Resolution of cutaneous leishmaniasis: interleukin 12 initiates a protective T helper type 1 immune response

doi:10.1084/jem.177.6.1797

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Resolution of cutaneous leishmaniasis: interleukin 12 initiates a protective T helper type 1 immune response

JP Sypek, CL Chung, SE Mayor, JM Subramanyam, SJ Goldman, DS Sieburth, SF Wolf and RG Schaub
Department of Preclinical Biology, Genetics Institute, Inc., Cambridge, Massachusetts 02140.

Resistance to Leishmania major in mice is associated with the appearance of distinct T helper type 1 (Th1) and Th2 subsets. T cells from lymph nodes draining cutaneous lesions of resistant mice are primarily interferon gamma (IFN-gamma)-producing Th1 cells. In contrast, T cells from susceptible mice are principally Th2 cells that generate interleukin 4 (IL-4). Although existing evidence is supportive of a role for IFN-gamma in the generation of Th1 cells, additional factors may be required for a protective response to be maintained. A potential candidate is IL-12, a heterodimeric cytokine produced by monocytes and B cells that has multiple effects on T and natural killer cell function, including inducing IFN-gamma production. Using an experimental leishmanial model we have observed that daily intraperitoneal administration at the time of parasite challenge of either 0.33 micrograms IL-12 (a consecutive 5 d/wk for 5 wk) or 1.0 micrograms IL-12 per mouse (only a consecutive 5 d) caused a > 75% reduction in parasite burden at the site of infection, in highly susceptible BALB/c mice. Delay of treatment by 1 wk had less of a protective effect. Concomitant with these protective effects was an increase in IFN-gamma and a decrease in IL-4 production, as measured by enzyme-linked immunosorbent assay of supernatants generated from popliteal lymph node cells stimulated with leishmanial antigen in vitro. The reduction in parasite numbers induced by IL-12 therapy was still apparent at 10 wk postinfection. In addition, we observed that the administration of a rabbit anti-recombinant murine IL-12 polyclonal antibody (200 micrograms i.p. every other day for 25 d) at the time of infection to resistant C57Bl/6 mice exacerbated disease. These effects were accompanied by a shift in IFN-gamma production in vitro by antigen- stimulated lymph node cells indicative of a Th2-like response. These findings suggest that IL-12 has an important role in initiating a Th1 response and protective immunity.
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Walker, P. S., Scharton-Kersten, T., Krieg, A. M., Love-Homan, L., Rowton, E. D., Udey, M. C., Vogel, J. C. (1999). Immunostimulatory oligodeoxynucleotides promote protective immunity and provide systemic therapy for leishmaniasis via IL-12- and IFN-gamma -dependent mechanisms. Proc. Natl. Acad. Sci. USA 96: 6970-6975 [Abstract] [Full Text]
Elloso, M. M., Scott, P. (1999). Expression and Contribution of B7-1 (CD80) and B7-2 (CD86) in the Early Immune Response to Leishmania major Infection. J. Immunol. 162: 6708-6715 [Abstract] [Full Text]
Manca, C., Tsenova, L., Barry, C. E. III, Bergtold, A., Freeman, S., Haslett, P. A. J., Musser, J. M., Freedman, V. H., Kaplan, G. (1999). Mycobacterium tuberculosis CDC1551 Induces a More Vigorous Host Response In Vivo and In Vitro, But Is Not More Virulent Than Other Clinical Isolates. J. Immunol. 162: 6740-6746 [Abstract] [Full Text]
Schopf, L. R., Bliss, J. L., Lavigne, L. M., Chung, C. L., Wolf, S. F., Sypek, J. P. (1999). Interleukin-12 Is Capable of Generating an Antigen-Specific Th1-Type Response in the Presence of an Ongoing Infection-Driven Th2-Type Response. Infect. Immun. 67: 2166-2171 [Abstract] [Full Text]
Cousens, L. P., Peterson, R., Hsu, S., Dorner, A., Altman, J. D., Ahmed, R., Biron, C. A. (1999). Two Roads Diverged: Interferon alpha /beta - and Interleukin 12-mediated Pathways in Promoting T Cell Interferon gamma �Responses during Viral Infection. J. Exp. Med. 189: 1315-1328 [Abstract] [Full Text]
Babik, J. M., Adams, E., Tone, Y., Fairchild, P. J., Tone, M., Waldmann, H. (1999). Expression of Murine IL-12 Is Regulated by Translational Control of the p35 Subunit. J. Immunol. 162: 4069-4078 [Abstract] [Full Text]
Guler, M. L., Gorham, J. D., Dietrich, W. F., Murphy, T. L., Steen, R. G., Parvin, C. A., Fenoglio, D., Grupe, A., Peltz, G., Murphy, K. M. (1999). Tpm1, a Locus Controlling IL-12 Responsiveness, Acts by a Cell-Autonomous Mechanism. J. Immunol. 162: 1339-1347 [Abstract] [Full Text]
Bushell, A., Niimi, M., Morris, P. J., Wood, K. J. (1999). Evidence for Immune Regulation in the Induction of Transplantation Tolerance: A Conditional but Limited Role for IL-4. J. Immunol. 162: 1359-1366 [Abstract] [Full Text]
Gabaglia, C. R., Pedersen, B., Hitt, M., Burdin, N., Sercarz, E. E., Graham, F. L., Gauldie, J., Braciak, T. A. (1999). A Single Intramuscular Injection with an Adenovirus- Expressing IL-12 Protects BALB/c Mice Against Leishmania major Infection, While Treatment with an IL-4-Expressing Vector Increases Disease Susceptibility in B10.D2 Mice. J. Immunol. 162: 753-760 [Abstract] [Full Text]
Oxenius, A., Karrer, U., Zinkernagel, R. M., Hengartner, H. (1999). IL-12 Is Not Required for Induction of Type 1 Cytokine Responses in Viral Infections. J. Immunol. 162: 965-973 [Abstract] [Full Text]
Li, J., Hunter, C. A., Farrell, J. P. (1999). Anti-TGF-{beta} Treatment Promotes Rapid Healing of Leishmania major Infection in Mice by Enhancing In Vivo Nitric Oxide Production. J. Immunol. 162: 974-979 [Abstract] [Full Text]
Alexander, J, Satoskar, A., Russell, D. (1999). Leishmania species: models of intracellular parasitism. J. Cell Sci. 112: 2993-3002 [Abstract]
Marinaro, M., Boyaka, P. N., Jackson, R. J., Finkelman, F. D., Kiyono, H., Jirillo, E., McGhee, J. R. (1999). Use of Intranasal IL-12 to Target Predominantly Th1 Responses to Nasal and Th2 Responses to Oral Vaccines Given with Cholera Toxin. J. Immunol. 162: 114-121 [Abstract] [Full Text]
Alexander, J., Coombs, G. H., Mottram, J. C. (1998). Leishmania mexicana Cysteine Proteinase-Deficient Mutants Have Attenuated Virulence for Mice and Potentiate a Th1 Response. J. Immunol. 161: 6794-6801 [Abstract] [Full Text]
Wilson, M. E., Young, B. M., Davidson, B. L., Mente, K. A., McGowan, S. E. (1998). The Importance of TGF-{beta} in Murine Visceral Leishmaniasis. J. Immunol. 161: 6148-6155 [Abstract] [Full Text]
Skeiky, Y. A. W., Kennedy, M., Kaufman, D., Borges, M. M., Guderian, J. A., Scholler, J. K., Ovendale, P. J., Picha, K. S., Morrissey, P. J., Grabstein, K. H., Campos-Neto, A., Reed, S. G. (1998). LeIF: A Recombinant Leishmania Protein That Induces an IL-12-Mediated Th1 Cytokine Profile. J. Immunol. 161: 6171-6179 [Abstract] [Full Text]
Silva, R. A., Pais, T. F., Appelberg, R. (1998). Evaluation of IL-12 in Immunotherapy and Vaccine Design in Experimental Mycobacterium avium Infections. J. Immunol. 161: 5578-5585 [Abstract] [Full Text]
Gurunathan, S., Irvine, K. R., Wu, C.-Y., Cohen, J. I., Thomas, E., Prussin, C., Restifo, N. P., Seder, R. A. (1998). CD40 Ligand/Trimer DNA Enhances Both Humoral and Cellular Immune Responses and Induces Protective Immunity to Infectious and Tumor Challenge. J. Immunol. 161: 4563-4571 [Abstract] [Full Text]
Hoffmann, K. F., Caspar, P., Cheever, A. W., Wynn, T. A. (1998). IFN-{gamma}, IL-12, and TNF-{alpha} Are Required to Maintain Reduced Liver Pathology in Mice Vaccinated with Schistosoma mansoni Eggs and IL-12. J. Immunol. 161: 4201-4210 [Abstract] [Full Text]
Michailowsky, V., Murta, S. M.�F., Carvalho-Oliveira, L., Pereira, M. E.�S., Ferreira, L. R.�P., Brener, Z., Romanha, A. J., Gazzinelli, R. T. (1998). Interleukin-12 Enhances In Vivo Parasiticidal Effect of Benznidazole during Acute Experimental Infection with a Naturally Drug-Resistant Strain of Trypanosoma cruzi. Antimicrob. Agents Chemother. 42: 2549-2556 [Abstract] [Full Text]