IL-15 has innate anti-tumor activity independent of NK and CD8 T cells

Journal of Leukocyte Biology

Volumn 88, Issue 3, 2010, Pages 529-536

  Davies, Elizabeth ^a   Reid, Sarah ^a   Medina, Maria Fe ^a   Lichty, Brian ^a   Ashkar, Ali A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Cytokine; Immunity; Immunotherapy; Melanoma; Mouse model

Indexed keywords

ADENOVIRUS VECTOR; COMPLEMENTARY DNA; FLUOROURACIL; INTERLEUKIN 12; INTERLEUKIN 15; RAG2 PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DNA TRANSFECTION; ELECTROPORATION; INTRACELLULAR SIGNALING; LUNG ALVEOLUS MACROPHAGE; LYMPHOCYTE DEPLETION; MELANOMA; METASTASIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; TISSUE CULTURE;

ADAPTIVE IMMUNITY; ADENOVIRIDAE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL COUNT; CELL LINE, TUMOR; DNA-BINDING PROTEINS; HUMANS; IMMUNITY, INNATE; IMMUNOGLOBULIN GAMMA-CHAINS; INTERLEUKIN-12; INTERLEUKIN-15; KILLER CELLS, NATURAL; LUNG; MACROPHAGES; MELANOMA; MICE; MICE, INBRED C57BL; NITRIC OXIDE; PHENOTYPE; SIGNAL TRANSDUCTION;

ADENOVIRIDAE; MUS;

EID: 77957108904     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0909648     Document Type: Article

References (38)

1. Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J., Schreiber, R. D. (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3, 991-998. (Pubitemid 35363648)
2. Yokoyama, W. M., Scalzo, A. A. (2002) Natural killer cell activation receptors in innate immunity to infection. Microbes Infect. 4, 1513-1521. (Pubitemid 36050820)
3. Moretta, L., Bottino, C., Pende, D., Mingari, M. C., Biassoni, R., Moretta, A. (2002) Human natural killer cells: their origin, receptors and function. Eur. J. Immunol. 32, 1205-1211. (Pubitemid 34546247)
4. Wu, J., Lanier, L. L. (2003) Natural killer cells and cancer. Adv. Cancer Res. 90, 127-156.
5. Kennedy, M. K., Glaccum, M., Brown, S. N., Butz, E. A., Viney, J. L., Embers, M., Matsuki, N., Charrier, K., Sedger, L., Willis, C. R., K. Brasel, Morrissey, P. J., Stocking, K., Schuh, J. C., Joyce, S., Peschon, J. J. (2000) Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191, 771-780.
6. Lodolce, J. P., Boone, D. L., Chai, S., Swain, R. E., Dassopoulos, T., Trettin, S., Ma, A. (1998) IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9, 669-676. (Pubitemid 28557595)
7. Schluns, K. S., Nowak, E. C., Cabrera-Hernandez, A., Puddington, L., Lefrancois, L., Aguila, H. L. (2004) Distinct cell types control lymphoid sub-set development by means of IL-15 and IL-15 receptor α expression. Proc. Natl. Acad. Sci. USA 101, 5616-5621.
8. Koka, R., Burkett, P. R., Chien, M., Chai, S., Chan, F., Lodolce, J. P., Boone, D. L., Ma, A. (2003) Interleukin (IL)-15R[α]-deficient natural killer cells survive in normal but not IL-15R[α]-deficient mice. J. Exp. Med. 197, 977-984. (Pubitemid 36523195)
9. Sandau, M. M., Schluns, K. S., Lefrancois, L., Jameson, S. C. (2004) Cutting edge: transpresentation of IL-15 by bone marrow-derived cells necessitates expression of IL-15 and IL-15Rα by the same cells. J. Immunol. 173, 6537-6541. (Pubitemid 39541036)
10. Kokaji, A. I., Hockley, D. L., Kane, K. P. (2008) IL-15 transpresentation augments CD8+ T cell activation and is required for optimal recall responses by central memory CD8+ T cells. J. Immunol. 180, 4391-4401.
11. Rowley, J., Monie, A., Hung, C. F., Wu, T. C. (2008) Inhibition of tumor growth by NK1.1+ cells and CD8+ T cells activated by IL-15 through receptor β/common γ signaling in trans. J. Immunol. 181, 8237-8247.
12. Epardaud, M., Elpek, K. G., Rubinstein, M. P., Yonekura, A. R., Bellemare-Pelletier, A., Bronson, R., Hamerman, J. A., Goldrath, A. W., Turley, S. J. (2008) Interleukin-15/interleukin-15R α complexes promote destruction of established tumors by reviving tumor-resident CD8+ T cells. Cancer Res. 68, 2972-2983.
13. Dubois, S., Patel, H. J., Zhang, M., Waldmann, T. A., Muller, J. R. (2008) Preassociation of IL-15 with IL-15R α-IgG1-Fc enhances its activity on proliferation of NK and CD8+/CD44high T cells and its antitumor action. J. Immunol. 180, 2099-2106.
14. Teague, R. M., Sather, B. D., Sacks, J. A., Huang, M. Z., Dossett, M. L., Morimoto, J., Tan, X., Sutton, S. E., Cooke, M. P., Ohlen, C., Greenberg, P. D. (2006) Interleukin-15 rescues tolerant CD8+ T cells for use in adoptive immunotherapy of established tumors. Nat. Med. 12, 335-341.
15. Ohteki, T. (2002) Critical role for IL-15 in innate immunity. Curr. Mol. Med. 2, 371-380. (Pubitemid 35452885)
16. Liu, G., Zhai, Q., Schaffner, D., Bradburne, C., Wu, A., Hayford, A., Popov, S., Grene, E., Bailey, C., Alibek, K. (2004) IL-15 induces IFN-β and iNOS gene expression, and antiviral activity of murine macrophage RAW 264.7 cells. Immunol. Lett. 91, 171-178. (Pubitemid 38296376)
17. Yanagita, M., Shimabukuro, Y., Nozaki, T., Yoshimura, N., Watanabe, J., Koide, H., Terakura, M., Saho, T., Takedachi, M., Jang, M. H., Kiyono, H., Murakami, S. (2002) IL-15 up-regulates iNOS expression and NO production by gingival epithelial cells. Biochem. Biophys. Res. Commun. 297, 329-334. (Pubitemid 35216174)
18. Umemura, M., Nishimura, H., Hirose, K., Matsuguchi, T., Yoshikai, Y. (2001) Overexpression of IL-15 in vivo enhances protection against Mycobacterium bovis bacillus Calmette-Guerin infection via augmentation of NK and T cytotoxic 1 responses. J. Immunol. 167, 946-956.
19. Fehniger, T. A., Suzuki, K., VanDeusen, J. B., Cooper, M. A., Freud, A. G., Caligiuri, M. A. (2001) Fatal leukemia in interleukin-15 transgenic mice. Blood Cells Mol. Dis. 27, 223-230. (Pubitemid 32299778)
20. Yajima, T., Nishimura, H., Wajjwalku, W., Harada, M., Kuwano, H., Yoshikai, Y. (2002) Overexpression of interleukin-15 in vivo enhances antitumor activity against MHC class I-negative and -positive malignant melanoma through augmented NK activity and cytotoxic T-cell response. Int. J. Cancer 99, 573-578. (Pubitemid 34461611)
21. Kobayashi, H., Dubois, S., Sato, N., Sabzevari, H., Sakai, Y., Waldmann, T. A., Tagaya, Y. (2005) The role of trans-cellular IL-15 presentation in the activation of NK-mediated killing, which leads to enhanced tumor immunesurveillance. Blood 105, 721-727. (Pubitemid 40070758)
22. Mirandola, P., Ponti, C., Gobbi, G., Sponzilli, I., Vaccarezza, M., Cocco, L., Zauli, G., Secchiero, P., Manzoli, F. A., Vitale, M. (2004) Activated human NK and CD8+ T cells express both TNF-related apoptosis-inducing ligand (TRAIL) and TRAIL receptors but are resistant to TRAIL-mediated cytotoxicity. Blood 104, 2418-2424.
23. Gill, N., Paltser, G., Ashkar, A. A. (2009) Interleukin-15 expression affects homeostasis and function of B cells through NK cell-derived interferon-γ. Cell. Immunol. 258, 59-64.
24. Kutzler, M. A., Robinson, T. M., Chattergoon, M. A., Choo, D. K., Choo, A. Y., Choe, P. Y., Ramanathan, M. P., Parkinson, R., Kudchodkar, S., Tamura, Y., Sidhu, M., Roopchand, V., Kim, J. J., Pavlakis, G. N., Felber, B. K., Waldmann, T. A., Boyer, J. D., Weiner, D. B. (2005) Coimmunization with an optimized IL-15 plasmid results in enhanced function and longevity of CD8 T cells that are partially independent of CD4 T cell help. J. Immunol. 175, 112-123.
25. Ugen, K. E., Kutzler, M. A., Marrero, B., Westover, J., Coppola, D., Weiner, D. B., Heller, R. (2006) Regression of subcutaneous B16 melanoma tumors after intratumoral delivery of an IL-15-expressing plasmid followed by in vivo electroporation. Cancer Gene Ther. 13, 969-974. (Pubitemid 44373797)
26. Berard, M., Brandt, K., Bulfone-Paus, S., Tough, D. F. (2003) IL-15 promotes the survival of naive and memory phenotype CD8+ T cells. J. Immunol. 170, 5018-5026. (Pubitemid 36554732)
27. Weng, N. P., Liu, K., Catalfamo, M., Li, Y., Henkart, P. A. (2002) IL-15 is a growth factor and an activator of CD8 memory T cells. Ann. N. Y. Acad. Sci. 975, 46-56. (Pubitemid 36131113)
28. Wherry, E. J., Becker, T. C., Boone, D., Kaja, M. K., Ma, A., Ahmed, R. (2002) Homeostatic proliferation but not the generation of virus specific memory CD8 T cells is impaired in the absence of IL-15 or IL-15Rα. Adv. Exp. Med. Biol. 512, 165-175. (Pubitemid 35335203)
29. Becker, T. C., Wherry, E. J., Boone, D., Murali-Krishna, K., Antia, R., Ma, A., Ahmed, R. (2002) Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J. Exp. Med. 195, 1541-1548. (Pubitemid 34666068)
30. Ashkar, A. A., Black, G. P., Wei, Q., He, H., Liang, L., Head, J. R., Croy, B. A. (2003) Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J. Immunol. 171, 2937-2944. (Pubitemid 37093515)
31. Gosselin, J., Tomolu, A., Gallo, R. C., Flamand, L. (1999) Interleukin-15 as an activator of natural killer cell-mediated antiviral response. Blood 94, 4210-4219.
32. Mingari, M. C., Vitale, C., Cantoni, C., Bellomo, R., Ponte, M., Schiavetti, F., Bertone, S., Moretta, A., Moretta, L. (1997) Interleukin-15-induced maturation of human natural killer cells from early thymic precursors: selective expression of CD94/NKG2-A as the only HLA class I-specific inhibitory receptor. Eur. J. Immunol. 27, 1374-1380.
33. Farag, S. S., Caligiuri, M. A. (2006) Human natural killer cell development and biology. Blood Rev. 20, 123-137. (Pubitemid 43786166)
34. Carson, W., Caligiuri, M. A. (1998) Interleukin-15 as a potential regulator of the innate immune response. Braz. J. Med. Biol. Res. 31, 1-9. (Pubitemid 128524605)
35. Perera, L. P. (2000) Interleukin 15: its role in inflammation and immunity. Arch. Immunol. Ther. Exp. (Warsz.) 48, 457-464.
36. Waldmann, T. (2002) The contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for the immunotherapy of rheumatological diseases. Arthritis Res. 4 (Suppl. 3), S161-S167.
37. Alpdogan, O., van den Brink, M. R. (2005) IL-7 and IL-15: therapeutic cytokines for immunodeficiency. Trends Immunol. 26, 56-64. (Pubitemid 40051993)
38. Tagaya, Y., Bamford, R. N., DeFilippis, A. P., Waldmann, T. A. (1996) IL-15: a pleiotropic cytokine with diverse receptor/signaling pathways whose expression is controlled at multiple levels. Immunity 4, 329-336.