Targeting NKG2D in tumor surveillance

Expert Opinion on Therapeutic Targets

Volumn 16, Issue 6, 2012, Pages 587-599

  Hayakawa, Yoshihiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

cancer; immune escape; immunosurveillance; immunotherapy; NKG2D

Indexed keywords

ALPHA INTERFERON; ATM PROTEIN; ATR PROTEIN; HISTONE DEACETYLASE; INTERLEUKIN 15; INTERLEUKIN 21; INTERLEUKIN 7; MEMBRANE PROTEIN; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN KINASE B; RETINOIC ACID; RETINOIC ACID INDUCIBLE PROTEIN I;

ACUTE GRANULOCYTIC LEUKEMIA; BREAST CARCINOMA; CANCER EPIDEMIOLOGY; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CELL SURFACE; CELLULAR STRESS RESPONSE; CYTOTOXICITY; DISEASE SURVEILLANCE; DNA DAMAGE; GLIOMA; HOMEOSTASIS; HUMAN; IMMUNOSURVEILLANCE; IMMUNOTHERAPY; LUNG CARCINOMA; MELANOMA; NEUROBLASTOMA; NONHUMAN; OVARY CARCINOMA; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; REGULATORY MECHANISM; REVIEW; RNA INTERFERENCE; TUMOR CELL;

ANIMALS; HUMANS; NEOPLASMS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K;

EID: 84861305574     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2012.681378     Document Type: Review

References (127)

1. Dunn GP, Bruce AT, Ikeda H, et al. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002;3(11):991-8 (Pubitemid 35363648)
2. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol 2004;22:329-60 (Pubitemid 38680426)
3. Smyth MJ, Thia KY, Street SE, et al. Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J Exp Med 2000;192(5):755-60
4. Shankaran V, Ikeda H, Bruce AT, et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001;410(6832):1107-11 (Pubitemid 32391043)
5. Takeda K, Smyth MJ, Cretney E, et al. Critical role for tumor necrosis factor-related apoptosis-inducing ligand in immune surveillance against tumor development. J Exp Med 2002;195(2):161-9 (Pubitemid 34461260)
6. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004;21(2):137-48 (Pubitemid 39094044)
7. Dunn GP, Bruce AT, Sheehan KC, et al. A critical function for type I interferons in cancer immunoediting. Nat Immunol 2005;6(7):722-9 (Pubitemid 41716746)
8. Wu J, Song Y, Bakker AB, et al. An activating immunoreceptor complex formed by NKG2D and DAP10. Science 1999;285(5428):730-2
9. Jamieson AM, Diefenbach A, McMahon CW, et al. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 2002;17(1):19-29 (Pubitemid 34874615)
10. Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 2003;3(10):781-90 (Pubitemid 37328656)
11. Groh V, Rhinehart R, Secrist H, et al. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA 1999;96(12):6879-84 (Pubitemid 29274978)
12. Champsaur M, Lanier LL. Effect of NKG2D ligand expression on host immune responses. Immunol Rev 2010;235(1):267-85
13. Gasser S, Raulet D. The DNA damage response, immunity and cancer. Semin Cancer Biol 2006;16(5):344-7 (Pubitemid 44311502)
14. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001;413(6852):165-71 (Pubitemid 32867877)
15. Cerwenka A, Baron JL, Lanier LL. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc Natl Acad Sci USA 2001;98(20):11521-6 (Pubitemid 32928761)
16. Hayakawa Y, Kelly JM, Westwood JA, et al. Cutting edge: Tumor rejection mediated by NKG2D receptor-ligand interaction is dependent upon perforin. J Immunol 2002;169(10):5377-81 (Pubitemid 35291630)
17. Hayakawa Y, Smyth MJ. NKG2D and cytotoxic effector function in tumor immune surveillance. Semin Immunol 2006;18(3):176-85 (Pubitemid 43817565)
18. Bauer S, Groh V, Wu J, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999;285(5428):727-9
19. Nausch N, Cerwenka A. NKG2D ligands in tumor immunity. Oncogene 2008;27(45):5944-58
20. Diefenbach A, Tomasello E, Lucas M, et al. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol 2002;3(12):1142-9 (Pubitemid 35469698)
21. Gilfillan S, Ho EL, Cella M, et al. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat Immunol 2002;3(12):1150-5 (Pubitemid 35469699)
22. Zompi S, Hamerman JA, Ogasawara K, et al. NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases. Nat Immunol 2003;4(6):565-72 (Pubitemid 36701340)
23. Maasho K, Opoku-Anane J, Marusina AI, et al. NKG2D is a costimulatory receptor for human naive CD8+ T cells. J Immunol 2005;174(8):4480-4
24. Dhanji S, Teh HS. IL-2-activated CD8+CD44high cells express both adaptive and innate immune system receptors and demonstrate specificity for syngeneic tumor cells. J Immunol 2003;171(7):3442-50 (Pubitemid 37254545)
25. Dann SM, Wang HC, Gambarin KJ, et al. Interleukin-15 activates human natural killer cells to clear the intestinal protozoan cryptosporidium. J Infect Dis 2005;192(7):1294-302 (Pubitemid 41368432)
26. Roberts AI, Lee L, Schwarz E, et al. NKG2D receptors induced by IL-15 costimulate CD28-negative effector CTL in the tissue microenvironment. J Immunol 2001;167(10):5527-30 (Pubitemid 33062738)
27. Brady J, Hayakawa Y, Smyth MJ, Nutt SL. IL-21 induces the functional maturation of murine NK cells. J Immunol 2004;172(4):2048-58 (Pubitemid 38182350)
28. Takaki R, Hayakawa Y, Nelson A, et al. IL-21 enhances tumor rejection through a NKG2D-dependent mechanism. J Immunol 2005;175(4):2167-73 (Pubitemid 41113822)
29. Burgess SJ, Marusina AI, Pathmanathan I, et al. IL-21 down-regulates NKG2D/DAP10 expression on human NK and CD8+ T cells. J Immunol 2006;176(3):1490-7 (Pubitemid 43134292)
30. Zhang C, Zhang J, Sun R, et al. Opposing effect of IFNgamma and IFNalpha on expression of NKG2 receptors: Negative regulation of IFNgamma on NK cells. Int Immunopharmacol 2005;5(6):1057-67
31. Castriconi R, Cantoni C, Della Chiesa M, 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(7):4120-5 (Pubitemid 36418167)
32. Dasgupta S, Bhattacharya-Chatterjee M, O'Malley BW Jr, Chatterjee SK. Inhibition of NK Cell Activity through TGF-{beta}1 by Down-Regulation of NKG2D in a Murine Model of Head and Neck Cancer. J Immunol 2005;175(8):5541-50 (Pubitemid 41456442)
33. Friese MA, Wischhusen J, Wick W, et al. RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo. Cancer Res 2004;64(20):7596-603 (Pubitemid 39372105)
34. Crane CA, Han SJ, Barry JJ, et al. TGF-beta downregulates the activating receptor NKG2D on NK cells and CD8+ T cells in glioma patients. Neuro-oncol 2010;12(1):7-13
35. Ghiringhelli F, Menard C, Terme M, 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(8):1075-85 (Pubitemid 41464501)
36. Smyth MJ, Teng MW, Swann J, et al. CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer. J Immunol 2006;176(3):1582-7 (Pubitemid 43134302)
37. Dupuy S, Lambert M, Zucman D, et al. Human Herpesvirus 8 (HHV8) sequentially shapes the NK cell repertoire during the course of asymptomatic infection and Kaposi sarcoma. PLoS Pathog 2012;8(1):e1002486
38. Pietra G, Manzini C, Rivara S, et al. Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity. Cancer Res 2012;72(6):1407-15
39. Gonzalez S, Lopez-Soto A, Suarez-Alvarez B, et al. NKG2D ligands: key targets of the immune response. Trends Immunol 2008;29(8):397-403
40. Groh V, Bahram S, Bauer S, et al. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci USA 1996;93(22):12445-50 (Pubitemid 26367163)
41. Pende D, Rivera P, Marcenaro S, 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(21):6178-86 (Pubitemid 35244469)
42. Vetter CS, Groh V, thor Straten P, et al. Expression of stress-induced MHC class I related chain molecules on human melanoma. J Invest Dermatol 2002;118(4):600-5 (Pubitemid 34309978)
43. Friese MA, Platten M, Lutz SZ, et al. MICA/NKG2D-mediated immunogene therapy of experimental gliomas. Cancer Res 2003;63(24):8996-9006 (Pubitemid 38064081)
44. Salih HR, Antropius H, Gieseke F, et al. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 2003;102(4):1389-96 (Pubitemid 36988048)
45. Watson NF, Spendlove I, Madjd Z, et al. Expression of the stress-related MHC class I chain-related protein MICA is an indicator of good prognosis in colorectal cancer patients. Int J Cancer 2006;118(6):1445-52
46. Castriconi R, Dondero A, Negri F, et al. Both CD133+ and CD133-medulloblastoma cell lines express ligands for triggering NK receptors and are susceptible to NK-mediated cytotoxicity. Eur J Immunol 2007;37(11):3190-6 (Pubitemid 350131297)
47. Cosman D, Mullberg J, Sutherland CL, et al. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001;14(2):123-33 (Pubitemid 32206515)
48. Kubin M, Cassiano L, Chalupny J, et al. ULBP1, 2, 3: Novel MHC class I-related molecules that bind to human cytomegalovirus glycoprotein UL16, activate NK cells. Eur J Immunol 2001;31(5):1428-37 (Pubitemid 32454690)
49. Jan Chalupny N, Sutherland CL, Lawrence WA, et al. ULBP4 is a novel ligand for human NKG2D. Biochem Biophys Res Commun 2003;305(1):129-35 (Pubitemid 36535417)
50. Eagle RA, Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 2007;7(9):737-44 (Pubitemid 47327391)
51. Cerwenka A, Bakker AB, McClanahan T, et al. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 2000;12(6):721-7
52. Carayannopoulos LN, Naidenko OV, Fremont DH, Yokoyama WM. Cutting edge: Murine UL16-binding protein-like transcript 1: A newly described transcript encoding a high-affinity ligand for murine NKG2D. J Immunol 2002;169(8):4079-83 (Pubitemid 35178173)
53. Malarkannan S, Shih PP, Eden PA, et al. The molecular and functional characterization of a dominant minor H antigen, H60. J Immunol 1998;161(7):3501-9
54. Takada A, Yoshida S, Kajikawa M, et al. Two novel NKG2D ligands of the mouse H60 family with differential expression patterns and binding affinities to NKG2D. J Immunol 2008;180(3):1678-85
55. Whang MI, Guerra N, Raulet DH. Costimulation of dendritic epidermal gammadelta T cells by a new NKG2D ligand expressed specifically in the skin. J Immunol 2009;182(8):4557-64
56. Groh V, Steinle A, Bauer S, Spies T. Recognition of stress-induced MHC molecules by intestinal epithelial gammadelta T cells. Science 1998;279(5357):1737-40 (Pubitemid 28164472)
57. Carbone E, Neri P, Mesuraca M, et al. HLA class I, NKG2D, and natural cytotoxicity receptors regulate multiple myeloma cell recognition by natural killer cells. Blood 2005;105(1):251-8 (Pubitemid 40053090)
58. Smyth MJ, Swann J, Kelly JM, et al. NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer. J Exp Med 2004;200(10):1325-35 (Pubitemid 39552573)
59. Braud VM, Allan DS, McMichael AJ. Functions of nonclassical MHC and non-MHC-encoded class I molecules. Curr Opin Immunol 1999;11(1):100-8 (Pubitemid 29082345)
60. Hamerman JA, Ogasawara K, Lanier LL. Cutting edge: Toll-like receptor signaling in macrophages induces ligands for the NKG2D receptor. J Immunol 2004;172(4):2001-5 (Pubitemid 38182343)
61. Rolle A, Mousavi-Jazi M, Eriksson M, et al. Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: up-regulation of UL16-binding protein (ULBP)1 and ULBP2 is counteracted by the viral UL16 protein. J Immunol 2003;171(2):902-8 (Pubitemid 36871403)
62. Bartkova J, Horejsi Z, Koed K, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005;434(7035):864-70 (Pubitemid 40558993)
63. Gorgoulis VG, Vassiliou LV, Karakaidos P, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005;434(7035):907-13 (Pubitemid 40559004)
64. Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005;436(7054):1186-90 (Pubitemid 41232299)
65. Diefenbach A, Jamieson AM, Liu SD, et al. Ligands for the murine NKG2D receptor: Expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 2000;1(2):119-26
66. Hayakawa Y, Sato-Matsushita M, Takeda K, et al. Early activation and interferon-gamma production of tumor-infiltrating mature CD27 high natural killer cells. Cancer Sci 2011;102(11):1967-71
67. Smyth MJ, Swann J, Cretney E, et al. NKG2D function protects the host from tumor initiation. J Exp Med 2005;202(5):583-8 (Pubitemid 41248410)
68. Hayakawa Y, Smyth MJ. Innate immune recognition and suppression of tumors. Adv Cancer Res 2006;95:293-322 (Pubitemid 44066529)
69. Guerra N, Tan YX, Joncker NT, et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 2008;28(4):571-80
70. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: Integrating immunity's roles in cancer suppression and promotion. Science 2011;331(6024):1565-70
71. Textor S, Fiegler N, Arnold A, et al. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res 2011;71(18):5998-6009
72. Li H, Lakshmikanth T, Garofalo C, et al. Pharmacological activation of p53 triggers anticancer innate immune response through induction of ULBP2. Cell Cycle 2011;10(19):3346-58
73. Bedel R, Thiery-Vuillemin A, Grandclement C, et al. Novel role for STAT3 in transcriptional regulation of NK immune cell targeting receptor MICA on cancer cells. Cancer Res 2011;71(5):1615-26
74. Glozak MA, Seto E. Histone deacetylases and cancer. Oncogene 2007;26(37):5420-32 (Pubitemid 47255924)
75. Armeanu S, Bitzer M, Lauer UM, et al. Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate. Cancer Res 2005;65(14):6321-9 (Pubitemid 40994418)
76. Skov S, Pedersen MT, Andresen L, et al. Cancer cells become susceptible to natural killer cell killing after exposure to histone deacetylase inhibitors due to glycogen synthase kinase-3-dependent expression of MHC class I-related chain A and B. Cancer Res 2005;65(23):11136-45 (Pubitemid 41713385)
77. Kato N, Tanaka J, Sugita J, et al. Regulation of the expression of MHC class I-related chain A, B (MICA, MICB) via chromatin remodeling and its impact on the susceptibility of leukemic cells to the cytotoxicity of NKG2D-expressing cells. Leukemia 2007;21(10):2103-8 (Pubitemid 47423800)
78. Lopez-Soto A, Folgueras AR, Seto E, Gonzalez S. HDAC3 represses the expression of NKG2D ligands ULBPs in epithelial tumour cells: Potential implications for the immunosurveillance of cancer. Oncogene 2009;28(25):2370-82
79. Nice TJ, Deng W, Coscoy L, Raulet DH. Stress-regulated targeting of the NKG2D ligand Mult1 by a membrane-associated RING-CH family E3 ligase. J Immunol 2010;185(9):5369-76
80. Kobata A, Amano J. Altered glycosylation of proteins produced by malignant cells, and application for the diagnosis and immunotherapy of tumours. Immunol Cell Biol 2005;83(4):429-39 (Pubitemid 41044621)
81. Tsuboi S, Sutoh M, Hatakeyama S, et al. A novel strategy for evasion of NK cell immunity by tumours expressing core2 O-glycans. Embo J 2011;30(15):3173-85
82. Andresen L, Skovbakke SL, Persson G, et al. 2-Deoxy D-glucose prevents cell surface expression of NKG2D ligands through inhibition of N-linked glycosylation. J Immunol 2012;188(4):1847-55
83. Yadav D, Ngolab J, Lim RS, et al. Cutting edge: Down-regulation of MHC class I-related chain A on tumor cells by IFN-gamma-induced microRNA. J Immunol 2009;182(1):39-43
84. Heinemann A, Zhao F, Pechlivanis S, et al. Tumor suppressive microRNAs miR-34a/c control cancer cell expression of ULBP2, a stress-induced ligand of the natural killer cell receptor NKG2D. Cancer Res 2012;72(2):460-71
85. Wiemann K, Mittrucker HW, Feger U, et al. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. J Immunol 2005;175(2):720-9 (Pubitemid 41094952)
86. Oppenheim DE, Roberts SJ, Clarke SL, et al. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 2005;6(9):928-37 (Pubitemid 43090448)
87. Zafirova B, Mandaric S, Antulov R, et al. Altered NK cell development and enhanced NK cell-mediated resistance to mouse cytomegalovirus in NKG2D-deficient mice. Immunity 2009;31(2):270-82
88. Champsaur M, Beilke JN, Ogasawara K, et al. Intact NKG2D-independent function of NK cells chronically stimulated with the NKG2D ligand Rae-1. J Immunol 2010;185(1):157-65
89. Ogasawara K, Hamerman JA, Ehrlich LR, et al. NKG2D blockade prevents autoimmune diabetes in NOD mice. Immunity 2004;20(6):757-67 (Pubitemid 38757445)
90. Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002;419(6908):734-8 (Pubitemid 35177960)
91. Holdenrieder S, Stieber P, Peterfi A, et al. Soluble MICA in malignant diseases. Int J Cancer 2006;118(3):684-7 (Pubitemid 43076018)
92. Wu JD, Higgins LM, Steinle A, et al. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J Clin Invest 2004;114(4):560-8 (Pubitemid 39572106)
93. Clayton A, Mitchell JP, Court J, et al. Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol 2008;180(11):7249-58
94. Hedlund M, Stenqvist AC, Nagaeva O, et al. Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: Evidence for immunosuppressive function. J Immunol 2009;183(1):340-51
95. Ashiru O, Boutet P, Fernandez-Messina L, et al. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA. *008 that is shed by tumor cells in exosomes. Cancer Res 2010;70(2):481-9
96. Hedlund M, Nagaeva O, Kargl D, et al. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS One 2011;6(2):e16899
97. Coudert JD, Zimmer J, Tomasello E, et al. Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood 2005;106(5):1711-17 (Pubitemid 41208585)
98. Waldhauer I, Goehlsdorf D, Gieseke F, et al. Tumor-associated MICA is shed by ADAM proteases. Cancer Res 2008;68(15):6368-76
99. Waldhauer I, Steinle A. Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res 2006;66(5):2520-6
100. Boutet P, Aguera-Gonzalez S, Atkinson S, et al. Cutting edge: The metalloproteinase ADAM17/TNF-alphaconverting enzyme regulates proteolytic shedding of the MHC class I-related chain B protein. J Immunol 2009;182(1):49-53
101. Liu G, Atteridge CL, Wang X, et al. The membrane type matrix metalloproteinase MMP14 mediates constitutive shedding of MHC class I chain-related molecule A independent of A disintegrin and metalloproteinases. J Immunol 2010;184(7):3346-50
102. Kaiser BK, Yim D, Chow IT, et al. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature 2007;447(7143):482-6 (Pubitemid 46816733)
103. Zocchi MR, Catellani S, Canevali P, et al. High ERp5/ADAM10 expression in lymph node microenvironment and impaired NKG2D ligands recognition in Hodgkin lymphomas. Blood 2012;119(6):1479-89
104. Bui JD, Carayannopoulos LN, Lanier LL, et al. IFN-Dependent Down-Regulation of the NKG2D Ligand H60 on Tumors. J Immunol 2006;176(2):905-13 (Pubitemid 43099688)
105. Eisele G, Wischhusen J, Mittelbronn M, et al. TGF-beta and metalloproteinases differentially suppress NKG2D ligand surface expression on malignant glioma cells. Brain 2006;129(Pt 9):2416-25 (Pubitemid 44522126)
106. Serrano AE, Menares-Castillo E, Garrido-Tapia M, et al. Interleukin 10 decreases MICA expression on melanoma cell surface. Immunol Cell Biol 2011;89(3):447-57
107. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004;22:531-62 (Pubitemid 38680433)
108. Song H, Hur DY, Kim KE, et al. IL-2/IL-18 prevent the down-modulation of NKG2D by TGF-beta in NK cells via the c-Jun N-terminal kinase (JNK) pathway. Cell Immunol 2006;242(1):39-45 (Pubitemid 44894394)
109. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011;144(5):646-74
110. Keith B, Johnson RS, Simon MC. HIF1alpha and HIF2alpha: Sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2011;12(1):9-22
111. Siemens DR, Hu N, Sheikhi AK, et al. Hypoxia increases tumor cell shedding of MHC class I chain-related molecule: Role of nitric oxide. Cancer Res 2008;68(12):4746-53
112. Gray-Owen SD, Blumberg RS. CEACAM1: Contact-dependent control of immunity. Nat Rev Immunol 2006;6(6):433-46
113. Chen Z, Chen L, Baker K, et al. CEACAM1 dampens antitumor immunity by down-regulating NKG2D ligand expression on tumor cells. J Exp Med 2011;208(13):2633-40
114. Rohner A, Langenkamp U, Siegler U, et al. Differentiation-promoting drugs up-regulate NKG2D ligand expression and enhance the susceptibility of acute myeloid leukemia cells to natural killer cell-mediated lysis. Leuk Res 2007;31(10):1393-402 (Pubitemid 47212430)
115. Poggi A, Venturino C, Catellani S, et al. Vdelta1 T lymphocytes from B-CLL patients recognize ULBP3 expressed on leukemic B cells and up-regulated by trans-retinoic acid. Cancer Res 2004;64(24):9172-9 (Pubitemid 39665533)
116. Catellani S, Poggi A, Bruzzone A, et al. Expansion of Vdelta1 T lymphocytes producing IL-4 in low-grade non-Hodgkin lymphomas expressing UL-16-binding proteins. Blood 2007;109(5):2078-85 (Pubitemid 46348208)
117. Bae JH, Kim SJ, Kim MJ, et al. Susceptibility to natural killer cell-mediated lysis of colon cancer cells is enhanced by treatment with epidermal growth factor receptor inhibitors through UL16-binding protein-1 induction. Cancer Sci 2012;103(1):7-16
118. Zhang T, Barber A, Sentman CL. Chimeric NKG2D modified T cells inhibit systemic T-cell lymphoma growth in a manner involving multiple cytokines and cytotoxic pathways. Cancer Res 2007;67(22):11029-36 (Pubitemid 350145933)
119. Morgan SM, Hodges E, Mitchell TJ, et al. Molecular analysis of T-cell receptor beta genes in cutaneous T-cell lymphoma reveals Jbeta1 bias. J Invest Dermatol 2006;126(8):1893-9 (Pubitemid 44086525)
120. Fine JH, Chen P, Mesci A, et al. Chemotherapy-induced genotoxic stress promotes sensitivity to natural killer cell cytotoxicity by enabling missing-self recognition. Cancer Res 2010;70(18):7102-13
121. Kohga K, Takehara T, Tatsumi T, et al. Anticancer chemotherapy inhibits MHC class I-related chain a ectodomain shedding by downregulating ADAM10 expression in hepatocellular carcinoma. Cancer Res 2009;69(20):8050-7
122. Poggi A, Catellani S, Garuti A, et al. Effective in vivo induction of NKG2D ligands in acute myeloid leukaemias by all-trans-retinoic acid or sodium valproate. Leukemia 2009;23(4):641-8
123. Soriani A, Zingoni A, Cerboni C, et al. ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood 2009;113(15):3503-11
124. Kim JY, Son YO, Park SW, et al. Increase of NKG2D ligands and sensitivity to NK cell-mediated cytotoxicity of tumor cells by heat shock and ionizing radiation. Exp Mol Med 2006;38(5):474-84
125. Fregni G, Perier A, Pittari G, et al. Unique functional status of natural killer cells in metastatic stage IV melanoma patients and its modulation by chemotherapy. Clin Cancer Res 2011;17(9):2628-37
126. Cho HM, Rosenblatt JD, Tolba K, et al. Delivery of NKG2D ligand using an anti-HER2 antibody-NKG2D ligand fusion protein results in an enhanced innate and adaptive antitumor response. Cancer Res 2010;70(24):10121-30
127. Litzinger MT, Fernando R, Curiel TJ, et al. IL-2 immunotoxin denileukin diftitox reduces regulatory T cells and enhances vaccine-mediated T-cell immunity. Blood 2007;110(9):3192-201 (Pubitemid 350106311)