Natural Killer Cell-Based Cancer Immunotherapy: A Review on 10 Years Completed Clinical Trials

References

• Kumar H, Kawai T, Akira S. Pathogen recognition by the innate immune system. Int Rev Immunol. 2011;30(1):16–34. doi:10.3109/08830185.2010.529976
   PubMed Web of Science ®Google Scholar
• Kiessling R, Klein E, Wigzell H. “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(2):112–117. doi:10.1002/eji.1830050208
   PubMed Web of Science ®Google Scholar
• Herberman RB, Nunn ME, Holden HT, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int J Cancer. 1975;16(2):230–239. doi:10.1002/eji.1830050208
   PubMed Web of Science ®Google Scholar
• Kalland T. Generation of natural killer cells from bone marrow precursors in vitro. Immunology. 1986;57(4):493–498.
   PubMed Web of Science ®Google Scholar
• Colucci F, Caligiuri MA, Di Santo JP. What does it take to make a natural killer?. Nat Rev Immunol. 2003;3(5):413–425. doi:10.1038/nri1088
   PubMed Web of Science ®Google Scholar
• Caldera LH, Leon-Ponte M, Acquatella G, Bianco NE, Blanca I. Bone marrow and peripheral blood natural killer cell activity in lymphomas. Its response to IL-2. Clin Exp Immunol. 1992;88(1):143–148. doi:10.1111/j.1365-2249.1992.tb03054.x
   PubMed Web of Science ®Google Scholar
• Freud AG, Yu J, Caligiuri MA. Human natural killer cell development in secondary lymphoid tissues. Seminars in Immunology. 2014;26(2):132–137. doi:10.1016/j.smim.2014.02.008
   PubMed Web of Science ®Google Scholar
• Carotta S, Pang SH, Nutt SL, Belz GT. Identification of the earliest NK-cell precursor in the mouse BM. Blood. 2011;117(20):5449–5452. doi:10.1182/blood-2010-11-318956
   PubMed Web of Science ®Google Scholar
• Freud AG, Yokohama A, Becknell B, Lee MT, Mao HC, Ferketich AK, Caligiuri MA. Evidence for discrete stages of human natural killer cell differentiation in vivo. J Exp Med. 2006;203(4):1033–1043. doi:10.1084/jem.20052507
   PubMed Web of Science ®Google Scholar
• Hughes T, Becknell B, Freud AG, McClory S, Briercheck E, Yu J, Mao C, Giovenzana C, Nuovo G, Wei L, et al. Interleukin-1beta selectively expands and sustains interleukin-22+ immature human natural killer cells in secondary lymphoid tissue. Immunity. 2010;32(6):803–814. doi:10.1016/j.immuni.2010.06.007
   PubMed Web of Science ®Google Scholar
• Yu J, Mao HC, Wei M, Hughes T, Zhang J, Park IK, et al. CD94 surface density identifies a functional intermediary between the CD56bright and CD56dim human NK-cell subsets. Blood. 2010;115(2):274–281. doi:10.1182/blood-2009-04-215491
   PubMed Web of Science ®Google Scholar
• Strowig T, Brilot F, Munz C. Noncytotoxic functions of NK cells: direct pathogen restriction and assistance to adaptive immunity. J Immunol. 2008;180(12):7785–7791. doi:10.4049/jimmunol.180.12.7785
   PubMed Web of Science ®Google Scholar
• Wu L, Van Kaer L. Natural killer T cells and autoimmune disease. Curr Mol Med. 2009;9(1):4–14. doi:10.2174/156652409787314534
   PubMed Web of Science ®Google Scholar
• Health NIo. Definition of cytokine-induced killer cells – NCI Drug Dictionary. National Cancer Institute; 2017. https://www.cancer.gov/publications/dictionaries/cancer-drug/def/cytokine-induced-killer-cells
   Google Scholar
• Guo Y, Han W. Cytokine-induced killer (CIK) cells: from basic research to clinical translation. Chin J Cancer. 2015;34(3):99–107. doi:10.1186/s40880-015-0002-1
   PubMedGoogle Scholar
• O'Sullivan TE, Sun JC, Lanier LL. Natural killer cell memory. Immunity. 2015;43(4):634–645. doi:10.1016/j.immuni.2015.09.013
   PubMed Web of Science ®Google Scholar
• Rolle A, Pollmann J, Cerwenka A. Memory of infections: an emerging role for natural killer cells. PLoS Pathog. 2013;9(9):e1003548 doi:10.1371/journal.ppat.1003548
   PubMed Web of Science ®Google Scholar
• Davis ZB, Felices M, Verneris MR, Miller JS. Natural killer cell adoptive transfer therapy: exploiting the first line of defense against. Cancer J. 2015;21(6):486–491. doi:10.1097/PPO.0000000000000156
   PubMed Web of Science ®Google Scholar
• Cerwenka A, Lanier LL. Natural killer cell memory in infection, inflammation and cancer. Nat Rev Immunol. 2016;16(2):112–123. doi:10.1038/nri.2015.9
   PubMed Web of Science ®Google Scholar
• Foley B, Cooley S, Verneris MR, Curtsinger J, Luo X, Waller EK, Anasetti C, Weisdorf D, Miller JS. Human cytomegalovirus (CMV)-induced memory-like NKG2C(+) NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J Immunol. 2012;189(10):5082–5088. doi:10.4049/jimmunol.1201964
   PubMed Web of Science ®Google Scholar
• Pegram HJ, Andrews DM, Smyth MJ, Darcy PK, Kershaw MH. Activating and inhibitory receptors of natural killer cells. Immunol Cell Biol. 2011;89(2):216–224. doi:10.1038/icb.2010.78
   PubMed Web of Science ®Google Scholar
• Medicherla S, Li L, Ma JY, Kapoun AM, Gaspar NJ, Liu YW, et al. Antitumor activity of TGF-beta inhibitor is dependent on the microenvironment. Anticancer Res. 2007;27(6B):4149–4157.
   PubMed Web of Science ®Google Scholar
• Davis DM, Chiu I, Fassett M, Cohen GB, Mandelboim O, Strominger JL. The human natural killer cell immune synapse. Proc Natl Acad Sci U S A. 1999;96(26):15062–15067. doi:10.1073/pnas.96.26.15062
   PubMed Web of Science ®Google Scholar
• Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005;105(8):3051–3057. doi:10.1182/blood-2004-07-2974
   PubMed Web of Science ®Google Scholar
• Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature. 1986;319(6055):675–678. doi:10.1038/319675a0
   PubMed Web of Science ®Google Scholar
• Bashirova AA, Martin MP, McVicar DW, Carrington M. The killer immunoglobulin-like receptor gene cluster: tuning the genome for defense. Annu Rev Genomics Hum Genet. 2006;7:277–300. doi:10.1146/annurev.genom.7.080505.115726
   PubMed Web of Science ®Google Scholar
• Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J Exp Med. 1998;187(5):813–818. doi:10.1084/jem.187.5.813
   PubMed Web of Science ®Google Scholar
• Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol. 2008;9(5):495–502. doi:10.1038/ni1581
   PubMed Web of Science ®Google Scholar
• Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature. 2002;419(6908):734–738. doi:10.1038/nature01112
   PubMed Web of Science ®Google Scholar
• Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J Immunol. 1998;160(10):4951–4960.
   PubMed Web of Science ®Google Scholar
• Forslund E, Sohlberg E, Enqvist M, Olofsson PE, Malmberg KJ, Önfelt B. Microchip-based single-cell imaging reveals that CD56dimCD57-KIR-NKG2A + NK cells have more dynamic migration associated with increased target cell conjugation and probability of killing compared to CD56dimCD57-KIR-NKG2A- NK cells. J Immunol. 2015;195(7):3374–3381. doi:10.4049/jimmunol.1500171
   PubMed Web of Science ®Google Scholar
• Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol. 2001;19:275–290. doi:10.1146/annurev.immunol.19.1.275
   PubMed Web of Science ®Google Scholar
• Romee R, Foley B, Lenvik T, Wang Y, Zhang B, Ankarlo D, et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood. 2013;121(18):3599–3608. doi:10.1182/blood-2012-04-425397
   PubMed Web of Science ®Google Scholar
• McQueen KL, Parham P. Variable receptors controlling activation and inhibition of NK cells. Curr Opin Immunol. 2002;14(5):615–621. doi:10.1016/S0952-7915(02)00380-1
   PubMed Web of Science ®Google Scholar
• Fuchs A, Cella M, Kondo T, Colonna M. Paradoxic inhibition of human natural interferon-producing cells by the activating receptor NKp44. Blood. 2005;106(6):2076–2082. doi:10.1182/blood-2004-12-4802
   PubMed Web of Science ®Google Scholar
• Moretta A. Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat Rev Immunol. 2002;2(12):957–964. doi:10.1038/nri956
   PubMed Web of Science ®Google Scholar
• Viel S, Marçais A, Guimaraes FSF, Loftus R, Rabilloud J, Grau M, et al. TGF-β inhibits the activation and functions of NK cells by repressing the mTOR pathway. Sci Signal. 2016;9(415):ra19 doi:10.1126/scisignal.aad1884
   PubMed Web of Science ®Google Scholar
• Chavez-Galan L, Arenas-Del Angel MC, Zenteno E, Chavez R, Lascurain R. Cell death mechanisms induced by cytotoxic lymphocytes. Cell Mol Immunol. 2009;6(1):15–25. doi:10.1038/cmi.2009.3
   PubMed Web of Science ®Google Scholar
• Moulian N, Berrih-Aknin S. Fas/APO-1/CD95 in health and autoimmune disease: thymic and peripheral aspects. Semin Immunol. 1998;10(6):449–456. doi:10.1006/smim.1998.0155
   PubMed Web of Science ®Google Scholar
• Herberman RB, Nunn ME, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer. 1975;16(2):216–229. doi:10.1002/ijc.2910160204
   PubMed Web of Science ®Google Scholar
• Carlsten M, Björkström NK, Norell H, Bryceson Y, van Hall T, Baumann BC, et al. DNAX accessory molecule-1 mediated recognition of freshly isolated ovarian carcinoma by resting natural killer cells. Cancer Res. 2007;67(3):1317–1325. doi:10.1158/0008-5472.CAN-06-2264
   PubMed Web of Science ®Google Scholar
• Re F, Staudacher C, Zamai L, Vecchio V, Bregni M. Killer cell Ig-like receptors ligand-mismatched, alloreactive natural killer cells lyse primary solid tumors. Cancer. 2006;107(3):640–648. doi:10.1002/cncr.22002
   PubMed Web of Science ®Google Scholar
• Alici E, Sutlu T, Björkstrand B, Gilljam M, Stellan B, Nahi H, et al. Autologous antitumor activity by NK cells expanded from myeloma patients using GMP-compliant components. Blood. 2008;111(6):3155–3162. doi:10.1182/blood-2007-09-110312
   PubMed Web of Science ®Google Scholar
• Grimm EA, Mazumder A, Zhang HZ, Rosenberg SA. Lymphokine-activated killer cell phenomenon. Lysis of natural killer-resistant fresh solid tumor cells by interleukin 2-activated autologous human peripheral blood lymphocytes. J Exp Med. 1982;155(6):1823–1841.
   PubMed Web of Science ®Google Scholar
• 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. 2000;356(9244):1795–1799. doi:10.1016/S0140-6736(00)03231-1
   PubMed Web of Science ®Google Scholar
• Valiante NM, Parham P. Natural killer cells, HLA class I molecules, and marrow transplantation. Biol Blood Marrow Transplant. 1997;3(5):229–235.
   PubMedGoogle Scholar
• Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295(5562):2097–2100. doi:10.1126/science.1068440
   PubMed Web of Science ®Google Scholar
• Rosenberg SA, Lotze MT, Muul LM, Chang AE, Avis FP, Leitman S, et al. A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high-dose interleukin-2 alone. N Engl J Med. 1987;316(15):889–897. doi:10.1056/NEJM198704093161501
   PubMed Web of Science ®Google Scholar
• Rosenberg SA, Lotze MT, Muul LM, Leitman S, Chang AE, Ettinghausen SE, et al. Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med. 1985;313(23):1485–1492. doi:10.1056/NEJM198512053132327
   PubMed Web of Science ®Google Scholar
• Rezvani K, Rouce RH. The application of natural killer cell immunotherapy for the treatment of cancer. Front Immunol. 2015;6:578 doi:10.3389/fimmu.2015.00578
   PubMed Web of Science ®Google Scholar
• Miller JS. Therapeutic applications: natural killer cells in the clinic. Hematology Am Soc Hematol Educ Program. 2013;2013(1):247–253. doi:10.1182/asheducation-2013.1.247
   PubMedGoogle Scholar
• Rosenberg SA, Lotze MT, Yang JC, Aebersold PM, Linehan WM, Seipp CA, et al. Experience with the use of high-dose interleukin-2 in the treatment of 652 cancer patients. Ann Surg. 1989;210(4):474–484; discussion 484–5.
   PubMed Web of Science ®Google Scholar
• Rudman SM, Jameson MB, McKeage MJ, Savage P, Jodrell DI, Harries M, et al. A phase 1 study of AS1409, a novel antibody-cytokine fusion protein, in patients with malignant melanoma or renal cell carcinoma. Clin Cancer Res. 2011;17(7):1998–2005. doi:10.1158/1078-0432.CCR-10-2490
   PubMed Web of Science ®Google Scholar
• Guo Y, Luan L, Rabacal W, Bohannon JK, Fensterheim BA, Hernandez A, et al. IL-15 superagonist-mediated immunotoxicity: role of NK cells and IFN-γ. J Immunol. 2015;195(5):2353–2364. doi:10.4049/jimmunol.1500300
   PubMed Web of Science ®Google Scholar
• Stroncek DF, Fellowes V, Pham C, Khuu H, Fowler DH, Wood LV, et al. Counter-flow elutriation of clinical peripheral blood mononuclear cell concentrates for the production of dendritic and T cell therapies. J Transl Med. 2014;12(1):241. doi:10.1186/s12967-014-0241-y
   PubMedGoogle Scholar
• Granzin M, Wagner J, Kohl U, Cerwenka A, Huppert V, Ullrich E. Shaping of natural killer cell antitumor activity by ex vivo cultivation. Front Immunol. 2017;8:458 doi:10.3389/fimmu.2017.00458
   PubMed Web of Science ®Google Scholar
• Fujisaki H, Kakuda H, Shimasaki N, Imai C, Ma J, Lockey T, et al. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res. 2009;69(9):4010–4017. doi:10.1158/0008-5472.CAN-08-3712
   PubMed Web of Science ®Google Scholar
• Gong W, Xiao W, Hu M, Weng X, Qian L, Pan X, et al. Ex vivo expansion of natural killer cells with high cytotoxicity by K562 cells modified to co-express major histocompatibility complex class I chain-related protein A, 4-1BB ligand, and interleukin-15. Tissue Antigens. 2010;76(6):467–475. doi:10.1111/j.1399-0039.2010.01535.x
   PubMedGoogle Scholar
• Denman CJ, Senyukov VV, Somanchi SS, Phatarpekar PV, Kopp LM, Johnson JL, et al. Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PloS One. 2012;7(1):e30264. doi:10.1371/journal.pone.0030264
   PubMed Web of Science ®Google Scholar
• Sutlu T, Stellan B, Gilljam M, Quezada HC, Nahi H, Gahrton G, et al. Clinical-grade, large-scale, feeder-free expansion of highly active human natural killer cells for adoptive immunotherapy using an automated bioreactor. Cytotherapy. 2010;12(8):1044–1055. doi:10.3109/14653249.2010.504770
   PubMed Web of Science ®Google Scholar
• Koehl U, Kalberer C, Spanholtz J, Lee DA, Miller JS, Cooley S, et al. Advances in clinical NK cell studies: donor selection, manufacturing and quality control. Oncoimmunology. 2016;5(4):e1115178. doi:10.1080/2162402X.2015.1115178
   PubMed Web of Science ®Google Scholar
• Luhm J, Brand JM, Koritke P, Hoppner M, Kirchner H, Frohn C. Large-scale generation of natural killer lymphocytes for clinical application. J Hematother Stem Cell Res. 2002;11(4):651–657. doi:10.1089/15258160260194794
   PubMedGoogle Scholar
• Oren A, Husebo C, Iversen AC, Austgulen R. A comparative study of immunomagnetic methods used for separation of human natural killer cells from peripheral blood. J Immunol Methods. 2005;303(1–2):1–10. doi:10.1016/j.jim.2005.04.022
   PubMed Web of Science ®Google Scholar
• Knorr DA, Ni Z, Hermanson D, Hexum MK, Bendzick L, Cooper LJN, et al. Clinical-scale derivation of natural killer cells from human pluripotent stem cells for cancer therapy. Stem Cells. Transl Med. 2013;2(4):274–283. doi:10.5966/sctm.2012-0084
   Google Scholar
• Yoon SR, Lee YS, Yang SH, Ahn KH, Lee JH, Lee JH, et al. Generation of donor natural killer cells from CD34(+) progenitor cells and subsequent infusion after HLA-mismatched allogeneic hematopoietic cell transplantation: a feasibility study. Bone Marrow Transplant. 2010;45(6):1038–1046. doi:10.1038/bmt.2009.304
   PubMed Web of Science ®Google Scholar
• Mrozek E, Anderson P, Caligiuri MA. Role of interleukin-15 in the development of human CD56+ natural killer cells from CD34+ hematopoietic progenitor cells. Blood. 1996;87(7):2632–2640.
   PubMed Web of Science ®Google Scholar
• Miller JS, Alley KA, McGlave P. Differentiation of natural killer (NK) cells from human primitive marrow progenitors in a stroma-based long-term culture system: identification of a CD34 + 7+ NK progenitor. Blood. 1994;83(9):2594–2601.
   PubMed Web of Science ®Google Scholar
• Luevano M, Daryouzeh M, Alnabhan R, Querol S, Khakoo S, Madrigal A, et al. The unique profile of cord blood natural killer cells balances incomplete maturation and effective killing function upon activation. Hum Immunol. 2012;73(3):248–257. doi:10.1016/j.humimm.2011.12.015
   PubMed Web of Science ®Google Scholar
• Tonn T, Schwabe D, Klingemann HG, Becker S, Esser R, Koehl U, et al. Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy. 2013;15(12):1563–1570. doi:10.1016/j.jcyt.2013.06.017
   PubMed Web of Science ®Google Scholar
• Arai S, Meagher R, Swearingen M, Myint H, Rich E, Martinson J, et al. Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy. 2008;10(6):625–632. doi:10.1080/14653240802301872
   PubMed Web of Science ®Google Scholar
• Tonn T, Becker S, Esser R, Schwabe D, Seifried E. Cellular immunotherapy of malignancies using the clonal natural killer cell line NK-92. J Hematother Stem Cell Res. 2001;10(4):535–544. doi:10.1089/15258160152509145
   PubMedGoogle Scholar
• Maki G, Klingemann HG, Martinson JA, Tam YK. Factors regulating the cytotoxic activity of the human natural killer cell line, NK-92. J Hematother Stem Cell Res. 2001;10(3):369–383. doi:10.1089/152581601750288975
   PubMedGoogle Scholar
• Yagita M, Huang CL, Umehara H, Matsuo Y, Tabata R, Miyake M, et al. A novel natural killer cell line (KHYG-1) from a patient with aggressive natural killer cell leukemia carrying a p53 point mutation. Leukemia. 2000;14(5):922–930.
   PubMed Web of Science ®Google Scholar
• Suck G, Branch DR, Smyth MJ, Miller RG, Vergidis J, Fahim S, et al. KHYG-1, a model for the study of enhanced natural killer cell cytotoxicity. Exp Hematol. 2005;33(10):1160–1171. doi:10.1016/j.exphem.2005.06.024
   PubMed Web of Science ®Google Scholar
• Burns LJ, Weisdorf DJ, DeFor TE, Vesole DH, Repka TL, Blazar BR, et al. IL-2-based immunotherapy after autologous transplantation for lymphoma and breast cancer induces immune activation and cytokine release: a phase I/II trial. Bone Marrow Transplant. 2003;32(2):177–186. doi:10.1038/sj.bmt.1704086
   PubMed Web of Science ®Google Scholar
• Rosenberg SA. Immunotherapy of cancer by systemic administration of lymphoid cells plus interleukin-2. J Biol Response Mod. 1984;3(5):501–511.
   PubMedGoogle Scholar
• Ruggeri L, Mancusi A, Perruccio K, Burchielli E, Martelli MF, Velardi A. Natural killer cell alloreactivity for leukemia therapy. J Immunother. 2005;28(3):175–182. doi:10.1097/01.cji.0000161395.88959.1f
   PubMed Web of Science ®Google Scholar
• Bachanova V, Burns LJ, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lindgren BR, et al. Allogeneic natural killer cells for refractory lymphoma. Cancer Immunol Immunother. 2010;59(11):1739–1744. doi:10.1007/s00262-010-0896-z
   PubMed Web of Science ®Google Scholar
• Doubrovina ES, Doubrovin MM, Vider E, Sisson RB, O'Reilly RJ, Dupont B, et al. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J Immunol. 2003;171(12):6891–6899. doi:10.4049/jimmunol.171.12.6891
   PubMed Web of Science ®Google Scholar
• Xu X, Rao GS, Groh V, Spies T, Gattuso P, Kaufman HL, et al. Major histocompatibility complex class I-related chain A/B (MICA/B) expression in tumor tissue and serum of pancreatic cancer: role of uric acid accumulation in gemcitabine-induced MICA/B expression. BMC Cancer. 2011;11(1):194. doi:10.1186/1471-2407-11-194
   PubMedGoogle Scholar
• Sconocchia G, Lau M, Provenzano M, Rezvani K, Wongsena W, Fujiwara H, et al. The antileukemia effect of HLA-matched NK and NK-T cells in chronic myelogenous leukemia involves NKG2D-target-cell interactions. Blood. 2005;106(10):3666–3672. doi:10.1182/blood-2005-02-0479
   PubMed Web of Science ®Google Scholar
• Jonsson AH, Yokoyama WM. Natural killer cell tolerance licensing and other mechanisms. Adv Immunol. 2009;101:27–79. doi:10.1016/S0065-2776(08)01002-X
   PubMed Web of Science ®Google Scholar
• Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, Yang L, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436(7051):709–713. doi:10.1038/nature03847
   PubMed Web of Science ®Google Scholar
• Yokoyama WM, Kim S. Licensing of natural killer cells by self-major histocompatibility complex class I. Immunol Rev. 2006;214(1):143–154. doi:10.1111/j.1600-065X.2006.00458.x
   PubMedGoogle Scholar
• Brodin P, Karre K, Hoglund P. NK cell education: not an on-off switch but a tunable rheostat. Trends Immunol. 2009;30(4):143–149. doi:10.1016/j.it.2009.01.006
   PubMed Web of Science ®Google Scholar
• Joncker NT, Shifrin N, Delebecque F, Raulet DH. Mature natural killer cells reset their responsiveness when exposed to an altered MHC environment. J Exp Med. 2010;207(10):2065–2072. doi:10.1084/jem.20100570
   PubMed Web of Science ®Google Scholar
• Orr MT, Murphy WJ, Lanier LL. Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat Immunol. 2010;11(4):321–327. doi:10.1038/ni.1849
   PubMed Web of Science ®Google Scholar
• He Y, Tian Z. NK cell education via nonclassical MHC and non-MHC ligands. Cell Mol Immunol. 2017;14(4):321–330. doi:10.1038/cmi.2016.26
   PubMed Web of Science ®Google Scholar
• Lisovsky I, Isitman G, Song R, DaFonseca S, Tremblay-McLean A, Lebouché B, et al. A higher frequency of NKG2A + than of NKG2A- NK cells responds to autologous HIV-infected CD4 cells irrespective of whether or not they coexpress KIR3DL1. J Virol. 2015;89(19):9909–9919. doi:10.1128/JVI.01546-15
   PubMed Web of Science ®Google Scholar
• Ivarsson MA, Loh L, Marquardt N, Kekäläinen E, Berglin L, Björkström NK, et al. Differentiation and functional regulation of human fetal NK cells. J Clin Invest. 2013;123(9):3889–3901. doi:10.1172/JCI68989
   PubMed Web of Science ®Google Scholar
• Fernandez NC, Treiner E, Vance RE, Jamieson AM, Lemieux S, Raulet DH. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood. 2005;105(11):4416–4423. doi:10.1182/blood-2004-08-3156
   PubMed Web of Science ®Google Scholar
• Tu MM, Mahmoud AB, Makrigiannis AP. Licensed and unlicensed NK cells: differential roles in cancer and viral control. Front Immunol. 2016;7:166doi:10.3389/fimmu.2016.00166
   PubMed Web of Science ®Google Scholar
• Venstrom JM, Zheng J, Noor N, Danis KE, Yeh AW, Cheung IY, et al. KIR and HLA genotypes are associated with disease progression and survival following autologous hematopoietic stem cell transplantation for high-risk neuroblastoma. Clin Cancer Res. 2009;15(23):7330–7334. doi:10.1158/1078-0432.CCR-09-1720
   PubMed Web of Science ®Google Scholar
• Leung W, Handgretinger R, Iyengar R, Turner V, Holladay MS, Hale GA. Inhibitory KIR-HLA receptor-ligand mismatch in autologous haematopoietic stem cell transplantation for solid tumour and lymphoma. Br J Cancer. 2007;97(4):539–542. doi:10.1038/sj.bjc.6603913
   PubMed Web of Science ®Google Scholar
• Cooley S, Weisdorf DJ, Guethlein LA, Klein JP, Wang T, Le CT, et al. Donor selection for natural killer cell receptor genes leads to superior survival after unrelated transplantation for acute myelogenous leukemia. Blood. 2010;116(14):2411–2419. doi:10.1182/blood-2010-05-283051
   PubMed Web of Science ®Google Scholar
• Wang W, Erbe AK, DeSantes KB, Sondel PM. Donor selection for ex vivo-expanded natural killer cells as adoptive cancer immunotherapy. Future Oncol. 2017;13(12):1043–1047. doi:10.2217/fon-2017-0039
   PubMed Web of Science ®Google Scholar
• Brehm C, Huenecke S, Quaiser A, Esser R, Bremm M, Kloess S, et al. IL-2 stimulated but not unstimulated NK cells induce selective disappearance of peripheral blood cells: concomitant results to a phase I/II study. PloS ONE. 2011;6(11):e27351doi:10.1371/journal.pone.0027351
   PubMed Web of Science ®Google Scholar
• Choi I, Yoon SR, Park SY, Kim H, Jung SJ, Jang YJ, et al. Donor-derived natural killer cells infused after human leukocyte antigen-haploidentical hematopoietic cell transplantation: a dose-escalation study. Biol Blood Marrow Transplant. 2014;20(5):696–704. doi:10.1016/j.bbmt.2014.01.031
   PubMed Web of Science ®Google Scholar
• Bari R, Leung M, Turner VE, Embrey C, Rooney B, Holladay M, Leung W. Molecular determinant-based typing of KIR alleles and KIR ligands. Clin Immunol. 2011;138(3):274–281. doi:10.1016/j.clim.2010.12.002
   PubMed Web of Science ®Google Scholar
• Bari R, Rujkijyanont P, Sullivan E, Kang G, Turner V, Gan K, et al. Effect of donor KIR2DL1 allelic polymorphism on the outcome of pediatric allogeneic hematopoietic stem-cell transplantation. J Clin Oncol. 2013;31(30):3782–3790. doi:10.1200/JCO.2012.47.4007
   PubMed Web of Science ®Google Scholar
• Leung W. Infusions of allogeneic natural killer cells as cancer therapy. Clin Cancer Res. 2014;20(13):3390–3400. doi:10.1158/1078-0432.CCR-13-1766
   PubMed Web of Science ®Google Scholar
• Geller MA, Cooley S, Judson PL, Ghebre R, Carson LF, Argenta PA, et al. A phase II study of allogeneic natural killer cell therapy to treat patients with recurrent ovarian and breast cancer. Cytotherapy. 2011;13(1):98–107. doi:10.3109/14653249.2010.515582
   PubMed Web of Science ®Google Scholar
• Pandiyan P, Zheng L, Ishihara S, Reed J, Lenardo MJ. CD4 + CD25 + Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nat Immunol. 2007;8(12):1353–1362. doi:10.1038/ni1536
   PubMed Web of Science ®Google Scholar
• Gasteiger G, Hemmers S, Firth MA, Le Floc'h A, Huse M, Sun JC, et al. IL-2-dependent tuning of NK cell sensitivity for target cells is controlled by regulatory T cells. J Exp Med. 2013;210(6):1167–1178. doi:10.1084/jem.20122462
   PubMed Web of Science ®Google Scholar
• Zhou Q, Bucher C, Munger ME, Highfill SL, Tolar J, Munn DH, et al. Depletion of endogenous tumor-associated regulatory T cells improves the efficacy of adoptive cytotoxic T-cell immunotherapy in murine acute myeloid leukemia. Blood. 2009;114(18):3793–3802. doi:10.1182/blood-2009-03-208181
   PubMed Web of Science ®Google Scholar
• Bachanova V, Cooley S, Defor TE, Verneris MR, Zhang B, McKenna DH, et al. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood. 2014;123(25):3855–3863. doi:10.1182/blood-2013-10-532531
   PubMed Web of Science ®Google Scholar
• Miroux C, Moralès O, Carpentier A, Dharancy S, Conti F, Boleslowski E, et al. Inhibitory effects of cyclosporine on human regulatory T cells in vitro. Transplant Proc. 2009;41(8):3371–3374. doi:10.1016/j.transproceed.2009.08.043
   PubMed Web of Science ®Google Scholar
• Rizzieri DA, Storms R, Chen DF, Long G, Yang Y, Nikcevich DA, et al. Natural killer cell-enriched donor lymphocyte infusions from A 3-6/6 HLA matched family member following nonmyeloablative allogeneic stem cell transplantation. Biol Blood Marrow Transplant. 2010;16(8):1107–1114. doi:10.1016/j.bbmt.2010.02.018
   PubMed Web of Science ®Google Scholar
• Ghiringhelli F, Ménard C, Terme M, Flament C, Taieb J, Chaput N, 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(8):1075–1085. doi:10.1084/jem.20051511
   PubMed Web of Science ®Google Scholar
• Knorr DA, Bachanova V, Verneris MR, Miller JS. Clinical utility of natural killer cells in cancer therapy and transplantation. Semin Immunol. 2014;26(2):161–172. doi:10.1016/j.smim.2014.02.002
   PubMed Web of Science ®Google Scholar
• Larsen SK, Gao Y, Basse PH. NK cells in the tumor microenvironment. Crit Rev Oncog. 2014;19(1–2):91–105. doi: 10.1615/CritRevOncog.2014011142
   PubMedGoogle Scholar
• Basse PH, Goldfarb RH, Herberman RB, Hokland ME. Accumulation of adoptively transferred A-NK cells in murine metastases: kinetics and role of interleukin-2. In Vivo. 1994;8(1):17–24. doi:10.1615/CritRevOncog.2014011142
   PubMedGoogle Scholar
• Carson WE, Fehniger TA, Haldar S, Eckhert K, Lindemann MJ, Lai CF, et al. A potential role for interleukin-15 in the regulation of human natural killer cell survival. J Clin Invest. 1997;99(5):937–943. doi:10.1172/JCI119258
   PubMed Web of Science ®Google Scholar
• Cooper MA, Bush JE, Fehniger TA, VanDeusen JB, Waite RE, Liu Y, et al. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood. 2002;100(10):3633–3638. doi:10.1182/blood-2001-12-0293
   PubMed Web of Science ®Google Scholar
• Szmania S, Lapteva N, Garg T, Greenway A, Lingo J, Nair B, et al. Ex vivo-expanded natural killer cells demonstrate robust proliferation in vivo in high-risk relapsed multiple myeloma patients. J Immunother. 2015;38(1):24–36. doi:10.1097/CJI.0000000000000059
   PubMed Web of Science ®Google Scholar
• Rodella L, Zamai L, Rezzani R, Artico M, Peri G, Falconi M, et al. Interleukin 2 and interleukin 15 differentially predispose natural killer cells to apoptosis mediated by endothelial and tumour cells. Br J Haematol. 2001;115(2):442–450. doi:10.1046/j.1365-2141.2001.03055.x
   PubMed Web of Science ®Google Scholar
• Cho D, Campana D. Expansion and activation of natural killer cells for cancer immunotherapy. Korean J Lab Med. 2009;29(2):89–96. doi:10.3343/kjlm.2009.29.2.89
   PubMedGoogle Scholar
• Frei GM, Persi N, Lador C, Peled A, Cohen Y, C, Nagler A, et al. Nicotinamide, a form of Vitamin B3, promotes expansion of natural killer cells that display increased in vivo survival and cytotoxic activity. Blood. 2011;118(21):4035. doi:http://www.bloodjournal.org/content/118/21/4035
   Web of Science ®Google Scholar
• Butler MO, Hirano N. Human cell-based artificial antigen-presenting cells for cancer immunotherapy. Immunol Rev. 2014;257(1):191–209. doi:10.1111/imr.12129
   PubMed Web of Science ®Google Scholar
• Katakam AK, Yang Q, Goding S, Kumar P, Basse PH. The RheoSwitch® therapeutic system precisely regulates IL-2 expression in melanoma cells and supports survival of NK cells at the tumor site. Mol Ther. 2006. Volume 13, page S103; doi:10.1016/j.ymthe.2006.08.324
   Web of Science ®Google Scholar
• Fehniger TA, Bluman EM, Porter MM, Mrózek E, Cooper MA, VanDeusen JB, et al. Potential mechanisms of human natural killer cell expansion in vivo during low-dose IL-2 therapy. J Clin Invest. 2000;106(1):117–124. doi:10.1172/JCI6218
   PubMed Web of Science ®Google Scholar
• Sygna K, Johansen S, Ruland CM. Recruitment challenges in clinical research including cancer patients and their caregivers. A randomized controlled trial study and lessons learned. Trials. 2015;16(1):428. doi:10.1186/s13063-015-0948-y
   PubMedGoogle Scholar
• Parkhurst MR, Riley JP, Dudley ME, Rosenberg SA. Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res. 2011;17(19):6287–6297. doi:10.1158/1078-0432.CCR-11-1347
   PubMed Web of Science ®Google Scholar
• Sakamoto N, Ishikawa T, Kokura S, Okayama T, Oka K, Ideno M, et al. Phase I clinical trial of autologous NK cell therapy using novel expansion method in patients with advanced digestive cancer. J Transl Med. 2015;13(1):277. doi:10.1186/s12967-015-0632-8
   PubMedGoogle Scholar
• Ishikawa T, Okayama T, Sakamoto N, Ideno M, Oka K, Enoki T, et al. Phase I clinical trial of adoptive transfer of expanded natural killer cells in combination with IgG1 antibody in patients with gastric or colorectal cancer. Int J Cancer. 2018; 142(12):2599-2609, doi:10.1002/ijc.31285
   PubMed Web of Science ®Google Scholar
• Rubnitz JE, Inaba H, Ribeiro RC, Pounds S, Rooney B, Bell T, et al. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol. 2010;28(6):955–959. doi:10.1200/JCO.2009.24.4590
   PubMed Web of Science ®Google Scholar
• Iliopoulou EG, Kountourakis P, Karamouzis MV, Doufexis D, Ardavanis A, Baxevanis CN, et al. A phase I trial of adoptive transfer of allogeneic natural killer cells in patients with advanced non-small cell lung cancer. Cancer Immunol Immunother. 2010;59(12):1781–1789. doi:10.1007/s00262-010-0904-3
   PubMed Web of Science ®Google Scholar
• Shah NN, Baird K, Delbrook CP, Fleisher TA, Kohler ME, Rampertaap S, et al. Acute GVHD in patients receiving IL-15/4-1BBL activated NK cells following T-cell-depleted stem cell transplantation. Blood. 2015;125(5):784–792. doi:10.1182/blood-2014-07-592881
   PubMed Web of Science ®Google Scholar
• Yang Y, Lim O, Kim TM, Ahn YO, Choi H, Chung H, et al. Phase I study of random healthy donor-derived allogeneic natural killer cell therapy in patients with malignant lymphoma or advanced solid tumors. Cancer Immunol Res. 2016;4(3):215–224. doi:10.1158/2326-6066.CIR-15-0118
   PubMed Web of Science ®Google Scholar
• Toze CL, Galal A, Barnett MJ, Shepherd JD, Conneally EA, Hogge DE, et al. Myeloablative allografting for chronic lymphocytic leukemia: evidence for a potent graft-versus-leukemia effect associated with graft-versus-host disease. Bone Marrow Transplant. 2005;36(9):825–830. doi:10.1038/sj.bmt.1705130
   PubMed Web of Science ®Google Scholar
• Kumar P, Defor TE, Brunstein C, Barker JN, Wagner JE, Weisdorf DJ, et al. Allogeneic hematopoietic stem cell transplantation in adult acute lymphocytic leukemia: impact of donor source on survival. Biol Blood Marrow Transplant. 2008;14(12):1394–1400. doi:10.1016/j.bbmt.2008.09.021
   PubMed Web of Science ®Google Scholar
• McSweeney PA, Niederwieser D, Shizuru JA, Sandmaier BM, Molina AJ, Maloney DG, et al. Hematopoietic cell transplantation in older patients with hematologic malignancies: replacing high-dose cytotoxic therapy with graft-versus-tumor effects. Blood. 2001;97(11):3390–3400. doi:10.1182/blood.V97.11.3390
   PubMed Web of Science ®Google Scholar
• Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science. 2002;298(5594):850–854. doi:10.1126/science.1076514
   PubMed Web of Science ®Google Scholar
• Bachanova V, Miller JS. NK cells in therapy of cancer. Crit Rev Oncog. 2014;19(1–2):133–141.
   PubMedGoogle Scholar
• Davies FE, Raje N, Hideshima T, Lentzsch S, Young G, Tai YT, et al. Thalidomide and immunomodulatory derivatives augment natural killer cell cytotoxicity in multiple myeloma. Blood. 2001;98(1):210–216. doi:10.1182/blood.V98.1.210
   PubMed Web of Science ®Google Scholar
• Hayashi T, Hideshima T, Akiyama M, Podar K, Yasui H, Raje N, et al. Molecular mechanisms whereby immunomodulatory drugs activate natural killer cells: clinical application. Br J Haematol. 2005;128(2):192–203. doi:10.1111/j.1365-2141.2004.05286.x
   PubMed Web of Science ®Google Scholar
• Jungkunz-Stier I, Zekl M, Stuhmer T, Einsele H, Seggewiss-Bernhardt R. Modulation of natural killer cell effector functions through lenalidomide/dasatinib and their combined effects against multiple myeloma cells. Leuk Lymphoma. 2014;55(1):168–176. doi:10.3109/10428194.2013.794270
   PubMed Web of Science ®Google Scholar
• Lotze MT, Frana LW, Sharrow SO, Robb RJ, Rosenberg SA. In vivo administration of purified human interleukin 2. I. Half-life and immunologic effects of the Jurkat cell line-derived interleukin 2. J Immunol. 1985;134(1):157–166.
   PubMed Web of Science ®Google Scholar
• Pachella LA, Madsen LT, Dains JE. The toxicity and benefit of various dosing strategies for interleukin-2 in metastatic melanoma and renal cell carcinoma. J Adv Pract Oncol. 2015;6(3):212–221. doi:10.6004/jadpro.2015.6.3.3
   PubMedGoogle Scholar
• de Rham C, Ferrari-Lacraz S, Jendly S, Schneiter G, Dayer JM, Villard J. The proinflammatory cytokines IL-2, IL-15 and IL-21 modulate the repertoire of mature human natural killer cell receptors. Arthritis Res Ther. 2007;9(6):R125. doi:10.1186/ar2336
   PubMed Web of Science ®Google Scholar
• Porrata LF, Inwards DJ, Micallef IN, Johnston PB, Ansell SM, Hogan WJ, Markovic SN. Interleukin-15 affects patient survival through natural killer cell recovery after autologous hematopoietic stem cell transplantation for non-Hodgkin lymphomas. Clin Dev Immunol. 2010;2010:914945 doi:10.1155/2010/914945
   PubMedGoogle Scholar
• Huntington ND. The unconventional expression of IL-15 and its role in NK cell homeostasis. Immunol Cell Biol. 2014;92(3):210–213. doi:10.1038/icb.2014.1
   PubMed Web of Science ®Google Scholar
• Xia J, Liu W, Hu B, Tian Z, Yang Y. IL-15 promotes regulatory T cell function and protects against diabetes development in NK-depleted NOD mice. Clin Immunol. 2010;134(2):130–139. doi:10.1016/j.clim.2009.09.011
   PubMed Web of Science ®Google Scholar
• Roychowdhury S, Blaser BW, Freud AG, Katz K, Bhatt D, Ferketich AK. IL-15 but not IL-2 rapidly induces lethal xenogeneic graft-versus-host disease. Blood. 2005;106(7):2433–2435. doi:10.1182/blood-2005-04-1597
   PubMed Web of Science ®Google Scholar
• Gowda A, Ramanunni A, Cheney C, Rozewski D, Kindsvogel W, Lehman A, et al. Differential effects of IL-2 and IL-21 on expansion of the CD4+ CD25+ Foxp3+ T regulatory cells with redundant roles in natural killer cell mediated antibody dependent cellular cytotoxicity in chronic lymphocytic leukemia. MAbs. 2010;2(1):35–41.
   PubMed Web of Science ®Google Scholar
• Carlsten M, Childs RW. Genetic manipulation of NK cells for cancer immunotherapy: techniques and clinical implications. Front Immunol. 2015;6:266. doi:10.3389/fimmu.2015.00266
   PubMed Web of Science ®Google Scholar
• Nagashima S, Mailliard R, Kashii Y, Reichert TE, Herberman RB, Robbins P, et al. Stable transduction of the interleukin-2 gene into human natural killer cell lines and their phenotypic and functional characterization in vitro and in vivo. Blood. 1998;91(10):3850–3861.
   PubMed Web of Science ®Google Scholar
• Tam YK, Maki G, Miyagawa B, Hennemann B, Tonn T, Klingemann HG. Characterization of genetically altered, interleukin 2-independent natural killer cell lines suitable for adoptive cellular immunotherapy. Hum Gene Ther. 1999;10(8):1359–1373. doi:10.1089/10430349950018030
   PubMed Web of Science ®Google Scholar
• Konstantinidis KV, Alici E, Aints A, Christensson B, Ljunggren HG, Dilber MS. Targeting IL-2 to the endoplasmic reticulum confines autocrine growth stimulation to NK-92 cells. Exp Hematol. 2005;33(2):159–164. doi:10.1016/j.exphem.2004.11.003
   PubMed Web of Science ®Google Scholar
• Jochems C, Hodge JW, Fantini M, Fujii R, Morillon YM, Greiner JW, et al. An NK cell line (haNK) expressing high levels of granzyme and engineered to express the high affinity CD16 allele. Oncotarget. 2016;7(52):86359–86373. doi:10.18632/oncotarget.13411
   PubMedGoogle Scholar
• Zhang J, Sun R, Wei H, Zhang J, Tian Z. Characterization of interleukin-15 gene-modified human natural killer cells: implications for adoptive cellular immunotherapy. Haematologica. 2004;89(3):338–347.
   PubMed Web of Science ®Google Scholar
• Imamura M, Shook D, Kamiya T, Shimasaki N, Chai SMH, Coustan-Smith E, et al. Autonomous growth and increased cytotoxicity of natural killer cells expressing membrane-bound interleukin-15. Blood. 2014;124(7):1081–1088. doi:10.1182/blood-2014-02-556837
   PubMed Web of Science ®Google Scholar
• Mentlik James A, Cohen AD, Campbell KS. Combination immune therapies to enhance anti-tumor responses by NK cells. Front Immunol. 2013;4:481 doi:10.3389/fimmu.2013.00481
   PubMed Web of Science ®Google Scholar
• Kalaycio ME, George Negrea O, Allen SL, Rai KR, Abbasi RM, Horne H, et al. Subcutaneous injections of low doses of humanized anti-CD20 veltuzumab: a phase I study in chronic lymphocytic leukemia. Leuk Lymphoma. 2016;57(4):803–811. doi:10.3109/10428194.2015.1085531
   PubMed Web of Science ®Google Scholar
• Furtado M, Dyer MJ, Johnson R, Berrow M, Rule S. Ofatumumab monotherapy in relapsed/refractory mantle cell lymphoma-a phase II trial. Br J Haematol. 2014;165(4):575–578. doi:10.1111/bjh.12769
   PubMed Web of Science ®Google Scholar
• Ganjoo KN, de Vos S, Pohlman BL, Flinn IW, Forero-Torres A, Enas NH, et al. Phase 1/2 study of ocaratuzumab, an Fc-engineered humanized anti-CD20 monoclonal antibody, in low-affinity FcgammaRIIIa patients with previously treated follicular lymphoma. Leuk Lymphoma. 2015;56(1):42–48. doi:10.3109/10428194.2014.911859
   PubMed Web of Science ®Google Scholar
• Cartron G, de Guibert S, Dilhuydy MS, Morschhauser F, Leblond V, Dupuis J, et al. Obinutuzumab (GA101) in relapsed/refractory chronic lymphocytic leukemia: final data from the phase 1/2 GAUGUIN study. Blood. 2014;124(14):2196–2202. doi:10.1182/blood-2014-07-586610
   PubMed Web of Science ®Google Scholar
• Sehn LH, Goy A, Offner FC, Martinelli G, Caballero MD, Gadeberg O, et al. Randomized phase II trial comparing obinutuzumab (GA101) with rituximab in patients with relapsed CD20+ indolent B-cell non-Hodgkin lymphoma: final analysis of the GAUSS Study. J Clin Oncol. 2015;33(30):3467–3474. doi:10.1200/JCO.2014.59.2139
   PubMed Web of Science ®Google Scholar
• Marcus RE, Davies AJ, Ando K, Klapper W, Opat S, Owen CJ, et al. Obinutuzumab-based induction and maintenance prolongs progression-free survival (PFS) in patients with previously untreated follicular lymphoma: primary results of the Randomized Phase 3 GALLIUM Study. Blood. 2016;128(22):6. http://www.bloodjournal.org/content/128/22/6
   Web of Science ®Google Scholar
• Romagne F, Andre P, Spee P, Zahn S, Anfossi N, Gauthier L, 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. 2009;114(13):2667–2677. doi:10.1182/blood-2009-02-206532
   PubMed Web of Science ®Google Scholar
• Benson DM, Cohen AD, Jagannath S, Munshi NC, Spitzer G, Hofmeister CC, et al. A phase I trial of the anti-KIR antibody IPH2101 and lenalidomide in patients with relapsed/refractory multiple myeloma. Clin Cancer Res. 2015;21(18):4055–4061. doi:10.1158/1078-0432.CCR-15-0304
   PubMed Web of Science ®Google Scholar
• Korde N, Carlsten M, Lee MJ, Minter A, Tan E, Kwok M, et al. A phase II trial of pan-KIR2D blockade with IPH2101 in smoldering multiple myeloma. Haematologica. 2014;99(6):e81–e83. doi:10.3324/haematol.2013.103085
   PubMed Web of Science ®Google Scholar
• Godal R, Bachanova V, Gleason M, McCullar V, Yun GH, Cooley S, et al. Natural killer cell killing of acute myelogenous leukemia and acute lymphoblastic leukemia blasts by killer cell immunoglobulin-like receptor-negative natural killer cells after NKG2A and LIR-1 blockade. Biol Blood Marrow Transplant. 2010;16(5):612–621. doi:10.1016/j.bbmt.2010.01.019
   PubMed Web of Science ®Google Scholar
• Nguyen S, Beziat V, Dhedin N, Kuentz M, Vernant JP, Debre P, Vieillard V. HLA-E upregulation on IFN-gamma-activated AML blasts impairs CD94/NKG2A-dependent NK cytolysis after haplo-mismatched hematopoietic SCT. Bone Marrow Transplant. 2009;43(9):693–699. doi:10.1038/bmt.2008.380
   PubMed Web of Science ®Google Scholar
• Gleason MK, Verneris MR, Todhunter DA, Zhang B, McCullar V, Zhou SX, et al. 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(12):2674–2684. doi:10.1158/1535-7163.MCT-12-0692
   PubMed Web of Science ®Google Scholar
• Gleason MK, Ross JA, Warlick ED, Lund TC, Verneris MR, Wiernik A, et al. CD16xCD33 bispecific killer cell engager (BiKE) activates NK cells against primary MDS and MDSC CD33+ targets. Blood. 2014;123(19):3016–3026. doi:10.1182/blood-2013-10-533398
   PubMed Web of Science ®Google Scholar
• Wiernik A, Foley B, Zhang B, Verneris MR, Warlick E, Gleason MK, et al. Targeting natural killer cells to acute myeloid leukemia in vitro with a CD16 x 33 bispecific killer cell engager and ADAM17 inhibition. Clin Cancer Res. 2013;19(14):3844–3855. doi:10.1158/1078-0432.CCR-13-0505
   PubMed Web of Science ®Google Scholar
• Schmohl JU, Gleason MK, Dougherty PR, Miller JS, Vallera DA. Heterodimeric bispecific single chain variable fragments (scFv) killer engagers (BiKEs) enhance NK-cell activity against CD133+ colorectal cancer cells. Targ Oncol. 2016;11(3):353–361. doi:10.1007/s11523-015-0391-8
   PubMed Web of Science ®Google Scholar
• Vallera DA, Felices M, McElmurry R, McCullar V, Zhou X, Schmohl JU, et al. IL15 trispecific killer engagers (TriKE) make natural killer cells specific to CD33+ targets while also inducing persistence, in vivo expansion, and enhanced function. Clin Cancer Res. 2016;22(14):3440–3450. doi:10.1158/1078-0432.CCR-15-2710
   PubMed Web of Science ®Google Scholar
• Buhtoiarov IN, Neal ZC, Gan J, Buhtoiarova TN, Patankar MS, Gubbels JAA, et al. Differential internalization of hu14.18-IL2 immunocytokine by NK and tumor cell: impact on conjugation, cytotoxicity, and targeting. J Leukoc Biol. 2011;89(4):625–638. doi:10.1189/jlb.0710422
   PubMed Web of Science ®Google Scholar
• Koehn TA, Trimble LL, Alderson KL, Erbe AK, McDowell KA, Grzywacz B, Hank JA, Sondel PM. Increasing the clinical efficacy of NK and antibody-mediated cancer immunotherapy: potential predictors of successful clinical outcome based on observations in high-risk neuroblastoma. Front Pharmacol. 2012;3:91. doi:10.3389/fphar.2012.00091
   PubMed Web of Science ®Google Scholar
• Johnson EE, Lum HD, Rakhmilevich AL, Schmidt BE, Furlong M, Buhtoiarov IN, et al. Intratumoral immunocytokine treatment results in enhanced antitumor effects. Cancer Immunol Immunother. 2008;57(12):1891–1902. doi:10.1007/s00262-008-0519-0
   PubMed Web of Science ®Google Scholar
• Rubinstein MP, Kovar M, Purton JF, Cho JH, Boyman O, Surh CD, et al. Converting IL-15 to a superagonist by binding to soluble IL-15R{alpha}. Proc Natl Acad Sci U S A. 2006;103(24):9166–9171. doi:10.1073/pnas.0600240103
   PubMed Web of Science ®Google Scholar
• Davies E, Reid S, Medina MF, Lichty B, Ashkar AA. IL-15 has innate anti-tumor activity independent of NK and CD8 T cells. J Leukoc Biol. 2010;88(3):529–536. doi:10.1189/jlb.0909648
   PubMed Web of Science ®Google Scholar
• Conlon KC, Lugli E, Welles HC, Rosenberg SA, Fojo AT, Morris JC, 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. 2015;33(1):74–82. doi:10.1200/JCO.2014.57.3329
   PubMed Web of Science ®Google Scholar
• Felices M, Chu S, Kodal B, Bendzick L, Ryan C, Lenvik AJ, et al. IL-15 super-agonist (ALT-803) enhances natural killer (NK) cell function against ovarian cancer. Gynecol Oncol. 2017;145(3):453–461. doi:10.1016/j.ygyno.2017.02.028
   PubMed Web of Science ®Google Scholar
• Rosario M, Liu B, Kong L, Collins LI, Schneider SE, Chen X, et al. The IL-15-based ALT-803 complex enhances FcgammaRIIIa-triggered NK cell responses and in vivo clearance of B cell lymphomas. Clin Cancer Res. 2016;22(3):596–608. doi:10.1158/1078-0432.CCR-15-1419
   PubMed Web of Science ®Google Scholar
• Kim PS, Kwilas AR, Xu W, Alter S, Jeng EK, Wong HC, Schlom J, Hodge JW. 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. 2016;7(13):16130–16145. doi:10.18632/oncotarget.7470
   PubMedGoogle Scholar
• Romee R, Cooley S, Berrien-Elliott MM, Westervelt P, Verneris MR, Wagner JE, et al. First-in-human phase 1 clinical study of the IL-15 superagonist complex ALT-803 to treat relapse after transplantation. Blood. 2018;131(23):2515-2527, doi:10.1182/blood-2017-12-823757
   PubMed Web of Science ®Google Scholar
• Glienke W, Esser R, Priesner C, Suerth JD, Schambach A, Wels WS, et al. Advantages and applications of CAR-expressing natural killer cells. Front Pharmacol. 2015;6:21 doi:10.3389/fphar.2015.00021
   PubMed Web of Science ®Google Scholar
• Novartis. Novartis CAR-T cell therapy CTL019 unanimously (10-0) recommended for approval by FDA advisory committee to treat pediatric, young adult r/r B-cell ALL. 2017. https://www.novartis.com/news/media-releases/novartis-car-t-cell-therapy-ctl019-unanimously-10-0-recommended-approval-fda
   Google Scholar
• Staines R. Natural killer cells ‘a hundred times cheaper’ than CAR-T pharmaphorum 2018 [updated 2018 Feb 13]. Available from: https://pharmaphorum.com/news/natural-killer-cancer-therapy-a-hundred-times-cheaper-than-car-t/.
   Google Scholar
• Imai C, Iwamoto S, Campana D. Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood. 2005;106(1):376–383. doi:10.1182/blood-2004-12-4797
   PubMed Web of Science ®Google Scholar
• Schönfeld K, Sahm C, Zhang C, Naundorf S, Brendel C, Odendahl M, et al. Selective inhibition of tumor growth by clonal NK cells expressing an ErbB2/HER2-specific chimeric antigen receptor. Mol Ther. 2015;23(2):330–338. doi:10.1038/mt.2014.219
   PubMed Web of Science ®Google Scholar
• Bonifant CL, Jackson HJ, Brentjens RJ, Curran KJ. Toxicity and management in CAR T-cell therapy. Mol Ther Oncolytics. 2016;3:16011 doi:10.1038/mto.2016.11
   PubMed Web of Science ®Google Scholar
• Klingemann H. Are natural killer cells superior CAR drivers?. Oncoimmunology. 2014;3:e28147 doi:10.4161/onci.28147
   PubMed Web of Science ®Google Scholar
• Curti A, Ruggeri L, D'Addio A, Bontadini A, Dan E, Motta MR, et al. Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood. 2011;118(12):3273–3279. doi:10.1182/blood-2011-01-329508
   PubMed Web of Science ®Google Scholar
• Curti A, Ruggeri L, Parisi S, Bontadini A, Dan E, Motta MR, 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. 2016;22(8):1914–1921. doi:10.1158/1078-0432.CCR-15-1604
   PubMed Web of Science ®Google Scholar
• Bjorklund AT, Carlsten M, Sohlberg E, Liu LL, Clancy T, Karimi M, et al. Complete remission with reduction of high-risk clones following haploidentical NK-cell therapy against MDS and AML. Clin Cancer Res. 2018; 24(8). doi:10.1158/1078-0432.CCR-17-3196
   PubMed Web of Science ®Google Scholar
• Shi J, Tricot G, Szmania S, Rosen N, Garg TK, Malaviarachchi PA, et al. Infusion of haplo-identical killer immunoglobulin-like receptor ligand mismatched NK cells for relapsed myeloma in the setting of autologous stem cell transplantation. Br J Haematol. 2008;143(5):641–653. doi:10.1111/j.1365-2141.2008.07340.x
   PubMed Web of Science ®Google Scholar
• Barkholt L, Alici E, Conrad R, Sutlu T, Gilljam M, Stellan B, et al. Safety analysis of ex vivo-expanded NK and NK-like T cells administered to cancer patients: a phase I clinical study. Immunotherapy. 2009;1(5):753–764. doi:10.2217/imt.09.47
   PubMed Web of Science ®Google Scholar