Journal of Experimental Medicine, Vol 183, 147-157, Copyright © 1996 by Rockefeller University Press

ARTICLES

The interleukin 12 p40 gene promoter is primed by interferon gamma in monocytic cells

X Ma, JM Chow, G Gri, G Carra, F Gerosa, SF Wolf, R Dzialo and G Trinchieri
Wistar Institute of Anatomy and Biology, Philadelphia, Pennsylvania 19104, USA.

Interleukin (IL) 12 is a proinflammatory cytokine produced by phagocytic cells, B cells, and other antigen-presenting cells that modulates adaptive immune responses by favoring the generation of T helper type 1 cells. IL-12 mediates some of its physiological activities by acting as a potent inducer of interferon (IFN) gamma production by T and natural killer cells. IFN-gamma enhances the ability of the phagocytic cells to produce IL-12 and other proinflammatory cytokines. Thus, IL-12-induced IFN-gamma acts in a positive feedback loop that represents an important amplifying mechanism in the inflammatory response to infections. We show here that IFN-gamma enhances IL-12 production mostly by priming phagocytic cells for lipopolysaccharide (LPS)-induced transcription of the IL-12 p40 gene, which encodes the heavy chain of the IL-12 heterodimer; furthermore, IFN-gamma directly induces transcription of the IL-12 p35 gene, which encodes the light chain of IL-12, and has at least an additive effect with LPS stimulation in inducing its transcription. The priming effect of IFN-gamma on the LPS-induced p40 gene transcription requires preincubation of the cells with IFN-gamma for at least 8 h to obtain a maximal effect. The priming effect of IFN-gamma for IL-12 production is predominantly at the transcriptional level for both the p40 and the p35 gene, and no evidence for a major role of posttranscriptional or translational mechanisms was found. A 3.3-kb human IL-12 p40 promoter construct transfected into cell lines recapitulated the tissue specificity of the endogenous gene, being silent in two human T cell lines, constitutively active in two human Epstein-Barr virus-positive B lymphoblastoid cell lines, and LPS inducible in the human THP-1 and mouse RAW264.7 monocytic cell lines. Because the RAW264.7 cell line is easily transfectable and regulates the endogenous IL-12 p40 gene in response to IFN-gamma or LPS similarly to human monocytes, it was used for analysis of the regulation of the cloned human IL-12 p40 promoter. A requirement for the region between - 222 and -204 in both LPS responsiveness and IFN-gamma priming was established. This region contains an ets consensus sequence that was shown to mediate activation of the promoter by IFN-gamma and LPS, as well as by a cotransfected ets-2. The -222 construct was also regulated in a tissue-specific manner. Two other elements, IRF-1 located at -730 to -719, and NF-IL6 at -520 to -512, were also studied by deletion analysis, which did not result in decreased response to IFN-gamma and LPS stimulation.
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• Godshall, C. J., Lentsch, A. B., Peyton, J. C., Scott, M. J., Cheadle, W. G. (2001). STAT4 Is Required for Antibacterial Defense but Enhances Mortality during Polymicrobial Sepsis. CVI 8: 1044-1048 [Abstract] [Full Text]  
• Qadir, K., Metwali, A., Blum, A. M., Li, J., Elliott, D. E., Weinstock, J. V. (2001). TGF-beta and IL-10 regulation of IFN-gamma produced in Th2-type schistosome granulomas requires IL-12. Am. J. Physiol. Gastrointest. Liver Physiol. 281: G940-G946 [Abstract] [Full Text]  
• Becker, C., Wirtz, S., Ma, X., Blessing, M., Galle, P. R., Neurath, M. F. (2001). Regulation of IL-12 p40 Promoter Activity in Primary Human Monocytes: Roles of NF-{kappa}B, CCAAT/Enhancer-Binding Protein {beta}, and PU.1 and Identification of a Novel Repressor Element (GA-12) That Responds to IL-4 and Prostaglandin E2. J. Immunol. 167: 2608-2618 [Abstract] [Full Text]  
• Wesa, A. K., Galy, A. (2001). IL-1{beta} induces dendritic cells to produce IL-12. Int Immunol 13: 1053-1061 [Abstract] [Full Text]  
• Mattei, F., Schiavoni, G., Belardelli, F., Tough, D. F. (2001). IL-15 Is Expressed by Dendritic Cells in Response to Type I IFN, Double-Stranded RNA, or Lipopolysaccharide and Promotes Dendritic Cell Activation. J. Immunol. 167: 1179-1187 [Abstract] [Full Text]  
• Grohmann, U., Belladonna, M. L., Vacca, C., Bianchi, R., Fallarino, F., Orabona, C., Fioretti, M. C., Puccetti, P. (2001). Positive Regulatory Role of IL-12 in Macrophages and Modulation by IFN-{{gamma}}. J. Immunol. 167: 221-227 [Abstract] [Full Text]  
• Vankayalapati, R., Wizel, B., Lakey, D. L., Zhang, Y., Coffee, K. A., Griffith, D. E., Barnes, P. F. (2001). T Cells Enhance Production of IL-18 by Monocytes in Response to an Intracellular Pathogen. J. Immunol. 166: 6749-6753 [Abstract] [Full Text]  
• Braun, M. C., Wang, J. M., Lahey, E., Rabin, R. L., Kelsall, B. L. (2001). Activation of the formyl peptide receptor by the HIV-derived peptide T-20 suppresses interleukin-12 p70 production by human monocytes. Blood 97: 3531-3536 [Abstract] [Full Text]  
• Grazia Cappiello, M., Sutterwala, F. S., Trinchieri, G., Mosser, D. M., Ma, X. (2001). Suppression of IL-12 Transcription in Macrophages Following Fc{{gamma}} Receptor Ligation. J. Immunol. 166: 4498-4506 [Abstract] [Full Text]  
• Das, L., Datta, N., Bandyopadhyay, S., Das, P. K. (2001). Successful Therapy of Lethal Murine Visceral Leishmaniasis with Cystatin Involves Up-Regulation of Nitric Oxide and a Favorable T Cell Response. J. Immunol. 166: 4020-4028 [Abstract] [Full Text]  
• Tone, M., Tone, Y., Fairchild, P. J., Wykes, M., Waldmann, H. (2001). Regulation of CD40 function by its isoforms generated through alternative splicing. Proc. Natl. Acad. Sci. USA 98: 1751-1756 [Abstract] [Full Text]  
• Walter, M. J., Kajiwara, N., Karanja, P., Castro, M., Holtzman, M. J. (2001). Interleukin 12 p40 Production by Barrier Epithelial Cells during Airway Inflammation. J. Exp. Med. 193: 339-352 [Abstract] [Full Text]  
• Malmgaard, L., Paludan, S. R., Mogensen, S. C., Ellermann-Eriksen, S. (2000). Herpes simplex virus type 2 induces secretion of IL-12 by macrophages through a mechanism involving NF-{kappa}B. J. Gen. Virol. 81: 3011-3020 [Abstract] [Full Text]  
• Sanjabi, S., Hoffmann, A., Liou, H.-C., Baltimore, D., Smale, S. T. (2000). Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc. Natl. Acad. Sci. USA 10.1073/pnas.230436397v1 [Abstract] [Full Text]  
• O’Regan, A. W., Hayden, J. M, Berman, J. S. (2000). Osteopontin augments CD3-mediated interferon-{gamma} and CD40 ligand expression by T cells, which results in IL-12 production from peripheral blood mononuclear cells. J. Leukoc. Biol. 68: 495-502 [Abstract] [Full Text]  
• Thoma-Uszynski, S., Kiertscher, S. M., Ochoa, M. T., Bouis, D. A., Norgard, M. V., Miyake, K., Godowski, P. J., Roth, M. D., Modlin, R. L. (2000). Activation of Toll-Like Receptor 2 on Human Dendritic Cells Triggers Induction of IL-12, But Not IL-10. J. Immunol. 165: 3804-3810 [Abstract] [Full Text]  

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