Recognition of tumors by the innate immune system and natural killer cells

Advances in Immunology

Volumn 122, Issue , 2014, Pages 91-128

  Marcus, Assaf ^a   Gowen, Benjamin G ^a   Thompson, Thornton W ^a   Iannello, Alexandre ^a   Ardolino, Michele ^a   Deng, Weiwen ^a   Wang, Lin ^a   Shifrin, Nataliya ^a   Raulet, David H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer; DNA damage response; DNAM 1; Immunoediting; Innate immunity; NKG2D; Proliferation; Senescence; Tumor immunosurveillance

Indexed keywords

CELL ADHESION MOLECULE; CELL PROTEIN; GAMMA INTERFERON; IMMUNOGLOBULIN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN DNAM 1; PROTEIN NKP80; PROTEIN RAE 1; RECEPTOR; SIGNALING LYMPHOCYTE ACTIVATING MOLECULE RELATED RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; ARTICLE; CANCER PREVENTION; CELL AGING; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DNA DAMAGE; GENE FUNCTION; GERM LINE; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IMMUNOSTIMULATION; IMMUNOSURVEILLANCE; INNATE IMMUNITY; LYMPHOCYTIC INFILTRATION; MOLECULAR RECOGNITION; NATURAL KILLER T CELL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TUMOR CELL; TUMOR ESCAPE; TUMOR IMMUNITY;

CANCER; DNA-DAMAGE RESPONSE; DNAM-1; IMMUNOEDITING; INNATE IMMUNITY; NKG2D; PROLIFERATION; SENESCENCE; TUMOR IMMUNOSURVEILLANCE;

ANIMALS; BINDING SITES; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; LIGANDS; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS;

EID: 84893352557     PISSN: 00652776     EISSN: 15578445     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800267-4.00003-1     Document Type: Chapter

References (203)

1. Ames E., Murphy W.J. Advantages and clinical applications of natural killer cells in cancer immunotherapy. Cancer Immunology, Immunotherapy. 2013, epub 2013/08/31.
2. Andre M.C., Sigurdardottir D., Kuttruff S., Pommerl B., Handgretinger R., Rammensee H.G., et al. Impaired tumor rejection by memory CD8 T cells in mice with NKG2D dysfunction. International Journal of Cancer 2012, 131:1601-1610.
3. Ardolino M., Zingoni A., Cerboni C., Cecere F., Soriani A., Iannitto M.L., et al. DNAM-1 ligand expression on Ag-stimulated T lymphocytes is mediated by ROS-dependent activation of DNA-damage response: Relevance for NK-T cell interaction. Blood 2011, 117:4778.
4. Arnon T.I., Achdout H., Lieberman N., Gazit R., Gonen-Gross T., Katz G., et al. The mechanisms controlling the recognition of tumor- and virus-infected cells by NKp46. Blood 2004, 103:664.
5. Barber D.F., Faure M., Long E.O. LFA-1 contributes an early signal for NK cell cytotoxicity. The Journal of Immunology 2004, 173:3653.
6. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864.
7. Bauer S., Groh V., Wu J., Steinle A., Phillips J.H., Lanier L.L., et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999, 285:727.
8. Benoit L., Wang X., Pabst H.F., Dutz J., Tan R. Defective NK cell activation in X-linked lymphoproliferative disease. The Journal of Immunology 2000, 165:3549.
9. Billadeau D.D., Brumbaugh K.M., Dick C.J., Schoon R.A., Bustelo X.R., Leibson P.J. The Vav-Rac1 pathway in cytotoxic lymphocytes regulates the generation of cell-mediated killing. Journal of Experimental Medicine 1998, 188:549.
10. Binstadt B.A., Brumbaugh K.M., Dick C.J., Scharenberg A.M., Williams B.L., Colonna M., et al. Sequential involvement of Lck and SHP-1 with MHC-recognizing receptors on NK cells inhibits FcR-initiated tyrosine kinase activation. Immunity 1996, 5:629.
11. Bix M., Liao N.S., Zijlstra M., Loring J., Jaenisch R., Raulet D. Rejection of class I MHC-deficient haemopoietic cells by irradiated MHC-matched mice. Nature 1991, 349:329.
12. Bloch-Queyrat C., Fondaneche M.C., Chen R., Yin L., Relouzat F., Veillette A., et al. Regulation of natural cytotoxicity by the adaptor SAP and the Src-related kinase Fyn. The Journal of Experimental Medicine 2005, 202:181.
13. Boissel N., Rea D., Tieng V., Dulphy N., Brun M., Cayuela J.M., et al. BCR/ABL oncogene directly controls MHC class I chain-related molecule A expression in chronic myelogenous leukemia. The Journal of Immunology 2006, 176:5108.
14. Bottino C., Castriconi R., Pende D., Rivera P., Nanni M., Carnemolla B., et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. The Journal of Experimental Medicine 2003, 198:557.
15. Braig M., Schmitt C.A. Oncogene-induced senescence: Putting the brakes on tumor development. Cancer Research 2006, 66:2881.
16. Brandt C.S., Baratin M., Yi E.C., Kennedy J., Gao Z., Fox B., et al. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. The Journal of Experimental Medicine 2009, 206:1495.
17. Braud V.M., Allan D.S., O'Callaghan C.A., Soderstrom K., D'Andrea A., Ogg G.S., et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 1998, 391:795.
18. Braumuller H., Wieder T., Brenner E., Assmann S., Hahn M., Alkhaled M., et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 2013, 494:361.
19. Bryceson Y.T., March M.E., Barber D.F., Ljunggren H.G., Long E.O. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. The Journal of Experimental Medicine 2005, 202:1001.
20. Bryceson Y.T., March M.E., Ljunggren H.G., Long E.O. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 2006, 107:159.
21. Burns G.F., Triglia T., Werkmeister J.A., Begley C.G., Boyd A.W. TLiSA1, a human T lineage-specific activation antigen involved in the differentiation of cytotoxic T lymphocytes and anomalous killer cells from their precursors. The Journal of Experimental Medicine 1985, 161:1063.
22. Burshtyn D., Scharenberg A., Wagtmann N., Rajagopalan S., Peruzzi M., Kinet J.-P., et al. Recruitment of tyrosine phosphatase HCP by the NK cell inhibitory receptor. Immunity 1996, 4:77.
23. Campbell K.S., Dessing M., Lopez-Botet M., Cella M., Colonna M. Tyrosine phosphorylation of a human killer inhibitory receptor recruits protein tyrosine phosphatase 1C. Journal of Experimental Medicine 1996, 184:93.
24. Campisi J. Aging, cellular senescence, and cancer. Annual Review of Physiology 2013, 75:685-705.
25. Cantoni C., Bottino C., Augugliaro R., Morelli L., Marcenaro E., Castriconi R., et al. Molecular and functional characterization of IRp60, a member of the immunoglobulin superfamily that functions as an inhibitory receptor in human NK cells. European Journal of Immunology 1999, 29:3148.
26. Castriconi R., Dondero A., Corrias M.V., Lanino E., Pende D., Moretta L., et al. Natural killer cell-mediated killing of freshly isolated neuroblastoma cells: Critical role of DNAX accessory molecule-1-poliovirus receptor interaction. Cancer Research 2004, 64:9180.
27. Cella M., Fujikawa K., Tassi I., Kim S., Latinis K., Nishi S., et al. Differential requirements for Vav proteins in DAP10- and ITAM-mediated NK cell cytotoxicity. The Journal of Experimental Medicine 2004, 200:817.
28. Cerboni C., Zingoni A., Cippitelli M., Piccoli M., Frati L., Santoni A. Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK- cell lysis. Blood 2007, 110:606.
29. Cerwenka A., Bakker A.B.H., McClanahan T., Wagner J., Wu J., Phillips J.H., et al. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 2000, 12:721.
30. Cerwenka A., Baron J.L., Lanier L.L. 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. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:11521.
31. Champsaur M., Beilke J.N., Ogasawara K., Koszinowski U.H., Jonjic S., Lanier L.L. Intact NKG2D-independent function of NK cells chronically stimulated with the NKG2D ligand Rae-1. The Journal of Immunology 2010, 185:157.
32. Champsaur M., Lanier L.L. Effect of NKG2D ligand expression on host immune responses. Immunological Reviews 2010, 235:267.
33. Chang Y.T., Wu C.C., Shyr Y.M., Chen T.C., Hwang T.L., Yeh T.S., et al. Secretome-based identification of ULBP2 as a novel serum marker for pancreatic cancer detection. PLoS One 2011, 6:e20029.
34. Chauveau A., Aucher A., Eissmann P., Vivier E., Davis D.M. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:5545.
35. Chen H.L., Gabrilovich D., Tampe R., Girgis K.R., Nadaf S., Carbone D.P. A functionally defective allele of TAP1 results in loss of MHC class I antigen presentation in a human lung cancer. Nature Genetics 1996, 13:210.
36. Chitadze G., Bhat J., Lettau M., Janssen O., Kabelitz D. Generation of soluble NKG2D ligands: Proteolytic cleavage, exosome secretion and functional implications. Scandinavian Journal of Immunology 2013, 78:120.
37. Cimprich K.A., Cortez D. ATR: An essential regulator of genome integrity. Nature Reviews Molecular Cell Biology 2008, 9:616.
38. Coca S., Perez-Piqueras J., Martinez D., Colmenarejo A., Saez M.A., Vallejo C., et al. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 1997, 79:2320.
39. Collado M., Serrano M. Senescence in tumours: Evidence from mice and humans. Nature Reviews Cancer 2010, 10:51.
40. Costello R.T., Sivori S., Marcenaro E., Lafage-Pochitaloff M., Mozziconacci M.J., Reviron D., et al. Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood 2002, 99:3661.
41. Coudert J.D., Scarpellino L., Gros F., Vivier E., Held W. Sustained NKG2D engagement induces cross-tolerance of multiple distinct NK cell activation pathways. Blood 2008, 111:3571.
42. Coudert J.D., Zimmer J., Tomasello E., Cebecauer M., Colonna M., Vivier E., et al. Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood 2005, 106:1711.
43. Crowe N.Y., Smyth M.J., Godfrey D.I. A critical role for natural killer T cells in immunosurveillance of methylcholanthrene-induced sarcomas. The Journal of Experimental Medicine 2002, 196:119.
44. Croxford J.L., Tang M.L., Pan M.F., Huang C.W., Kamran N., Phua C.M., et al. ATM-dependent spontaneous regression of early Emu-myc-induced murine B-cell leukemia depends on natural killer and T cells. Blood 2013, 121:2512.
45. Davis J.E., Smyth M.J., Trapani J.A. Granzyme A and B-deficient killer lymphocytes are defective in eliciting DNA fragmentation but retain potent in vivo anti-tumor capacity. European Journal of Immunology 2001, 31:39.
46. Deguine J., Breart B., Lemaitre F., Di Santo J.P., Bousso P. Intravital imaging reveals distinct dynamics for natural killer and CD8(+) T cells during tumor regression. Immunity 2010, 33:632.
47. Dennehy K.M., Klimosch S.N., Steinle A. Cutting edge: NKp80 uses an atypical hemi-ITAM to trigger NK cytotoxicity. The Journal of Immunology 2011, 186:657.
48. Diamond M.S., Kinder M., Matsushita H., Mashayekhi M., Dunn G.P., Archambault J.M., et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. The Journal of Experimental Medicine 2011, 208:1989.
49. Diefenbach A., Jamieson A.M., Liu S.D., Shastri N., Raulet D.H. Ligands for the murine NKG2D receptor: Expression by tumor cells and activation of NK cells and macrophages. Nature Immunology 2000, 1:119.
50. Diefenbach A., Jensen E.R., Jamieson A.M., Raulet D.H. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001, 413:165.
51. Diefenbach A., Tomasello E., Lucas M., Jamieson A.M., Hsia J.K., Vivier E., et al. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nature Immunology 2002, 3:1142.
52. Diermayr S., Himmelreich H., Durovic B., Mathys-Schneeberger A., Siegler U., Langenkamp U., et al. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities. Blood 2008, 111:1428.
53. Dighe A.S., Richards E., Old L.J., Schreiber R.D. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity 1994, 1:447.
54. Dong Z., Cruz-Munoz M.E., Zhong M.C., Chen R., Latour S., Veillette A. Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nature Immunology 2009, 10:973.
55. Doubrovina E.S., Doubrovin M.M., Vider E., Sisson R.B., O'Reilly R.J., Dupont B., et al. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. The Journal of Immunology 2003, 171:6891.
56. Dunn G.P., Bruce A.T., Ikeda H., Old L.J., Schreiber R.D. Cancer immunoediting: From immunosurveillance to tumor escape. Nature Immunology 2002, 3:991.
57. Dunn G.P., Old L.J., Schreiber R.D. The three Es of cancer immunoediting. Annual Review of Immunology 2004, 22:329.
58. Eisele G., Wischhusen J., Mittelbronn M., Meyermann R., Waldhauer I., Steinle A., et al. TGF-beta and metalloproteinases differentially suppress NKG2D ligand surface expression on malignant glioma cells. Brain 2006, 129:2416.
59. Elboim M., Gazit R., Gur C., Ghadially H., Betser-Cohen G., Mandelboim O. Tumor immunoediting by NKp46. The Journal of Immunology 2010, 184:5637.
60. Epling-Burnette P.K., Bai F., Painter J.S., Rollison D.E., Salih H.R., Krusch M., et al. Reduced natural killer (NK) function associated with high-risk myelodysplastic syndrome (MDS) and reduced expression of activating NK receptors. Blood 2007, 109:4816.
61. Fauriat C., Just-Landi S., Mallet F., Arnoulet C., Sainty D., Olive D., et al. Deficient expression of NCR in NK cells from acute myeloid leukemia: Evolution during leukemia treatment and impact of leukemia cells in NCR dull phenotype induction. Blood 2007, 109:323.
62. Fauriat C., Moretta A., Olive D., Costello R.T. Defective killing of dendritic cells by autologous natural killer cells from acute myeloid leukemia patients. Blood 2005, 106:2186.
63. Fernandez-Messina L., Ashiru O., Boutet P., Aguera-Gonzalez S., Skepper J.N., Reyburn H.T., et al. Differential mechanisms of shedding of the glycosyl-phosphatidylinositol (GPI)-anchored NKG2D ligands. The Journal of Biological Chemistry 2010, 285:8543.
64. Friese M.A., Platten M., Lutz S.Z., Naumann U., Aulwurm S., Bischof F., et al. MICA/NKG2D-mediated immunogene therapy of experimental gliomas. Cancer Research 2003, 63:8996.
65. Fuchs A., Cella M., Giurisato E., Shaw A.S., Colonna M. Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). Journal of Immunology 2004, 172:3994.
66. Fuchs A., Colonna M. The role of NK cell recognition of nectin and nectin-like proteins in tumor immunosurveillance. Seminars in Cancer Biology 2006, 16:359.
67. Galon J., Costes A., Sanchez-Cabo F., Kirilovsky A., Mlecnik B., Lagorce-Pages C., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313:1960.
68. Gao Y., Yang W., Pan M., Scully E., Girardi M., Augenlicht L.H., et al. Gamma delta T cells provide an early source of interferon gamma in tumor immunity. The Journal of Experimental Medicine 2003, 198:433.
69. Garrido F., Algarra I. MHC antigens and tumor escape from immune surveillance. Advances in Cancer Research 2001, 83:117.
70. Garrido F., Cabrera T., Lopez-Nevot M.A., Ruiz-Cabello F. HLA class I antigens in human tumors. Advances in Cancer Research 1995, 67:155.
71. Garrido F., Ruiz-Cabello F., Cabrera T., Perez-Villar J.J., Lopez-Botet M., Duggan-Keen M., et al. Implications for immunosurveillance of altered HLA class I phenotypes in human tumours. Immunology Today 1997, 18:89.
72. Gasser S., Orsulic S., Brown E.J., Raulet D.H. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005, 436:1186.
73. Gasser S., Raulet D.H. Activation and self-tolerance of natural killer cells. Immunological Reviews 2006, 214:130.
74. Gilfillan S., Chan C.J., Cella M., Haynes N.M., Rapaport A.S., Boles K.S., et al. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. The Journal of Experimental Medicine 2008, 205:2965.
75. Gilfillan S., Ho E.L., Cella M., Yokoyama W.M., Colonna M. NKG2D recruits two distinct adapters to trigger natural killer cell activation and costimulation. Nature Immunology 2002, 3:1150.
76. Girardi M., Oppenheim D.E., Steele C.R., Lewis J.M., Glusac E., Filler R., et al. Regulation of cutaneous malignancy by gammadelta T cells. Science 2001, 294:605.
77. Glasner A., Ghadially H., Gur C., Stanietsky N., Tsukerman P., Enk J., et al. Recognition and prevention of tumor metastasis by the NK receptor NKp46/NCR1. Journal of Immunology 2012, 188:2509.
78. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005, 434:907.
79. Groh V., Bahram S., Bauer S., Herman A., Beauchamp M., Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:12445.
80. Groh V., Wu J., Yee C., Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T- cell activation. Nature 2002, 419:734.
81. Guerra N., Tan Y.X., Joncker N.T., Choy A., Gallardo F., Xiong N., et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 2008, 28:571.
82. Hallett W.H., Ames E., Motarjemi M., Barao I., Shanker A., Tamang D.L., et al. Sensitization of tumor cells to NK cell-mediated killing by proteasome inhibition. The Journal of Immunology 2008, 180:163.
83. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57.
84. Hanahan D., Weinberg R.A. Hallmarks of cancer: The next generation. Cell 2011, 144:646.
85. Hayakawa Y., Kelly J.M., Westwood J., Darcy P.K., Diefenbach A., Raulet D.H., et al. Tumor rejection mediated by NKG2D receptor-ligand interaction is strictly dependent on perforin. The Journal of Immunology 2002, 169:5377.
86. Heinemann A., Zhao F., Pechlivanis S., Eberle J., Steinle A., Diederichs 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 Research 2012, 72:460.
87. Hilpert J., Grosse-Hovest L., Grunebach F., Buechele C., Nuebling T., Raum T., et al. Comprehensive analysis of NKG2D ligand expression and release in leukemia: Implications for NKG2D-mediated NK cell responses. The Journal of Immunology 2012, 189:1360.
88. Hirano F., Kaneko K., Tamura H., Dong H., Wang S., Ichikawa M., et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Research 2005, 65:1089.
89. Hodi F.S., O'Day S.J., McDermott D.F., Weber R.W., Sosman J.A., Haanen J.B., et al. Improved survival with ipilimumab in patients with metastatic melanoma. The New England Journal of Medicine 2010, 363:711.
90. Houchins J.P., Yabe T., McSherry C., Bach F.H. DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells. The Journal of Experimental Medicine 1991, 173:1017.
91. Iannello A., Thompson T.W., Ardolino M., Lowe S.W., Raulet D.H. p53-dependent chemokine production by senescent tumor cells supports NKG2D-dependent tumor elimination by natural killer cells. The Journal of Experimental Medicine 2013, 210:2057.
92. Iguchi-Manaka A., Kai H., Yamashita Y., Shibata K., Tahara-Hanaoka S., Honda S., et al. Accelerated tumor growth in mice deficient in DNAM-1 receptor. The Journal of Experimental Medicine 2008, 205:2959.
93. Ishigami S., Natsugoe S., Tokuda K., Nakajo A., Che X., Iwashige H., et al. Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 2000, 88:577.
94. Jinushi M., Takehara T., Tatsumi T., Hiramatsu N., Sakamori R., Yamaguchi S., et al. Impairment of natural killer cell and dendritic cell functions by the soluble form of MHC class I-related chain A in advanced human hepatocellular carcinomas. Journal of Hepatology 2005, 43:1013.
95. Jinushi M., Vanneman M., Munshi N.C., Tai Y.T., Prabhala R.H., Ritz J., et al. MHC class I chain-related protein A antibodies and shedding are associated with the progression of multiple myeloma. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:1285.
96. Johnsen A.C., Haux J., Steinkjer B., Nonstad U., Egeberg K., Sundan A., et al. Regulation of APO-2 ligand/trail expression in NK cells-involvement in NK cell-mediated cytotoxicity. Cytokine 1999, 11:664.
97. Jung H., Hsiung B., Pestal K., Procyk E., Raulet D.H. RAE-1 ligands for the NKG2D receptor are regulated by E2F transcription factors, which control cell cycle entry. The Journal of Experimental Medicine 2012, 209:2409.
98. Kagi D., Ledermann B., Burki K., Seiler P., Odermatt B., Olsen K.J., et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 1994, 369:31.
99. Kaifu T., Escaliere B., Gastinel L.N., Vivier E., Baratin M. B7-H6/NKp30 interaction: A mechanism of alerting NK cells against tumors. Cellular and Molecular Life Sciences 2011, 68:3531.
100. Kang T.W., Yevsa T., Woller N., Hoenicke L., Wuestefeld T., Dauch D., et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 2011, 479:547.
101. Karre K., Ljunggren H.G., Piontek G., Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defense strategy. Nature 1986, 319:675.
102. Krizhanovsky V., Yon M., Dickins R.A., Hearn S., Simon J., Miething C., et al. Senescence of activated stellate cells limits liver fibrosis. Cell 2008, 134:657.
103. Lakshmikanth T., Burke S., Ali T.H., Kimpfler S., Ursini F., Ruggeri L., et al. NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo. The Journal of Clinical Investigation 2009, 119:1251.
104. Lanier L.L. NK cell receptors. Annual Review of Immunology 1998, 16:359.
105. Lee J.C., Lee K.M., Kim D.W., Heo D.S. Elevated TGF-beta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. The Journal of Immunology 2004, 172:7335.
106. Lee N., Llano M., Carretero M., Ishitani A., Navarro F., Lopez-Botet M., et al. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:5199.
107. Lee K.M., McNerney M.E., Stepp S.E., Mathew P.A., Schatzle J.D., Bennett M., et al. 2B4 acts as a non-major histocompatibility complex binding inhibitory receptor on mouse natural killer cells. The Journal of Experimental Medicine 2004, 199:1245.
108. Lee R.K., Spielman J., Zhao D.Y., Olsen K.J., Podack E.R. Perforin, Fas ligand, and tumor necrosis factor are the major cytotoxic molecules used by lymphokine-activated killer cells. The Journal of Immunology 1996, 157:1919.
109. Li H., Lakshmikanth T., Garofalo C., Enge M., Spinnler C., Anichini A., et al. Pharmacological activation of p53 triggers anticancer innate immune response through induction of ULBP2. Cell Cycle 2011, 10:3346.
110. Liu Z., Eltoum I.E., Guo B., Beck B.H., Cloud G.A., Lopez R.D. Protective immunosurveillance and therapeutic antitumor activity of {gamma}{delta} T Cells demonstrated in a mouse model of prostate cancer. The Journal of Immunology 2008, 180:6044.
111. Liu X.V., Ho S.S., Tan J.J., Kamran N., Gasser S. Ras activation induces expression of Raet1 family NK receptor ligands. Journal of Immunology 2012, 189:1826.
112. Ljunggren H.-G., Karre K. Host resistance directed selectively against H-2-deficient lymphoma variants. The Journal of Experimental Medicine 1985, 162:1745.
113. Ljunggren H.G., Karre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunology Today 1990, 11:237.
114. Long E. Regulation of immune responses through inhibitory receptors. Annual Review of Immunology 1999, 17:875.
115. Long E.O., Sik Kim H., Liu D., Peterson M.E., Rajagopalan S. Controlling natural killer cell responses: Integration of signals for activation and inhibition. Annual Review of Immunology 2013, 31:227.
116. Lord C.J., Ashworth A. The DNA damage response and cancer therapy. Nature 2012, 481:287.
117. Marten A., von Lilienfeld-Toal M., Buchler M.W., Schmidt J. Soluble MIC is elevated in the serum of patients with pancreatic carcinoma diminishing gammadelta T cell cytotoxicity. International Journal of Cancer 2006, 119:2359.
118. Martin-Fontecha A., Thomsen L.L., Brett S., Gerard C., Lipp M., Lanzavecchia A., et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nature Immunology 2004, 5:1260.
119. Masson D., Jarry A., Baury B., Blanchardie P., Laboisse C., Lustenberger P., et al. Overexpression of the CD155 gene in human colorectal carcinoma. Gut 2001, 49:236.
120. Matsushita H., Vesely M.D., Koboldt D.C., Rickert C.G., Uppaluri R., Magrini V.J., et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012, 482:400.
121. McNerney M.E., Guzior D., Kumar V. 2B4 (CD244)-CD48 interactions provide a novel MHC class I-independent system for NK cell self-tolerance in mice. Blood 2005, 106:1337.
122. Menard C., Blay J.Y., Borg C., Michiels S., Ghiringhelli F., Robert C., et al. Natural killer cell IFN-gamma levels predict long-term survival with imatinib mesylate therapy in gastrointestinal stromal tumor-bearing patients. Cancer Research 2009, 69:3563.
123. Mentlik A.N., Sanborn K.B., Holzbaur E.L., Orange J.S. Rapid lytic granule convergence to the MTOC in natural killer cells is dependent on dynein but not cytolytic commitment. Molecular Biology of the Cell 2010, 21:2241.
124. Moretta A., Bottino C., Vitale M., Pende D., Biassoni R., Mingari M.C., et al. Receptors for HLA class-I molecules in human natural killer cells. Annual Review of Immunology 1996, 14:619.
125. Moretta A., Bottino C., Vitale M., Pende D., Cantoni C., Mingari M.C., et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annual Review of Immunology 2001, 19:197.
126. Moretta A., Marcenaro E., Sivori S., Della Chiesa M., Vitale M., Moretta L. Early liaisons between cells of the innate immune system in inflamed peripheral tissues. Trends in Immunology 2005, 26:668.
127. Nakajima H., Cella M., Bouchon A., Grierson H.L., Lewis J., Duckett C.S., et al. Patients with X-linked lymphoproliferative disease have a defect in 2B4 receptor-mediated NK cell cytotoxicity. European Journal of Immunology 2000, 30:3309.
128. Navin N., Kendall J., Troge J., Andrews P., Rodgers L., McIndoo J., et al. Tumour evolution inferred by single-cell sequencing. Nature 2011, 472:90.
129. Nuckel H., Switala M., Sellmann L., Horn P.A., Durig J., Duhrsen U., et al. The prognostic significance of soluble NKG2D ligands in B-cell chronic lymphocytic leukemia. Leukemia 2010, 24:1152.
130. Ogasawara K., Benjamin J., Takaki R., Phillips J.H., Lanier L.L. Function of NKG2D in natural killer cell-mediated rejection of mouse bone marrow grafts. Nature Immunology 2005, 6:938.
131. Olcese L., Lang P., Vely F., Cambiaggi A., Marguet D., Blery M., et al. Human and mouse killer-cell inhibitory receptors recruit Ptp1c and Ptp1d protein tyrosine phosphatases. The Journal of Immunology 1996, 156:4531.
132. Oppenheim D.E., Roberts S.J., Clarke S.L., Filler R., Lewis J.M., Tigelaar R.E., et al. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nature Immunology 2005, 6:928.
133. O'Sullivan T., Saddawi-Konefka R., Vermi W., Koebel C.M., Arthur C., White J.M., et al. Cancer immunoediting by the innate immune system in the absence of adaptive immunity. The Journal of Experimental Medicine 2012, 209:1869.
134. Paschen A., Sucker A., Hill B., Moll I., Zapatka M., Nguyen X.D., et al. Differential clinical significance of individual NKG2D ligands in melanoma: Soluble ULBP2 as an indicator of poor prognosis superior to S100B. Clinical Cancer Research 2009, 15:5208.
135. Pende D., Parolini S., Pessino A., Sivori S., Augugliaro R., Morelli L., et al. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. Journal of Experimental Medicine 1999, 190:1505.
136. Pessino A., Sivori S., Bottino C., Malaspina A., Morelli L., Moretta L., et al. Molecular cloning of NKp46: A novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. Journal of Experimental Medicine 1998, 188:953.
137. Peter M.E., Krammer P.H. The CD95(APO-1/Fas) DISC and beyond. Cell Death and Differentiation 2003, 10:26.
138. Pogge von Strandmann E., Simhadri V.R., von Tresckow B., Sasse S., Reiners K.S., Hansen H.P., 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.
139. Raulet D.H. Roles of the NKG2D immunoreceptor and its ligands. Nature Reviews Immunology 2003, 3:781.
140. Raulet D.H., Gasser S., Gowen B.G., Deng W., Jung H. Regulation of ligands for the NKG2D activating receptor. Annual Review of Immunology 2013, 31:413.
141. Raulet D.H., Vance R.E., McMahon C.W. Regulation of the natural killer cell receptor repertoire. Annual Review of Immunology 2001, 19:291.
142. Ravetch J.V., Lanier L.L. Immune inhibitory receptors. Science 2000, 290:84.
143. Rosen D.B., Araki M., Hamerman J.A., Chen T., Yamamura T., Lanier L.L. A structural basis for the association of DAP12 with mouse, but not human, NKG2D. The Journal of Immunology 2004, 173:2470.
144. Ruckrich T., Steinle A. Attenuated natural killer (NK) cell activation through C-type lectin-like receptor NKp80 is due to an anomalous hemi-immunoreceptor tyrosine-based activation motif (HemITAM) with impaired Syk kinase recruitment capacity. The Journal of Biological Chemistry 2013, 288:17725.
145. Salih H.R., Antropius H., Gieseke F., Lutz S.Z., Kanz L., Rammensee H.G., et al. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 2003, 102:1389.
146. Salih H.R., Goehlsdorf D., Steinle A. Release of MICB molecules by tumor cells: Mechanism and soluble MICB in sera of cancer patients. Human Immunology 2006, 67:188.
147. Salih H.R., Rammensee H.G., Steinle A. Cutting edge: Down-regulation of MICA on human tumors by proteolytic shedding. The Journal of Immunology 2002, 169:4098.
148. Schreiber R.D., Old L.J., Smyth M.J. Cancer immunoediting: Integrating immunity's roles in cancer suppression and promotion. Science 2011, 331:1565.
149. Scott J.L., Dunn S.M., Jin B., Hillam A.J., Walton S., Berndt M.C., et al. Characterization of a novel membrane glycoprotein involved in platelet activation. The Journal of Biological Chemistry 1989, 264:13475.
150. Seaman W., Sleisenger M., Eriksson E., Koo G. Depletion of natural killer cells in mice by monoclonal antibody to NK-1.1. Reduction in host defense against malignancy without loss of cellular or humoral immunity. The Journal of Immunology 1987, 138:4539.
151. Seliger B., Ritz U., Abele R., Bock M., Tampe R., Sutter G., et al. Immune escape of melanoma: First evidence of structural alterations in two distinct components of the MHC class I antigen processing pathway. Cancer Research 2001, 61:8647.
152. Shankaran V., Ikeda H., Bruce A.T., White J.M., Swanson P.E., Old L.J., et al. IFN gamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001, 410:1107.
153. Shibuya A., Campbell D., Hannum C., Yssel H., Franz-Bacon K., McClanahan T., et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 1996, 4:573.
154. Shibuya K., Lanier L.L., Phillips J.H., Ochs H.D., Shimizu K., Nakayama E., et al. Physical and functional association of LFA-1 with DNAM-1 adhesion molecule. Immunity 1999, 11:615.
155. Shibuya K., Shirakawa J., Kameyama T., Honda S., Tahara-Hanaoka S., Miyamoto A., et al. CD226 (DNAM-1) is involved in lymphocyte function-associated antigen 1 costimulatory signal for naive T cell differentiation and proliferation. The Journal of Experimental Medicine 2003, 198:1829.
156. Shilling H.G., Young N., Guethlein L.A., Cheng N.W., Gardiner C.M., Tyan D., et al. Genetic control of human NK cell repertoire. The Journal of Immunology 2002, 169:239.
157. Shiloh Y., Ziv Y. The ATM protein kinase: Regulating the cellular response to genotoxic stress, and more. Nature Reviews Molecular Cell Biology 2013, 14:197.
158. Simhadri V.R., Reiners K.S., Hansen H.P., Topolar D., Simhadri V.L., Nohroudi K., et al. Dendritic cells release HLA-B-associated transcript-3 positive exosomes to regulate natural killer function. PLoS One 2008, 3:e3377.
159. Sivori S., Pende D., Bottino C., Marcenaro E., Pessino A., Biassoni R., et al. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells. European Journal of Immunology 1999, 29:1656.
160. Sivori S., Vitale M., Morelli L., Sanseverino L., Augugliaro R., Bottino C., et al. p46, a novel natural killer cell-specific surface molecule that mediates cell activation. The Journal of Experimental Medicine 1997, 186:1129.
161. Sloan K.E., Eustace B.K., Stewart J.K., Zehetmeier C., Torella C., Simeone M., et al. CD155/PVR plays a key role in cell motility during tumor cell invasion and migration. BMC Cancer 2004, 4:73.
162. Smyth M.J., Crowe N.Y., Godfrey D.I. NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. International Immunology 2001, 13:459.
163. Smyth M.J., Thia K.Y., Cretney E., Kelly J.M., Snook M.B., Forbes C.A., et al. Perforin is a major contributor to NK cell control of tumor metastasis. Journal of Immunology 1999, 162:6658.
164. Song H., Kim J., Cosman D., Choi I. Soluble ULBP suppresses natural killer cell activity via down-regulating NKG2D expression. Cellular Immunology 2006, 239:22.
165. Soriani A., Zingoni A., Cerboni C., Iannitto M.L., Ricciardi M.R., Di Gialleonardo V., 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, 113:3503.
166. Spaggiari G.M., Carosio R., Pende D., Marcenaro S., Rivera P., Zocchi M.R., et al. NK cell-mediated lysis of autologous antigen-presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30 and NKp46. European Journal of Immunology 2001, 31:1656.
167. Stanietsky N., Rovis T.L., Glasner A., Seidel E., Tsukerman P., Yamin R., et al. Mouse TIGIT inhibits NK-cell cytotoxicity upon interaction with PVR. European Journal of Immunology 2013, 43:2138.
168. Stewart S.A., Weinberg R.A. Telomeres: Cancer to human aging. Annual Review of Cell and Developmental Biology 2006, 22:531.
169. Sun J.C., Lanier L.L. Cutting edge: Viral infection breaks NK cell tolerance to "missing self". The Journal of Immunology 2008, 181:7453.
170. Sutherland C.L., Chalupny N.J., Schooley K., VandenBos T., Kubin M., Cosman D. UL16-binding proteins, novel MHC class I-related proteins, bind to NKG2D and activate multiple signaling pathways in primary NK cells. The Journal of Immunology 2002, 168:671.
171. Swann J.B., Vesely M.D., Silva A., Sharkey J., Akira S., Schreiber R.D., et al. Demonstration of inflammation-induced cancer and cancer immunoediting during primary tumorigenesis. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:652.
172. Tahara-Hanaoka S., Shibuya K., Onoda Y., Zhang H., Yamazaki S., Miyamoto A., et al. Functional characterization of DNAM-1 (CD226) interaction with its ligands PVR (CD155) and nectin-2 (PRR-2/CD112). International Immunology 2004, 16:533.
173. Tangye S.G., Phillips J.H., Lanier L.L., Nichols K.E. Functional requirement for SAP in 2B4-mediated activation of human natural killer cells as revealed by the X-linked lymphoproliferative syndrome. The Journal of Immunology 2000, 165:2932.
174. Tassi I., Presti R., Kim S., Yokoyama W.M., Gilfillan S., Colonna M. Phospholipase C-gamma 2 is a critical signaling mediator for murine NK cell activating receptors. Journal of Immunology 2005, 175:749.
175. Tchkonia T., Zhu Y., van Deursen J., Campisi J., Kirkland J.L. Cellular senescence and the senescent secretory phenotype: Therapeutic opportunities. The Journal of Clinical Investigation 2013, 123:966.
176. Textor S., Fiegler N., Arnold A., Porgador A., Hofmann T.G., Cerwenka A. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Research 2011, 71:5998.
177. Tokuyama M., Lorin C., Delebecque F., Jung H., Raulet D.H., Coscoy L. Expression of the RAE-1 family of stimulatory NK-cell ligands requires activation of the PI3K pathway during viral infection and transformation. PLoS Pathogens 2011, 7:e1002265.
178. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. The New England Journal of Medicine 2012, 366:2443.
179. Upshaw J.L., Schoon R.A., Dick C.J., Billadeau D.D., Leibson P.J. The isoforms of phospholipase C-gamma are differentially used by distinct human NK activating receptors. The Journal of Immunology 2005, 175:213.
180. Vaidya S.V., Stepp S.E., McNerney M.E., Lee J.K., Bennett M., Lee K.M., et al. Targeted disruption of the 2B4 gene in mice reveals an in vivo role of 2B4 (CD244) in the rejection of B16 melanoma cells. The Journal of Immunology 2005, 174:800.
181. van den Broek M.E., Kagi D., Ossendorp F., Toes R., Vamvakas S., Lutz W.K., et al. Decreased tumor surveillance in perforin-deficient mice. The Journal of Experimental Medicine 1996, 184:1781.
182. van den Broek M.F., Kagi D., Zinkernagel R.M., Hengartner H. Perforin dependence of natural killer cell-mediated tumor control in vivo. European Journal of Immunology 1995, 25:3514.
183. van der Bruggen P., Traversari C., Chomez P., Lurquin C., de Plaen E., van den Eynde B., et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 1991, 254:1643.
184. b. The Journal of Experimental Medicine 1998, 188:1841.
185. Veillette A. Immune regulation by SLAM family receptors and SAP-related adaptors. Nature Reviews Immunology 2006, 6:56.
186. Vermijlen D., Luo D., Froelich C.J., Medema J.P., Kummer J.A., Willems E., et al. Hepatic natural killer cells exclusively kill splenic/blood natural killer-resistant tumor cells by the perforin/granzyme pathway. Journal of Leukocyte Biology 2002, 72:668.
187. Vesely M.D., Kershaw M.H., Schreiber R.D., Smyth M.J. Natural innate and adaptive immunity to cancer. Annual Review of Immunology 2011, 29:235.
188. Vetter C.S., Groh V., thor Straten P., Spies T., Brocker E.B., Becker J.C. Expression of stress-induced MHC class I related chain molecules on human melanoma. The Journal of Investigative Dermatology 2002, 118:600.
189. Viaud S., Terme M., Flament C., Taieb J., Andre F., Novault S., et al. Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: A role for NKG2D ligands and IL-15Ralpha. PLoS One 2009, 4:e4942.
190. Vitale M., Bottino C., Sivori S., Sanseverino L., Castraconi R., Marcenaro E., 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. The Journal of Experimental Medicine 1998, 187:2065.
191. Vivier E., Raulet D.H., Moretta A., Caligiuri M.A., Zitvogel L., Lanier L.L., et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011, 331:44.
192. von Lilienfeld-Toal M., Frank S., Leyendecker C., Feyler S., Jarmin S., Morgan R., et al. Reduced immune effector cell NKG2D expression and increased levels of soluble NKG2D ligands in multiple myeloma may not be causally linked. Cancer Immunology, Immunotherapy 2010, 59:829.
193. Vousden K.H., Prives C. Blinded by the light: The growing complexity of p53. Cell 2009, 137:413.
194. Wang H., Yang D., Xu W., Wang Y., Ruan Z., Zhao T., et al. Tumor-derived soluble MICs impair CD3(+)CD56(+) NKT-like cell cytotoxicity in cancer patients. Immunology Letters 2008, 120:65.
195. Watson N.F., Spendlove I., Madjd Z., McGilvray R., Green A.R., Ellis I.O., et al. Expression of the stress-related MHC class I chain-related protein MICA is an indicator of good prognosis in colorectal cancer patients. International Journal of Cancer 2006, 118:1445.
196. Watzl C., Long E.O. Signal transduction during activation and inhibition of natural killer cells. Current Protocols in Immunology 2010, /edited by John E. Coligan [et al.] Chapter 11, Unit 11 9B.
197. Welte S., Kuttruff S., Waldhauer I., Steinle A. Mutual activation of natural killer cells and monocytes mediated by NKp80-AICL interaction. Nature Immunology 2006, 7:1334.
198. Wiemann K., Mittrucker H.W., Feger U., Welte S.A., Yokoyama W.M., Spies T., et al. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. The Journal of Immunology 2005, 175:720.
199. Wu J., Song Y., Bakker A.B., Bauer S., Spies T., Lanier L.L., et al. An activating immunoreceptor complex formed by NKG2D and DAP10. Science 1999, 285:730.
200. Xue W., Zender L., Miething C., Dickins R.A., Hernando E., Krizhanovsky V., et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007, 445:656.
201. Zamai L., Ahmad M., Bennett I.M., Azzoni L., Alnemri E.S., Perussia B. Natural killer (NK) cell-mediated cytotoxicity: Differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. The Journal of Experimental Medicine 1998, 188:2375.
202. Zingoni A., Ardolino M., Santoni A., Cerboni C. NKG2D and DNAM-1 activating receptors and their ligands in NK-T cell interactions: Role in the NK cell-mediated negative regulation of T cell responses. Frontiers in Immunology 2012, 3:408.
203. Zompi S., Hamerman J.A., Ogasawara K., Schweighoffer E., Tybulewicz V.L., Santo J.P., et al. NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases. Nature Immunology 2003, 4:565.