Effect of tumor cells and tumor microenvironment on NK-cell function

European Journal of Immunology

Volumn 44, Issue 6, 2014, Pages 1582-1592

  Vitale, Massimo ^a   Cantoni, Claudia ^b,c,d   Pietra, Gabriella ^a,b   Mingari, Maria Cristina ^a,b,c   Moretta, Lorenzo ^d  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

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

^d G GASLINI INSTITUTE   (Italy)

Author keywords

Inflammation; NK cells; Tumor escape

Indexed keywords

ANTINEOPLASTIC ACTIVITY; CANCER INFILTRATION; CARCINOGENESIS; CELL ACTIVATION; CYTOTOXICITY; DENDRITIC CELL; FIBROBLAST; HOST CELL; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOGENETICS; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; LYMPHOID CELL; MACROPHAGE; MOLECULAR INTERACTION; NATURAL KILLER CELL; PRIORITY JOURNAL; REVIEW; STROMA CELL; TUMOR CELL; TUMOR MICROENVIRONMENT;

INFLAMMATION; NK CELLS; TUMOR ESCAPE;

ANIMALS; DENDRITIC CELLS; HUMANS; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; MACROPHAGES; NEOPLASMS; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 84901857205     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344272     Document Type: Review

References (101)

1. 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.
2. Moretta, A., Bottino, C., Vitale, M., Pende, D., Cantoni, C., Biassoni, R., Mingari, M. C. et al., Activating receptors and coreceptors involved in the Natural cytolysis. Annu. Rev. Immunol. 2001. 19: 197-223.
3. Vivier, E., Tomasello, E., Baratin, M., Walzer, T. and Ugolini, S., Functions of natural killer cells. Nat. Immunol. 2008. 9: 503-510.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. Elboim, M., Gazit, R., Gur, C., Ghadially, H., Betser-Cohen, G. and Mandelboim, O., Tumor immunoediting by NKp46. J. Immunol. 2010. 184: 5637-5644.
10. Vesely, M. D., Kershaw, M. H., Schreiber, R. D. and Smyth, M. J., Natural innate and adaptive immunity to cancer. Annu. Rev. Immunol. 2011. 29: 235-271.
11. Pradeu, T., Jaeger, S. and Vivier, E., The speed of change: towards a discontinuity theory of immunity? Nat. Rev. Immunol. 2013. 13: 764-769.
12. Moretta, A., Vitale, M., Bottino, C., Orengo, A. M., Morelli, L., Augugliaro, R., Barbaresi, M. et al., P58 molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells. Anti-p58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J. Exp. Med. 1993. 178: 597-604.
13. Sivori, S., Vitale, M., Morelli, L., Sanseverino, L., Augugliaro, R., Bottino, C., Moretta, L. et al., p46, a novel natural killer cell-specific surface molecule that mediates cell activation. J. Exp. Med. 1997. 186: 1129-1136.
14. Pessino, A., Sivori, S., Bottino, C., Malaspina, A., Morelli, L., Moretta, L., Biassoni, R. et al., Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J. Exp. Med. 1998. 188: 953-960.
15. Pende, D., Parolini, S., Pessino, A., Sivori, S., Augugliaro, R., Morelli, L., Marcenaro, E. et al., Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J. Exp. Med. 1999. 190: 1505-1516.
16. 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-major histocompatibility complex-restricted tumor cell lysis. J. Exp. Med. 1998. 187: 2065-2072.
17. Cantoni, C., Bottino, C., Vitale, M., Pessino, A., Augugliaro, R., Malaspina, A., Parolini, S. et al., NKp44, a triggering receptor involved in tumor cell lysis by activated human natural killer cells, is a novel member of the immunoglobulin superfamily. J. Exp. Med. 1999. 189: 787-796.
18. Vacca, P., Moretta, L., Moretta, A. and Mingari, M.C., Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol. 2011. 32: 517-523.
19. Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J. P., Eberl, G., Koyasu, S. et al., Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013. 13: 145-149.
20. Mantovani, A., Allavena, P., Sica, A. and Balkwill, F., Cancer-related inflammation. Nature 2008. 454: 436-444.
21. Colotta, F., Allavena, P., Sica, A., Garlanda, C. and Mantovani, A., Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009. 30: 1073-1081.
22. Karin, M., Nuclear factor-kappaB in cancer development and progression. Nature 2006. 441: 431-436.
23. Yu, H., Kortylewski, M. and Pardoll, D., Crosstalk between cancer and immune cells: role of STAT3 in the tumor microenvironment. Nat. Rev. Immunol. 2007. 7: 41-51.
24. Harris, A. L., Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer. 2002. 2: 38-47.
25. Servais, C. and Erez, N., From sentinel cells to inflammatory culprits: cancer-associated fibroblasts in tumor-related inflammation. J. Pathol. 2013. 229: 198-207.
26. Biswas, S. K. and Mantovani, A., Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010. 11: 889-897.
27. Gabrilovich, D. I., Ostrand-Rosenberg, S. and Bronte, V., Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 2012. 12: 253-268.
28. Fridlender, Z. G. and Albelda, S. M., Tumor-associated neutrophils: friend or foe? Carcinogenesis 2012. 33: 949-955.
29. Whiteside, T., The tumor microenvironment and its role in tumor growth. Oncogene 2008. 27: 5904-5912.
30. Zitvogel, L., Tesniere, A. and Kroemer, G., Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat. Rev. Immunol. 2006. 6: 715-727.
31. Facciabene, A., Motz, G. T. and Coukos, G., T-regulatory T cells: key players in tumor immune escape and angiogenesis. Cancer Res. 2012. 72: 2162-2171.
32. 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. U. S. A. 2010. 107: 21659-21664.
33. Jaeger, B. N., Donadieu, J., Cognet, C., Bernat, C., Ordoneez-Rueda, D., Barlogis, V., Mahlaoui, N. et al., Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J. Exp. Med. 2012. 209: 565-580.
34. Brillard, E., Pallandre, J. R., Chalmers, D., Ryffel, B., Radlovic, A., Seilles, E., Rohrlich, P. S. et al., Natural killer cells prevent CD28-mediated Foxp3 transcription in CD4+CD25- T lymphocytes. Exp. Hematol. 2007. 35: 416-425.
35. Bellora, F., Castriconi, R., Dondero, A., Pessino, A., Nencioni, A., Liggieri, G., Moretta, L. et al., TLR activation of tumor-associated macrophages from ovarian cancer patients triggers cytolytic activity of NK cells. Eur. J. Immunol. 2014. doi:10.1002/eji.201344130. [Epub ahead of print]
36. 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. U. S. A. 2003. 100: 4120-4125.
37. Marcenaro, E., Della Chiesa, M., Bellora, F., Parolini, S., Millo, R., Moretta, L. and Moretta, A., IL-12 or IL-4 prime human NK cells to mediate functionally divergent interactions with dendritic cells or tumors. J. Immunol. 2005. 17: 3992-3998.
38. 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.
39. Ghiringhelli, F., Ménard, C., Martin, F. and Zitvogel, L., The role of regulatory T cells in the control of natural killer cells: relevance during tumor progression. Immunol. Rev. 2006. 214: 229-238.
40. Ghiringhelli, F., Menard, C., Terme, M., Flament, C., Taieb, J., Chaput, N., Puig, P. E. et al., CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J. Exp. Med. 2005. 202: 1075-1085.
41. Sitrin, J., Ring, A., Garcia, K. C., Benoist, C. and Mathis, D., Regulatory T cells control NK cells in an insulitic lesion by depriving them of IL-2. J. Exp. Med. 2013. 210: 1153-1165.
42. Hoechst, B., Voigtlaender, T., Ormandy, L., Gamrekelashvili, J., Zhao, F., Wedemeyer, H., Lehner, F. et al., Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 2009. 50: 799-807.
43. Sprinzl, M. F., Reisinger, F., Puschnik, A., Ringelhan, M., Ackermann, K., Hartmann, D., Schiemann, M. et al., Sorafenib perpetuates cellular anticancer effector functions by modulating the crosstalk between macrophages and natural killer cells. Hepatology 2013. 57: 2358-2368.
44. 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. U. S. A. 2009. 106: 20847-20852.
45. Li, T., Yang, Y., Hua, X., Wang, G., Liu, W., Jia, C., Tai, Y. et al., Hepatocellular carcinoma-associated fibroblasts trigger NK cell dysfunction via PGE2 and IDO. Cancer Lett. 2012. 318: 154-161.
46. Li, T., Yi, S., Liu, W., Jia, C., Wang, G., Hua, X., Tai, Y. et al., Colorectal carcinoma-derived fibroblasts modulate natural killer cell phenotype and antitumor cytotoxicity. Med. Oncol. 2013. 30: 663.
47. 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.
48. El-Gazzar, A., Groh, V. and Spies, T., Immunobiology and conflicting roles of the human NKG2D lymphocyte receptor and its ligands in cancer. J. Immunol. 2013. 191: 1509-1515.
49. Castriconi, R., Dondero, A., Bellora, F., Moretta, L., Castellano, A., Locatelli, F., Corrias, M. V. et al., Neuroblastoma-derived TGF-b1 modulates the chemokine receptor repertoire of human resting NK cells. J. Immunol. 2013. 190: 5321-5328.
50. Balsamo, M., Manzini, C., Pietra, G., Raggi, F., Blengio, F., Mingari, M. C., Varesio, L. et al., Hypoxia downregulates the expression of activating receptors involved in NK-cell-mediated target cell killing without affecting ADCC. Eur. J. Immunol. 2013. 43: 2756-2764.
51. Balsamo, M., Vermi, W., Parodi, M., Pietra, G., Manzini, C., Queirolo, P., Lonardi, S. et al., Melanoma cells become resistant to NK-cell-mediated killing when exposed to NK-cell numbers compatible with NK-cell infiltration in the tumor. Eur. J. Immunol. 2012. 42: 1833-1842.
52. Rosental, B., Brusilovsky, M., Hadad, U., Oz, D., Appel, M. Y., Afergan, F., Yossef, R. et al., Proliferating cell nuclear antigen is a novel inhibitory ligand for the natural cytotoxicity receptor NKp44. J. Immunol. 2011. 187: 5693-5702.
53. Horton, N. C., Mathew, S. O. and Mathew, P. A., Novel interaction between proliferating cell nuclear antigen and HLA I on the surface of tumor cells inhibits NK cell function through NKp44. PLOS One 2011. 187: 5693-5702.
54. Cella, M., Fuchs, A., Vermi, W., Facchetti, F., Otero, K., Lennerz, J. K., Doherty, J. M. et al., A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009. 457: 722-7255.
55. Sanos, S. L., Bui, V. L., Mortha, A., Oberle, K., Heners, C., Johner C. and Diefenbach, A., RORYt and commensal microflora are required for the differentiation of mucosal interleukin 22 producing NKp46 +cells. Nat. Immunol. 2009. 10: 83-91.
56. Luci, C., Reynders, A., Ivanov, I. I., Cognet, C., Chiche, L., Chasson, L., Hardwigsen, J. et al., Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 2009. 10: 75-82.
57. Glatzer T., Killig, M., Meisig, J., Ommert, I., Luetke-Eversloh, M., Babic, M., Paclik, D. et al., RORyt+ innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44. Immunity 2013. 38: 1223-1235.
58. Geremia, A., Arancibia-Cárcamo, C. V., Fleming, M. P., Rust, N., Singh, B., Mortensen, N. J., Travis, S. P. et al., IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J. Exp. Med. 2011. 208: 1127-1133.
59. Kirchberger, S., Royston, D. J., Boulard, O., Thornton, E., Franchini, F., Szabady, R. L., Harrison, O. et al., Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 2013. 210: 917-931.
60. Shi, F. D., Ljunggren, H. G., La Cava, A. and Van Kaer, L., Organ-specific features of natural killer cells. Nat. Rev. Immunol. 2011. 11: 658-671.
61. Tu, Z., Bozorgzadeh, A., Pierce, R. H., Kurtis, J., Crispe, I. N. and Orloff, M. S., TLR-dependent cross talk between human Kupffer cells and NK cells. J. Exp. Med. 2008. 205: 233-244.
62. Hanna, J., Goldman-Wohl, D., Hamani, Y., Avraham, I., Greenfield, C., Natanson-Yaron, S., Prus, D. et al., Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 2006. 12: 1065-1074.
63. Burke, S., Lakshmikanth, T., Colucci, F. and Carbone, E., New views on natural killer cell-based immunotherapy for melanoma treatment. Trends Immunol. 2010. 31: 339-345.
64. Cooper, M. A., Fehniger, T. A. and Caligiuri, M. A., The biology of human natural killer-cell subsets. Trends Immunol. 2001. 22: 633-640.
65. Wendel, M., Galani, I. E., Suri-Payer, E. and Cerwenka, A., Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands. Cancer Res. 2008. 68: 8437-8445.
66. 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.
67. Mamessier, E., Sylvain, A., Thibult, M. L., Houvenaeghel, G., Jacquemier, J., Castellano, R., Gonçalves, 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.
68. 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.
69. Halama, N., Braun, M., Kahlert, C., Spille, A., Quack, C., Rahbari, N., Koch, M. et al., Natural killer cells are scarce in colorectal carcinoma tissue despite high levels of chemokines and cytokines. Clin. Cancer Res. 2011. 17: 678-689.
70. Pachynski, R. K., Zabel, B. A., Kohrt, H. E., Tejeda, N. M., Monnier, J., Swanson, C. D., Holzer, A. K. et al., The chemoattractant chemerin suppresses melanoma by recruiting natural killer cell antitumor defenses. J. Exp. Med. 2012. 209: 1427-1435.
71. dim human NK cells. Blood 2010. 116: 3689-3691.
72. Remark, R., Alifano, M., Cremer, I., Lupo, A., Dieu-Nosjean, M. C., Riquet, M., Crozet, L. et al., Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: influence of tumor origin. Clin. Cancer Res. 2013. 19: 4079-4091.
73. Delahaye, N. F., Rusakiewicz, S., Martins, I., Ménard, C., Roux, S., Lyonnet, L., Paul, P. et al., Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat. Med. 2011. 17: 700-707.
74. Sconocchia, G., Arriga, R., Tornillo, L., Terracciano, L., Ferrone, S. and Spagnoli, G. C., Melanoma cells inhibit NK cell functions. Cancer Res. 2012. 72: 5428-5429.
75. Ni, J., Miller, M., Stojanovic, A., Garbi, N. and Cerwenka, A., Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors. J. Exp. Med. 2012. 209: 2351-2365.
76. Wong, J. L., Berk, E., Edwards, R. P. and Kalinski, P., IL-18-primed helper NK cells collaborate with dendritic cells to promote recruitment of effector CD8+ T cells to the tumor microenvironment. Cancer Res. 2013. 73: 4653-4662.
77. Segler, A. and Tsimberidou, AM., Lenalidomide in solid tumors. Cancer Chemother. Pharmacol. 2012. 69: 1393-1406.
78. Hervieu, A., Rébé, C., Végran, F., Chalmin, F., Bruchard, M., Vabres, P., Apetoh, L. et al., Dacarbazine-mediated upregulation of NKG2D ligands on tumor cells activates NK and CD8 T cells and restrains melanoma growth. J. Invest. Dermatol. 2013. 133: 499-508.
79. Zitvogel, L. and Kroemer, G., Anticancer effects of imatinib via immunostimulation. Nat. Med. 2011. 17: 1050-1051.
80. Gur, C., Porgador, A., Elboim, M., Gazit, R., Mizrahi, S., Stern-Ginossar, N., Achdout, H. et al., The activating receptor NKp46 is essential for the development of type 1 diabetes. Nat. Immunol. 2010 11: 121-128.
81. Gur, C., Doron, S., Kfir-Erenfeld, S., Horwitz, E., Abu-Tair, L., Safadi, R. and Mandelboim, O., NKp46-mediated killing of human and mouse hepatic stellate cells attenuates liver fibrosis. Gut 2012 61: 885-893.
82. Hecht, M. L., Rosental, B., Horlacher, T., Hershkrovitz, O., de Paz, J. L., Noti, C., Schauer, S. et al., Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences. J. Proteom. Res. 2009 8: 712-720.
83. Pogge von Strandmann, E., Simhadri, V. R., von Tresckow, B., Sasse, S., Reiners, K. S., Hansen, H. P., Rothe, A. et al., A. 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.
84. Simhadri, V. R., Reiners, K. S., Hansen, H. P., Topolar, D., Simhadri, V. L., Nohroudi, K., Kufer, T. A. et al., Dendritic cells release HLA-B-associated transcript-3 positive exosomes to regulate natural killer function. PLoS One 2008. 3: e3377.
85. Reiners, K. S., Topolar, D., Henke, A., Simhadri, V. R., Kessler, J., Sauer, M., Bessler, M. et al., Soluble ligands for NK cell receptors promote evasion of chronic lymphocytic leukemia cells from NK cell anti-tumor activity. Blood 2013. 121: 3658-3665.
86. Lam, R. A., Chweel, J. Y., Le Bert, N., Sauer, M., Pogge von Strandmann, E. and Gasser, G., Regulation of self-ligands for activating natural killer cell receptors. Ann. Med. 2013. 45: 384-394.
87. Brandt, C. S., Baratin, M., Yi, E. C., Kennedy, J., Gao, Z., Fox, B., Halderman, B. et al., The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer receptor NKp30 in humans. J. Exp. Med. 2009. 206: 1495-1503.
88. Matta, J., Baratin, M., Chiche, L., Forel, J-M., Cognet, C., Thomas, G., Farnarier, C. et al., Induction of B7-H6, a ligand for the natural killer cell-activating receptor NKp30, in inflammatory conditions. Blood 2013. 122: 394-404.
89. Baychelier, F., Sennepin, A., Ermonval, M., Dorgham, K., Debre, P. and Vieillard, V., Identification of a cellular ligand for NKp44. Blood 2013. 122: 2935-2942.
90. 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.
91. Welte, S., Kuttruff, S., Waldhauer, I. and Steinle, A., Mutual activation of natural killer cells and monocytes mediated by NKp80-AICL interaction. Nat. Immunol. 2006. 7: 1334-1342.
92. Akatsuka, A., Ito, M., Yamauchi, C., Ochiai, A., Yamamoto, K. and Matsumoto, N., Tumor cells of non-hematopoietic and hematopoietic origins express activation-induced C-type lectin, the ligand for killer cell lectin-like receptor F1. Int. Immunol. 2010. 22: 783-790.
93. Hosen, N., Ichihara, H., Mugitani, A., Aoyama, Y., Fukuda, Y., Kishida, S., Matsuoka, Y. et al., CD48 as a novel molecular target for antibody therapy in multiple myeloma. Br. J. Hematol. 2012. 156: 213-224.
94. Pickup, M., Novitskiy, S. and Moses, H. L., The roles of TGFβ in the tumour microenvironment. Nat. Rev. Cancer. 2013. 13: 788-799.
95. 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-β. J. Immunol. 2009. 182: 240-249.
96. Tecchio, C., Scapini, P., Pizzolo, G. and Cassatella, M., On the cytokines produced by human neutrophils in tumors. Sem. Cancer Biol. 2013. 23: 159-170.
97. Houghton, A. M., Rzymkiewicz, M., Ji, H., Gregory, A. D., Egea, E. E., Metz, H. E., Stolz, D. B. et al., Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat. Med. 2010. 16: 219-224.
98. Krockenberger, M., Dombrowski, Y., Weidler, C., Ossadnik, M., Honig, A., Hausler, S., Voigt, H. et al., Macrophage migration inhibitory factor contributes to the immune escape of ovarian cancer by downregulating NKG2D. J. Immunol. 2008. 180: 7338-7348.
99. Gubbels, J. A., Felder, M., Horibata, S., Belisle, J. A., Kapur, A., Holden, H., Petrie, S. et al., MUC16 provides immune protection by inhibiting synapse formation between NK and ovarian tumor cells. Mol. Cancer. 2010. 9: 11.
100. Patankar, M. S., Jing, Y., Morrison, J. C., Belisle, J. A., Lattanzio F. A., Deng, Y., Wong, N. K. et al., Potent suppression of natural killer cell response mediated by the ovarian tumor marker CA125. Gynecol. Oncol. 2005. 99: 704-713.
101. Lankry, D., Rovis, T. L., Jonjic, S. and Mandelboim, O., The interaction between CD300a and phosphatidylserine inhibits tumor cell killing by NK cells. Eur. J. Immunol. 2013. 43: 2151-2161.