Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor

doi:10.1084/jem.180.4.1395

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Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor

WE Carson, JG Giri, MJ Lindemann, ML Linett, M Ahdieh, R Paxton, D Anderson, J Eisenmann, K Grabstein and MA Caligiuri
Department of Medicine, Roswell Park Cancer Institute, Buffalo, New York 14263.

Interleukin 15 (IL-15) is a novel cytokine that has recently been cloned and expressed. Whereas it has no sequence homology with IL-2, IL- 15 interacts with components of the IL-2 receptor (IL-2R). In the present study we performed a functional analysis of recombinant IL-15 on phenotypically and functionally distinct populations of highly purified human natural killer (NK) cells. The CD56bright subset of human NK cells constitutively expresses the high affinity IL-2R and exhibits a brisk proliferative response after the binding of picomolar amounts of IL-2. Using a proliferation assay, IL-15 demonstrated a very steep dose-response curve that was distinct from the dose-response curve for IL-2. The proliferative effects of IL-15 could be abrogated by anti-IL-2R beta (p75), but not by anti-IL-2R alpha (p55). The proliferative effects of IL-2 on CD56bright NK cells could be inhibited by both antibodies. CD56dim NK cells express the intermediate affinity IL-2R in the absence of the high affinity IL-2R. Activation of CD56dim NK cells by IL-15 was similar to that of IL-2 as measured by enhanced NK cytotoxic activity, antibody-dependent cellular cytotoxicity, and NK cell production of interferon gamma, tumor necrosis factor alpha, and granulocyte/macrophage colony-stimulating factor. The IL-15-enhanced NK cytotoxic activity could be completely blocked by anti-IL-2R beta monoclonal antibody. The binding of radiolabeled IL-2 and IL-15 to CD56dim NK cells was inhibited in the presence of anti-IL-2R beta. Scatchard analysis of radiolabeled IL-15 and IL-2 binding to NK- enriched human lymphocytes revealed the presence of high and intermediate affinity receptors for both ligands. IL-15 is a ligand that activates human NK cells through components of the IL-2R in a pattern that is similar but not identical to that of IL-2. Unlike IL-2, IL-15 is produced by activated monocytes/macrophages. The discovery of IL-15 may increase our understanding of how monocytes/macrophages participate in the regulation of NK cell function.
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Dunne, J., Lynch, S., O'Farrelly, C., Todryk, S., Hegarty, J. E., Feighery, C., Doherty, D. G. (2001). Selective Expansion and Partial Activation of Human NK Cells and NK Receptor-Positive T Cells by IL-2 and IL-15. J. Immunol. 167: 3129-3138 [Abstract] [Full Text]
Yoshida, H., Kawamoto, H., Santee, S. M., Hashi, H., Honda, K., Nishikawa, S., Ware, C. F., Katsura, Y., Nishikawa, S.-I. (2001). Expression of {alpha}4{beta}7 Integrin Defines a Distinct Pathway of Lymphoid Progenitors Committed to T Cells, Fetal Intestinal Lymphotoxin Producer, NK, and Dendritic Cells. J. Immunol. 167: 2511-2521 [Abstract] [Full Text]
Wuttge, D. M., Eriksson, P., Sirsjo, A., Hansson, G. K., Stemme, S. (2001). Expression of Interleukin-15 in Mouse and Human Atherosclerotic Lesions. Am. J. Pathol. 159: 417-423 [Abstract] [Full Text]
Baldassarre, G., Fedele, M., Battista, S., Vecchione, A., Klein-Szanto, A. J. P., Santoro, M., Waldmann, T. A., Azimi, N., Croce, C. M., Fusco, A. (2001). Onset of natural killer cell lymphomas in transgenic mice carrying a truncated HMGI-C gene by the chronic stimulation of the IL-2 and IL-15 pathway. Proc. Natl. Acad. Sci. USA 10.1073/pnas.141224998v1 [Abstract] [Full Text]
Martin, S. M., Mehta, I. K., Yokoyama, W. M., Thomas, M. L., Lorenz, R. G. (2001). Development of Intestinal Intraepithelial Lymphocytes, NK Cells, and NK 1.1+ T Cells in CD45-Deficient Mice. J. Immunol. 166: 6066-6073 [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]
Ikawa, T., Fujimoto, S., Kawamoto, H., Katsura, Y., Yokota, Y. (2001). Commitment to natural killer cells requires the helix-loop-helix inhibitor Id2. Proc. Natl. Acad. Sci. USA 10.1073/pnas.091537598v1 [Abstract] [Full Text]
Suzuki, K., Nakazato, H., Matsui, H., Hasumi, M., Shibata, Y., Ito, K., Fukabori, Y., Kurokawa, K., Yamanaka, H. (2001). NK cell-mediated anti-tumor immune response to human prostate cancer cell, PC-3: immunogene therapy using a highly secretable form of interleukin-15 gene transfer. J. Leukoc. Biol. 69: 531-537 [Abstract] [Full Text]
Monson, N. L., Fenske, T. J., Wei, S., Okragly, A. J., de Jong, J. L.O., Haak-Frendscho, M., O’Shea, J., Djeu, J., Sondel, P. M. (2001). A p74 common gamma receptor chain isoform facilitates IL-2 and IL-15 responses by the myelomonocytic cell line Tf-1{beta}2. J. Leukoc. Biol. 69: 419-425 [Abstract] [Full Text]
Tateda, K., Moore, T. A., Deng, J. C., Newstead, M. W., Zeng, X., Matsukawa, A., Swanson, M. S., Yamaguchi, K., Standiford, T. J. (2001). Early Recruitment of Neutrophils Determines Subsequent T1/T2 Host Responses in a Murine Model of Legionella pneumophila Pneumonia. J. Immunol. 166: 3355-3361 [Abstract] [Full Text]
Fehniger, T. A., Suzuki, K., Ponnappan, A., VanDeusen, J. B., Cooper, M. A., Florea, S. M., Freud, A. G., Robinson, M. L., Durbin, J., Caligiuri, M. A. (2001). Fatal Leukemia in Interleukin 15 Transgenic Mice Follows Early Expansions in Natural Killer and Memory Phenotype CD8+ T Cells. J. Exp. Med. 193: 219-232 [Abstract] [Full Text]
Joshi, P. C., Zhou, X., Cuchens, M., Jones, Q. (2001). Prostaglandin E2 Suppressed IL-15-Mediated Human NK Cell Function Through Down-Regulation of Common {{gamma}}-Chain. J. Immunol. 166: 885-891 [Abstract] [Full Text]
Agarwal, R., Loganath, A., Roy, A.C., Wong, Y.C., Ng, S.C. (2001). Expression profiles of interleukin-15 in early and late gestational human placenta and in pre-eclamptic placenta. Mol Hum Reprod 7: 97-101 [Abstract] [Full Text]
Umemura, M., Hirose, K., Wajjwalku, W., Nishimura, H., Matsuguchi, T., Gotoh, Y., Takahashi, M., Makino, M., Yoshikai, Y. (2001). Impaired IL-15 production associated with susceptibility of murine AIDS to mycobacterial infection. J. Leukoc. Biol. 69: 138-148 [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]
Fehniger, T. A., Caligiuri, M. A. (2001). Interleukin 15: biology and relevance to human disease. Blood 97: 14-32 [Full Text]
Okada, H., Nakajima, T., Sanezumi, M., Ikuta, A., Yasuda, K., Kanzaki, H. (2000). Progesterone Enhances Interleukin-15 Production in Human Endometrial Stromal Cells in Vitro. J. Clin. Endocrinol. Metab. 85: 4765-4770 [Abstract] [Full Text]