Melanoma cells become resistant to NK-cell-mediated killing when exposed to NK-cell numbers compatible with NK-cell infiltration in the tumor

European Journal of Immunology

Volumn 42, Issue 7, 2012, Pages 1833-1842

  Balsamo, Mirna ^a   Vermi, William ^b   Parodi, Monica ^c   Pietra, Gabriella ^c   Manzini, Claudia ^c   Queirolo, Paola ^d   Lonardi, Silvia ^b   Augugliaro, Raffaella ^d   Moretta, Alessandro ^c,e   Facchetti, Fabio ^b   Moretta, Lorenzo ^a   Mingari, Maria Cristina ^c,d,e   Vitale, Massimo ^d  

^a G GASLINI INSTITUTE   (Italy)

^b Servizio di Anatomia Patologica   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

^e Centro di Eccellenza per la Ricerca Biomedica   (Italy)

Author keywords

Cytokines; HLA I molecules; Melanoma; NK cells; Tumor escape

Indexed keywords

GAMMA INTERFERON; HLA ANTIGEN CLASS 1; INTERLEUKIN 2; NATURAL KILLER CELL RECEPTOR NKG2D;

ARTICLE; CELL INFILTRATION; CELL KILLING; COCULTURE; CYTOKINE RELEASE; CYTOLYSIS; DOWN REGULATION; HISTOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; MELANOMA CELL; NATURAL KILLER CELL; OUTCOME ASSESSMENT; PHENOTYPE; PRIORITY JOURNAL; TUMOR; TUMOR LOCALIZATION;

ANIMALS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-15; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MELANOMA;

EID: 84864003859     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201142179     Document Type: Article

References (51)

1. Smyth, M. J., Thia, K. Y. T., Street, S. E. A., Cretney, E., Trapani, J. A., Taniguchi, M., Kawano, T. et al., Differential tumor surveillance by natural killer and NKT cells. J. Exp. Med. 2000. 191: 661-668.
2. Kim, S., Iizuka, K., Aguila, H. L., Weissman, I. L. and Yokoyama, W. M., In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc. Natl. Acad. Sci. USA 2000. 97: 2731-2736.
3. Imai, K., Matsuyama, S., Miyake, S., Suga, K. and Nakachi, K., Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 2000. 356: 1795-1799.
4. Lakshmikanth, T., Burke, S., Ali, T. H., Kimpfler, S., Ursini, F., Ruggeri, L., Capanni, M. et al., NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo. J. Clin. Invest. 2009. 119: 1251-1263.
5. Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W. D., Tosti, A., Posati, S. et al., Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002. 295: 2097-3000.
6. 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.
7. Vivier, E., Tomasello, E., Baratin, M., Walzer, T. and Ugolini, S., Functions of natural killer cells. Nat. Immunol. 2008. 9: 503-510.
8. Moretta, A., Marcenaro, E., Sivori, S., Della Chiesa, M., Vitale, M. and Moretta, L., Early liaisons between cells of the innate immune system in inflamed peripheral tissues. Trends Immunol. 2005. 26: 668-675.
9. Caligiuri, M. A., Human natural killer cells. Blood 2008. 112: 461-469.
10. Bellora, F., Castriconi, R., Dondero, A., Reggiardo, G., Moretta, L., Mantovani, A., Moretta, A.et al., The interaction of human natural killer cells with either unpolarized or polarized macrophages results in different functional outcomes. Proc. Natl. Acad. Sci. USA 2010. 107: 21659-21664.
11. Bottino, C., Moretta, L., Pende, D., Vitale, M. and Moretta, A., Learning how to discriminate between friends and enemies, a lesson from natural killer cells. Mol. Immunol. 2004. 41: 569-575.
12. Lanier, L. L., NK cell recognition. Annu. Rev. Immunol. 2005. 23: 225-274.
13. Bryceson, Y. T., March, M. E., Ljunggren, H. G. and Long, E. O., Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 2006. 107: 159-166.
14. 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.
15. Bauer, S., Groh, V., Wu, J., Steinle, A., Phillips, J. H., Lanier, L. L. and Spies, T., Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999. 285: 727-729.
16. Cosman, D., Mülberg, J., Sutherland, C. L., Chin, W., Armitage, R., Fanslow, W., Kubin, M. and Chalupny, N. J., ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001. 14: 123-133.
17. 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.
18. Fuchs, A. and Colonna, M., The role of NK cell recognition of nectin and nectin-like proteins in tumor immunosurveillance. Semin. Cancer. Biol. 2006. 16: 359-366.
19. Pogge von Strandmann, E., Simhadri, V. R., von Tresckow, B., Sasse, S., Reiners, K. S., Hansen, H. P., Rothe, A. et al., Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity 2007. 27: 965-974.
20. Brandt, C. S., Baratin, M., Yi, E. C., Kennedy, J., Gao, Z., Fox, B., Haldeman, B. et al., The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J. Exp. Med. 2009. 206: 1495-1503.
21. Vitale, M., Bottino, C., Sivori, S., Sanseverino, L., Castriconi, R., Marcenaro, E., Augugliaro, R. et al., NKp44, a novel triggering surface molecule specifically expressed by activated Natural Killer cells is involved in non-MHCrestricted tumor cell lysis. J. Exp. Med. 1998. 187: 2065-2072.
22. Halfteck, G. G., Elboim, M., Gur, C., Achdout, H., Ghadially, H. and Mandelboim, O., Enhanced in vivo growth of lymphoma tumors in the absence of the NK-activating receptor NKp46/NCR1. J. Immunol. 2009. 182: 2221-2230.
23. Castriconi, R., Dondero, A., Augugliaro, R., Cantoni, C., Carnemolla, B., Sementa, A. R., Negri, F. et al., Identification of 4Ig-B7-H3 as a neuroblastoma-associated molecule that exerts a protective role from an NK cell-mediated lysis. Proc. Natl. Acad. Sci. USA 2004. 101: 12640-12645.
24. Trinchieri, G., Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 2003. 3: 133-146.
25. Ferlazzo, G., Pack, M., Thomas, D., Paludan, C., Schmid, D., Strowig, T., Bougras, G. et al., Distinct roles of IL-12 and IL-15 in human Natural Killer cell activation by DC from secondary lymphoid organs. Proc. Natl. Acad. Sci. USA 2004. 101: 16606-16611.
26. Overwijk, W. W. and Schluns, K. S., Functions of gammaCcytokines in immune homeostasis: current and potential clinical applications. Clin. Immunol. 2009. 132: 153-165.
27. Parrish-Novak, J., Dillon, S. R., Nelson, A., Hammond, A., Sprecher, C., Gross, J. A., Johnston, J. et al., Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 2000. 408: 57-63.
28. + NK helper cells. J. Exp. Med. 2005. 202: 941-953.
29. Marcenaro, E., Della Chiesa, M., Bellora, F., Parolini, S., Millo, R., Moretta, L. and Moretta, A., IL-12 or IL-4 prime humanNKcells to mediate functionally divergent interactions with dendritic cells or tumors. J. Immunol. 2005. 17: 3992-3998.
30. Castriconi, R., Cantoni, C., Della Chiesa, M., Vitale, M., Marcenaro, E., Conte, R., Biassoni, R. et al., Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc. Natl. Acad. Sci. USA 2003. 100: 4120-4125.
31. Della Chiesa, M., Carlomagno, S., Frumento, G., Balsamo, M., Cantoni, C., Conte, R., Moretta, L. et al., The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function. Blood 2006. 108: 4118-4125.
32. 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.
33. Pende, D., Rivera, P., Marcenaro, S., Chang, C. C., Biassoni, R., Conte, R., Kubin, M. et al., Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res. 2002. 62: 6178-6186.
34. Pietra, G., Manzini, C., Vitale, M., Balsamo, M., Ognio, E., Boitano, M., Queirolo, P. et al., Natural Killer cells kill human melanoma cells with phenotypic characteristics of cancer stem cells. Int. Immunol. 2009. 21: 793-801.
35. Wang, Z., Hu, X. Z., Tatake, R. J., Yang, S. Y., Zeff, R. A. and Ferrone, S., Differential effect of human and mouse beta 2-microglobulin on the induction and the antigenic profile of endogenous HLA-A and -B antigens synthesized by beta 2-microglobulin gene-null FO-1 melanoma cells. Cancer Res. 1993. 53: 4303-4309.
36. + NK cell subset both in blood stream and inflamed peripheral tissues. Int. Immunol. 2010. 22: 91-100.
37. Xu, L., Begum, S., Hearn, J. D. and Hynes, R. O., GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis Proc. Natl. Acad. Sci. USA 2006. 103: 9023-9028.
38. Carosella, E. D., Favier, B., Rouas-Freiss, N., Moreau, P. and Lemaoult, J., Beyond the increasing complexity of the immunomodulatory HLA-G molecule. Blood 2008. 111: 4862-4870.
39. Marín, R., Riuz-Cabello, F., Pedrinaci, S., Mendez, R., Jimenez, P., Geraghty, D. E. and Garrido, F., Analysis of HLA-E expression in human tumors. Immunogenetics 2003. 54: 767-775.
40. López-Botet, M., Llano, M., Navarro, F. and Bellón, T., NK cell recognition of non-classical HLA class I molecules. Semin. Immunol. 2000. 12: 109-119.
41. Platonova, S., Cherfils-Vicini, J., Damotte, D., Crozet, L., Vieillard, V., Validire, P., André, P. et al., Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res. 2011. 71: 5412-5422.
42. Malmberg, K. J., Levitsky, V., Norell, H., Teixeira de Matos, C., Carlsten, M., Schedvins, K., Rabbani, H. et al., IFN-gamma protects short-term ovarian carcinoma cell lines from CTL lysis via a CD94/NKG2A-dependent mechanism. J. Clin. Invest. 2002. 110: 1515-1523.
43. Rebmann, V., Wagner, S. and Grosse-Wilde, H., HLA-G expression in malignant melanoma. Semin. Cancer. Biol. 2007. 17: 422-429.
44. Lin, A., Zhu, C. C., Chen, H. X., Chen, B. F., Zhang, X., Zhang, J. G., Wang, Q. et al., Clinical relevance and functional implications for human leucocyte antigen-G expression in non-small-cell lung cancer. J. Cell. Mol. Med. 2010. 14: 2318-2329.
45. de Kruijf E. M., Sajet, A., van Nes, J. G. H., Natanov, R., Putter, H., Smit, V. T., Liefers, G. J. et al., HLA-E and HLA-G expression in classical HLA class I-negative tumors is of prognostic value for clinical outcome of early breast cancer patients. J. Immunol. 2010. 185: 7452-7459.
46. Groh, V., Wu, J., Yee, C. and Spies, T., Tumor-derived solubile MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002. 419: 734-738.
47. Schwinn, N., Vokhminova, D., Sucker, A., Textor, S., Striegel, S., Moll, I., Nausch, N. et al., Interferon-gamma down-regulates NKG2D ligand expression and impairs the NKG2D-mediated cytolysis of MHC class I-deficient melanoma by natural killer cells. Int. J. Cancer 2009. 124: 1594-1504.
48. 3enhances NK susceptibility of human melanoma cells via Hsp60-mediated FAS expression. Eur. J. Immunol. 2011. 41:2937-2946.
49. Terme, M., Ullrich, E., Delahaye, N. F., Chaput, N. and Zitvogel, L., Natural killer cell-directed therapies: moving from unexpected results to successful strategies. Nat. Immunol. 2008. 9: 486-494.
50. Mortier, E., Woo, T., Advincula, R., Gozalo, S. and Ma, A., IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J. Exp. Med. 2008. 205: 1213-1225.
51. Chang, C. M., Lo, C. H., Shih, Y. M., Chen, Y., Wu, P. Y., Tsuneyama, K., Roffler, S. R. et al., Treatment of hepatocellular carcinoma with adeno-associated virus encoding interleukin-15 superagonist. Hum. Gene Ther. 2010. 21: 611-621.