Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells

doi:10.1084/jem.176.5.1387

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Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells

A D'Andrea, M Rengaraju, NM Valiante, J Chehimi, M Kubin, M Aste, SH Chan, M Kobayashi, D Young and E Nickbarg
Wistar Institute of Anatomy and Biology, Children's Hospital of Philadelphia, Pennsylvania 19104.

Natural killer cell stimulatory factor (NKSF), or interleukin 12 (IL- 12), is a 70-kD heterodimeric cytokine composed of two covalently linked chains, p40 and p35. NKSF/IL-12 has multiple effects on T and NK cells and was originally identified and purified from the supernatant fluid of Epstein-Barr virus (EBV)-transformed human B lymphoblastoid cell lines. We have produced a panel of monoclonal antibodies against both chains of NKSF/IL-12. Some of these antibodies have neutralizing activity, and several combinations of them have been used to establish sensitive radioimmunoassays detecting the free p40 chain, the free p35 chain, or the p70 heterodimer. Using these reagents, we have determined that most EBV-transformed human B lymphoblastoid cell lines constitutively produce low levels of the p70 heterodimer and an excess of the free p40 chain, whereas Burkitt lymphoma-derived, T, myeloid, and many solid tumor-derived cell lines produce neither. Production of both p40 and p70 is increased several-fold upon stimulation of the EBV- transformed cell lines with phorbol diesters. The ability of supernatant fluids from unstimulated and phorbol diester-stimulated cell lines to induce interferon gamma (IFN-gamma) production from T and NK cells, one of the effects of NKSF/IL-12, parallels the levels of production of the p70 heterodimer, known to be the biologically active form of NKSF/IL-12. Staphylococcus aureus Cowan I strain (SAC) and other stimuli induce accumulation of p40 mRNA and production of both p40 and p70 by peripheral blood mononuclear cells (PBMC). The producer cells appear to include both adherent cells and nonadherent lymphocytes, possibly B cells. The supernatant fluids from SAC- stimulated PBMC mediate the typical functions of NKSF/IL-12 (i.e., IFN- gamma induction, mitogenic effects on T/NK blasts, enhancement of NK cell cytotoxicity) at concentrations of p70 similar to those at which recombinant NKSF/IL-12 mediates the same functions. Moreover, these activities are significantly inhibited by anti-NKSF/IL-12 antibodies. The neutralizing anti-NKSF/IL-12 antibodies also inhibit 85% of the IFN- gamma production in response to SAC, an NKSF/IL-12 inducer, and approximately 50% of the IFN-gamma production in response to non- NKSF/IL-12-inducers such as IL-2, phytohemagglutinin, and anti-CD3 antibodies. These results indicate that induced or constitutively produced NKSF/IL-12 has a major role in facilitating IFN-gamma production by peripheral blood lymphocytes.(ABSTRACT TRUNCATED AT 400 WORDS)
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Wang, K. S., Zorn, E., Ritz, J. (2001). Specific down-regulation of interleukin-12 signaling through induction of phospho-STAT4 protein degradation. Blood 97: 3860-3866 [Abstract] [Full Text]
Maeyama, T., Kuwano, K., Kawasaki, M., Kunitake, R., Hagimoto, N., Hara, N. (2001). Attenuation of bleomycin-induced pneumopathy in mice by monoclonal antibody to interleukin-12. Am. J. Physiol. Lung Cell. Mol. Physiol. 280: L1128-L1137 [Abstract] [Full Text]
Cooper, M. A., Fehniger, T. A., Turner, S. C., Chen, K. S., Ghaheri, B. A., Ghayur, T., Carson, W. E., Caligiuri, M. A. (2001). Human natural killer cells: a unique innate immunoregulatory role for the CD56bright subset. Blood 97: 3146-3151 [Abstract] [Full Text]
Pekkari, K., Avila-Carino, J., Bengtsson, A., Gurunath, R., Scheynius, A., Holmgren, A. (2001). Truncated thioredoxin (Trx80) induces production of interleukin-12 and enhances CD14 expression in human monocytes. Blood 97: 3184-3190 [Abstract] [Full Text]
Hensmann, M., Kwiatkowski, D. (2001). Cellular Basis of Early Cytokine Response to Plasmodium falciparum. Infect. Immun. 69: 2364-2371 [Abstract] [Full Text]
El-Ghrably, I A, Dua, H. S, Orr, G. M, Fischer, D., Tighe, P. J (2001). Intravitreal invading cells contribute to vitreal cytokine milieu in proliferative vitreoretinopathy. Br J Ophthalmol 85: 461-470 [Abstract] [Full Text]
Matsunaga, K., Klein, T. W., Newton, C., Friedman, H., Yamamoto, Y. (2001). Legionella pneumophila Suppresses Interleukin-12 Production by Macrophages. Infect. Immun. 69: 1929-1933 [Abstract] [Full Text]
Matsunaga, K., Klein, T. W., Friedman, H., Yamamoto, Y. (2001). Alveolar Macrophage Cell Line MH-S Is Valuable as an In Vitro Model for Legionella pneumophila Infection. Am. J. Respir. Cell Mol. Bio. 24: 326-331 [Abstract] [Full Text]
Ito, H., Kurtz, J., Shaffer, J., Sykes, M. (2001). CD4 T Cell-Mediated Alloresistance to Fully MHC-Mismatched Allogeneic Bone Marrow Engraftment Is Dependent on CD40-CD40 Ligand Interactions, and Lasting T Cell Tolerance Is Induced by Bone Marrow Transplantation with Initial Blockade of this Pathway. J. Immunol. 166: 2970-2981 [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. JEM 193: 339-352 [Abstract] [Full Text]
Merlin, T., Sing, A., Nielsen, P. J., Galanos, C., Freudenberg, M. A. (2001). Inherited IL-12 Unresponsiveness Contributes to the High LPS Resistance of the Lpsd C57BL/10ScCr Mouse. J. Immunol. 166: 566-573 [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]
Yang, Y.-F., Tomura, M., Ono, S., Hamaoka, T., Fujiwara, H. (2000). Requirement for IFN-{gamma} in IL-12 production induced by collaboration between V{alpha}14+ NKT cells and antigen-presenting cells. Int Immunol 12: 1669-1675 [Abstract] [Full Text]
Infante-Duarte, C., Horton, H. F., Byrne, M. C., Kamradt, T. (2000). Microbial Lipopeptides Induce the Production of IL-17 in Th Cells. J. Immunol. 165: 6107-6115 [Abstract] [Full Text]
Mosca, P. J., Hobeika, A. C., Clay, T. M., Nair, S. K., Thomas, E. K., Morse, M. A., Lyerly, H. K. (2000). A subset of human monocyte-derived dendritic cells expresses high levels of interleukin-12 in response to combined CD40 ligand and interferon-gamma treatment. Blood 96: 3499-3504 [Abstract] [Full Text]
Chakir, H., Camilucci, A. A., Filion, L. G., Webb, J. R. (2000). Differentiation of Murine NK Cells into Distinct Subsets Based on Variable Expression of the IL-12R{beta}2 Subunit. J. Immunol. 165: 4985-4993 [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]
Salkowski, C. A., Thomas, K. E., Cody, M. J., Vogel, S. N. (2000). Impaired IFN-{gamma} Production in IFN Regulatory Factor-1 Knockout Mice During Endotoxemia Is Secondary to a Loss of Both IL-12 and IL-12 Receptor Expression. J. Immunol. 165: 3970-3977 [Abstract] [Full Text]
Hochrein, H., O'Keeffe, M., Luft, T., Vandenabeele, S., Grumont, R. J., Maraskovsky, E., Shortman, K. (2000). Interleukin (Il)-4 Is a Major Regulatory Cytokine Governing Bioactive IL-12 Production by Mouse and Human Dendritic Cells. JEM 192: 823-834 [Abstract] [Full Text]