by 109 · see citing works
Intestinal Preconditioning Is Mediated by a Transient Increase in Nitric Oxide
Hotter, G., Closa, D., Prados, M., et al. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.0692 · Cited by 183 · see citing works
Real-Time Measurement of Murine Hippocampus NO Levels in Response to Cerebral Ischemia/Reperfusion
Zheng, X., Liu, K., & Yang, Y. (2010) · Methods in molecular biology · doi:10.1007/978-1-61737-964-2_6 · Cited by 4 · see citing works

Authors: Liew, F. Y., Li, Y., & Millott, S.
Affiliations: Wellcome Trust (GB)
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 1990-12
Volume: 145
Issue: 12
Pages: 4306-4310
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.145.12.4306
OpenAlex: W1739247159
Cited by: 522
References: 0
Citations by year: 2026: 1 · 2025: 5 · 2024: 5 · 2023: 9 · 2022: 10 · 2021: 9 · 2020: 16 · 2019: 7 · 2018: 14 · 2017: 16 · 2016: 11 · 2015: 13 · 2014: 21 · 2013: 16 · 2012: 15
FWCI: 37.31
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Research on Leishmaniasis Studies
Health Sciences › Medicine › Infectious Diseases › Leprosy Research and Treatment
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords: Leishmania major, cutaneous leishmaniasis, TNF-α, interferon-gamma, nitric oxide, macrophage activation, antileishmanial activity, L-NG-monomethylarginine, superoxide, cytokine synergy
MeSH terms: Animals, Arginine, Cytotoxicity, Immunologic, Drug Synergism, Hydrogen Peroxide, Immunity, Cellular, Interferon-gamma, Leishmania tropica, Leishmaniasis, Macrophages, Mice, Inbred CBA, Nitric Oxide, Nitrites, Superoxides, Tumor Necrosis Factor-alpha, omega-N-Methylarginine, Mice

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Tumor necrosis factor- alpha synergizes with IFN- gamma in mediating killing of Leishmania major through the induction of nitric oxide.

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