Targeting the tumor microenvironment to improve natural killer cell-based immunotherapies: On being in the right place at the right time, with resilience

Human Vaccines and Immunotherapeutics

Volumn 12, Issue 3, 2016, Pages 607-611

  Murray, Shannon ^a   Lundqvist, Andreas ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Homing receptors; immunotherapy; myeloid derived suppressor cells (MDSC); natural killer (NK) cells; tumor microenvironment

Indexed keywords

CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CX3CR1; CHIMERIC ANTIGEN RECEPTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IPILIMUMAB; NATURAL KILLER CELL RECEPTOR NKG2D; PROSTAGLANDIN E2; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; ZOLEDRONIC ACID;

ANAPLASTIC THYROID CANCER; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; BONE METASTASIS; CANCER GROWTH; CANCER IMMUNOTHERAPY; CELL ISOLATION; CELL MIGRATION; HUMAN; IMMUNE RESPONSE; KIDNEY CARCINOMA; LYMPHOCYTIC INFILTRATION; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL; NONHUMAN; NOTE; REGULATORY T LYMPHOCYTE; SOLID TUMOR; SUPPRESSOR CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASMS; PROCEDURES;

ANIMALS; HUMANS; IMMUNOTHERAPY; KILLER CELLS, NATURAL; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84976476014     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1096458     Document Type: Note

References (50)

1. S.A.Rosenberg, N.P.Restifo, J.C.Yang, R.A.Morgan, M.E.Dudley. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008; 8:299-308; PMID:18354418; http://dx.doi.org/10.1038/nrc2355
2. M.K.Callahan, J.D.Wolchok. At the bedside: CTLA-4- and PD-1-blocking antibodies in cancer immunotherapy. J Leukoc Biol 2013; 94:41-53; PMID:23667165; http://dx.doi.org/10.1189/jlb.1212631
3. P.Leone, E.C.Shin, F.Perosa, A.Vacca, F.Dammacco, V.Racanelli. MHC class I antigen processing and presenting machinery: organization, function, and defects in tumor cells. J Natl Cancer Inst 2013; 105:1172-87; PMID:23852952; http://dx.doi.org/10.1093/jnci/djt184
4. B.Seliger, U.Wollscheid, F.Momburg, T.Blankenstein, C.Huber. Coordinate downregulation of multiple MHC class I antigen processing genes in chemical-induced murine tumor cell lines of distinct origin. Tissue antigens 2000; 56:327-36; PMID:11098932; http://dx.doi.org/10.1034/j.1399-0039.2000.560404.x
5. D.Atkins, S.Ferrone, G.E.Schmahl, S.Storkel, B.Seliger. Down-regulation of HLA class I antigen processing molecules: an immune escape mechanism of renal cell carcinoma? J Urol 2004; 171:885-9; PMID:14713847; http://dx.doi.org/10.1097/01.ju.0000094807.95420.fe
6. B.Seliger, A.Hohne, A.Knuth, H.Bernhard, B.Ehring, R.Tampe, C.Huber. Reduced membrane major histocompatibility complex class I density and stability in a subset of human renal cell carcinomas with low TAP and LMP expression. Clin Cancer Res 1996; 2:1427-33; PMID:9816317
7. D.J.Hicklin, Z.Wang, F.Arienti, L.Rivoltini, G.Parmiani, S.Ferrone. beta2-Microglobulin mutations, HLA class I antigen loss, and tumor progression in melanoma. J Clin Investig 1998; 101:2720-9; PMID:9637706; http://dx.doi.org/10.1172/JCI498
8. R.Kiessling, E.Klein, H.Wigzell. “Natural” killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol 1975; 5:112-7; PMID:1234049; http://dx.doi.org/10.1002/eji.1830050208
9. R.Kiessling, E.Klein, H.Pross, H.Wigzell. “Natural” killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol 1975; 5:117-21; PMID:1086218; http://dx.doi.org/10.1002/eji.1830050209
10. E.O.Long, H.S.Kim, D.Liu, M.E.Peterson, S.Rajagopalan. Controlling natural killer cell responses: integration of signals for activation and inhibition. Ann Rev Immunol 2013; 31:227-58; PMID:23516982; http://dx.doi.org/10.1146/annurev-immunol-020711-075005
11. K.Karre. Natural killer cell recognition of missing self. Nat Immunol 2008; 9:477-80; PMID:18425103; http://dx.doi.org/10.1038/ni0508-477
12. S.Bauer, V.Groh, J.Wu, A.Steinle, J.H.Phillips, L.L.Lanier, T.Spies. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999; 285:727-9; PMID:10426993; http://dx.doi.org/10.1126/science.285.5428.727
13. S.Kim, J.Poursine-Laurent, S.M.Truscott, L.Lybarger, Y.J.Song, L.Yang, A.R.French, J.B.Sunwoo, S.Lemieux, T.H.Hansen, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 2005; 436:709-13; PMID:16079848; http://dx.doi.org/10.1038/nature03847
14. J.M.Elliott, W.M.Yokoyama. Unifying concepts of MHC-dependent natural killer cell education. Trends Immunol 2011; 32:364-72; PMID:21752715; http://dx.doi.org/10.1016/j.it.2011.06.001
15. R.W.Childs, M.Carlsten. Therapeutic approaches to enhance natural killer cell cytotoxicity against cancer: the force awakens. Nat Rev Drug Dis 2015; 14:487-98; PMID:26000725; http://dx.doi.org/10.1038/nrd4506
16. J.S.Miller, Y.Soignier, A.Panoskaltsis-Mortari, S.A.McNearney, G.H.Yun, S.K.Fautsch, D.McKenna, C.Le, T.E.Defor, L.J.Burns, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 2005; 105:3051-7; PMID:15632206; http://dx.doi.org/10.1182/blood-2004-07-2974
17. A.Lundqvist, M.Berg, A.Smith, R.W.Childs. Bortezomib Treatment to Potentiate the Anti-tumor Immunity of Ex-vivo Expanded Adoptively Infused Autologous Natural Killer Cells. J Cancer 2011; 2:383-5; PMID:21750690; http://dx.doi.org/10.7150/jca.2.383
18. S.S.Somanchi, A.Somanchi, L.J.Cooper, D.A.Lee. Engineering lymph node homing of ex vivo-expanded human natural killer cells via trogocytosis of the chemokine receptor CCR7. Blood 2012; 119:5164-72; PMID:22498742; http://dx.doi.org/10.1182/blood-2011-11-389924
19. N.Shimasaki, H.Fujisaki, D.Cho, M.Masselli, T.Lockey, P.Eldridge, W.Leung, D.Campana. A clinically adaptable method to enhance the cytotoxicity of natural killer cells against B-cell malignancies. Cytotherapy 2012; 14:830-40; PMID:22458956; http://dx.doi.org/10.3109/14653249.2012.671519
20. F.N.Cho, T.H.Chang, C.W.Shu, M.C.Ko, S.K.Liao, K.H.Wu, M.S.Yu, S.J.Lin, Y.C.Hong, C.H.Chen, et al. Enhanced cytotoxicity of natural killer cells following the acquisition of chimeric antigen receptors through trogocytosis. PloS one 2014; 9:e109352.
21. M.K.Gleason, M.R.Verneris, D.A.Todhunter, B.Zhang, V.McCullar, S.X.Zhou, A.Panoskaltsis-Mortari, L.M.Weiner, D.A.Vallera, J.S.Miller. Bispecific and trispecific killer cell engagers directly activate human NK cells through CD16 signaling and induce cytotoxicity and cytokine production. Mol Cancer ther 2012; 11:2674-84; PMID:23075808; http://dx.doi.org/10.1158/1535-7163.MCT-12-0692
22. A.Lundqvist, S.I.Abrams, D.S.Schrump, G.Alvarez, D.Suffredini, M.Berg, R.Childs. Bortezomib and depsipeptide sensitize tumors to tumor necrosis factor-related apoptosis-inducing ligand: a novel method to potentiate natural killer cell tumor cytotoxicity. Cancer Res 2006; 66:7317-25; PMID:16849582; http://dx.doi.org/10.1158/0008-5472.CAN-06-0680
23. D.Sarhan, E.Wennerberg, P.D'Arcy, D.Gurajada, S.Linder, A.Lundqvist. A novel inhibitor of proteasome deubiquitinating activity renders tumor cells sensitive to TRAIL-mediated apoptosis by natural killer cells and T cells. Cancer Immunol Immunother 2013; 62:1359-68; PMID:23689729; http://dx.doi.org/10.1007/s00262-013-1439-1
24. E.Wennerberg, D.Sarhan, M.Carlsten, V.O.Kaminskyy, P.D'Arcy, B.Zhivotovsky, R.Childs, A.Lundqvist. Doxorubicin sensitizes human tumor cells to NK cell- and T-cell-mediated killing by augmented TRAIL receptor signaling. Int J Cancer J Int du Cancer 2013; 133:1643-52; PMID:23504627; http://dx.doi.org/10.1002/ijc.28163
25. D.Sarhan, P.D'Arcy, E.Wennerberg, M.Liden, J.Hu, O.Winqvist, C.Rolny, A.Lundqvist. Activated monocytes augment TRAIL-mediated cytotoxicity by human NK cells through release of IFN-gamma. Eur J Immunol 2012; PMID:22996291
26. I.Takanami, K.Takeuchi, M.Giga. The prognostic value of natural killer cell infiltration in resected pulmonary adenocarcinoma. The J Thorac Cardiovasc Surg 2001; 121:1058-63; PMID:11385371; http://dx.doi.org/10.1067/mtc.2001.113026
27. S.Ishigami, S.Natsugoe, K.Tokuda, A.Nakajo, X.Che, H.Iwashige, K.Aridome, S.Hokita, T.Aikou. Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 2000; 88:577-83; PMID:10649250; http://dx.doi.org/10.1002/(SICI)1097-0142(20000201)88:3%3c577::AID-CNCR13%3e3.0.CO;2-V
28. F.Donskov, H.von der Maase. Impact of immune parameters on long-term survival in metastatic renal cell carcinoma. J Clin Oncol 2006; 24:1997-2005; PMID:16648500; http://dx.doi.org/10.1200/JCO.2005.03.9594
29. C.Jochems, J.Schlom. Tumor-infiltrating immune cells and prognosis: the potential link between conventional cancer therapy and immunity. Exp Biol Med 2011; 236:567-79; PMID:21486861; http://dx.doi.org/10.1258/ebm.2011.011007
30. E.Wennerberg, V.Kremer, R.Childs, A.Lundqvist. CXCL10-induced migration of adoptively transferred human natural killer cells toward solid tumors causes regression of tumor growth in vivo. Cancer Immunol Immunother 2015; 64:225-35; PMID:25344904; http://dx.doi.org/10.1007/s00262-014-1629-5
31. M.Wendel, I.E.Galani, E.Suri-Payer, A.Cerwenka. Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands. Cancer Res 2008; 68:8437-45; PMID:18922917; http://dx.doi.org/10.1158/0008-5472.CAN-08-1440
32. E.Lavergne, B.Combadiere, O.Bonduelle, M.Iga, J.L.Gao, M.Maho, A.Boissonnas, P.M.Murphy, P.Debre, C.Combadiere. Fractalkine mediates natural killer-dependent antitumor responses in vivo. Cancer Res 2003; 63:7468-74; PMID:14612547
33. E.Wennerberg, A.Pfefferle, L.Ekblad, Y.Yoshimoto, V.Kremer, V.O.Kaminskyy, C.C.Juhlin, A.Hoog, I.Bodin, V.Svjatoha, et al. Human anaplastic thyroid carcinoma cells are sensitive to NK cell-mediated lysis via ULBP2/5/6 and chemoattract NK cells. Clin Cancer Res 2014; 20:5733-44; PMID:25212604; http://dx.doi.org/10.1158/1078-0432.CCR-14-0291
34. S.Platonova, J.Cherfils-Vicini, D.Damotte, L.Crozet, V.Vieillard, P.Validire, P.Andre, M.C.Dieu-Nosjean, M.Alifano, J.F.Regnard, et al. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res 2011; 71:5412-22; PMID:21708957; http://dx.doi.org/10.1158/0008-5472.CAN-10-4179
35. E.M.Levy, M.P.Roberti, J.Mordoh. Natural killer cells in human cancer: from biological functions to clinical applications. J Biomed Biotechnol 2011; 2011:676198; PMID:21541191; http://dx.doi.org/10.1155/2011/676198
36. T.F.Gajewski, H.Schreiber, Y.X.Fu. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 2013; 14:1014-22; PMID:24048123; http://dx.doi.org/10.1038/ni.2703
37. C.M.Diaz-Montero, M.L.Salem, M.I.Nishimura, E.Garrett-Mayer, D.J.Cole, A.J.Montero. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 2009; 58:49-59; PMID:18446337; http://dx.doi.org/10.1007/s00262-008-0523-4
38. K.Kono, H.Kawaida, A.Takahashi, H.Sugai, K.Mimura, N.Miyagawa, H.Omata, H.Fujii. CD4(+)CD25high regulatory T cells increase with tumor stage in patients with gastric and esophageal cancers. Cancer Immunol Immunother 2006; 55:1064-71; PMID:16328385; http://dx.doi.org/10.1007/s00262-005-0092-8
39. F.Ichihara, K.Kono, A.Takahashi, H.Kawaida, H.Sugai, H.Fujii. Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers. Clin Cancer Res 2003; 9:4404-8; PMID:14555512
40. M.R.Porembka, J.B.Mitchem, B.A.Belt, C.S.Hsieh, H.M.Lee, J.Herndon, W.E.Gillanders, D.C.Linehan, P.Goedegebuure. Pancreatic adenocarcinoma induces bone marrow mobilization of myeloid-derived suppressor cells which promote primary tumor growth. Cancer Immunol Immunother 2012; 61:1373-85; PMID:22215137; http://dx.doi.org/10.1007/s00262-011-1178-0
41. I.Poschke, R.Kiessling. On the armament and appearances of human myeloid-derived suppressor cells. Clin Immunol 2012; 144:250-68; PMID:22858650; http://dx.doi.org/10.1016/j.clim.2012.06.003
42. Y.Mao, I.Poschke, E.Wennerberg, Y.Pico de Coana, S.Egyhazi Brage, I.Schultz, J.Hansson, G.Masucci, A.Lundqvist, R.Kiessling. Melanoma-Educated CD14+ Cells Acquire a Myeloid-Derived Suppressor Cell Phenotype through COX-2-Dependent Mechanisms. Cancer Res 2013; 73:3877-87; PMID:23633486; http://dx.doi.org/10.1158/0008-5472.CAN-12-4115
43. I.Poschke, D.Mougiakakos, J.Hansson, G.V.Masucci, R.Kiessling. Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign. Cancer Res 2010; 70:4335-45; PMID:20484028; http://dx.doi.org/10.1158/0008-5472.CAN-09-3767
44. S.Kitano, M.A.Postow, C.G.Ziegler, D.Kuk, K.S.Panageas, C.Cortez, T.Rasalan, M.Adamow, J.Yuan, P.Wong, et al. Computational algorithm-driven evaluation of monocytic myeloid-derived suppressor cell frequency for prediction of clinical outcomes. Cancer Immunol Res 2014; 2:812-21; PMID:24844912; http://dx.doi.org/10.1158/2326-6066.CIR-14-0013
45. Y.Mao, D.Sarhan, A.Steven, B.Seliger, R.Kiessling, A.Lundqvist. Inhibition of tumor-derived prostaglandin-e2 blocks the induction of myeloid-derived suppressor cells and recovers natural killer cell activity. Clin Cancer Res 2014; 20:4096-106; PMID:24907113; http://dx.doi.org/10.1158/1078-0432.CCR-14-0635
46. Y.Pico de Coana, I.Poschke, G.Gentilcore, Y.Mao, M.Nystrom, J.Hansson, G.V.Masucci, R.Kiessling. Ipilimumab treatment results in an early decrease in the frequency of circulating granulocytic myeloid-derived suppressor cells as well as their Arginase1 production. Cancer Immunol Res 2013; 1:158-62; PMID:24777678; http://dx.doi.org/10.1158/2326-6066.CIR-13-0016
47. F.Ghiringhelli, C.Menard, M.Terme, C.Flament, J.Taieb, N.Chaput, P.E.Puig, S.Novault, B.Escudier, E.Vivier, et al. CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J Exp Med 2005; 202:1075-85; PMID:16230475; http://dx.doi.org/10.1084/jem.20051511
48. G.Gasteiger, S.Hemmers, M.A.Firth, A.Le Floc'h, M.Huse, J.C.Sun, A.Y.Rudensky. IL-2-dependent tuning of NK cell sensitivity for target cells is controlled by regulatory T cells. J Exp Med 2013; 210:1167-78; PMID:23650441; http://dx.doi.org/10.1084/jem.20122462
49. A.Lundqvist, H.Yokoyama, A.Smith, M.Berg, R.Childs. Bortezomib treatment and regulatory T-cell depletion enhance the antitumor effects of adoptively infused NK cells. Blood 2009; 113:6120-7; PMID:19202127; http://dx.doi.org/10.1182/blood-2008-11-190421
50. B.Yang, H.Liu, W.Shi, Z.Wang, S.Sun, G.Zhang, Y.Hu, T.Liu, S.Jiao. Blocking transforming growth factor-beta signaling pathway augments antitumor effect of adoptive NK-92 cell therapy. Int Immunopharmacol 2013; 17:198-204; PMID:23806302; http://dx.doi.org/10.1016/j.intimp.2013.06.003