Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets

doi:10.1084/jem.169.1.59

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Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets

FP Heinzel, MD Sadick, BJ Holaday, RL Coffman and RM Locksley
Department of Medicine, University of California, San Francisco Medical Center 94143.

We purified poly(A)+ mRNA from the spleen and lymph nodes at designated times after infection with Leishmania major in genetically susceptible BALB/c and resistant C57BL/6 mice. The steady-state levels of IL-2, IFN- gamma, IL-4, and IL-1 beta mRNA were determined using Northern hybridizations. IL-2 mRNA levels in the infected organs of BALB/c and C57BL/6 mice were comparable after infection, but IFN-gamma and IL-4 mRNA levels were reciprocally expressed. Levels of IFN-gamma mRNA in C57BL/6 draining nodes and spleen were significantly greater than in BALB/c mice except at 4 and 6 wk of infection, when splenic IFN-gamma mRNA levels were transiently comparable. In contrast, IL-4 mRNA was apparent only in BALB/c and not in C57BL/6 nodes and spleen. Tissue levels of IL-1 beta mRNA were 10-20-fold greater in BALB/c mice. BALB/c mice were pretreated with GK1.5 mAb, a manipulation that promotes healing of subsequent infection by transiently depleting L3T4+ cells. At 8 wk of infection, by which time lymphoid organs were repopulated with L3T4+ cells, GK1.5-pretreated BALB/c mice produced IFN-gamma, but not IL-4 message. Serum levels of IgE were markedly elevated in infected BALB/c, but not in infected C57BL/6 or GK1.5-pretreated BALB/c mice, consistent with in vivo biologic activity of IL-4 in nonhealing mice. Treatment of infected BALB/c mice with neutralizing anti-IL-4 antibody abolished the elevation of serum IgE and significantly attenuated the progression of disease as assessed by size and ulceration of the lesion, and by reduction in the number of tissue parasites. Both protective and deleterious responses to Leishmania infection have previously been shown to be L3T4+ cell dependent. Our findings are consistent with the differential expansion of protective, IFN-gamma-producing Th1 cells in healing mice, and the expansion of deleterious, IL-4-producing Th2 cells in nonhealing mice. The inverse relationship of IFN-gamma and IL-4 gene expression during leishmaniasis may underlie the divergence of cellular and humoral immunity that occurs during chronic infection with Leishmania and possibly other intracellular parasites.
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Ishikawa, H., Hisaeda, H., Taniguchi, M., Nakayama, T., Sakai, T., Maekawa, Y., Nakano, Y., Zhang, M., Zhang, T., Nishitani, M., Takashima, M., Himeno, K. (2000). CD4+ V{alpha}14 NKT cells play a crucial role in an early stage of protective immunity against infection with Leishmania major. Int Immunol 12: 1267-1274 [Abstract] [Full Text]
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Tanghe, A., Denis, O., Lambrecht, B., Motte, V., van den Berg, T., Huygen, K. (2000). Tuberculosis DNA Vaccine Encoding Ag85A Is Immunogenic and Protective When Administered by Intramuscular Needle Injection but Not by Epidermal Gene Gun Bombardment. Infect. Immun. 68: 3854-3860 [Abstract] [Full Text]
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Jones, D. E., Buxbaum, L. U., Scott, P. (2000). IL-4-Independent Inhibition of IL-12 Responsiveness During Leishmania amazonensis Infection. J. Immunol. 165: 364-372 [Abstract] [Full Text]
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Ohkusu, K., Yoshimoto, T., Takeda, K., Ogura, T., Kashiwamura, S.-i., Iwakura, Y., Akira, S., Okamura, H., Nakanishi, K. (2000). Potentiality of Interleukin-18 as a Useful Reagent for Treatment and Prevention of Leishmania major Infection. Infect. Immun. 68: 2449-2456 [Abstract] [Full Text]
He, J., Gurunathan, S., Iwasaki, A., Ash-Shaheed, B., Kelsall, B. L. (2000). Primary Role for GI Protein Signaling in the Regulation of Interleukin 12 Production and the Induction of T Helper Cell Type 1 Responses. JEM 191: 1605-1610 [Abstract] [Full Text]
Mohrs, M., Holscher, C., Brombacher, F. (2000). Interleukin-4 Receptor Alpha-Deficient BALB/c Mice Show an Unimpaired T Helper 2 Polarization in Response to Leishmania major Infection. Infect. Immun. 68: 1773-1780 [Abstract] [Full Text]
Ribas, A., Butterfield, L. H., Hu, B., Dissette, V. B., Meng, W. S., Koh, A., Andrews, K. J., Lee, M., Amar, S. N., Glaspy, J. A., McBride, W. H., Economou, J. S. (2000). Immune Deviation and Fas-mediated Deletion Limit Antitumor Activity after Multiple Dendritic Cell Vaccinations in Mice. Cancer Res. 60: 2218-2224 [Abstract] [Full Text]
Mukhopadhyay, S., Bhattacharyya, S., Majhi, R., De, T., Naskar, K., Majumdar, S., Roy, S. (2000). Use of an Attenuated Leishmanial Parasite as an Immunoprophylactic and Immunotherapeutic Agent against Murine Visceral Leishmaniasis. CVI 7: 233-240 [Abstract] [Full Text]
Suffia, I., Ferrua, B., Stien, X., Mograbi, B., Marty, P., Rousseau, D., Fragaki, K., Kubar, J. (2000). A Novel Leishmania infantum Recombinant Antigen Which Elicits Interleukin 10 Production by Peripheral Blood Mononuclear Cells of Patients with Visceral Leishmaniasis. Infect. Immun. 68: 630-636 [Abstract] [Full Text]
Vuola, J. M., Puurula, V., Anttila, M., Makela, P. H., Rautonen, N. (2000). Acquired Immunity to Chlamydia pneumoniae Is Dependent on Gamma Interferon in Two Mouse Strains That Initially Differ in This Respect after Primary Challenge. Infect. Immun. 68: 960-964 [Abstract] [Full Text]