The application of natural killer cell immunotherapy for the treatment of cancer

Frontiers in Immunology

Volumn 6, Issue NOV, 2015, Pages

  Rezvani, Katayoun ^a   Rouce, Rayne H ^b,c  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

ADCC; Adoptive immunotherapy; Anti KIR antibody; CAR NK cells; Natural killer cells; NK 92; Transplantation

Indexed keywords

CD137 ANTIGEN; CD16 ANTIGEN; CD19 ANTIGEN; CD20 ANTIGEN; CD64 ANTIGEN; CD86 ANTIGEN; CD94 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; FAS LIGAND; FLUDARABINE; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; LIRILUMAB; METHYLPREDNISOLONE; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; OBINUTUZUMAB; RITUXIMAB; TRANSFORMING GROWTH FACTOR BETA; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNINDEXED DRUG;

ACUTE MYELOBLASTIC LEUKEMIA; ADOPTIVE IMMUNOTHERAPY; ANTIGEN BINDING; ANTINEOPLASTIC ACTIVITY; CANCER IMMUNOTHERAPY; CELL MEDIATED CYTOTOXICITY; CYTOLOGY; GENETIC ENGINEERING; GRAFT VERSUS HOST REACTION; HUMAN; IMMUNOREACTIVITY; IMMUNOSUPPRESSIVE TREATMENT; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; TRANSLATIONAL RESEARCH; TUMOR CELL; UMBILICAL CORD BLOOD;

EID: 84949544206     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00578     Document Type: Review

References (116)

1. Lotzova E, Savary CA, Herberman RB. Inhibition of clonogenic growth of fresh leukemia cells by unstimulated and IL-2 stimulated NK cells of normal donors. Leuk Res (1987) 11(12):1059-66. doi:10.1016/0145-2126(87)90158-5.
2. Lowdell MW, Craston R, Samuel D, Wood ME, O'Neill E, Saha V, et al. Evidence that continued remission in patients treated for acute leukaemia is dependent upon autologous natural killer cells. Br J Haematol (2002) 117(4):821-7. doi:10.1046/j.1365-2141.2002.03495.x.
3. Davies J, Stringaris K, Barrett AJ, Rezvani K. Opportunities and limitations of NK cells as adoptive therapy for malignant disease. Cytotherapy (2014) 16(11):1453-66. doi:10.1016/j.jcyt.2014.03.009.
4. Lanier LL, Le AM, Civin CI, Loken MR, Phillips JH. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol (1986) 136(12):4480-6.
5. Locatelli F, Moretta F, Brescia L, Merli P. Natural killer cells in the treatment of high-risk acute leukaemia. Semin Immunol (2014) 26(2):173-9. doi:10.1016/j.smim.2014.02.004.
6. Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood (2001) 97(10):3146-51. doi:10.1182/blood. V97.10.3146.
7. Campbell JJ, Qin S, Unutmaz D, Soler D, Murphy KE, Hodge MR, et al. Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J Immunol (2001) 166(11):6477-82. doi:10.4049/jimmunol.166.11.6477.
8. De Maria A, Bozzano F, Cantoni C, Moretta L. Revisiting human natural killer cell subset function revealed cytolytic CD56(dim)CD16+ NK cells as rapid producers of abundant IFN-gamma on activation. Proc Natl Acad Sci U S A (2011) 108:728-32. doi:10.1073/pnas.1012356108.
9. Farag S, Caligiuri M. Human natural killer cell development and biology. Blood Rev (2006) 20(3):123-37. doi:10.1016/j.blre.2005.10.001.
10. Moretta L, Pietra G, Montaldo E, Vacca P, Pende D, Falco M, et al. Human NK cells: from surface receptors to the therapy of leukemias and solid tumors. Front Immunol (2014) 5:87. doi:10.3389/fimmu.2014.00087.
11. Liu J, Xiao Z. Activating killer immunoglobulin-like receptor 2DSs2 binds to HLA A*11. Proc Natl Acad Sci U S A (2014) 111(7):2662-7. doi:10.1073/pnas.1322052111.
12. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood (2010) 115:2167-76. doi:10.1182/blood-2009-08-238469.
13. Karre K. Immunology. A perfect mismatch. Science (2002) 295:2029-31.
14. Campbell K, Hasegawa J. Natural killer cell biology: an update and future directions. J Allergy Clin Immuol. (2013) 32(3):536-44. doi:10.1016/j.jaci.2013.07.006.
15. Caligiuri MA. Human natural killer cells. Blood (2008) 112:461-9. doi:10.1182/blood-2007-09-077438.
16. Bradley M, Zeytun A, Rafi-Janajreh A, Nagarkatti PS, Nagarkatti M. Role of spontaneous and interleukin-2-induced natural killer cell activity in the cytotoxicity and rejection of Fas1 and Fas-tumor cells. Blood (1998) 92:4248-55.
17. Screpanti V, Wallin RP, Ljunggren HG, Grandien A. A central role for death receptor-mediated apoptosis in the rejection of tumors by NK cells. J Immunol (2001) 167:2068-73. doi:10.4049/jimmunol.167.4.2068.
18. Kayagaki N, Yamaguchi N, Nakayama M, Takeda K, Akiba H, Tsutsui H, et al. Expression and function of TNF-related apoptosis-inducing ligand on murine activated NK cells. J Immunol (1999) 163:1906-13.
19. 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):2065-72. doi:10.1084/jem.20100570.
20. Martin-Fontecha A, Thomsen L, Brett S, Gerard C, Lipp M, Lanzavecchia A, et al. Induced recruitment of NK cells to lymph nodes provides IFN-γ for TH1 priming. Nat Immunol (2004) 5:1260-5. doi:10.1038/ni1138.
21. Agaugue S, Marcenaro E. Human natural killer cells exposed to IL-2, IL-12, IL-18 or IL-4 differently modulate priming of naïve T cells by monocyte-derived dendritic cells. Blood (2008) 112(5):1776-83. doi:10.1182/blood-2008-02-135871.
22. Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, Munz C. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med (2002) 195(3):343-511. doi:10.1084/jem.20011149.
23. Bellora F, Castriconi R, Dondero A, Reggiardo G, Moretta L, Mantovani A, et al. The interaction of human natural killer cells with either unpolarized or polarized macrophages results in different functional outcomes. Proc Natl Acad Sci U S A (2010) 107(50):21641-59. doi:10.1073/pnas.1007654108.
24. Murphy WJ, Parham P, Miller JS. NK cells-from bench to clinic. Biol Blood Marrow Transplant (2012) 18(1 Suppl):S2-7. doi:10.1016/j.bbmt.2011.10.033.
25. Castriconi R, Dondero A, Bellora F, Moretta L, Castellano A, Locatelli F, et al. Neuroblastoma-derived TGF-beta1 modulates the chemokine receptor repertoire of human resting NK cells. J Immunol. (2013) 190:5321-8. doi:10.4049/jimmunol.1202693.
26. Lee HM, Kim KS, Kim J. A comparative study of the effects of inhibitory cytokines on human natural killer cells and the mechanistic features of transforming growth factor-beta. Cell Immunol (2014) 290:52-61. doi:10.1016/j.cellimm.2014.05.001.
27. Romain G, Senyukov V, Rey-Villamizar N, Merouane A, Kelton W, Liadi I, et al. Antibody Fc-engineering improves frequency and promotes kinetic boosting of serial killing mediated by NK cells. Blood (2014) 124(22):3241-9. doi:10.1182/blood-2014-04-569061.
28. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med (2000) 6(4):443-6. doi:10.1038/74704.
29. de Haij S, Jansen JH, Boross P, Beurskens FJ, Bakema JE, Bos DL, et al. In vivo cytotoxicity of type I CD20 antibodies critically depends on Fc receptor ITAM signaling. Cancer Res (2010) 70(8):3209-17. doi:10.1158/0008-5472.CAN-09-4109.
30. Kanazawa T, Hiramatsu Y, Iwata S, Siddiquey M, Sato Y, Suzuki M, et al. Anti CCR-4 monoclonal antibody mogamulizumab for the treatment of EBV-associated T-and NK-cell lymphoproliferative diseases. Clin Cancer Res (2014) 20(19):5075-84. doi:10.1158/1078-0432.CCR-14-0580.
31. Terszowski G, Klein CKIR./HLA interactions negatively affect rituximab-but not GA101 (obinutuzumab)-induced antibody-dependent cellular cytotoxicity. J Immunol (2014) 192(12):5618-24. doi:10.4049/jimmunol.1400288.
32. Binyamin L, Alpaugh RK, Hughes TL, Lutz CT, Campbell KS, Weiner LM. Blocking NK cell inhibitory self-recognition promotes antibody-dependent cellular cytotoxicity in a model of anti-lymphoma therapy. J Immunol (2008) 180(9):6392-401. doi:10.4049/jimmunol.180.9.6392.
33. Kohrt H, Thielens A. Anti-KIR antibody enhancement of anti-lymphoma activity of natural killer cells as monotherapy and in combination with anti-CD20 antibodies. Blood (2014) 123(5):678-86. doi:10.1182/blood-2013-08-519199.
34. Romagne F, Andre P, Spee P, Zahn S, Anfossi N, Gauthier L, et al. Preclinical characterization of I-7F9, a novel human anti-KIR receptor therapeutic antibody that augments natural killer-mediated killing of tumor cells. Blood (2009) 114(13):2667-77. doi:10.1182/blood-2009-02-206532.
35. Vey N, Bourhis JH, Boissel N, Bordessoule D, Prebet T, Charbonnier A, et al. A phase 1 trial of the anti-inhibitory KIR mAb IPH2101 for AML in complete remission. Blood (2012) 120(22):4317-23. doi:10.1182/blood-2012-06-437558.
36. Lin W, Voskens C, Zhang X, Schindler DG, Wood A, Burch E, et al. Fc-dependent expression of CD137 on human NK cells: insights into "agonistic" effects of anti-CD137 monoclonal antibodies. Blood (2008) 112(3):699-707. doi:10.1182/blood-2007-11-122465.
37. Benson DM Jr, Bakan CE, Zhang S, Collins SM, Liang J, Srivastava S, et al. IPH2101, a novel anti-inhibitory KIR antibody, and lenalidomide combine to enhance the natural killer cell versus multiple myeloma effect. Blood (2011) 118(24):6387-91. doi:10.1182/blood-2011-06-360255.
38. Kohrt HE, Houot R, Goldstein MJ, Weiskopf K, Alizadeh AA, Brody J, et al. CD137 stimulation enhances the antilymphoma activity of anti-CD20 antibodies. Blood (2011) 117(8):2423-32. doi:10.1182/blood-2010-08-301945 Epub 2011/01/05.,.
39. Wilcox RA, Tamada K, Strome SE, 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 (2002) 169(8):4230-6. doi:10.4049/jimmunol.169.8.4230.
40. Seidel UJ, Schlegel P, Lang P. Natural killer cell mediated antibody-dependent cellular cytotoxicity in tumor immunotherapy with therapeutic antibodies. Front Immunol (2013) 4:76. doi:10.3389/fimmu.2013.00076.
41. Cartron G, Dacheux L. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood (2002) 99(3):754-8. doi:10.1182/blood. V99.3.754.
42. Weng WK, Levy R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol (2012) 21(21):3940-7. doi:10.1200/JCO.2003.05.013.
43. 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) 32:177-86. doi:10.1038/sj.bmt.1704086.
44. 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) 313:1485-92. doi:10.1056/NEJM198512053132327.
45. 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) 17:6287-97. doi:10.1158/1078-0432.CCR-11-1347.
46. Benyunes MC, Higuchi C. Immunotherapy with interleukin 2 with or without lymphokine-activated killer cells after autologous bone marrow transplantation for malignant lymphoma: a feasibility trial. Bone Marrow Transplant (1995) 16(2):283-8.
47. Cheng M, Chen Y, Xiao W, Sun R, Tian Z. NK cell-based immunotherapy for malignant diseases. Cell Mol Immunology (2013) 10(3):230-52. doi:10.1038/cmi.2013.10.
48. Stern M, Passweg JR, Meyer-Monard S, Esser R, Tonn T, Soerensen J, et al. Pre-emptive immunotherapy with purified natural killer cells after haploidentical SCT: a prospective phase II study in two centers. Bone Marrow Transplant (2013) 48:433-8. doi:10.1038/bmt.2012.162.
49. 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):1038-46. doi:10.1038/bmt.2009.304.
50. Miller JS, Soignier Y. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood (2005) 105(8):3051-7. doi:10.1182/blood-2004-07-2974.
51. Rubnitz JE, Inaba H. 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):955-9. doi:10.1200/JCO.2009.24.4590.
52. Curti A, Ruggeri L. Succesful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood (2011) 118(12):3273-9. doi:10.1182/blood-2011-01-329508.
53. Rusakiewicz S, Semeraro M, Sarabi M, Desbois M, Locher C, Mendez R, et al. Immune infiltrates are prognostic factors in localized gastrointestinal stromal tumors. Cancer Res (2013) 73(12):3499-510. doi:10.1158/0008-5472.CAN-13-0371.
54. Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J. Clin. Invest (2011) 121:3609-22. doi:10.1172/JCI45816.
55. Navarro A, Bjorklund A, Chekenya M. Therapeutic potential and challenges of natural killer cells in treatment of solid tumors. Front Immunol (2015) 29(6):202. doi:10.3389/fimmu.2015.00202.
56. Stringaris K, Sekine T, Khoder A, Alsuliman A, Razzaghi B, Sargeant R, et al. Leukemia-induced phenotypic and functional defects in natural killer cells predict failure to achieve remission in acute myeloid leukemia. Haematologica (2014) 99(5):836-47. doi:10.3324/haematol.2013.087536.
57. Rouce R, Shaim H, Sekine T, et al. The TGF-β/SMAD pathway is an important mechanism for NK cell immune evasion in childhood B acute lymphoblastic leukemia. Leukemia (in press).
58. Murray S, Lundqvist A. Targeting the tumor microenvironment to improve natural killer cell-based immunotherapies: on being in the right place at the right time, with resilience. Hum Vaccin Immunother (2015) 24:0. doi:10.1080/21645515.2015.1096458.
59. Nausch N, Galani I, Schlecker E, Cerwenka A. Mononuclear myeloid-derived "suppressor" cells express RAE-1 and activate natural killer cells. Blood (2008) 112(10):4080-9. doi:10.1182/blood-2008-03-143776.
60. 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.
61. Koepsell SA, Miller JS. Natural killer cells: a review of manufacturing and clinical utility. Transfusion (2013) 53(2):404-10. doi:10.1111/j.1537-2995.2012.03724.x.
62. Lang P, Pfeiffer M, Teltschik HM, Schlegel P, Feuchtinger T, Ebinger M, et al. Natural killer cell activity influences outcome after T cell depleted stem cell transplantation from matched unrelated and haploidentical donors. Best Pract Res Clin Haematol (2011) 24:403-11. doi:10.1016/j.beha.2011.04.009.
63. Pfeiffer M, Schumm M, Feuchtinger T, Dietz K, Handgretinger R, Lang P. Intensity of HLA class I expression and KIR-mismatch determine NK-cell mediated lysis of leukaemic blasts from children with acute lymphatic leukaemia. Br J Haematol (2007) 138:97-100. doi:10.1111/j.1365-2141.2007.06631.x.
64. Leong W, Chase JM, Romee R, Schneider SE, Sullivan RP, Cooper MA, et al. Pre-activation with IL-12, IL-15, and IL-18 induces CD25 and a functional high affinity IL-2 receptor on human cytokine-induced memory-like NK cells. Biol Blood Marrow Transplant (2014) 20(4):463-73. doi:10.1016/j.bbmt.2014.01.006.
65. Ni J, Miller M, Stojanovic A, Garbi N, Cerwenka A. Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors. J Exp Med (2012) 209:2351-65. doi:10.1084/jem.20120944.
66. Miller J, Rooney C, Curtsinger J, McElmurry R, McCullar V, Verneris MR, et al. Expansion and homing of adoptively transferred human natural killer cells in immunodeficient mice varies with product preparation and in vivo cytokine administration: implications for clinical therapy. Biol Blood Marrow Transplant (2014) 20(8):1252-7. doi:10.1016/j.bbmt.2014.05.004.
67. 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) 69:4010-7. doi:10.1158/0008-5472.CAN-08-3712.
68. Berg M, Lundqvist A, McCoy P Jr, Samsel L, Fan Y, Tawab A, et al. Clinical-grade ex vivo-expanded human natural killer cells up-regulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy (2009) 11:341-55. doi:10.1080/14653240902807034.
69. Lundqvist A, Yokoyama H, Smith A, Berg M, Childs R. Bortezomib treatment and regulatory T-cell depletion enhance the antitumor effects of adoptively infused NK cells. Blood (2009) 113:6120-7. doi:10.1182/blood-2008-11-190421.
70. Bachanova C. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood (2014) 123(25):3855-63. doi:10.1182/blood-2013-10-532531.
71. Klingemann H, Grodman C. Autologous stem cell transplant recipients tolerate haploidentical related-donor natural killer cell-enriched infusions. Transfusion (2013) 53:412-8. doi:10.1111/j.1537-2995.2012.03764.x.
72. Reed W, Noga SJ, Gee AP, Rooney CM, Wagner JE, McCullough J, et al. Production assistance for cellular therapies (PACT): four-year experience from the United States National Heart, Lung, and Blood Institute (NHLBI) contract research program in cell and tissue therapies. Transfusion (2009) 49:786-96. doi:10.1111/j.1537-2995.2008.02027.x.
73. Koepsell SA, Kadidlo DM, Fautsch S, McCullough J, Klingemann H, Wagner JE, et al. Successful "in-flight" activation of natural killer cells during long-distance shipping. Transfusion (2013) 53:398-403. doi:10.1111/j.1537-2995.2012.03695.x.
74. Woll P, Grzywacz B, Tian X, Marcus RK, Knorr DA, Verneris MR, et al. Human embryonic stem cells differentiate into a homogenous population of natural killer cells with potent in vivo antitumor activity. Blood (2009) 113(24):6094-101. doi:10.1182/blood-2008-06-165225.
75. Chouaib S, Pittari G, Nanbakhsh A, ElAyoubi H, Amsellem S, Bourhis JH, et al. Improving the outcome of leukemia by natural killer cell-based immunotherapeutic strategies. Front Immunol (2014) 5:95. doi:10.3389/fimmu.2014.00095.
76. Spanholtz J, Preijers F, Tordoir M, Trilsbeek C, Paardekooper J, de Witte T, et al. Clinical-grade generation of active NK cells from cord blood hematopoietic progenitor cells for immunotherapy using a closed-system culture process. PLoS One (2011) 6:e20740. doi:10.1371/journal.pone.0020740.
77. Shah N, Martin-Antonio B, Yang H, Ku S, Lee DA, Cooper LJ, et al. Antigen presenting cell-mediated expansion of human umbilical cord blood yields log-scale expansion of natural killer cells with anti-myeloma activity. PLoS One (2013) 8(10):e76781. doi:10.1371/journal.pone.0076781.
78. Shaim H, Yvon E. Cord blood: a promising source of allogeneic natural killer cells for immunotherapy. Cytotherapy (2015) 17(1):1-2. doi:10.1016/j.jcyt.2014.12.001.
79. Dalle JH, Menezes J, Wagner E, Blagdon M, Champagne J, Champagne MA, et al. Characterization of cord blood natural killer cells: implications for transplantation and neonatal infections. Pediatr Res (2005):57.
80. Tomchuck S, Leung W, Dallas M. Enhanced cytotoxic function of natural killer and CD3+CD56+ cells in cord blood after culture. Biol Blood Marrow Transplant (2015) 21(1):39-49. doi:10.1016/j.bbmt.2014.10.014.
81. Della C, Falco M, Podesta M, Locatelli F, Moretta L, Frassoni F, et al. Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus. Blood (2012) 119(2):399-410. doi:10.1182/blood-2011-08-372003.
82. Xing R. Cord blood natural killer cells exhibit impaired lytic immunological synapse formation that is reversed with IL-2 ex vivo expansion. J Immunother (2010) 33(7):684-96. doi:10.1097/CJI.0b013e3181e475e9.
83. Alnabhan R, Madrigal A, Saudemont A. Differential activation of cord blood and peripheral blood NK cells by cytokines. Cytotherapy (2015) 17(1):73-85. doi:10.1016/j.jcyt.2014.08.003.
84. 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:e30264. doi:10.1371/journal.pone.0030264.
85. Pittari G, Filippini P, Gentilcore G, Grivel JC, Rutella S. Revving up natural killer cells and cytokine-induced killer cells against hematological malignancies. Front Immunol (2015) 6:230. doi:10.3389/fimmu.2015.00230.
86. Klingemann HG, Wong E, Maki GA. cytotoxic NK-cell line (NK-92) for ex vivo purging of leukemia from blood. Biol Blood Marrow Transplant (1996) 2:68-75.
87. Yagita M, Huang C, 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):922-30. doi:10.1038/sj.leu.2401769.
88. Tonn T, Schwabe D, Klingemann H, 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):1563-70. doi:10.1016/j.jcyt.2013.06.017.
89. Swift B, Williams B. Natural killer cell lines preferentially kill clonogenic multiple myeloma cells and decrease myeloma engraftment in a bioluminescent xenograft mouse model. Haematologica (2012) 97(7):1020-8. doi:10.3324/haematol.2011.054254.
90. Yan Y, Steinherz P, Klingemann HG, Dennig D, Childs BH, McGuirk J, et al. Antileukemia activity of a natural killer cell line against human leukemias. Clin Cancer Res (1998) 4:2859-68.
91. Tam YK, Miyagawa B, Ho VC, Klingemann HG. Immunotherapy of malignant melanoma in a SCID mouse model using the highly cytotoxic natural killer cell line NK-92. J Hematother (1999) 8:281-90. doi:10.1089/106161299320316.
92. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. Journal of Clinical Oncology (2005) 23:2346-57. doi:10.1200/JCO.2005.00.240.
93. Conlon K, Lugli E, Welles H. 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.
94. Pegram H, Smith E, Rafiq S, Brentgens R. CAR therapy for hematological cancers: can success seen in the treatment of B-cell acute lymphoblastic leukemia be applied to other hematological malignancies? Immunotherapy (2015) 7(5):545-61. doi:10.2217/imt.15.6.
95. Grupp S, Kalos M, Barrett D, Aplenc R, Porter D, Rheingold S, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med (2013) 368(16):1509-18. doi:10.1056/NEJMoa1215134.
96. Lee DW, Kochenderfer JN, Stetler-Stevenson M, Cui YK, Delbrook C, Feldman SA, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet (2015) 385(9967):517-28. doi:10.1016/S0140-6736(14)61403-3.
97. Glienke W, Esser R, Priesner C, Suerth J, Schambach A, Wels WS, et al. Advantages and applications of CAR-expressing NK cells. Front Pharmacol (2015) 6:21. doi:10.3389/fphar.2015.00021.
98. Tettamanti S, Marin V, Pizzitola I, Magnani CF, Giordano Attianese GM, Cribioli E, et al. Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor. Br J Haematol (2013) 161:389-401. doi:10.1111/bjh.12282.
99. Shimasaki N, Fujisaki H, Cho D, Masselli M, Lockey T, Eldridge P, et al. A clinically adaptable method to enhance the cytotoxicity of natural killer cells against B-cell malignancies. Cytotherapy (2012) 14(7):830-40. doi:10.3109/14653249.2012.671519.
100. Chang YH, Connolly J, Shimasaki N, Mimura K, Kono K, Campana D. A chimeric receptor with NKG2D specificity enhances natural killer cell activation and killing of tumor cells. Cancer Res (2013) 73(6):1777-86. doi:10.1158/0008-5472.CAN-12-3558.
101. Altvater B, Landmeier S, Pscherer S, Temme J, Schweer K, Kailayangiri S, et al. 2B4(CD244) signaling by recombinant antigen-specific chimeric receptors costimulates natural killer cell activation to leukemia and neuroblastoma cells. Clin. Cancer Res (2009) 15(15):4857-66. doi:10.1158/1078-0432.CCR-08-2810.
102. Esser R, Muller T, Stefes D, Kloess S, Seidel D, Gillies S, et al. NK cells engineered to express a GD2-specific antigen receptor display built-in ADCC-like activity against tumour cells of neuroectodermal origin. J. Cell Mol. Med (2012) 16(3):569-81. doi:10.1111/j.1582-4934.2011.01343.x.
103. Battula VL, Shi Y, Evans KW, Wang RY, Spaeth EL, Jacamo RO, et al. Ganglioside GD2 identifies breast cancer stem cells and promotes tumorigenesis. J Clin Invest (2012) 122(6):2066-78. doi:10.1172/JCI59735.
104. Jiang H, Zhang W, Shang P, Zhang H, Fu W, Ye F, et al. Transfection of chimeric anti-CD138 gene enhances natural killer cell activation and killing of multiple myeloma cells. Mol. Oncol (2014) 8(2):297-310. doi:10.1016/j.molonc.2013.12.001.
105. Chu J, Deng Y, Benson DM, He S, Hughes T, Zhang J, et al. CS1-specific chimeric antigen receptor (CAR)-engineered natural killer cells enhance in vitro and in vivo antitumor activity against human multiple myeloma. Leukemia (2014) 28(4):917-27. doi:10.1038/leu.2013.279.
106. Boissel L, Betancur-Boissel M, Lu W, Krause DS, Van Etten RA, Wels WS, et al. Retargeting NK-92 cells by means of CD19-and CD20-specific chimeric antigen receptors compares favorably with antibody-dependent cellular cytotoxicity. OncoImmunology (2013) 2(10):e26527. doi:10.4161/onci.26527.
107. Ferrara JL, Levine JE, Reddy P, Holler E. Graft-versus-host disease. Lancet (2009) 373(9674):1550-61. doi:10.1016/S0140-6736(09)60237-3.
108. Stauss H, Morris E. Immunotherapy with gene-modified T cells: limiting side effects provides new challenges. Gene Ther (2013) 20(11):1029-32. doi:10.1038/gt.2013.34.
109. Maus M, Grupp S, Porter D, June C. Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood (2014) 123(17):2625-35. doi:10.1182/blood-2013-11-492231.
110. Shah N, Baird K, Delbrook C, Fleisher T, Kohler M, 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):784-92. doi:10.1182/blood-2014-07-592881.
111. Jones B, Lamb L, Goldman F, DiStasi A. Improving the safety of cell therapy products by suicide gene transfer. Front Pharmacol (2014) 5:254. doi:10.3389/fphar.2014.00254.
112. Zhou X, Dotti G, Krance R, Martinez C, Naik S, Kamble R, et al. Inducible caspase-9 suicide gene controls adverse effects from alloreplete T cells after haploidentical stem cell transplantation. Blood (2015) 125(26):4103-13. doi:10.1182/blood-2015-02-628354.
113. Gleason R. CD16xCD33 bispecific killer cell engager (BiKE) activates NK cells against primary MDS and MDSC CD33+ targets. Blood (2014) 123(19):3016-26. doi:10.1182/blood-2013-10-533398.
114. Wiernik A, Foley B, Zhang B, Verneris MR, Warlick E, Gleason MK, et al. Targeting natural killer cells to AML in vitro with a CD16x33 engager. Clin Cancer Res (2013) 19(14):3844-55. doi:10.1158/1078-0432.CCR-13-0505.
115. Romee R, Foley B, Lenvik T, Wang Y, Zhang B, Ankarlo D, et al. NK cell CD16 surface expression is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood (2013) 121(18):3599-608. doi:10.1182/blood-2012-04-425397.
116. Choi I, Yoon SR, Park SY, Kim H, Jung SJ, 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