Tailoring Natural Killer cell immunotherapy to the tumour microenvironment

Morvan, 2016, NK cells and cancer: you can teach innate cells new tricks, Nat. Rev. Cancer, 16, 7, 10.1038/nrc.2015.5 Müller-Hermelink, 2008, TNFR1 signaling and IFN-gamma signaling determine whether T cells induce tumor dormancy or promote multistage carcinogenesis, Cancer Cell, 13, 507, 10.1016/j.ccr.2008.04.001 Lanier, 2008, Up on the tightrope: natural killer cell activation and inhibition, Nat. Immunol., 9, 495, 10.1038/ni1581 Sivori, 2014, TLR/NCR/KIR. Which one to use and when?, Front. Immunol., 5, 105, 10.3389/fimmu.2014.00105 Iannello, 2016, Immunosurveillance and immunotherapy of tumors by innate immune cells, Curr. Opin. Immunol., 38, 52, 10.1016/j.coi.2015.11.001 Malmberg, 2017, Immune selection during tumor checkpoint inhibition therapy paves way for NK-cell missing self recognition, Immunogenetics, 69, 547, 10.1007/s00251-017-1011-9 Hilton, 2017, Missing or altered self: human NK cell receptors that recognize HLA-C, Immunogenetics, 69, 567, 10.1007/s00251-017-1001-y Shifrin, 2014, NK cell self tolerance, responsiveness and missing self recognition, Semin. Immunol., 26, 138, 10.1016/j.smim.2014.02.007 Raulet, 2013, Regulation of ligands for the NKG2D activating receptor, Annu. Rev. Immunol., 31, 413, 10.1146/annurev-immunol-032712-095951 Eagle, 2009, Beyond stressed self: evidence for NKG2D ligand expression on healthy cells, Curr. Immunol. Rev., 5, 22, 10.2174/157339509787314369 Kruse, 2014, Natural cytotoxicity receptors and their ligands, Immunol. Cell Biol., 92, 221, 10.1038/icb.2013.98 Guillerey, 2016, Targeting natural killer cells in cancer immunotherapy, Nat. Immunol., 17, 1025, 10.1038/ni.3518 Rusakiewicz, 2013, Immune infiltrates are prognostic factors in localized gastrointestinal stromal tumors, Cancer Res., 73, 3499, 10.1158/0008-5472.CAN-13-0371 Imai, 2000, Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population, Lancet Lond. Engl., 356, 1795, 10.1016/S0140-6736(00)03231-1 Deng, 2015, Antitumor immunity. A shed NKG2D ligand that promotes natural killer cell activation and tumor rejection, Science, 348, 136, 10.1126/science.1258867 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 Grossenbacher, 2017, Leveraging natural killer cells for cancer immunotherapy, Immunotherapy, 9, 487, 10.2217/imt-2017-0013 Bachanova, 2014, NK cells in therapy of cancer, Crit. Rev. Oncogen., 19, 133, 10.1615/CritRevOncog.2014011091 Schreiber, 2011, Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion, Science, 331, 1565, 10.1126/science.1203486 Crome, 2013, Natural killer cells regulate diverse T cell responses, Trends Immunol., 34, 342, 10.1016/j.it.2013.03.002 Gasteiger, 2014, Interactions between innate and adaptive lymphocytes, Nat. Rev. Immunol., 14, 631, 10.1038/nri3726 Ugel, 2015, Tumor-induced myeloid deviation: when myeloid-derived suppressor cells meet tumor-associated macrophages, J. Clin. Invest., 125, 3365, 10.1172/JCI80006 Cao, 2009, Comparative genomics indicates the mammalian CD33rSiglec locus evolved by an ancient large-scale inverse duplication and suggests all Siglecs share a common ancestral region, Immunogenetics, 61, 401, 10.1007/s00251-009-0372-0 Cohen, 2010, Sialylation of 3-methylcholanthrene-induced fibrosarcoma determines antitumor immune responses during immunoediting, J. Immunol. Baltim. Md., 185, 5869 Ogata, 1992, Mucins bearing the cancer-associated sialosyl-Tn antigen mediate inhibition of natural killer cell cytotoxicity, Cancer Res., 52, 4741 Van Rinsum, 1986, Specific inhibition of human natural killer cell-mediated cytotoxicity by sialic acid and sialo-oligosaccharides, Int. J. Cancer, 38, 915, 10.1002/ijc.2910380620 Yogeeswaran, 1981, Correlation of glycosphingolipids and sialic acid in YAC-1 lymphoma variants with their sensitivity to natural killer-cell-mediated lysis, Int. J. Cancer, 28, 517, 10.1002/ijc.2910280419 Hudak, 2014, Glycocalyx engineering reveals a Siglec-based mechanism for NK cell immunoevasion, Nat. Chem. Biol., 10, 69, 10.1038/nchembio.1388 Jandus, 2014, Interactions between Siglec-7/9 receptors and ligands influence NK cell-dependent tumor immunosurveillance, J. Clin. Invest., 124, 1810, 10.1172/JCI65899 Xiao, 2016, Precision glycocalyx editing as a strategy for cancer immunotherapy, Proc. Natl. Acad. Sci. U. S. A., 113, 10304, 10.1073/pnas.1608069113 Prescher, 2017, Design, synthesis, and biological evaluation of small, high-affinity siglec-7 ligands: toward novel inhibitors of cancer immune evasion, J. Med. Chem., 60, 941, 10.1021/acs.jmedchem.6b01111 Tarbell, 2016, The glycocalyx and its significance in human medicine, J. Intern. Med., 280, 97, 10.1111/joim.12465 Hammond, 2014, The role of heparanase and sulfatases in the modification of heparan sulfate proteoglycans within the tumor microenvironment and opportunities for novel cancer therapeutics, Front. Oncol., 4, 195, 10.3389/fonc.2014.00195 Raman, 2010, Chemical tumor biology of heparan sulfate proteoglycans, Curr. Chem. Biol., 4, 20 Hecht, 2009, Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences, J. Proteome Res., 8, 712, 10.1021/pr800747c Brusilovsky, 2013, Genome-wide siRNA screen reveals a new cellular partner of NK cell receptor KIR2DL4: heparan sulfate directly modulates KIR2DL4-mediated responses, J. Immunol. Baltim. Md., 191, 5256 Warren, 2005, Evidence that the cellular ligand for the human NK cell activation receptor NKp30 is not a heparan sulfate glycosaminoglycan, J. Immunol. Baltim. Md., 175, 207 Hershkovitz, 2008, Altered glycosylation of recombinant NKp30 hampers binding to heparan sulfate: a lesson for the use of recombinant immunoreceptors as an immunological tool, Glycobiology, 18, 28, 10.1093/glycob/cwm125 Brandt, 2009, The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans, J. Exp. Med., 206, 1495, 10.1084/jem.20090681 Li, 2011, Structure of the human activating natural cytotoxicity receptor NKp30 bound to its tumor cell ligand B7-H6, J. Exp. Med., 208, 703, 10.1084/jem.20102548 Brusilovsky, 2015, Regulation of natural cytotoxicity receptors by heparan sulfate proteoglycans in–cis: a lesson from NKp44, Eur. J. Immunol., 45, 1180, 10.1002/eji.201445177 Bloushtain, 2004, Membrane-associated heparan sulfate proteoglycans are involved in the recognition of cellular targets by NKp30 and NKp46, J. Immunol. Baltim. Md., 173, 2392 Biroccio, 2013, TRF2 inhibits a cell-extrinsic pathway through which natural killer cells eliminate cancer cells, Nat. Cell Biol., 15, 818, 10.1038/ncb2774 Dredge, 2011, PG545, a dual heparanase and angiogenesis inhibitor, induces potent anti-tumour and anti-metastatic efficacy in preclinical models, Br. J. Cancer, 104, 635, 10.1038/bjc.2011.11 Brennan, 2016, Heparan sulfate mimetic PG545-mediated antilymphoma effects require TLR9-dependent NK cell activation, J. Clin. Invest., 126, 207, 10.1172/JCI76566 Erler, 2009, Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche, Cancer Cell, 15, 35, 10.1016/j.ccr.2008.11.012 Levental, 2009, Matrix crosslinking forces tumor progression by enhancing integrin signaling, Cell, 139, 891, 10.1016/j.cell.2009.10.027 Meyaard, 1997, LAIR-1, a novel inhibitory receptor expressed on human mononuclear leukocytes, Immunity, 7, 283, 10.1016/S1074-7613(00)80530-0 Lebbink, 2006, Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1, J. Exp. Med., 203, 1419, 10.1084/jem.20052554 Lebbink, 2009, Identification of multiple potent binding sites for human leukocyte associated Ig-like receptor LAIR on collagens II and III, Matrix Biol, J. Int. Soc. Matrix Biol., 28, 202, 10.1016/j.matbio.2009.03.005 Rygiel, 2011, Tumor-expressed collagens can modulate immune cell function through the inhibitory collagen receptor LAIR-1, Mol. Immunol., 49, 402, 10.1016/j.molimm.2011.09.006 Yang, 2006, Morphological appearance, content of extracellular matrix and vascular density of lung metastases predicts permissiveness to infiltration by adoptively transferred natural killer and T cells, Cancer Immunol. Immunother., 55, 699, 10.1007/s00262-005-0043-4 Afshar-Kharghan, 2017, The role of the complement system in cancer, J. Clin. Invest., 127, 780, 10.1172/JCI90962 Gelderman, 2004, Tumor-specific inhibition of membrane-bound complement regulatory protein Crry with bispecific monoclonal antibodies prevents tumor outgrowth in a rat colorectal cancer lung metastases model, Cancer Res., 64, 4366, 10.1158/0008-5472.CAN-03-2131 Watson, 2006, Expression of the membrane complement regulatory protein CD59 (protectin) is associated with reduced survival in colorectal cancer patients, Cancer Immunol. Immunother., 55, 973, 10.1007/s00262-005-0055-0 Caragine, 2002, Expression of rat complement control protein Crry on tumor cells inhibits rat natural killer cell-mediated cytotoxicity, Blood, 100, 3304, 10.1182/blood.V100.9.3304 Finberg, 1992, Decay-accelerating factor expression on either effector or target cells inhibits cytotoxicity by human natural killer cells, J. Immunol. Baltim. Md., 149, 2055 Macor, 2007, In vivo targeting of human neutralizing antibodies against CD55 and CD59 to lymphoma cells increases the antitumor activity of rituximab, Cancer Res., 67, 10556, 10.1158/0008-5472.CAN-07-1811 Bonavita, 2015, PTX3 is an extrinsic oncosuppressor regulating complement-dependent inflammation in cancer, Cell, 160, 700, 10.1016/j.cell.2015.01.004 Janelle, 2014, Transient complement inhibition promotes a tumor-specific immune response through the implication of natural killer cells, Cancer Immunol. Res., 2, 200, 10.1158/2326-6066.CIR-13-0173 Narni-Mancinelli, 2017, Complement factor P is a ligand for the natural killer cell-activating receptor NKp46, Sci. Immunol., 2, 10.1126/sciimmunol.aam9628 Narni-Mancinelli, 2012, Tuning of natural killer cell reactivity by NKp46 and helios calibrates T cell responses, Science, 335, 344, 10.1126/science.1215621 Alvarez-Breckenridge, 2012, NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors, Nat. Med., 18, 1827, 10.1038/nm.3013 Bulla, 2016, C1q acts in the tumour microenvironment as a cancer-promoting factor independently of complement activation, Nat. Commun., 7, 10.1038/ncomms10346 Son, 2012, C1q limits dendritic cell differentiation and activation by engaging LAIR-1, Proc. Natl. Acad. Sci. U. S. A., 109, E3160, 10.1073/pnas.1212753109 Trowsdale, 2015, Surveillance of cell and tissue perturbation by receptors in the LRC, Immunol. Rev., 267, 117, 10.1111/imr.12314 Lebbink, 2008, The soluble leukocyte-associated Ig-like receptor (LAIR)-2 antagonizes the collagen/LAIR-1 inhibitory immune interaction, J. Immunol. Baltim. Md., 180, 1662 Olde Nordkamp, 2014, Inhibition of the classical and lectin pathway of the complement system by recombinant LAIR-2, J. Innate Immun., 6, 284, 10.1159/000354976 Olde Nordkamp, 2011, Enhanced secretion of leukocyte-associated immunoglobulin-like receptor 2 (LAIR-2) and soluble LAIR-1 in rheumatoid arthritis: LAIR-2 is a more efficient antagonist of the LAIR-1-collagen inhibitory interaction than is soluble LAIR-1, Arthritis Rheum., 63, 3749, 10.1002/art.30612 Kang, 2015, The ITIM-containing receptor LAIR1 is essential for acute myeloid leukaemia development, Nat. Cell Biol., 17, 665, 10.1038/ncb3158 Xie, 2014, A non-stimulatory monoclonal antibody against the inhibitory immunoreceptor LAIR-1, Monoclon. Antibodies Immunodiagn. Immunother., 33, 141, 10.1089/mab.2013.0062 Collins, 2013, Elotuzumab directly enhances NK cell cytotoxicity against myeloma via CS1 ligation: evidence for augmented NK cell function complementing ADCC, Cancer Immunol. Immunother., 62, 1841, 10.1007/s00262-013-1493-8 Hsi, 2008, C.S.1, a potential new therapeutic antibody target for the treatment of multiple myeloma, Clin. Cancer Res., 14, 2775, 10.1158/1078-0432.CCR-07-4246 Tai, 2008, Anti-CS1 humanized monoclonal antibody HuLuc63 inhibits myeloma cell adhesion and induces antibody-dependent cellular cytotoxicity in the bone marrow milieu, Blood, 112, 1329, 10.1182/blood-2007-08-107292 Erdogan, 2017, Cancer-associated fibroblasts modulate growth factor signaling and extracellular matrix remodeling to regulate tumor metastasis, Biochem. Soc. Trans., 45, 229, 10.1042/BST20160387 Harper, 2014, Regulation of the anti-tumour immune response by cancer-associated fibroblasts, Semin. Cancer Biol., 25, 69, 10.1016/j.semcancer.2013.12.005 Park, 2011, Complex regulation of human NKG2D-DAP10 cell surface expression: opposing roles of the γc cytokines and TGF-β1, Blood, 118, 3019, 10.1182/blood-2011-04-346825 Siewiera, 2015, Natural cytotoxicity receptor splice variants orchestrate the distinct functions of human natural killer cell subtypes, Nat. Commun., 6, 10183, 10.1038/ncomms10183 Shemesh, 2016, Survival in acute myeloid leukemia is associated with NKp44 splice variants, Oncotarget, 7, 32933, 10.18632/oncotarget.8782 Delahaye, 2011, Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors, Nat. Med., 17, 700, 10.1038/nm.2366 Rusakiewicz, 2017, NKp30 isoforms and NKp30 ligands are predictive biomarkers of response to imatinib mesylate in metastatic GIST patients, Oncoimmunology, 6, e1137418, 10.1080/2162402X.2015.1137418 Viel, 2016, TGF-β inhibits the activation and functions of NK cells by repressing the mTOR pathway, Sci. Signal., 9, ra19, 10.1126/scisignal.aad1884 Pietra, 2012, Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity, Cancer Res., 72, 1407, 10.1158/0008-5472.CAN-11-2544 Li, 2012, Hepatocellular carcinoma-associated fibroblasts trigger NK cell dysfunction via PGE2 and IDO, Cancer Lett., 318, 154, 10.1016/j.canlet.2011.12.020 Kraman, 2010, Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha, Science, 330, 827, 10.1126/science.1195300 Özdemir, 2014, Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival, Cancer Cell, 25, 719, 10.1016/j.ccr.2014.04.005 Mancuso, 2017, Platelets: much more than bricks in a breached wall, Br. J. Haematol., 10.1111/bjh.14653 Ho-Tin-Noé, 2011, How platelets safeguard vascular integrity, J. Thromb. Haemost., 9, 56, 10.1111/j.1538-7836.2011.04317.x Astarita, 2012, Podoplanin: emerging functions in development, the immune system, and cancer, Front. Immunol., 3, 283, 10.3389/fimmu.2012.00283 Li, 2017, Elevated mean platelet volume predicts poor prognosis in colorectal cancer, Sci. Rep., 7, 10261, 10.1038/s41598-017-11053-y Ohuchi, 2017, Platelet count and mean platelet volume are associated with not only bone, soft tissue, and lymph node metastases but also with malignant pleural effusion in lung cancer patients, Neoplasma, 64, 140, 10.4149/neo_2017_118 Nieswandt, 1999, Lysis of tumor cells by natural killer cells in mice is impeded by platelets, Cancer Res., 59, 1295 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 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 Placke, 2012, GITR ligand provided by thrombopoietic cells inhibits NK cell antitumor activity, J. Immunol. Baltim. Md., 189, 154 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 Crome, 2017, A distinct innate lymphoid cell population regulates tumor-associated T cells, Nat. Med., 23, 368, 10.1038/nm.4278 Cortez, 2017, SMAD4 impedes the conversion of NK cells into ILC1-like cells by curtailing non-canonical TGF-β signaling, Nat. Immunol., 18, 995, 10.1038/ni.3809 Gao, 2017, Tumor immunoevasion by the conversion of effector NK cells into type 1 innate lymphoid cells, Nat. Immunol., 18, 1004, 10.1038/ni.3800 Buck, 2017, Metabolic instruction of immunity, Cell, 169, 570, 10.1016/j.cell.2017.04.004 Brand, 2016, LDHA-associated lactic acid production blunts tumor immunosurveillance by T and NK cells, Cell Metab., 24, 657, 10.1016/j.cmet.2016.08.011 Vaupel, 2016, Hypoxia-driven adenosine accumulation: a crucial microenvironmental factor promoting tumor progression, Adv. Exp. Med. Biol., 876, 177, 10.1007/978-1-4939-3023-4_22 Ohta, 2006, A2A adenosine receptor protects tumors from antitumor T cells, Proc. Natl. Acad. Sci. U. S. A., 103, 13132, 10.1073/pnas.0605251103 Beavis, 2012, CD73: a potent suppressor of antitumor immune responses, Trends Immunol., 33, 231, 10.1016/j.it.2012.02.009 Cortez, 2016, Transforming growth factor-β signaling guides the differentiation of innate lymphoid cells in salivary glands, Immunity, 44, 1127, 10.1016/j.immuni.2016.03.007 Young, 2014, Co-blockade of immune checkpoints and adenosine A2A receptor suppresses metastasis, Oncoimmunology, 3, 10.4161/21624011.2014.958952 Beavis, 2015, Adenosine receptor 2A blockade increases the efficacy of anti-PD-1 through enhanced antitumor T-cell responses, Cancer Immunol. Res., 3, 506, 10.1158/2326-6066.CIR-14-0211