Targeting NK-cell checkpoints for cancer immunotherapy

Current Opinion in Immunology

Volumn 45, Issue , 2017, Pages 73-81

  Muntasell, Aura ^a   Ochoa, Maria C ^b   Cordeiro, Luna ^b   Berraondo, Pedro ^a   López Díaz de Cerio, Ascension ^c   Cabo, Mariona ^a   López Botet, Miguel ^a   Melero, Ignacio ^b,c,d  

^a HOSPITAL DEL MAR   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c UNIVERSITY CLINIC OF NAVARRA   (Spain)

^d Autonomous University of Madrid Instituto de Investigación Hospital Universitario La Paz   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALT 803; CD137 ANTIGEN; HLA ANTIGEN CLASS 1; HYBRID PROTEIN; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 2; LIRILUMAB; MONALIZUMAB; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2A; PROGRAMMED DEATH 1 RECEPTOR; RITUXIMAB; TRASTUZUMAB; UNCLASSIFIED DRUG; URELUMAB; UTOMILUMAB; CANCER ANTIBODY; IL15 PROTEIN, HUMAN; IL2 PROTEIN, HUMAN; IMMUNOGLOBULIN RECEPTOR; RECOMBINANT PROTEIN;

ACUTE MYELOID LEUKEMIA; ADOPTIVE TRANSFER; ADVANCED CANCER; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN RECOGNITION; ANTINEOPLASTIC ACTIVITY; CANCER IMMUNOTHERAPY; CELL FUNCTION; CELL PROLIFERATION; DRUG EFFECT; DRUG HALF LIFE; DRUG SAFETY; DRUG TARGETING; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNOSURVEILLANCE; KIDNEY CARCINOMA; LOW DRUG DOSE; MELANOMA; MULTIPLE MYELOMA; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; REVIEW; SOLID TUMOR; TUMOR IMMUNITY; UNSPECIFIED SIDE EFFECT; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASM; PATHOLOGY; PROCEDURES;

ANTIBODIES, NEOPLASM; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-15; INTERLEUKIN-2; KILLER CELLS, NATURAL; NEOPLASMS; RECEPTORS, IMMUNOLOGIC; RECOMBINANT PROTEINS;

EID: 85013459761     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2017.01.003     Document Type: Review

References (104)

1. 1 Vivier, E., Tomasello, E., Baratin, M., Walzer, T., Ugolini, S., Functions of natural killer cells. Nat Immunol 9 (2008), 503–510.
2. 2 Lanier, L.L., Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 9 (2008), 495–502.
3. 3 Rydyznski, C.E., Waggoner, S.N., Boosting vaccine efficacy the natural (killer) way. Trends Immunol 36 (2015), 536–546.
4. 4 Schuster, I.S., Coudert, J.D., Andoniou, C.E., Degli-Esposti, M.A., Natural regulators: NK cells as modulators of T cell immunity. Front Immunol, 7, 2016, 235, 10.3389/fimmu.2016.00235 eCollection@2016.
5. 5 Kim, S., Iizuka, K., Aguila, H.L., Weissman, I.L., Yokoyama, W.M., In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc Natl Acad Sci U S A 97 (2000), 2731–2736.
6. 6 Smyth, M.J., Thia, K.Y., Cretney, E., Kelly, J.M., Snook, M.B., Forbes, C.A., Scalzo, A.A., Perforin is a major contributor to NK cell control of tumor metastasis. J Immunol 162 (1999), 6658–6662.
7. 7 Smyth, M.J., Swann, J., Cretney, E., Zerafa, N., Yokoyama, W.M., Hayakawa, Y., NKG2D function protects the host from tumor initiation. J Exp Med 202 (2005), 583–588.
8. 8 Street, S.E., Hayakawa, Y., Zhan, Y., Lew, A.M., MacGregor, D., Jamieson, A.M., Diefenbach, A., Yagita, H., Godfrey, D.I., Smyth, M.J., Innate immune surveillance of spontaneous B cell lymphomas by natural killer cells and gammadelta T cells. J Exp Med 199 (2004), 879–884.
9. 9 van den Broek, M.F., Kagi, D., Zinkernagel, R.M., Hengartner, H., Perforin dependence of natural killer cell-mediated tumor control in vivo. Eur J Immunol 25 (1995), 3514–3516.
10. 10 Imai, K., Matsuyama, S., Miyake, S., Suga, K., Nakachi, K., Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356 (2000), 1795–1799.
11. 11 Melero, I., Rouzaut, A., Motz, G., Coukos, G., T-Cell and NK-cell infiltration into solid tumors: a key limiting factor for efficacious cancer immunotherapy. Cancer Discov 4 (2014), 522–526.
12. 12 Cantoni, C., Huergo-Zapico, L., Parodi, M., Pedrazzi, M., Mingari, M.C., Moretta, A., Sparatore, B., Gonzalez, S., Olive, D., Bottino, C., et al. NK cells, tumor cell transition, and tumor progression in solid malignancies: new hints for NK-based immunotherapy?. J Immunol Res, 2016, 2016, 4684268, 10.1155/2016/4684268 Epub@2016.
13. 13 Gonzalez-Gugel, E., Saxena, M., Bhardwaj, N., Modulation of innate immunity in the tumor microenvironment. Cancer Immunol Immunother 65 (2016), 1261–1268.
14. 14 Ishigami, S., Natsugoe, S., Tokuda, K., Nakajo, A., Che, X., Iwashige, H., Aridome, K., Hokita, S., Aikou, T., Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 88 (2000), 577–583.
15. 15 Tian, W., Wang, L., Yuan, L., Duan, W., Zhao, W., Wang, S., Zhang, Q., A prognostic risk model for patients with triple negative breast cancer based on stromal natural killer cells, tumor-associated macrophages and growth-arrest specific protein 6. Cancer Sci 107 (2016), 882–889.
16. 16 Turkseven, M.R., Oygur, T., Evaluation of natural killer cell defense in oral squamous cell carcinoma. Oral Oncol 46 (2010), e34–e37.
17. 17 Michel, T., Poli, A., Cuapio, A., Briquemont, B., Iserentant, G., Ollert, M., Zimmer, J., Human CD56bright NK cells: an update. J Immunol 196 (2016), 2923–2931.
18. 18 Moretta, L., Dissecting CD56dim human NK cells. Blood 116 (2010), 3689–3691.
19. 19 Cerboni, C., Fionda, C., Soriani, A., Zingoni, A., Doria, M., Cippitelli, M., Santoni, A., The DNA damage response: a common pathway in the regulation of NKG2D and DNAM-1 ligand expression in normal, infected, and cancer cells. Front Immunol, 4, 2014, 508, 10.3389/fimmu.2013.00508 eCollection@2014.
20. 20 Marcus, A., Gowen, B.G., Thompson, T.W., Iannello, A., Ardolino, M., Deng, W., Wang, L., Shifrin, N., Raulet, D.H., Recognition of tumors by the innate immune system and natural killer cells. Adv Immunol 122 (2014), 91–128, 10.1016/B978-0-12-800267-4.00003-1.
21. 21 Pende, D., Rivera, P., Marcenaro, S., Chang, C.C., Biassoni, R., Conte, R., Kubin, M., Cosman, D., Ferrone, S., Moretta, L., Moretta, A., Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res 62 (2002), 6178–6186.
22. 22 Alvarez-Breckenridge, C.A., Yu, J., Price, R., Wojton, J., Pradarelli, J., Mao, H., Wei, M., Wang, Y., He, S., Hardcastle, J., et al. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat Med 18 (2012), 1827–1834.
23. 23 Delahaye, N.F., Rusakiewicz, S., Martins, I., Menard, C., Roux, S., Lyonnet, L., Paul, P., Sarabi, M., Chaput, N., Semeraro, M., et al. Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat Med 17 (2011), 700–707.
24. 24 Brandt, C.S., Baratin, M., Yi, E.C., Kennedy, J., Gao, Z., Fox, B., Haldeman, B., Ostrander, C.D., Kaifu, T., Chabannon, C., et al. 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 (2009), 1495–1503.
25. 25 Baychelier, F., Sennepin, A., Ermonval, M., Dorgham, K., Debre, P., Vieillard, V., Identification of a cellular ligand for the natural cytotoxicity receptor NKp44. Blood 122 (2013), 2935–2942.
26. 26 Pogge von, S.E., Simhadri, V.R., von, T.B., Sasse, S., Reiners, K.S., Hansen, H.P., Rothe, A., Boll, B., Simhadri, V.L., Borchmann, 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 27 (2007), 965–974.
27. 27 Bottino, C., Castriconi, R., Pende, D., Rivera, P., Nanni, M., Carnemolla, B., Cantoni, C., Grassi, J., Marcenaro, S., Reymond, N., et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med 198 (2003), 557–567.
28. 28 Iguchi-Manaka, A., Kai, H., Yamashita, Y., Shibata, K., Tahara-Hanaoka, S., Honda, S., Yasui, T., Kikutani, H., Shibuya, K., Shibuya, A., Accelerated tumor growth in mice deficient in DNAM-1 receptor. J Exp Med 205 (2008), 2959–2964.
29. 29 Baragano, R.A., Suarez-Alvarez, B., Lopez-Larrea, C., Secretory pathways generating immunosuppressive NKG2D ligands: new targets for therapeutic intervention. Oncoimmunology, 3, 2014, e28497 eCollection@2014.
30. 30 Concha-Benavente, F., Srivastava, R.M., Kansy, B., Ferris, R.L., PD-1 is a marker of activation on tumor infiltrating NK cells in head and neck cancer. J Immunother Cancer 3 (2015), 398–403.
31. 31• Schlecker, E., Fiegler, N., Arnold, A., Altevogt, P., Rose-John, S., Moldenhauer, G., Sucker, A., Paschen, A., von Strandmann, E.P., Textor, S., Cerwenka, A., Metalloprotease-mediated tumor cell shedding of B7-H6, the ligand of the natural killer cell-activating receptor NKp30. Cancer Res 74 (2014), 3429–3440 Identifies tumor-cell B7-H6 shedding as an immune escape mechanism from NKp30-mediated NK cell recognition.
32. 32 Diefenbach, A., Jensen, E.R., Jamieson, A.M., Raulet, D.H., Rae1 and H60 ligands of the NKG2D receptor stimulate tumor immunity. Nature 413 (2001), 165–171.
33. 33• Garrido, F., Aptsiauri, N., Doorduijn, E.M., Garcia Lora, A.M., van, H.T., The urgent need to recover MHC class I in cancers for effective immunotherapy. Curr Opin Immunol 39 (2016), 44–51, 10.1016/j.coi.2015.12.007 Epub@2016 Throughout review on reverisble and unreversible HLA class I alterations in diverse tumor settings.
34. 34 Kärre, K., Ljunggren, H.G., Piontek, G., Kiessling, R., Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319 (1986), 675–678.
35. 35 Parham, P., Moffett, A., Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat Rev Immunol 13 (2013), 133–144.
36. 36 Garcia-Beltran, W.F., Holzemer, A., Martrus, G., Chung, A.W., Pacheco, Y., Simoneau, C.R., Rucevic, M., Lamothe-Molina, P.A., Pertel, T., Kim, T.E., et al. Open conformers of HLA-F are high-affinity ligands of the activating NK-cell receptor KIR3DS1. Nat Immunol 17 (2016), 1067–1074.
37. 37 Chan, H.W., Kurago, Z.B., Stewart, C.A., Wilson, M.J., Martin, M.P., Mace, B.E., Carrington, M., Trowsdale, J., Lutz, C.T., DNA methylation maintains allele-specific KIR gene expression in human natural killer cells. J Exp Med 197 (2003), 245–255.
38. 38 Anfossi, N., Andre, P., Guia, S., Falk, C.S., Roetynck, S., Stewart, C.A., Breso, V., Frassati, C., Reviron, D., Middleton, D., et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 25 (2006), 331–342.
39. 39 Hoglund, P., Brodin, P., Current perspectives of natural killer cell education by MHC class I molecules. Nat Rev Immunol 10 (2010), 724–734.
40. 40 Raulet, D.H., Vance, R.E., Self-tolerance of natural killer cells. Nat Rev Immunol 6 (2006), 520–531.
41. 41 Björkström, N.K., Riese, P., Heuts, F., Andersson, S., Fauriat, C., Ivarsson, M.A., Björklund, A.T., Flodstrom-Tullberg, M., Michaëlsson, J., Rottenberg, M.E., et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 116 (2010), 3853–3864.
42. 42 Manser, A.R., Uhrberg, M., Age-related changes in natural killer cell repertoires: impact on NK cell function and immune surveillance. Cancer Immunol Immunother 65 (2016), 417–426.
43. 43 Béziat, V., Liu, L.L., Malmberg, J.A., Ivarsson, M.A., Sohlberg, E., Björklund, A.T., Retière, C., Sverremark-Ekström, E., Traherne, J., Ljungman, P., et al. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 121 (2013), 2678–2688.
44. 44 Gumá, M., Angulo, A., Vilches, C., Gómez-Lozano, N., Malats, N., López-Botet, M., Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104 (2004), 3664–3671.
45. 45• López-Botet, M., Muntasell, A., Vilches, C., The CD94/NKG2C+ NK-cell subset on the edge of innate and adaptive immunity to human cytomegalovirus infection. Semin Immunol 26 (2014), 145–151 Current overview on the mechanism underlying the differentiation and proliferation of adaptive NKG2C+ NK cells and their role in anti-viral defense.
46. 46•• Horowitz, A., Djaoud, Z., Nemat-Gorgani, N., Blokhuis, J., Hilton, H.G., Béziat, V., Malmberg, K.J., Norman, P.J., Guethlein, L.A., Class I HLA haplotypes form two schools that educate NK cells in different ways. Semin Immunol, 1, 2016, eaag1672 Genetic analysis of human populations worldwide showing the existance of two fundamental forms of HLA haplotype: one preferentially sulying CD94/NKG2A ligands and the other preferentially supplying KIR ligands.
47. 47 Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W.D., Tosti, A., Posati, S., Rogaia, D., Frassoni, F., Aversa, F., et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295 (2002), 2097–2100.
48. 48• Cichocki, F., Cooley, S., Davis, Z., Defor, T.E., Schlums, H., Zhang, B., Brunstein, C.G., Blazar, B.R., Wagner, J., Diamond, D.J., et al. CD56dimCD57+NKG2C+ NK cell expansion is associated with reduced leukemia relapse after reduced intensity HCT. Leukemia 30 (2016), 456–463 Data supporting that adaptive NKG2C+ NK cells expanding in response to CMV reactivation associate with reduced posttransplant leukemic relapse.
49. 49• Curti, A., Ruggeri, L., Parisi, S., Bontadini, A., Dan, E., Motta, M.R., Rizzi, S., Trabanelli, S., Ocadlikova, D., Lecciso, M., et al. Larger size of donor alloreactive NK cell repertoire correlates with better response to NK cell immunotherapy in elderly acute myeloid leukemia patients. Clin Cancer Res 22 (2016), 1914–1921 Shows that clinical efficacy of adoptively transferred haploidentical NK cells is influenced by the infused alloreactive NK-cell numbers.
50. 50 Miller, J.S., Soignier, Y., Panoskaltsis-Mortari, A., McNearney, S.A., Yun, G.H., Fautsch, S.K., McKenna, D., Le, C., Defor, T.E., Burns, L.J., et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105 (2005), 3051–3057.
51. 51 Cichocki, F., Verneris, M.R., Cooley, S., Bachanova, V., Brunstein, C.G., Blazar, B.R., Wagner, J., Schlums, H., Bryceson, Y.T., Weisdorf, D.J., Miller, J.S., The past, present, and future of NK cells in hematopoietic cell transplantation and adoptive transfer. Curr Top Microbiol Immunol 395 (2016), 225–243, 10.1007/82_2015_445.
52. 52 Della Chiesa, M., Moretta, L., Muccio, L., Bertaina, A., Moretta, F., Locatelli, F., Moretta, A., Haploidentical haematopoietic stem cell transplantation: role of NK cells and effect of cytomegalovirus infections. Curr Top Microbiol Immunol 395 (2016), 209–224, 10.1007/82_2015_450.
53. 53 Locatelli, F., Moretta, F., Brescia, L., Merli, P., Natural killer cells in the treatment of high-risk acute leukaemia. Semin Immunol 26 (2014), 173–179.
54. 54 Bryceson, Y.T., March, M.E., Ljunggren, H.G., Long, E.O., Activation, coactivation, and costimulation of resting human natural killer cells. Immunol Rev 214 (2006), 73–91.
55. 55 Awasthi, A., Ayello, J., Van de Ven, C., Elmacken, M., Sabulski, A., Barth, M.J., Czuczman, M.S., Islam, H., Klein, C., Cairo, M.S., Obinutuzumab (GA101) compared to rituximab significantly enhances cell death and antibody-dependent cytotoxicity and improves overall survival against CD20(+) rituximab-sensitive/-resistant Burkitt lymphoma (BL) and precursor B-acute lymphoblastic leukaemia (pre-B-ALL): potential targeted therapy in patients with poor risk CD20(+) BL and pre-B-ALL. Br J Haematol 171 (2015), 763–775.
56. 56 Trivedi, S., Srivastava, R.M., Concha-Benavente, F., Ferrone, S., Garcia-Bates, T.M., Li, J., Ferris, R.L., Anti-EGFR targeted monoclonal antibody isotype influences antitumor cellular immunity in head and neck cancer patients. Clin Cancer Res 22 (2016), 5229–5237.
57. 57 Varchetta, S., Gibelli, N., Oliviero, B., Nardini, E., Gennari, R., Gatti, G., Silva, L.S., Villani, L., Tagliabue, E., Menard, S., et al. Elements related to heterogeneity of antibody-dependent cell cytotoxicity in patients under trastuzumab therapy for primary operable breast cancer overexpressing Her2. Cancer Res 67 (2007), 11991–11999.
58. 58 Mellor, J.D., Brown, M.P., Irving, H.R., Zalcberg, J.R., Dobrovic, A., A critical review of the role of Fc gamma receptor polymorphisms in the response to monoclonal antibodies in cancer. J Hematol Oncol, 6, 2013, 1, 10.1186/1756-8722-6-1.
59. 59 Arnould, L., Gelly, M., Penault-Llorca, F., Benoit, L., Bonnetain, F., Migeon, C., Cabaret, V., Fermeaux, V., Bertheau, P., Garnier, J., et al. Trastuzumab-based treatment of HER2-positive breast cancer: an antibody-dependent cellular cytotoxicity mechanism?. Br J Cancer 94 (2006), 259–267.
60. 60 Romee, R., Foley, B., Lenvik, T., Wang, Y., Zhang, B., Ankarlo, D., Luo, X., Cooley, S., Verneris, M., Walcheck, B., Miller, J., NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood 121 (2013), 3599–3608.
61. 61•• Gleason, M.K., Ross, J.A., Warlick, E.D., Lund, T.C., Verneris, M.R., Wiernik, A., Spellman, S., Haagenson, M.D., Lenvik, A.J., Litzow, M.R., et al. CD16xCD33 bispecific killer cell engager (BiKE) activates NK cells against primary MDS and MDSC CD33+ targets. Blood 123 (2014), 3016–3026 Phase I clinical trial of CD16xCD33 BiKE in MDS patients showing successfully reversed immunosuppression of NK cells and induced MDS and MDSC target cell lysis.
62. 62 Romagne, F., Andre, P., Spee, P., Zahn, S., Anfossi, N., Gauthier, L., Capanni, M., Ruggeri, L., Benson, D.M. Jr., Blaser, B.W., et al. Preclinical characterization of 1-7F9, a novel human anti-KIR receptor therapeutic antibody that augments natural killer-mediated killing of tumor cells. Blood 114 (2009), 2667–2677.
63. 63• Ruggeri, L., Urbani, E., Andre, P., Mancusi, A., Tosti, A., Topini, F., Blery, M., Animobono, L., Romagne, F., Wagtmann, N., Velardi, A., Effects of anti-NKG2A antibody administration on leukemia and normal hematopoietic cells. Haematologica 101 (2016), 626–633 First characterisation of anti-NKG2A blocking antibody as enhancer of NK-cell anti-leukemic activity in immunodefficient mice engrafted with human NK and leukemic cells.
64. 64 Vey, N., Bourhis, J.H., Boissel, N., Bordessoule, D., Prebet, T., Charbonnier, A., Etienne, A., Andre, P., Romagne, F., Benson, D., et al. A phase 1 trial of the anti-inhibitory KIR mAb IPH2101 for AML in complete remission. Blood 120 (2012), 4317–4323.
65. 65•• Carlsten, M., Korde, N., Kotecha, R., Reger, R., Bor, S., Kazandjian, D., Landgren, O., Childs, R.W., Checkpoint inhibition of KIR2D with the monoclonal antibody IPH2101 induces contraction and hyporesponsiveness of NK-cells in patients with myeloma. Clin Cancer Res 22 (2016), 5211–5222 Shows that infusion of IPH2101 resulted in rapid reduction in both NK-cell responsiveness and KIR2D expression on the NK-cell surface.
66. 66 Korde, N., Carlsten, M., Lee, M.J., Minter, A., Tan, E., Kwok, M., Manasanch, E., Bhutani, M., Tageja, N., Roschewski, M., et al. A phase II trial of pan-KIR2D blockade with IPH2101 in smoldering multiple myeloma. Haematologica 99 (2014), e81–e83.
67. 67 Ardolino, M., Azimi, C.S., Iannello, A., Trevino, T.N., Horan, L., Zhang, L., Deng, W., Ring, A.M., Fischer, S., Garcia, K.C., Raulet, D.H., Cytokine therapy reverses NK cell anergy in MHC-deficient tumors. J Clin Invest 124 (2014), 4781–4794.
68. 68 Benson, D.M. Jr., Cohen, A.D., Jagannath, S., Munshi, N.C., Spitzer, G., Hofmeister, C.C., Efebera, Y.A., Andre, P., Zerbib, R., Caligiuri, M.A., A phase I trial of the Anti-KIR antibody IPH2101 and lenalidomide in patients with relapsed/refractory multiple myeloma. Clin Cancer Res 21 (2015), 4055–4061.
69. 69• Nijhof, I.S., Lammerts van Bueren, J.J., van, K.B., Andre, P., Morel, Y., Lokhorst, H.M., van de Donk, N.W., Parren, P.W., Daratumumab-mediated lysis of primary multiple myeloma cells is enhanced in combination with the human anti-KIR antibody IPH2102 and lenalidomide. Haematologica 100 (2015), 263–268 Shows the synergism of daratumumab-IPH2102 combination in improving NK cell-mediated myeloma cell lysis.
70. 70 Martinet, L., Smyth, M.J., Balancing natural killer cell activation through paired receptors. Nat Rev Immunol 15 (2015), 243–254.
71. 71 Bernhardt, G., TACTILE becomes tangible: CD96 discloses its inhibitory peculiarities. Nat Immunol 15 (2014), 406–408.
72. 72• Chan, C.J., Martinet, L., Gilfillan, S., Souza-Fonseca-Guimaraes, F., Chow, M.T., Town, L., Ritchie, D.S., Colonna, M., Andrews, D.M., Smyth, M.J., The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions. Nat Immunol 15 (2014), 431–438 First evidence on the role of CD96 as a checkpoint inhibitor of NK cells regulating metastasis control.
73. 73 Blake, S.J., Stannard, K., Liu, J., Allen, S., Yong, M.C., Mittal, D., Aguilera, A.R., Miles, J.J., Lutzky, V.P., de Andrade, L.F., et al. Suppression of metastases using a new lymphocyte checkpoint target for cancer immunotherapy. Cancer Discov 6 (2016), 446–459.
74. 74 Sarhan, D., Cichocki, F., Zhang, B., Yingst, A., Spellman, S.R., Cooley, S., Verneris, M.R., Blazar, B.R., Miller, J.S., Adaptive NK cells with low TIGIT expression are inherently resistant to myeloid-derived suppressor cells. Cancer Res 76 (2016), 5696–5706.
75. 75 Pesce, S., Greppi, M., Tabellini, G., Rampinelli, F., Parolini, S., Olive, D., Moretta, L., Moretta, A., Marcenaro, E., Identification of a subset of human natural killer cells expressing high levels of programmed death 1: a phenotypic and functional characterization. J Allergy Clin Immunol 139 (2017), 335–346.
76. 76 Beldi-Ferchiou, A., Lambert, M., Dogniaux, S., Vely, F., Vivier, E., Olive, D., Dupuy, S., Levasseur, F., Zucman, D., Lebbe, C., et al. PD-1 mediates functional exhaustion of activated NK cells in patients with Kaposi sarcoma. Oncotarget 7 (2016), 72961–72977.
77. 77 Benson, D.M. Jr., Bakan, C.E., Mishra, A., Hofmeister, C.C., Efebera, Y., Becknell, B., Baiocchi, R.A., Zhang, J., Yu, J., Smith, M.K., et al. 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 (2010), 2286–2294.
78. 78 Melero, I., Shuford, W.W., Newby, S.A., Aruffo, A., Ledbetter, J.A., Hellstrom, K.E., Mittler, R.S., Chen, L., Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat Med 3 (1997), 682–685.
79. 79 Melero, I., Johnston, J.V., Shufford, W.W., Mittler, R.S., Chen, L., NK1.1 cells express 4-1BB (CDw137) costimulatory molecule and are required for tumor immunity elicited by anti-4-1BB monoclonal antibodies. Cell Immunol 190 (1998), 167–172.
80. 80 Murillo, O., Arina, A., Hervas-Stubbs, S., Gupta, A., McCluskey, B., Dubrot, J., Palazon, A., Azpilikueta, A., Ochoa, M.C., Alfaro, C., et al. Therapeutic antitumor efficacy of anti-CD137 agonistic monoclonal antibody in mouse models of myeloma. Clin Cancer Res 14 (2008), 6895–6906.
81. 81 Murillo, O., Dubrot, J., Palazon, A., Arina, A., Azpilikueta, A., Alfaro, C., Solano, S., Ochoa, M.C., Berasain, C., Gabari, I., et al. In vivo depletion of DC impairs the anti-tumor effect of agonistic anti-CD137 mAb. Eur J Immunol 39 (2009), 2424–2436.
82. 82 Baessler, T., Charton, J.E., Schmiedel, B.J., Grunebach, F., Krusch, M., Wacker, A., Rammensee, H.G., Salih, H.R., CD137 ligand mediates opposite effects in human and mouse NK cells and impairs NK-cell reactivity against human acute myeloid leukemia cells. Blood 115 (2010), 3058–3069.
83. 83 Wilcox, R.A., Tamada, K., Strome, S.E., Chen, L., Signaling through NK cell-associated CD137 promotes both helper function for CD8+ cytolytic T cells and responsiveness to IL-2 but not cytolytic activity. J Immunol 169 (2002), 4230–4236.
84. 84 Lin, W., Voskens, C.J., Zhang, X., Schindler, D.G., Wood, A., Burch, E., Wei, Y., Chen, L., Tian, G., Tamada, K., et al. Fc-dependent expression of CD137 on human NK cells: insights into agonistic effects of anti-CD137 monoclonal antibodies. Blood 112 (2008), 699–707.
85. 85 Kohrt, H.E., Houot, R., Weiskopf, K., Goldstein, M.J., Scheeren, F., Czerwinski, D., Colevas, A.D., Weng, W.K., Clarke, M.F., Carlson, R.W., et al. Stimulation of natural killer cells with a CD137-specific antibody enhances trastuzumab efficacy in xenotransplant models of breast cancer. J Clin Invest 122 (2012), 1066–1075.
86. 86• Kohrt, H.E., Colevas, A.D., Houot, R., Weiskopf, K., Goldstein, M.J., Lund, P., Mueller, A., Sagiv-Barfi, I., Marabelle, A., Lira, R., et al. Targeting CD137 enhances the efficacy of cetuximab. J Clin Invest 124 (2014), 2668–2682 Together with Refs. [85] and [87], preclinical evidence on the synergy between CD137 agonist and ADCC inducing tumor-specific mAbs.
87. 87 Kohrt, H.E., Houot, R., Goldstein, M.J., Weiskopf, K., Alizadeh, A.A., Brody, J., Muller, A., Pachynski, R., Czerwinski, D., Coutre, S., et al. CD137 stimulation enhances the antilymphoma activity of anti-CD20 antibodies. Blood 117 (2011), 2423–2432.
88. 88 Delconte, R.B., Kolesnik, T.B., Dagley, L.F., Rautela, J., Shi, W., Putz, E.M., Stannard, K., Zhang, J.G., Teh, C., Firth, M., et al. CIS is a potent checkpoint in NK cell-mediated tumor immunity. Nat Immunol 17 (2016), 816–824.
89. 89 Gotthardt, D., Putz, E.M., Grundschober, E., Prchal-Murphy, M., Straka, E., Kudweis, P., Heller, G., Bago-Horvath, Z., Witalisz-Siepracka, A., Cumaraswamy, A.A., et al. STAT5 is a key regulator in NK cells and acts as a molecular switch from tumor surveillance to tumor promotion. Cancer Discov 6 (2016), 414–429.
90. 90 Waldmann, T.A., The shared and contrasting roles of IL2 and IL15 in the life and death of normal and neoplastic lymphocytes: implications for cancer therapy. Cancer Immunol Res 3 (2015), 219–227.
91. 91 Atkins, M.B., Regan, M., McDermott, D., Update on the role of interleukin 2 and other cytokines in the treatment of patients with stage IV renal carcinoma. Clin Cancer Res 10 (2004), 6342S–6346S.
92. 92 Vacchelli, E., Aranda, F., Bloy, N., Buque, A., Cremer, I., Eggermont, A., Fridman, W.H., Fucikova, J., Galon, J., Spisek, R., et al. Trial watch-immunostimulation with cytokines in cancer therapy. Oncoimmunology, 5, 2015, e1115942.
93. 93 Levin, A.M., Bates, D.L., Ring, A.M., Krieg, C., Lin, J.T., Su, L., Moraga, I., Raeber, M.E., Bowman, G.R., Novick, P., et al. Exploiting a natural conformational switch to engineer an interleukin-2 ‘superkine’. Nature 484 (2012), 529–533.
94. 94 Sim, G.C., Liu, C., Wang, E., Liu, H., Creasy, C., Dai, Z., Overwijk, W.W., Roszik, J., Marincola, F.M., Hwu, P., et al. IL-2 variant circumvents ICOS+ regulatory T cell expansion and promotes NK cell activation. Cancer Immunol Res 4 (2016), 983–994.
95. 95• Conlon, K.C., Lugli, E., Welles, H.C., Rosenberg, S.A., Fojo, A.T., Morris, J.C., Fleisher, T.A., Dubois, S.P., Perera, L.P., Stewart, D.M., et al. 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 (2015), 74–82 First-in-human clinical evidence on the effects of recombinant human IL-15 on NK cells following infusion to cancer patients.
96. 96• Liu, B., Kong, L., Han, K., Hong, H., Marcus, W.D., Chen, X., Jeng, E.K., Alter, S., Zhu, X., Rubinstein, M.P., et al. A novel fusion of ALT-803 (IL-15 Superagonist) with an antibody demonstrates antigen-specific antitumor responses. J Biol Chem 29 (2016), 23869–23881 Together with Ref. [97] characterization of IL-15N72D/IL-15RαSuFc complex, also known as ALT-803, as an IL-15 superagonist with potent antitumor immunotherapeutic potential.
97. 97• Kim, P.S., Kwilas, A.R., Xu, W., Alter, S., Jeng, E.K., Wong, H.C., Schlom, J., Hodge, J.W., IL-15 superagonist/IL-15RalphaSushi-Fc fusion complex (IL-15SA/IL-15RalphaSu-Fc; ALT-803) markedly enhances specific subpopulations of NK and memory CD8+ T cells, and mediates potent anti-tumor activity against murine breast and colon carcinomas. Oncotarget 7 (2016), 16130–16145 Together with Ref. [96] characterization of IL-15N72D/IL-15RαSuFc complex, also known as ALT-803, as an IL-15 superagonist with potent antitumor immunotherapeutic potential.
98. 98 Ng, S., Deng, J., Chinnadurai, R., Yuan, S., Pennati, A., Galipeau, J., Stimulation of natural killer cell-mediated tumor immunity by an IL15/TGFbeta-neutralizing fusion protein. Cancer Res 76 (2016), 5683–5695.
99. 99 Ochoa, M.C., Fioravanti, J., Rodriguez, I., Hervas-Stubbs, S., Azpilikueta, A., Mazzolini, G., Gurpide, A., Prieto, J., Pardo, J., Berraondo, P., Melero, I., Antitumor immunotherapeutic and toxic properties of an HDL-conjugated chimeric IL-15 fusion protein. Cancer Res 73 (2013), 139–149.
100. 100 Smyth, M.J., Taniguchi, M., Street, S.E., The anti-tumor activity of IL-12: mechanisms of innate immunity that are model and dose dependent. J Immunol 165 (2000), 2665–2670.
101. 101 Yue, T., Zheng, X., Dou, Y., Zheng, X., Sun, R., Tian, Z., Wei, H., Interleukin 12 shows a better curative effect on lung cancer than paclitaxel and cisplatin doublet chemotherapy. BMC Cancer, 16, 2016, 665, 10.1186/s12885-016-2701-7.
102. 102• Zhang, L., Morgan, R.A., Beane, J.D., Zheng, Z., Dudley, M.E., Kassim, S.H., Nahvi, A.V., Ngo, L.T., Sherry, R.M., Phan, G.Q., et al. Tumor-infiltrating lymphocytes genetically engineered with an inducible gene encoding interleukin-12 for the immunotherapy of metastatic melanoma. Clin Cancer Res 21 (2015), 2278–2288 First-in-human clinical trial, administration of TILs transduced with an inducible IL12 gene.
103. 103 Romee, R., Schneider, S.E., Leong, J.W., Chase, J.M., Keppel, C.R., Sullivan, R.P., Cooper, M.A., Fehniger, T.A., Cytokine activation induces human memory-like NK cells. Blood 120 (2012), 4751–4760.
104. 104• Romee, R., Rosario, M., Berrien-Elliott, M.M., Wagner, J.A., Jewell, B.A., Schappe, T., Leong, J.W., Abdel-Latif, S., Schneider, S.E., Willey, S., et al. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci Transl Med, 8, 2016, 357ra123 First-in-human phase 1 clinical trial with adoptive transfer of cytokine-induced memory-like NK cells in AML patients.