The absence or overexpression of IL-15 drastically alters breast cancer metastasis via effects on NK cells, CD4 T cells, and macrophages

Journal of Immunology

Volumn 193, Issue 12, 2014, Pages 6184-6191

  Gillgrass, Amy ^a   Gill, Navkiran ^a   Babian, Artem ^a   Ashkar, Ali A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; C57BL 6 MOUSE; CANCER CELL; CANCER RESISTANCE; CD4+ T LYMPHOCYTE; CELL POLARITY; CELL TYPE; CONTROLLED STUDY; IMMUNE DEFICIENCY; IN VIVO STUDY; LYMPHOCYTE FUNCTION; MACROPHAGE; MACROPHAGE FUNCTION; METASTASIS; METASTASIS INHIBITION; METASTASIS POTENTIAL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TH2 CELL; TRANSGENIC MOUSE; ANIMAL; BREAST TUMOR; DISEASE MODEL; EXPERIMENTAL MAMMARY NEOPLASM; EXPERIMENTAL MELANOMA; FEMALE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG TUMOR; METABOLISM; PATHOLOGY; SECONDARY;

ANIMALS; BREAST NEOPLASMS; CD4-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; INTERLEUKIN-15; KILLER CELLS, NATURAL; LUNG NEOPLASMS; MACROPHAGES; MAMMARY NEOPLASMS, EXPERIMENTAL; MELANOMA, EXPERIMENTAL; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOPLASM METASTASIS;

EID: 84916898536     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303175     Document Type: Article

References (52)

1. Ranson, T., C. A. Vosshenrich, E. Corcuff, O. Richard, W. Müller, and J. P. Di Santo. 2003. IL-15 is an essential mediator of peripheral NK-cell homeostasis. Blood 101: 4887-4893.
2. Carson, W. E., T. A. Fehniger, S. Haldar, K. Eckhert, M. J. Lindemann, C. F. Lai, C. M. Croce, H. Baumann, and M. A. Caligiuri. 1997. A potential role for interleukin-15 in the regulation of human natural killer cell survival. J. Clin. Invest. 99: 937-943.
3. Judge, A. D., X. Zhang, H. Fujii, C. D. Surh, and J. Sprent. 2002. Interleukin 15 controls both proliferation and survival of a subset of memory-phenotype CD8(+) T cells. J. Exp. Med. 196: 935-946.
4. Nelson, B. H. 2008. The impact of T-cell immunity on ovarian cancer outcomes. Immunol. Rev. 222: 101-116.
5. Marrogi, A. J., A. Munshi, A. J. Merogi, Y. Ohadike, A. El-Habashi, O. L. Marrogi, and S. M. Freeman. 1997. Study of tumor infiltrating lymphocytes and transforming growth factor-beta as prognostic factors in breast carcinoma. Int. J. Cancer 74: 492-501.
6. Blum, D. L., T. Koyama, A. E. M'Koma, J. M. Iturregui, M. Martinez-Ferrer, C. Uwamariya, J. A. Smith, Jr., P. E. Clark, and N. A. Bhowmick. 2008. Chemokine markers predict biochemical recurrence of prostate cancer following prostatectomy. Clin. Cancer Res. 14: 7790-7797.
7. Kobayashi, H., S. Dubois, N. Sato, H. Sabzevari, Y. Sakai, T. A. Waldmann, and Y. Tagaya. 2005. Role of trans-cellular IL-15 presentation in the activation of NK cell-mediated killing, which leads to enhanced tumor immunosurveillance. Blood 105: 721-727.
8. Tang, F., L. T. Zhao, Y. Jiang, D. N. Ba, L. X. Cui, and W. He. 2008. Activity of recombinant human interleukin-15 against tumor recurrence and metastasis in mice. Cell. Mol. Immunol. 5: 189-196.
9. Bessard, A., V. Solé, G. Bouchaud, A. Quéméner, and Y. Jacques. 2009. High antitumor activity of RLI, an interleukin-15 (IL-15)-IL-15 receptor alpha fusion protein, in metastatic melanoma and colorectal cancer. Mol. Cancer Ther. 8: 2736-2745.
10. Martinez, F. O., A. Sica, A. Mantovani, and M. Locati. 2008. Macrophage activation and polarization. Front. Biosci. 13: 453-461.
11. Joyce, J. A., and J. W. Pollard. 2009. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9: 239-252.
12. Mantovani, A., S. Sozzani, M. Locati, P. Allavena, and A. Sica. 2002. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23: 549-555.
13. Stout, R. D., C. Jiang, B. Matta, I. Tietzel, S. K. Watkins, and J. Suttles. 2005. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J. Immunol. 175: 342-349.
14. Sica, A., P. Larghi, A. Mancino, L. Rubino, C. Porta, M. G. Totaro, M. Rimoldi, S. K. Biswas, P. Allavena, and A. Mantovani. 2008. Macrophage polarization in tumour progression. Semin. Cancer Biol. 18: 349-355.
15. Kaplan, R. N., R. D. Riba, S. Zacharoulis, A. H. Bramley, L. Vincent, C. Costa, D. D. MacDonald, D. K. Jin, K. Shido, S. A. Kerns, et al. 2005. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438: 820-827.
16. Hiratsuka, S., A. Watanabe, H. Aburatani, and Y. Maru. 2006. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 8: 1369-1375.
17. Qian, B., and Y. Deng. J. H. Im, R. J. Muschel, Y. Zou, J. Li, R. A. Lang, and J.W. Pollard. 2009. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One 4: e6562.
18. Qian, B. Z., J. Li, H. Zhang, T. Kitamura, J. Zhang, L. R. Campion, E. A. Kaiser, L. A. Snyder, and J. W. Pollard. 2011. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475: 222-225.
19. Tiemessen, M. M., A. L. Jagger, H. G. Evans, M. J. van Herwijnen, S. John, and L. S. Taams. 2007. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc. Natl. Acad. Sci. USA 104: 19446-19451.
20. DeNardo, D. G., J. B. Barreto, P. Andreu, L. Vasquez, D. Tawfik, N. Kolhatkar, and L. M. Coussens. 2009. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 16: 91-102.
21. Chan, T., E. A. Pek, K. Huth, and A. A. Ashkar. 2011. CD4(+) T-cells are important in regulating macrophage polarization in C57BL/6 wild-type mice. Cell. Immunol. 266: 180-186.
22. Savage, N. D., T. de Boer, K. V. Walburg, S. A. Joosten, K. van Meijgaarden, A. Geluk, and T. H. Ottenhoff. 2008. Human anti-inflammatory macrophages induce Foxp3+ GITR+ CD25+ regulatory T cells, which suppress via membrane-bound TGFbeta-1. J. Immunol. 181: 2220-2226.
23. Wang, X., Y. Cui, G. Luo, Q. Wang, J. Hu, W. He, J. Yuan, J. Zhou, Y. Wu, X. Sun, et al. 2012. Activated mouse CD4(+)Foxp3(-) T cells facilitate melanoma metastasis via Qa-1-dependent suppression of NK-cell cytotoxicity. Cell Res. 22: 1696-1706.
24. Tan, W., W. Zhang, A. Strasner, S. Grivennikov, J. Q. Cheng, R. M. Hoffman, and M. Karin. 2011. Tumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKL-RANK signalling. Nature 470: 548-553.
25. Carson, W. E., M. E. Ross, R. A. Baiocchi, M. J. Marien, N. Boiani, K. Grabstein, and M. A. Caligiuri. 1995. Endogenous production of interleukin 15 by activated human monocytes is critical for optimal production of interferon-gamma by natural killer cells in vitro. J. Clin. Invest. 96: 2578-2582.
26. Alleva, D. G., S. B. Kaser, M. A. Monroy, M. J. Fenton, and D. I. Beller. 1997. IL-15 functions as a potent autocrine regulator of macrophage proinflammatory cytokine production: evidence for differential receptor subunit utilization associated with stimulation or inhibition. J. Immunol. 159: 2941-2951.
27. Liu, G., Q. Zhai, D. Schaffner, C. Bradburne, A. Wu, A. Hayford, S. Popov, E. Grene, C. Bailey, and K. Alibek. 2004. IL-15 induces IFN-beta and iNOS gene expression, and antiviral activity of murine macrophage RAW 264.7 cells. Immunol. Lett. 91: 171-178.
28. Rückert, R., K. Brandt, M. Ernst, K. Marienfeld, E. Csernok, C. Metzler, V. Budagian, E. Bulanova, R. Paus, and S. Bulfone-Paus. 2009. Interleukin-15 stimulates macrophages to activate CD4+ T cells: a role in the pathogenesis of rheumatoid arthritis? Immunology 126: 63-73.
29. Seder, R. A. 1996. High-dose IL-2 and IL-15 enhance the in vitro priming of naive CD4+ T cells for IFN-gamma but have differential effects on priming for IL-4. J. Immunol. 156: 2413-2422.
30. Niedbala, W., X. Wei, and F. Y. Liew. 2002. IL-15 induces type 1 and type 2 CD4+ and CD8+ T cells proliferation but is unable to drive cytokine production in the absence of TCR activation or IL-12/IL-4 stimulation in vitro. Eur. J. Immunol. 32: 341-347.
31. Geginat, J., F. Sallusto, and A. Lanzavecchia. 2001. Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4(+) T cells. J. Exp. Med. 194: 1711-1719.
32. Benito-Miguel, M., Y. García-Carmona, A. Balsa, C. Pérez de Ayala, T. Cobo-Ibáñez, E. Martín-Mola, and M. E. Miranda-Carús. 2009. A dual action of rheumatoid arthritis synovial fibroblast IL-15 expression on the equilibrium between CD4+CD25+ regulatory T cells and CD4+CD25- responder T cells. J. Immunol. 183: 8268-8279.
33. Ben Ahmed, M., N. Belhadj Hmida, N. Moes, S. Buyse, M. Abdeladhim, H. Louzir, and N. Cerf-Bensussan. 2009. IL-15 renders conventional lymphocytes resistant to suppressive functions of regulatory T cells through activation of the phosphatidylinositol 3-kinase pathway. J. Immunol. 182: 6763-6770.
34. Chow, K. P., J. M. Lee, J. T. Qiu, S. K. Liao, S. C. Lin, S. L. Hsu, N. N. Wu, Y. F. Lin, and T. S. Wu. 2011. Enhanced IL-10 production by CD4+ T cells primed in IL-15Ra-deficient mice. Eur. J. Immunol. 41: 3146-3156.
35. Kennedy, M. K., M. Glaccum, S. N. Brown, E. A. Butz, J. L. Viney, M. Embers, N. Matsuki, K. Charrier, L. Sedger, C. R. Willis, et al. 2000. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191: 771-780.
36. Fehniger, T. A., K. Suzuki, A. Ponnappan, J. B. VanDeusen, M. A. Cooper, S. M. Florea, A. G. Freud, M. L. Robinson, J. Durbin, and M. A. Caligiuri. 2001. Fatal leukemia in interleukin 15 transgenic mice follows early expansions in natural killer and memory phenotype CD8+ T cells. J. Exp. Med. 193: 219-231.
37. Rubinstein, M. P., M. Kovar, J. F. Purton, J. H. Cho, O. Boyman, C. D. Surh, and J. Sprent. 2006. Converting IL-15 to a superagonist by binding to soluble IL-15Ralpha. Proc. Natl. Acad. Sci. USA 103: 9166-9171.
38. Bergamaschi, C., M. Rosati, R. Jalah, A. Valentin, V. Kulkarni, C. Alicea, G. M. Zhang, V. Patel, B. K. Felber, and G. N. Pavlakis. 2008. Intracellular interaction of interleukin-15 with its receptor alpha during production leads to mutual stabilization and increased bioactivity. J. Biol. Chem. 283: 4189-4199.
39. Srivastava, S., A. Lundqvist, and R. W. Childs. 2008. Natural killer cell immunotherapy for cancer: a new hope. Cytotherapy 10: 775-783.
40. Dorner, B. G., A. Scheffold, M. S. Rolph, M. B. Huser, S. H. Kaufmann, A. Radbruch, I. E. Flesch, and R. A. Kroczek. 2002. MIP-1alpha, MIP-1beta, RANTES, and ATAC/lymphotactin function together with IFN-gamma as type 1 cytokines. Proc. Natl. Acad. Sci. USA 99: 6181-6186.
41. Dorner, B. G., H. R. Smith, A. R. French, S. Kim, J. Poursine-Laurent, D. L. Beckman, J. T. Pingel, R. A. Kroczek, and W. M. Yokoyama. 2004. Coordinate expression of cytokines and chemokines by NK cells during murine cytomegalovirus infection. J. Immunol. 172: 3119-3131.
42. Qian, B. Z., and J. W. Pollard. 2010. Macrophage diversity enhances tumor progression and metastasis. Cell 141: 39-51.
43. Connelly, L., W. Barham, H. M. Onishko, L. Chen, T. P. Sherrill, T. Zabuawala, M. C. Ostrowski, T. S. Blackwell, and F. E. Yull. 2011. NF-kappaB activation within macrophages leads to an anti-tumor phenotype in a mammary tumor lung metastasis model. Breast Cancer Res. 13: R83.
44. Müller, K., S. Bischof, F. Sommer, M. Lohoff, W. Solbach, and T. Laskay. 2003. Differential production of macrophage inflammatory protein 1gamma (MIP-1gamma), lymphotactin, and MIP-2 by CD4(+) Th subsets polarized in vitro and in vivo. Infect. Immun. 71: 6178-6183.
45. Takeda, K., M. Nakayama, M. Sakaki, Y. Hayakawa, M. Imawari, K. Ogasawara, K. Okumura, and M. J. Smyth. 2011. IFN- g production by lung NK cells is critical for the natural resistance to pulmonary metastasis of B16 melanoma in mice. J. Leukoc. Biol. 90: 777-785.
46. Mantovani, A. 2006. Macrophage diversity and polarization: in vivo veritas. Blood 108: 408-409.
47. Lapteva, N., and X. F. Huang. 2010. CCL5 as an adjuvant for cancer immunotherapy. Expert Opin. Biol. Ther. 10: 725-733.
48. Huang, H., F. Li, J. R. Gordon, and J. Xiang. 2002. Synergistic enhancement of antitumor immunity with adoptively transferred tumor-specific CD4+ and CD8+ T cells and intratumoral lymphotactin transgene expression. Cancer Res. 62: 2043-2051.
49. Emtage, P. C., Z. Xing, Y. Wan, A. Zlotnik, F. L. Graham, and J. Gauldie. 2002. Adenoviral-mediated gene transfer of lymphotactin to the lungs of mice and rats results in infiltration and direct accumulation of CD4+, CD8+, and NK cells. J. Interferon Cytokine Res. 22: 573-582.
50. Davies, E., S. Reid, M. F. Medina, B. Lichty, and A. A. Ashkar. 2010. IL-15 has innate anti-tumor activity independent of NK and CD8 T cells. J. Leukoc. Biol. 88: 529-536.
51. Albina, J. E., and J. S. Reichner. 1998. Role of nitric oxide in mediation of macrophage cytotoxicity and apoptosis. Cancer Metastasis Rev. 17: 39-53.
52. Mantovani, A., P. Allavena, A. Sica, and F. Balkwill. 2008. Cancer-related inflammation. Nature 454: 436-444.