Control of Metastasis by NK Cells

Ali, 2014, Enrichment of CD56(dim)KIR+CD57+ highly cytotoxic NK cells in tumour-infiltrated lymph nodes of melanoma patients, Nat. Commun., 5, 5639, 10.1038/ncomms6639 Ames, 2015, NK cells preferentially target tumor cells with a cancer stem cell phenotype, J. Immunol., 195, 4010, 10.4049/jimmunol.1500447 Andrews, 2010, Innate immunity defines the capacity of antiviral T cells to limit persistent infection, J. Exp. Med., 207, 1333, 10.1084/jem.20091193 Aranda, 2015, Trial watch: adoptive cell transfer for oncological indications, Oncoimmunology, 4, e1046673, 10.1080/2162402X.2015.1046673 Armeanu, 2005, Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate, Cancer Res., 65, 6321, 10.1158/0008-5472.CAN-04-4252 Avgustinova, 2016, Tumour cell-derived Wnt7a recruits and activates fibroblasts to promote tumour aggressiveness, Nat. Commun., 7, 10305, 10.1038/ncomms10305 Baginska, 2013, Granzyme B degradation by autophagy decreases tumor cell susceptibility to natural killer-mediated lysis under hypoxia, Proc. Natl. Acad. Sci. USA, 110, 17450, 10.1073/pnas.1304790110 Barber, 2007, NK cells negatively regulate antigen presentation and tumor-specific CTLs in a syngeneic lymphoma model, J. Immunol., 178, 6140, 10.4049/jimmunol.178.10.6140 Beavis, 2013, Blockade of A2A receptors potently suppresses the metastasis of CD73+ tumors, Proc. Natl. Acad. Sci. USA, 110, 14711, 10.1073/pnas.1308209110 Benson, 2010, The PD-1/PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody, Blood, 116, 2286, 10.1182/blood-2010-02-271874 Benson, 2011, IPH2101, a novel anti-inhibitory KIR antibody, and lenalidomide combine to enhance the natural killer cell versus multiple myeloma effect, Blood, 118, 6387, 10.1182/blood-2011-06-360255 Benson, 2015, A phase I trial of the anti-KIR antibody IPH2101 and lenalidomide in patients with relapsed/refractory multiple myeloma, Clin. Cancer Res., 21, 4055, 10.1158/1078-0432.CCR-15-0304 Benson, 2012, A phase 1 trial of the anti-KIR antibody IPH2101 in patients with relapsed/refractory multiple myeloma, Blood, 120, 4324, 10.1182/blood-2012-06-438028 Berchem, 2016, Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-beta and miR23a transfer, Oncoimmunology, 5, e1062968, 10.1080/2162402X.2015.1062968 Best, 2015, RNA-seq of tumor-educated platelets enables blood-based pan-cancer, multiclass, and molecular pathway cancer diagnostics, Cancer Cell, 28, 666, 10.1016/j.ccell.2015.09.018 Bidwell, 2012, Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape, Nat. Med., 18, 1224, 10.1038/nm.2830 Blake, 2016, Suppression of metastases using a new lymphocyte checkpoint target for cancer immunotherapy, Cancer Discov., 6, 446, 10.1158/2159-8290.CD-15-0944 Boire, 2017, Complement component 3 adapts the cerebrospinal fluid for leptomeningeal metastasis, Cell, 168, 1101, 10.1016/j.cell.2017.02.025 Bos, 2009, Genes that mediate breast cancer metastasis to the brain, Nature, 459, 1005, 10.1038/nature08021 Bottos, 2016, Decreased NK-cell tumour immunosurveillance consequent to JAK inhibition enhances metastasis in breast cancer models, Nat. Commun., 7, 12258, 10.1038/ncomms12258 Briercheck, 2015, PTEN is a negative regulator of NK cell cytolytic function, J. Immunol., 194, 1832, 10.4049/jimmunol.1401224 Britschgi, 2012, JAK2/STAT5 inhibition circumvents resistance to PI3K/mTOR blockade: a rationale for cotargeting these pathways in metastatic breast cancer, Cancer Cell, 22, 796, 10.1016/j.ccr.2012.10.023 Bruno, 2013, The proangiogenic phenotype of natural killer cells in patients with non-small cell lung cancer, Neoplasia, 15, 133, 10.1593/neo.121758 Buque, 2015, Trial Watch: immunomodulatory monoclonal antibodies for oncological indications, Oncoimmunology, 4, e1008814, 10.1080/2162402X.2015.1008814 Buque, 2016, Trial Watch-Small molecules targeting the immunological tumor microenvironment for cancer therapy, Oncoimmunology, 5, e1149674, 10.1080/2162402X.2016.1149674 Carlsten, 2016, Checkpoint inhibition of KIR2D with the monoclonal antibody IPH2101 induces contraction and hyporesponsiveness of NK cells in patients with myeloma, Clin. Cancer Res., 22, 5211, 10.1158/1078-0432.CCR-16-1108 Carosella, 2015, HLA-G: an immune checkpoint molecule, Adv. Immunol., 127, 33, 10.1016/bs.ai.2015.04.001 Castriconi, 2009, NK cells recognize and kill human glioblastoma cells with stem cell-like properties, J. Immunol., 182, 3530, 10.4049/jimmunol.0802845 Cekic, 2014, Myeloid expression of adenosine A2A receptor suppresses T and NK cell responses in the solid tumor microenvironment, Cancer Res., 74, 7250, 10.1158/0008-5472.CAN-13-3583 Cerwenka, 2016, Natural killer cell memory in infection, inflammation and cancer, Nat. Rev. Immunol., 16, 112, 10.1038/nri.2015.9 Chan, 2010, DNAM-1/CD155 interactions promote cytokine and NK cell-mediated suppression of poorly immunogenic melanoma metastases, J. Immunol., 184, 902, 10.4049/jimmunol.0903225 Chan, 2014, The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions, Nat. Immunol., 15, 431, 10.1038/ni.2850 Chitadze, 2013, Shedding of endogenous MHC class I-related chain molecules A and B from different human tumor entities: heterogeneous involvement of the “a disintegrin and metalloproteases” 10 and 17, Int. J. Cancer, 133, 1557, 10.1002/ijc.28174 Chow, 2012, NLRP3 suppresses NK cell-mediated responses to carcinogen-induced tumors and metastases, Cancer Res., 72, 5721, 10.1158/0008-5472.CAN-12-0509 Coca, 1997, The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma, Cancer, 79, 2320, 10.1002/(SICI)1097-0142(19970615)79:12<2320::AID-CNCR5>3.0.CO;2-P Conlon, 2015, Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during first-in-human clinical trial of recombinant human interleukin-15 in patients with cancer, J. Clin. Oncol., 33, 74, 10.1200/JCO.2014.57.3329 Crome, 2017, A distinct innate lymphoid cell population regulates tumor-associated T cells, Nat. Med., 23, 368, 10.1038/nm.4278 Delahaye, 2011, Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors, Nat. Med., 17, 700, 10.1038/nm.2366 Delconte, 2016, CIS is a potent checkpoint in NK cell-mediated tumor immunity, Nat. Immunol., 17, 816, 10.1038/ni.3470 Della Chiesa, 2006, The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function, Blood, 108, 4118, 10.1182/blood-2006-03-006700 Deng, 2015, Antitumor immunity. A shed NKG2D ligand that promotes natural killer cell activation and tumor rejection, Science, 348, 136, 10.1126/science.1258867 Diefenbach, 2001, Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity, Nature, 413, 165, 10.1038/35093109 Donskov, 2006, Impact of immune parameters on long-term survival in metastatic renal cell carcinoma, J. Clin. Oncol., 24, 1997, 10.1200/JCO.2005.03.9594 Dunn, 2005, Interferon-gamma and cancer immunoediting, Immunol. Res., 32, 231, 10.1385/IR:32:1-3:231 Dupaul-Chicoine, 2015, The Nlrp3 inflammasome suppresses colorectal cancer metastatic growth in the liver by promoting natural killer cell tumoricidal activity, Immunity, 43, 751, 10.1016/j.immuni.2015.08.013 Eckelhart, 2011, A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development, Blood, 117, 1565, 10.1182/blood-2010-06-291633 Erler, 2006, Lysyl oxidase is essential for hypoxia-induced metastasis, Nature, 440, 1222, 10.1038/nature04695 Ferlazzo, 2014, Dendritic cell editing by natural killer cells, Crit. Rev. Oncog., 19, 67, 10.1615/CritRevOncog.2014010827 Fernandez, 1999, Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo, Nat. Med., 5, 405, 10.1038/7403 Ferrari de Andrade, 2014, Natural killer cells are essential for the ability of BRAF inhibitors to control BRAFV600E-mutant metastatic melanoma, Cancer Res., 74, 7298, 10.1158/0008-5472.CAN-14-1339 Fischer, 2015, Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance, Nature, 527, 472, 10.1038/nature15748 Galluzzi, 2017, Pharmacological modulation of autophagy: therapeutic potential and persisting obstacles, Nat. Rev. Drug Discov., 10.1038/nrd.2017.22 Galluzzi, 2015, Immunological effects of conventional chemotherapy and targeted anticancer agents, Cancer Cell, 28, 690, 10.1016/j.ccell.2015.10.012 Galluzzi, 2017, Immunogenic cell death in cancer and infectious disease, Nat. Rev. Immunol., 17, 97, 10.1038/nri.2016.107 Galluzzi, 2015, Autophagy in malignant transformation and cancer progression, EMBO J., 34, 856, 10.15252/embj.201490784 Gannon, 2009, Characterization of the intra-prostatic immune cell infiltration in androgen-deprived prostate cancer patients, J. Immunol. Methods, 348, 9, 10.1016/j.jim.2009.06.004 Gao, 2016, Multi-organ site metastatic reactivation mediated by non-canonical discoidin domain receptor 1 signaling, Cell, 166, 47, 10.1016/j.cell.2016.06.009 Georgoudaki, 2016, Reprogramming tumor-associated macrophages by antibody targeting inhibits cancer progression and metastasis, Cell Rep., 15, 2000, 10.1016/j.celrep.2016.04.084 Ghajar, 2015, Metastasis prevention by targeting the dormant niche, Nat. Rev. Cancer, 15, 238, 10.1038/nrc3910 Glasner, 2012, Recognition and prevention of tumor metastasis by the NK receptor NKp46/NCR1, J. Immunol., 188, 2509, 10.4049/jimmunol.1102461 Gotthardt, 2016, STAT5 is a key regulator in NK cells and acts as a molecular switch from tumor surveillance to tumor promotion, Cancer Discov., 6, 414, 10.1158/2159-8290.CD-15-0732 Gotthardt, 2014, Loss of STAT3 in murine NK cells enhances NK cell-dependent tumor surveillance, Blood, 124, 2370, 10.1182/blood-2014-03-564450 Gotwals, 2017, Prospects for combining targeted and conventional cancer therapy with immunotherapy, Nat. Rev. Cancer, 17, 286, 10.1038/nrc.2017.17 Guerra, 2008, NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy, Immunity, 28, 571, 10.1016/j.immuni.2008.02.016 Guillerey, 2015, Toll-like receptor 3 regulates NK cell responses to cytokines and controls experimental metastasis, Oncoimmunology, 4, e1027468, 10.1080/2162402X.2015.1027468 Guillerey, 2016, Targeting natural killer cells in cancer immunotherapy, Nat. Immunol., 17, 1025, 10.1038/ni.3518 Han, 2015, CAR-engineered NK cells targeting wild-type EGFR and EGFRvIII enhance killing of glioblastoma and patient-derived glioblastoma stem cells, Sci. Rep., 5, 11483, 10.1038/srep11483 Hanna, 2006, Decidual NK cells regulate key developmental processes at the human fetal-maternal interface, Nat. Med., 12, 1065, 10.1038/nm1452 Hanna, 2015, Patrolling monocytes control tumor metastasis to the lung, Science, 350, 985, 10.1126/science.aac9407 Harper, 2016, Mechanism of early dissemination and metastasis in Her2+ mammary cancer, Nature, 10.1038/nature20609 Hatfield, 2015, Immunological mechanisms of the antitumor effects of supplemental oxygenation, Sci. Transl. Med., 7, 277ra230, 10.1126/scitranslmed.aaa1260 Hay, 2016, Targeting CD73 in the tumor microenvironment with MEDI9447, Oncoimmunology, 5, e1208875, 10.1080/2162402X.2016.1208875 Hoshino, 2015, Tumour exosome integrins determine organotropic metastasis, Nature, 527, 329, 10.1038/nature15756 Hosseini, 2016, Early dissemination seeds metastasis in breast cancer, Nature, 10.1038/nature20785 Iguchi-Manaka, 2008, Accelerated tumor growth in mice deficient in DNAM-1 receptor, J. Exp. Med., 205, 2959, 10.1084/jem.20081611 Ilander, 2017, Increased proportion of mature NK cells is associated with successful imatinib discontinuation in chronic myeloid leukemia, Leukemia, 31, 1108, 10.1038/leu.2016.360 Iraolagoitia, 2016, NK cells restrain spontaneous antitumor CD8+ T cell priming through PD-1/PD-L1 interactions with dendritic cells, J. Immunol., 197, 953, 10.4049/jimmunol.1502291 Iribarren, 2016, Trial Watch: immunostimulation with Toll-like receptor agonists in cancer therapy, Oncoimmunology, 5, e1088631, 10.1080/2162402X.2015.1088631 Ishigami, 2000, Prognostic value of intratumoral natural killer cells in gastric carcinoma, Cancer, 88, 577, 10.1002/(SICI)1097-0142(20000201)88:3<577::AID-CNCR13>3.0.CO;2-V Ivashkiv, 2014, Regulation of type I interferon responses, Nat. Rev. Immunol., 14, 36, 10.1038/nri3581 Junttila, 2010, Superior in vivo efficacy of afucosylated trastuzumab in the treatment of HER2-amplified breast cancer, Cancer Res., 70, 4481, 10.1158/0008-5472.CAN-09-3704 Kang, 2003, A multigenic program mediating breast cancer metastasis to bone, Cancer Cell, 3, 537, 10.1016/S1535-6108(03)00132-6 Katlinski, 2017, Inactivation of interferon receptor promotes the establishment of immune privileged tumor microenvironment, Cancer Cell, 31, 194, 10.1016/j.ccell.2017.01.004 Klein, 2013, Selection and adaptation during metastatic cancer progression, Nature, 501, 365, 10.1038/nature12628 Knight, 2013, Host immunity contributes to the anti-melanoma activity of BRAF inhibitors, J. Clin. Invest., 123, 1371, 10.1172/JCI66236 Kohrt, 2014, Anti-KIR antibody enhancement of anti-lymphoma activity of natural killer cells as monotherapy and in combination with anti-CD20 antibodies, Blood, 123, 678, 10.1182/blood-2013-08-519199 Kopp, 2009, Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity, Cancer Res., 69, 7775, 10.1158/0008-5472.CAN-09-2123 Korde, 2014, A phase II trial of pan-KIR2D blockade with IPH2101 in smoldering multiple myeloma, Haematologica, 99, e81, 10.3324/haematol.2013.103085 Lakshmikanth, 2009, 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., 119, 1251, 10.1172/JCI36022 Lasek, 2014, Interleukin 12: still a promising candidate for tumor immunotherapy?, Cancer Immunol. Immunother., 63, 419, 10.1007/s00262-014-1523-1 Leong, 2015, PTEN regulates natural killer cell trafficking in vivo, Proc. Natl. Acad. Sci. USA, 112, E700, 10.1073/pnas.1413886112 Levental, 2009, Matrix crosslinking forces tumor progression by enhancing integrin signaling, Cell, 139, 891, 10.1016/j.cell.2009.10.027 Levi, 2015, Characterization of tumor infiltrating natural killer cell subset, Oncotarget, 6, 13835, 10.18632/oncotarget.3453 Levin, 2012, Exploiting a natural conformational switch to engineer an interleukin-2 'superkine', Nature, 484, 529, 10.1038/nature10975 Li, 2009, Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1, J. Immunol., 182, 240, 10.4049/jimmunol.182.1.240 Li, 2009, Structure of natural killer cell receptor KLRG1 bound to E-cadherin reveals basis for MHC-independent missing self recognition, Immunity, 31, 35, 10.1016/j.immuni.2009.04.019 Lima, 2014, Leukocyte driven-decidual angiogenesis in early pregnancy, Cell Mol. Immunol., 11, 522, 10.1038/cmi.2014.63 Liu, 2010, 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., 184, 3346, 10.4049/jimmunol.0903789 Liu, 2010, Selective inhibition of IDO1 effectively regulates mediators of antitumor immunity, Blood, 115, 3520, 10.1182/blood-2009-09-246124 Liu, 2016, Tumor exosomal RNAs promote lung pre-metastatic niche formation by activating alveolar epithelial TLR3 to recruit neutrophils, Cancer Cell, 30, 243, 10.1016/j.ccell.2016.06.021 Lopez-Soto, 2009, HDAC3 represses the expression of NKG2D ligands ULBPs in epithelial tumour cells: potential implications for the immunosurveillance of cancer, Oncogene, 28, 2370, 10.1038/onc.2009.117 Lopez-Soto, 2013, Epithelial-mesenchymal transition induces an antitumor immune response mediated by NKG2D receptor, J. Immunol., 190, 4408, 10.4049/jimmunol.1202950 Maecker, 2002, Epigenetic changes in tumor Fas levels determine immune escape and response to therapy, Cancer Cell, 2, 139, 10.1016/S1535-6108(02)00095-8 Malaise, 2014, KLRG1+ NK cells protect T-bet-deficient mice from pulmonary metastatic colorectal carcinoma, J. Immunol., 192, 1954, 10.4049/jimmunol.1300876 Malladi, 2016, Metastatic latency and immune evasion through autocrine inhibition of WNT, Cell, 165, 45, 10.1016/j.cell.2016.02.025 Martinet, 2015, DNAM-1 expression marks an alternative program of NK cell maturation, Cell Rep., 11, 85, 10.1016/j.celrep.2015.03.006 Massague, 2016, Metastatic colonization by circulating tumour cells, Nature, 529, 298, 10.1038/nature17038 McCulloch, 1989, Warfarin inhibits metastasis of Mtln3 rat mammary carcinoma without affecting primary tumour growth, Br. J. Cancer, 59, 179, 10.1038/bjc.1989.37 McDonald, 2017, Epigenomic reprogramming during pancreatic cancer progression links anabolic glucose metabolism to distant metastasis, Nat. Genet., 49, 367, 10.1038/ng.3753 McNab, 2015, Type I interferons in infectious disease, Nat. Rev. Immunol., 15, 87, 10.1038/nri3787 McWilliams, 2016, Therapeutic CD94/NKG2A blockade improves natural killer cell dysfunction in chronic lymphocytic leukemia, Oncoimmunology, 5, e1226720, 10.1080/2162402X.2016.1226720 Menard, 2009, Natural killer cell IFN-gamma levels predict long-term survival with imatinib mesylate therapy in gastrointestinal stromal tumor-bearing patients, Cancer Res., 69, 3563, 10.1158/0008-5472.CAN-08-3807 Merzoug, 2014, Conditional ablation of NKp46+ cells using a novel Ncr1(greenCre) mouse strain: NK cells are essential for protection against pulmonary B16 metastases, Eur. J. Immunol., 44, 3380, 10.1002/eji.201444643 Messaoudene, 2014, Mature cytotoxic CD56(bright)/CD16(+) natural killer cells can infiltrate lymph nodes adjacent to metastatic melanoma, Cancer Res., 74, 81, 10.1158/0008-5472.CAN-13-1303 Mittal, 2014, Antimetastatic effects of blocking PD-1 and the adenosine A2A receptor, Cancer Res., 74, 3652, 10.1158/0008-5472.CAN-14-0957 Mlecnik, 2014, Functional network pipeline reveals genetic determinants associated with in situ lymphocyte proliferation and survival of cancer patients, Sci. Transl. Med., 6, 228ra237, 10.1126/scitranslmed.3007240 Morandi, 2012, Dendritic cell editing by activated natural killer cells results in a more protective cancer-specific immune response, PLoS One, 7, e39170, 10.1371/journal.pone.0039170 Morel, 2016, Abstract 1491: IPH4301, an antibody targeting MICA and MICB exhibits potent cytotoxic activity and immunomodulatory properties for the treatment of cancer, Cancer Res., 76, 1491, 10.1158/1538-7445.AM2016-1491 Morvan, 2016, NK cells and cancer: you can teach innate cells new tricks, Nat. Rev. Cancer, 16, 7, 10.1038/nrc.2015.5 Muntasell, 2017, Targeting NK-cell checkpoints for cancer immunotherapy, Curr. Opin. Immunol., 45, 73, 10.1016/j.coi.2017.01.003 Nishikado, 2011, NK cell-depleting anti-asialo GM1 antibody exhibits a lethal off-target effect on basophils in vivo, J. Immunol., 186, 5766, 10.4049/jimmunol.1100370 O'Sullivan, 2012, Cancer immunoediting by the innate immune system in the absence of adaptive immunity, J. Exp. Med., 209, 1869, 10.1084/jem.20112738 Padua, 2008, TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4, Cell, 133, 66, 10.1016/j.cell.2008.01.046 Paget, 1989, The distribution of secondary growths in cancer of the breast. 1889, Cancer Metastasis Rev., 8, 98 Palumbo, 2005, Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells, Blood, 105, 178, 10.1182/blood-2004-06-2272 Paolino, 2014, The E3 ligase Cbl-b and TAM receptors regulate cancer metastasis via natural killer cells, Nature, 507, 508, 10.1038/nature12998 Paschen, 2009, Differential clinical significance of individual NKG2D ligands in melanoma: soluble ULBP2 as an indicator of poor prognosis superior to S100B, Clin. Cancer Res., 15, 5208, 10.1158/1078-0432.CCR-09-0886 Pasero, 2016, Inherent and tumor-driven immune tolerance in the prostate microenvironment impairs natural killer cell antitumor activity, Cancer Res., 76, 2153, 10.1158/0008-5472.CAN-15-1965 Pedersen, 2016, Voluntary running suppresses tumor growth through epinephrine- and IL-6-dependent NK cell mobilization and redistribution, Cell Metab., 23, 554, 10.1016/j.cmet.2016.01.011 Pedroza-Pacheco, 2013, Interaction between natural killer cells and regulatory T cells: perspectives for immunotherapy, Cell Mol Immunol, 10, 222, 10.1038/cmi.2013.2 Peinado, 2017, Pre-metastatic niches: organ-specific homes for metastases, Nat. Rev. Cancer, 17, 302, 10.1038/nrc.2017.6 Placke, 2012, Platelet-derived MHC class I confers a pseudonormal phenotype to cancer cells that subverts the antitumor reactivity of natural killer immune cells, Cancer Res., 72, 440, 10.1158/0008-5472.CAN-11-1872 Platonova, 2011, Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma, Cancer Res., 71, 5412, 10.1158/0008-5472.CAN-10-4179 Polansky, 2016, High dose CD11c-driven IL15 is sufficient to drive NK cell maturation and anti-tumor activity in a trans-presentation independent manner, Sci. Rep., 6, 19699, 10.1038/srep19699 Putz, 2013, CDK8-mediated STAT1-S727 phosphorylation restrains NK cell cytotoxicity and tumor surveillance, Cell Rep., 4, 437, 10.1016/j.celrep.2013.07.012 Putz, 2017, Targeting cytokine signaling checkpoint CIS activates NK cells to protect from tumor initiation and metastasis, Oncoimmunology, 6, e1267892, 10.1080/2162402X.2016.1267892 Putz, 2017, NK cell heparanase controls tumor invasion and immune surveillance, J. Clin. Invest., 10.1172/JCI92958 Rankin, 2016, Hypoxic control of metastasis, Science, 352, 175, 10.1126/science.aaf4405 Reddy, 2008, Immunomodulatory drugs stimulate natural killer-cell function, alter cytokine production by dendritic cells, and inhibit angiogenesis enhancing the anti-tumour activity of rituximab in vivo, Br. J. Haematol., 140, 36 Rhim, 2012, EMT and dissemination precede pancreatic tumor formation, Cell, 148, 349, 10.1016/j.cell.2011.11.025 Ryan, 1968, Reduced incidence of spontaneous metastases with long-term Coumadin therapy, Ann. Surg., 168, 163, 10.1097/00000658-196807000-00021 Sahin, 1995, Human neoplasms elicit multiple specific immune responses in the autologous host, Proc. Natl. Acad. Sci. USA, 92, 11810, 10.1073/pnas.92.25.11810 Sathe, 2014, Innate immunodeficiency following genetic ablation of Mcl1 in natural killer cells, Nat. Commun., 5, 4539, 10.1038/ncomms5539 Sceneay, 2012, Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche, Cancer Res., 72, 3906, 10.1158/0008-5472.CAN-11-3873 Schlecker, 2014, Metalloprotease-mediated tumor cell shedding of B7-H6, the ligand of the natural killer cell-activating receptor NKp30, Cancer Res., 74, 3429, 10.1158/0008-5472.CAN-13-3017 Schneider, 2014, Interferon-stimulated genes: a complex web of host defenses, Annu. Rev. Immunol., 32, 513, 10.1146/annurev-immunol-032713-120231 Schonberg, 2015, JAK inhibition impairs NK cell function in myeloproliferative neoplasms, Cancer Res., 75, 2187, 10.1158/0008-5472.CAN-14-3198 Seimetz, 2010, Development and approval of the trifunctional antibody catumaxomab (anti-EpCAM x anti-CD3) as a targeted cancer immunotherapy, Cancer Treat. Rev., 36, 458, 10.1016/j.ctrv.2010.03.001 Semeraro, 2014, Novel insights into the mechanism of action of lenalidomide, Oncoimmunology, 3, e28386, 10.4161/onci.28386 Semeraro, 2015, Natural killer cell mediated immunosurveillance of pediatric neuroblastoma, Oncoimmunology, 4, e1042202, 10.1080/2162402X.2015.1042202 Semeraro, 2013, Trial watch: lenalidomide-based immunochemotherapy, Oncoimmunology, 2, e26494, 10.4161/onci.26494 Senovilla, 2012, Trial watch: prognostic and predictive value of the immune infiltrate in cancer, Oncoimmunology, 1, 1323, 10.4161/onci.22009 Shankaran, 2001, IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity, Nature, 410, 1107, 10.1038/35074122 Sheppard, 2017, The immunoreceptor NKG2D promotes tumour growth in a model of hepatocellular carcinoma, Nat. Commun., 8, 13930, 10.1038/ncomms13930 Shultz, 2007, Humanized mice in translational biomedical research, Nat. Rev. Immunol., 7, 118, 10.1038/nri2017 Sistigu, 2014, Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy, Nat. Med., 20, 1301, 10.1038/nm.3708 Smyth, 2001, NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma, Int. Immunol., 13, 459, 10.1093/intimm/13.4.459 Smyth, 1999, Perforin is a major contributor to NK cell control of tumor metastasis, J. Immunol., 162, 6658, 10.4049/jimmunol.162.11.6658 Smyth, 2000, Differential tumor surveillance by natural killer (NK) and NKT cells, J. Exp. Med., 191, 661, 10.1084/jem.191.4.661 Spiegel, 2016, Neutrophils suppress intraluminal NK cell-mediated tumor cell clearance and enhance extravasation of disseminated carcinoma cells, Cancer Discov., 6, 630, 10.1158/2159-8290.CD-15-1157 Spranger, 2015, Melanoma-intrinsic beta-catenin signalling prevents anti-tumour immunity, Nature, 523, 231, 10.1038/nature14404 Stanietsky, 2009, The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity, Proc. Natl. Acad. Sci. USA, 106, 17858, 10.1073/pnas.0903474106 Steeg, 2016, Targeting metastasis, Nat. Rev. Cancer, 16, 201, 10.1038/nrc.2016.25 Street, 2001, Perforin and interferon-gamma activities independently control tumor initiation, growth, and metastasis, Blood, 97, 192, 10.1182/blood.V97.1.192 Street, 2004, Innate immune surveillance of spontaneous B cell lymphomas by natural killer cells and gammadelta T cells, J. Exp. Med., 199, 879, 10.1084/jem.20031981 Sun, 2010, CD39/ENTPD1 expression by CD4+Foxp3+ regulatory T cells promotes hepatic metastatic tumor growth in mice, Gastroenterology, 139, 1030, 10.1053/j.gastro.2010.05.007 Takeda, 2001, Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells, Nat. Med., 7, 94, 10.1038/83416 Tallerico, 2013, Human NK cells selective targeting of colon cancer-initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules, J. Immunol., 190, 2381, 10.4049/jimmunol.1201542 Tang, 2017, Smad3 promotes cancer progression by inhibiting E4BP4-mediated NK cell development, Nat. Commun., 8, 14677, 10.1038/ncomms14677 Thienpont, 2016, Tumour hypoxia causes DNA hypermethylation by reducing TET activity, Nature, 537, 63, 10.1038/nature19081 Tian, 2017, Mutual regulation of tumour vessel normalization and immunostimulatory reprogramming, Nature, 544, 250, 10.1038/nature21724 Topalian, 2015, Immune checkpoint blockade: a common denominator approach to cancer therapy, Cancer Cell, 27, 450, 10.1016/j.ccell.2015.03.001 Tu, 2015, CD160 is essential for NK-mediated IFN-gamma production, J. Exp. Med., 212, 415, 10.1084/jem.20131601 Turajlic, 2016, Metastasis as an evolutionary process, Science, 352, 169, 10.1126/science.aaf2784 Vacca, 2010, Crosstalk between decidual NK and CD14+ myelomonocytic cells results in induction of Tregs and immunosuppression, Proc. Natl. Acad. Sci. USA, 107, 11918, 10.1073/pnas.1001749107 Vacchelli, 2016, Trial Watch-Immunostimulation with cytokines in cancer therapy, Oncoimmunology, 5, e1115942, 10.1080/2162402X.2015.1115942 Vadrevu, 2014, Complement c5a receptor facilitates cancer metastasis by altering T-cell responses in the metastatic niche, Cancer Res., 74, 3454, 10.1158/0008-5472.CAN-14-0157 van der Weyden, 2017, Genome-wide in vivo screen identifies novel host regulators of metastatic colonization, Nature, 541, 233, 10.1038/nature20792 van Helden, 2015, Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection, J. Exp. Med., 212, 2015, 10.1084/jem.20150809 Vanpouille-Box, 2017, DNA exonuclease Trex1 regulates radiotherapy-induced tumor immunogenicity, Nat. Commun., 8, 15618, 10.1038/ncomms15618 Vences-Catalan, 2015, Tetraspanin CD81 promotes tumor growth and metastasis by modulating the functions of T regulatory and myeloid-derived suppressor cells, Cancer Res., 75, 4517, 10.1158/0008-5472.CAN-15-1021 Viel, 2016, TGF-beta inhibits the activation and functions of NK cells by repressing the mTOR pathway, Sci. Signal., 9, ra19, 10.1126/scisignal.aad1884 Waggoner, 2011, Natural killer cells act as rheostats modulating antiviral T cells, Nature, 481, 394, 10.1038/nature10624 Waggoner, 2010, Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8+ T cells, leading to prolonged viral persistence and altered pathogenesis, J. Clin. Invest., 120, 1925, 10.1172/JCI41264 Walker, 2013, Innate lymphoid cells–how did we miss them?, Nat. Rev. Immunol., 13, 75, 10.1038/nri3349 Wculek, 2015, Neutrophils support lung colonization of metastasis-initiating breast cancer cells, Nature, 528, 413, 10.1038/nature16140 Weiner, 2010, Monoclonal antibodies: versatile platforms for cancer immunotherapy, Nat. Rev. Immunol., 10, 317, 10.1038/nri2744 Welch, 2016, Breast-cancer tumor size, overdiagnosis, and mammography screening effectiveness, N. Engl. J. Med., 375, 1438, 10.1056/NEJMoa1600249 Werneck, 2008, T-bet plays a key role in NK-mediated control of melanoma metastatic disease, J. Immunol., 180, 8004, 10.4049/jimmunol.180.12.8004 Woloshin, 2012, Cancer screening campaigns–getting past uninformative persuasion, N. Engl. J. Med., 367, 1677, 10.1056/NEJMp1209407 Wu, 2008, Lenalidomide enhances natural killer cell and monocyte-mediated antibody-dependent cellular cytotoxicity of rituximab-treated CD20+ tumor cells, Clin. Cancer Res., 14, 4650, 10.1158/1078-0432.CCR-07-4405 Yamaguchi, 2012, Diagnostic and prognostic impact of serum-soluble UL16-binding protein 2 in lung cancer patients, Cancer Sci., 103, 1405, 10.1111/j.1349-7006.2012.02330.x Young, 2014, Targeting cancer-derived adenosine: new therapeutic approaches, Cancer Discov., 4, 879, 10.1158/2159-8290.CD-14-0341 Young, 2016, Co-inhibition of CD73 and A2AR adenosine signaling improves anti-tumor immune responses, Cancer Cell, 30, 391, 10.1016/j.ccell.2016.06.025 Yu, 2012, RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis, Nature, 487, 510, 10.1038/nature11217 Zaynagetdinov, 2015, Interleukin-5 facilitates lung metastasis by modulating the immune microenvironment, Cancer Res., 75, 1624, 10.1158/0008-5472.CAN-14-2379 Zhang, 2015, NKG2D ligands in tumor immunity: two sides of a coin, Front. Immunol., 6, 97, 10.3389/fimmu.2015.00097 Zhang, 2015, Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth, Nature, 527, 100, 10.1038/nature15376 Zhang, 2009, Latent bone metastasis in breast cancer tied to Src-dependent survival signals, Cancer Cell, 16, 67, 10.1016/j.ccr.2009.05.017 Zheng, 2015, Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer, Nature, 527, 525, 10.1038/nature16064 Zhu, 2016, Identification of CD112R as a novel checkpoint for human T cells, J. Exp. Med., 213, 167, 10.1084/jem.20150785 Zingoni, 2015, Genotoxic stress induces senescence-associated ADAM10-dependent release of NKG2D MIC ligands in multiple myeloma cells, J. Immunol., 195, 736, 10.4049/jimmunol.1402643 Zitvogel, 2015, Type I interferons in anticancer immunity, Nat. Rev. Immunol., 15, 405, 10.1038/nri3845