NK cells from malignant pleural effusions are not anergic but produce cytokines and display strong antitumor activity on short-term IL-2 activation

European Journal of Immunology

Volumn 43, Issue 2, 2013, Pages 550-561

  Vacca, Paola ^a   Martini, Stefania ^b   Garelli, Valentina ^a,b   Passalacqua, Giovanni ^a,b   Moretta, Lorenzo ^c   Mingari, Maria Cristina ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c G GASLINI INSTITUTE   (Italy)

Author keywords

Cancer; Immune response; Immunotherapy; NK cells; Tumor immunology

Indexed keywords

CD56 ANTIGEN; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; INTERLEUKIN 2; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLADDER CANCER; BREAST CANCER; CANCER CHEMOTHERAPY; CLINICAL ARTICLE; COLON CANCER; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOLYSIS; FEMALE; HUMAN; LUNG CANCER; LYMPHOID CELL; MALE; MESOTHELIOMA; METASTASIS; NATURAL KILLER CELL; PHENOTYPE; PLEURA EFFUSION; PRIORITY JOURNAL; STOMACH CANCER; T LYMPHOCYTE; TUMOR CELL LINE; UTERUS CARCINOMA;

AGED; AGED, 80 AND OVER; ANTIGENS, CD56; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CELL LINE, TUMOR; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-2; KILLER CELLS, NATURAL; LIGANDS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MALE; MIDDLE AGED; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PLEURAL EFFUSION, MALIGNANT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84873750822     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242783     Document Type: Article

References (46)

1. Fridman, W. H., Mlecnik, B., Bindea, G., Pages, F. and Galon, J., Immunosurveillance in human non-viral cancers. Curr. Opin. Immunol. 2011. 23: 272-278.
2. Lee, P. P., Yee, C., Savage, P. A., Fong, L., Brockstedt, D., Weber, J. S., Johnson, D. et al., Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat. Med. 1999. 5: 677-685.
3. Fridman, W. H., Galon, J., Pages, F., Tartour, E., Sautes-Fridman, C. and Kroemer, G., Prognostic and predictive impact of intra- and peritumoral immune infiltrates. Cancer Res. 2011. 71: 5601-5605.
4. Sutlu, T. and Alici, E., Natural killer cell-based immunotherapy in cancer: current insights and future prospects. J. Intern. Med. 2009. 266: 154-181.
5. Bleakley, M. and Riddell, S. R., Exploiting T cells specific for human minor histocompatibility antigens for therapy of leukemia. Immunol. Cell Biol. 2011. 89: 396-407.
6. Locatelli, F., Vinti, L., Palumbo, G., Rossi, F., Bertaina, A., Mastronuzzi, A., Bernardo, M. E. et al., Strategies to optimize the outcome of children given T-cell depleted HLA-haploidentical hematopoietic stem cell transplantation. Best Pract. Res. Clin. Haematol. 2011. 24: 339-349.
7. Moretta, L., Locatelli, F., Pende, D., Sivori, S., Falco, M., Bottino, C., Mingari, M. C. et al., Human NK receptors: from the molecules to the therapy of high risk leukemias. FEBS Lett. 2011. 585: 1563-1567.
8. Moretta, L., Locatelli, F., Pende, D., Marcenaro, E., Mingari, M. C. and Moretta, A., Killer Ig-like receptor-mediated control of natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Blood 2011. 117: 764-771.
9. Den Otter, W., Jacobs, J. J., Battermann, J. J., Hordijk, G. J., Krastev, Z., Moiseeva, E. V., Stewart, R. J. et al., Local therapy of cancer with free IL-2. Cancer Immunol. Immunother. 2008. 57: 931-950.
10. Rabinovich, G. A., Gabrilovich, D. and Sotomayor, E. M., Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol. 2007. 25: 267-296.
11. Balsamo, M., Scordamaglia, F., Pietra, G., Manzini, C., Cantoni, C., Boitano, M., Queirolo, P. et al., Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity. Proc. Natl. Acad. Sci. USA 2009. 106: 20847-20852.
12. Gritsenko, P. G., Ilina, O. and Friedl, P., Interstitial guidance of cancer invasion. J. Pathol. 2012. 226: 185-199.
13. Ljunggren, H. G. and Malmberg, K. J., Prospects for the use of NK cells in immunotherapy of human cancer. Nat. Rev. Immunol. 2007. 7: 329-339.
14. Moretta, A., Bottino, C., Vitale, M., Pende, D., Biassoni, R., Mingari, M. C. and Moretta, L., Receptors for HLA class-I molecules in human natural killer cells. Annu. Rev. Immunol. 1996. 14: 619-648.
15. Moretta, A., Bottino, C., Vitale, M., Pende, D., Cantoni, C., Mingari, M. C., Biassoni, R. et al., Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 2001. 19: 197-223.
16. Bottino, C., Castriconi, R., Pende, D., Rivera, P., Nanni, M., Carnemolla, B., Cantoni, C. et al., Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J. Exp. Med. 2003. 198: 557-567.
17. Lanier, L. L., NK cell recognition. Annu. Rev. Immunol. 2005. 23: 225-274.
18. Caligiuri, M. A., Human natural killer cells. Blood 2008. 112: 461-469.
19. De Maria, A., Bozzano, F., Cantoni, C. and Moretta, L., Revisiting human natural killer cell subset function revealed cytolytic CD56(dim)CD16+ NK cells as rapid producers of abundant IFN-gamma on activation. Proc. Natl. Acad. Sci. USA 2011. 108: 728-732.
20. Fauriat, C., Long, E. O., Ljunggren, H. G. and Bryceson, Y. T., Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 2010. 115: 2167-2176.
21. Moretta, L., Ferlazzo, G., Bottino, C., Vitale, M., Pende, D., Mingari, M. C. and Moretta, A., Effector and regulatory events during natural killer-dendritic cell interactions. Immunol. Rev. 2006. 214: 219-228.
22. Martin-Fontecha, A., Thomsen, L. L., Brett, S., Gerard, C., Lipp, M., Lanzavecchia, A. and Sallusto, F., Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 2004. 5: 1260-1265.
23. Vivier, E., Raulet, D. H., Moretta, A., Caligiuri, M. A., Zitvogel, L., Lanier, L. L., Yokoyama, W. M. et al., Innate or adaptive immunity? The example of natural killer cells. Science 2011. 331: 44-49.
24. Carrega, P., Morandi, B., Costa, R., Frumento, G., Forte, G., Altavilla, G., Ratto, G. B. et al., Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(-) cells and display an impaired capability to kill tumor cells. Cancer 2008. 112: 863-875.
25. Atkins, M. B., Lotze, M. T., Dutcher, J. P., Fisher, R. I., Weiss, G., Margolin, K., Abrams, J. et al., High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J. Clin. Oncol. 1999. 17: 2105-2116.
26. Mamessier, E., Sylvain, A., Thibult, M. L., Houvenaeghel, G., Jacquemier, J., Castellano, R., Goncalves, A. et al., Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J. Clin. Invest. 2011. 121: 3609-3622.
27. Mamessier, E., Sylvain, A., Bertucci, F., Castellano, R., Finetti, P., Houvenaeghel, G., Charaffe-Jaufret, E. et al., Human breast tumor cells induce self-tolerance mechanisms to avoid NKG2D-mediated and DNAM-mediated NK cell recognition. Cancer Res. 2011. 71: 6621-6632.
28. Li, H., Han, Y., Guo, Q., Zhang, M. and Cao, X., Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J. Immunol. 2009. 182: 240-249.
29. Pietra, G., Manzini, C., Rivara, S., Vitale, M., Cantoni, C., Petretto, A., Balsamo, M. et al., Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity. Cancer Res. 2012. 72: 1407-1415.
30. McGilvray, R. W., Eagle, R. A., Watson, N. F., Al-Attar, A., Ball, G., Jafferji, I., Trowsdale, J. et al., NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clin. Cancer Res. 2009. 15: 6993-7002.
31. Le Maux Chansac, B., Moretta, A., Vergnon, I., Opolon, P., Lecluse, Y., Grunenwald, D., Kubin, M. et al., NK cells infiltrating a MHC class I-deficient lung adenocarcinoma display impaired cytotoxic activity toward autologous tumor cells associated with altered NK cell-triggering receptors. J. Immunol. 2005. 175: 5790-5798.
32. Carlsten, M., Norell, H., Bryceson, Y. T., Poschke, I., Schedvins, K., Ljunggren, H. G., Kiessling, R. et al., Primary human tumor cells expressing CD155 impair tumor targeting by down-regulating DNAM-1 on NK cells. J. Immunol. 2009. 183: 4921-4930.
33. Dalbeth, N., Gundle, R., Davies, R. J., Lee, Y. C., McMichael, A. J. and Callan, M. F., CD56bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J. Immunol. 2004. 173: 6418-6426.
34. Shevach, E. M., From vanilla to 28 flavors: multiple varieties of T regulatory cells. Immunity 2006. 25: 195-201.
35. Annunziato, F., Cosmi, L., Santarlasci, V., Maggi, L., Liotta, F., Mazzinghi, B., Parente, E. et al., Phenotypic and functional features of human Th17 cells. J. Exp. Med. 2007. 204: 1849-1861.
36. Ye, Z. J., Zhou, Q., Gu, Y. Y., Qin, S. M., Ma, W. L., Xin, J. B., Tao, X. N. et al., Generation and differentiation of IL-17-producing CD4+ T cells in malignant pleural effusion. J. Immunol. 2010. 185: 6348-6354.
37. Trinchieri, G., Biology of natural killer cells. Adv. Immunol. 1989. 47: 187-376.
38. Vivier, E., Tomasello, E., Baratin, M., Walzer, T. and Ugolini, S., Functions of natural killer cells. Nat. Immunol. 2008. 9: 503-510.
39. Mantovani, A., Allavena, P., Sica, A. and Balkwill, F., Cancer-related inflammation. Nature 2008. 454: 436-444.
40. Moretta, A., Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat. Rev. Immunol. 2002. 2: 957-964.
41. Dewan, M. Z., Terunuma, H., Takada, M., Tanaka, Y., Abe, H., Sata, T., Toi, M. et al., Role of natural killer cells in hormone-independent rapid tumor formation and spontaneous metastasis of breast cancer cells in vivo. Breast Cancer Res. Treat. 2007. 104: 267-275.
42. Coca, S., Perez-Piqueras, J., Martinez, D., Colmenarejo, A., Saez, M. A., Vallejo, C., Martos, J. A. et al., The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 1997. 79: 2320-2328.
43. Ishigami, S., Natsugoe, S., Tokuda, K., Nakajo, A., Che, X., Iwashige, H., Aridome, K. et al., Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 2000. 88: 577-583.
44. Smyth, M. J., Teng, M. W., Swann, J., Kyparissoudis, K., Godfrey, D. I. and Hayakawa, Y., CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer. J. Immunol. 2006. 176: 1582-1587.
45. Lee, J. C., Lee, K. M., Kim, D. W. and Heo, D. S., Elevated TGF-beta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J. Immunol. 2004. 172: 7335-7340.
46. Madjd, Z., Spendlove, I., Moss, R., Bevin, S., Pinder, S. E., Watson, N. F., Ellis, I. et al., Upregulation of MICA on high-grade invasive operable breast carcinoma. Cancer Immun. 2007. 7: 17.