Antibody-dependent cell cytotoxicity: Immunotherapy strategies enhancing effector NK cells

Immunology and Cell Biology

Volumn 95, Issue 4, 2017, Pages 347-355

  Ochoa, Maria Carmen ^a,b   Minute, Luna ^a,b   Rodriguez, Inmaculada ^a,b,c,d   Garasa, Saray ^a,b   Perez Ruiz, Elisabeth ^e   Inogés, Susana ^a,c,d   Melero, Ignacio ^a,b,c,d   Berraondo, Pedro ^a,b,c,d  

^a UNIVERSITY OF NAVARRA   (Spain)

^b IdiSNA Navarra Institute for Health Research   (Spain)

^c UNIVERSITY CLINIC OF NAVARRA   (Spain)

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

^e HOSPITAL COSTA DEL SOL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BISPECIFIC ANTIBODY; CD20 ANTIBODY; CD38 ANTIGEN; CYTOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GANGLIOSIDE GD2; MONOCLONAL ANTIBODY; NATURAL KILLER CELL RECEPTOR; SIGNALING LYMPHOCYTIC ACTIVATION MOLECULE; SLAMF7 PROTEIN; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR ANTIGEN; UNCLASSIFIED DRUG; FC RECEPTOR; FCGR3A PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE IMMUNOTHERAPY; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; CANCER IMMUNOTHERAPY; EFFECTOR CELL; ENHANCER REGION; HUMAN; IMMUNE RESPONSE; MALIGNANT NEOPLASM; NATURAL KILLER CELL; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); REVIEW; ANIMAL; ANTIBODY AFFINITY; IMMUNOLOGY; MACROPHAGE; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASM; PHYSIOLOGY; PROCEDURES; T LYMPHOCYTE; TRANSPLANTATION;

ANIMALS; ANTIBODY AFFINITY; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, NEOPLASM; CYTOKINES; HUMANS; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; MACROPHAGES; MOLECULAR TARGETED THERAPY; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, IGG; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS;

EID: 85013382039     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2017.6     Document Type: Review

References (95)

1. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013; 39: 1-10.
2. Karre K. Natural killer cell recognition of missing self. Nat Immunol 2008; 9: 477-480.
3. Lehmann B, Biburger M, Brückner C, Ipsen-Escobedo A, Gordan S, Lehmann C, et al. Tumor location determines tissue-specific recruitment of tumor-Associated macrophages and antibody-dependent immunotherapy response. Sci Immunol 2017; 2: 1-11.
4. Simpson TR, Li F, Montalvo-Ortiz W, Sepulveda MA, Bergerhoff K, Arce F, et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J Exp Med 2013; 210: 1695-1710.
5. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med 2000; 6: 443-446.
6. Manches O, Lui G, Chaperot L, Gressin R, Molens JP, Jacob MC, et al. In vitro mechanisms of action of rituximab on primary non-Hodgkin lymphomas. Blood 2003; 101: 949-954.
7. Hatjiharissi E, Xu L, Santos DD, Hunter ZR, Ciccarelli BT, Verselis S, et al. Increased natural killer cell expression of CD16, augmented binding and ADCC activity to rituximab among individuals expressing the Fc{gamma}RIIIa-158 V/V and V/F polymorphism. Blood 2007; 110: 2561-2564.
8. Veeramani S, Wang SY, Dahle C, Blackwell S, Jacobus L, Knutson T, et al. Rituximab infusion induces NK activation in lymphoma patients with the high-Affinity CD16 polymorphism. Blood 2011; 118: 3347-3349.
9. Farag SS, Flinn IW, Modali R, Lehman TA, Young D, Byrd JC. Fc gamma RIIIa and Fc gamma RIIa polymorphisms do not predict response to rituximab in B-cell chronic lymphocytic leukemia. Blood 2004; 103: 1472-1474.
10. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 2002; 99: 754-758.
11. 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: 803-811.
12. Wierda WG, Padmanabhan S, Chan GW, Gupta IV, Lisby S, Osterborg A, et al. Ofatumumab is active in patients with fludarabine-refractory CLL irrespective of prior rituximab: results from the phase 2 international study. Blood 2011; 118: 5126-5129.
13. Cheson BD. Ofatumumab, a novel anti-CD20 monoclonal antibody for the treatment of B-cell malignancies. J Clin Oncol 2010; 28: 3525-3530.
14. Barth MJ, Mavis C, Czuczman MS, Hernandez-Ilizaliturri FJ. Ofatumumab exhibits enhanced in vitro and in vivo activity compared to rituximab in preclinical models of mantle cell lymphoma. Clin Cancer Res 2015; 21: 4391-4397.
15. Martinez C, Diaz-Lopez A, Rodriguez-Calvillo M, Garcia-Sanz R, Terol MJ, Perez-Ceballos E, et al. Phase II trial of ofatumumab plus ESHAP (O-ESHAP) as salvage treatment for patients with relapsed or refractory classical Hodgkin lymphoma after firstline chemotherapy. Br J Haematol 2016; 174: 859-867.
16. Mossner E, Brunker P, Moser S, Puntener U, Schmidt C, Herter S, et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell-mediated B-cell cytotoxicity. Blood 2010; 115: 4393-4402.
17. Pott C, Hoster E, Kehden B, Unterhalt M, Herold M, van der Jagt RH, et al. Minimal residual disease in patients with follicular lymphoma treated with obinutuzumab or rituximab as first-line induction immunochemotherapy and maintenance in the phase 3 GALLIUM Study. Blood 2016; 128: 613.
18. Herter S, Herting F, Mundigl O, Waldhauer I, Weinzierl T, Fauti T, et al. Preclinical activity of the type II CD20 antibody GA101 (obinutuzumab) compared with rituximab and ofatumumab in vitro and in xenograft models. Mol Cancer Ther 2013; 12: 2031-2042.
19. Goede V, Fischer K, Busch R, Engelke A, Eichhorst B, Wendtner CM, et al. Obinutuzumab plus chlorambucil in patients with CLL and coexisting conditions. N Engl J Med 2014; 370: 1101-1110.
20. Sehn LH, Chua N, Mayer J, Dueck G, Trneny M, Bouabdallah K, et al. Obinutuzumab plus bendamustine versus bendamustine monotherapy in patients with rituximabrefractory indolent non-Hodgkin lymphoma (GADOLIN): a randomised, controlled, openlabel, multicentre, phase 3 trial. Lancet Oncol 2016; 17: 1081-1093.
21. 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: 42-48.
22. Wang SY, Racila E, Taylor RP, Weiner GJ. NK-cell activation and antibody-dependent cellular cytotoxicity induced by rituximab-coated target cells is inhibited by the C3b component of complement. Blood 2008; 111: 1456-1463.
23. Cragg MS, Morgan SM, Chan HT, Morgan BP, Filatov AV, Johnson PW, et al. Complement-mediated lysis by anti-CD20 mAb correlates with segregation into lipid rafts. Blood 2003; 101: 1045-1052.
24. Scheuer W, Friess T, Burtscher H, Bossenmaier B, Endl J, Hasmann M. Strongly enhanced antitumor activity of trastuzumab and pertuzumab combination treatment on HER2-positive human xenograft tumor models. Cancer Res 2009; 69: 9330-9336.
25. Kurai J, Chikumi H, Hashimoto K, Yamaguchi K, Yamasaki A, Sako T, et al. Antibodydependent cellular cytotoxicity mediated by cetuximab against lung cancer cell lines. Clin Cancer Res 2007; 13: 1552-1561.
26. Saloura V, Cohen EE, Licitra L, Billan S, Dinis J, Lisby S, et al. An open-label single-Arm, phase II trial of zalutumumab, a human monoclonal anti-EGFR antibody, in patients with platinum-refractory squamous cell carcinoma of the head and neck. Cancer Chemother Pharmacol 2014; 73: 1227-1239.
27. Dienstmann R, Tabernero J. Necitumumab, a fully human IgG1 mAb directed against the EGFR for the potential treatment of cancer. Curr Opin Investig Drugs 2010; 11: 1434-1441.
28. Gerdes CA, Nicolini VG, Herter S, van Puijenbroek E, Lang S, Roemmele M, et al. GA201 (RG7160): a novel, humanized, glycoengineered anti-EGFR antibody with enhanced ADCC and superior in vivo efficacy compared with cetuximab. Clin Cancer Res 2013; 19: 1126-1138.
29. Delord JP, Tabernero J, Garcia-Carbonero R, Cervantes A, Gomez-Roca C, Berge Y, et al. Open-label, multicentre expansion cohort to evaluate imgatuzumab in pre-Treated patients with KRAS-mutant advanced colorectal carcinoma. Eur J Cancer 2014; 50: 496-505.
30. Gonzalez-Nicolini V, Herter S, Lang S, Waldhauer I, Bacac M, Roemmele M, et al. Premedication and chemotherapy agents do not impair imgatuzumab (GA201)-mediated antibody-dependent cellular cytotoxicity and combination therapies enhance efficacy. Clin Cancer Res 2016; 22: 2453-2461.
31. Spiridon CI, Guinn S, Vitetta ES. A comparison of the in vitro and in vivo activities of IgG and F(ab') 2 fragments of a mixture of three monoclonal anti-Her-2 antibodies. Clin Cancer Res 2004; 10: 3542-3551.
32. Varchetta S, Gibelli N, Oliviero B, Nardini E, Gennari R, Gatti G, 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 2007; 67: 11991-11999.
33. Muraro E, Comaro E, Talamini R, Turchet E, Miolo G, Scalone S, et al. Improved Natural Killer cell activity and retained anti-Tumor CD8(+) T cell responses contribute to the induction of a pathological complete response in HER2-positive breast cancer patients undergoing neoadjuvant chemotherapy. J Transl Med 2015; 13: 1-14.
34. Albanell J, Codony J, Rovira A, Mellado B, Gascon P. Mechanism of action of anti-HER2 monoclonal antibodies: scientific update on trastuzumab and 2C4. Adv Exp Med Biol 2003; 532: 253-268.
35. Adams SR, Yang HC, Savariar EN, Aguilera J, Crisp JL, Jones KA, et al. Anti-Tubulin drugs conjugated to anti-ErbB antibodies selectively radiosensitize. Nat Commun 2016; 7: 13019.
36. Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012; 367: 1783-1791.
37. Nordstrom JL, Gorlatov S, Zhang W, Yang Y, Huang L, Burke S, et al. Anti-Tumor activity and toxicokinetics analysis of MGAH22, an anti-HER2 monoclonal antibody with enhanced Fcgamma receptor binding properties. Breast Cancer Res 2011; 13: R123.
38. Honsik CJ, Jung G, Reisfeld RA. Lymphokine-Activated killer cells targeted by monoclonal antibodies to the disialogangliosides GD2 and GD3 specifically lyse human tumor cells of neuroectodermal origin. Proc Natl Acad Sci USA 1986; 83: 7893-7897.
39. Hank JA, Robinson RR, Surfus J, Mueller BM, Reisfeld RA, Cheung NK, et al. Augmentation of antibody dependent cell mediated cytotoxicity following in vivo therapy with recombinant interleukin 2. Cancer Res 1990; 50: 5234-5239.
40. Dinutuximab: a review in high-risk neuroblastoma. Target Oncol 2016; 11: 247-253.
41. Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 2010; 363: 1324-1334.
42. Sorkin LS, Otto M, Baldwin WM 3rd, Vail E, Gillies SD, Handgretinger R, et al. Anti-GD (2) with an FC point mutation reduces complement fixation and decreases antibodyinduced allodynia. Pain 2010; 149: 135-142.
43. Hank JA, Gan J, Ryu H, Ostendorf A, Stauder MC, Sternberg A, et al. Immunogenicity of the hu14.18-IL2 immunocytokine molecule in adults with melanoma and children with neuroblastoma. Clin Cancer Res 2009; 15: 5923-5930.
44. Laubach JP, Paba Prada CE, Richardson PG, Longo DL. Daratumumab, elotuzumab, and the development of therapeutic monoclonal antibodies in multiple myeloma. Clin Pharmacol Ther 2016; 101: 81-88.
45. Vincent M, Bessard A, Cochonneau D, Teppaz G, Sole V, Maillasson M, et al. Tumor targeting of the IL-15 superagonist RLI by an anti-GD2 antibody strongly enhances its antitumor potency. Int J Cancer 2013; 133: 757-765.
46. de Weers M, Tai YT, van der Veer MS, Bakker JM, Vink T, Jacobs DC, et al. Daratumumab, a novel therapeutic human CD38 monoclonal antibody, induces killing of multiple myeloma and other hematological tumors. J Immunol 2011; 186: 1840-1848.
47. Deckert J, Wetzel MC, Bartle LM, Skaletskaya A, Goldmacher VS, Vallee F, et al. SAR650984, a novel humanized CD38-Targeting antibody, demonstrates potent antitumor activity in models of multiple myeloma and other CD38+ hematologic malignancies. Clin Cancer Res 2014; 20: 4574-4583.
48. Lonial S, Dimopoulos M, Palumbo A, White D, Grosicki S, Spicka I, et al. Elotuzumab therapy for relapsed or refractory multiple myeloma. N Engl J Med 2015; 373: 621-631.
49. Tai YT, Dillon M, Song W, Leiba M, Li XF, Burger P, et al. Anti-CS1 humanized monoclonal antibody HuLuc63 inhibits myeloma cell adhesion and induces antibodydependent cellular cytotoxicity in the bone marrow milieu. Blood 2008; 112: 1329-1337.
50. Trotta R, Dal Col J, Yu J, Ciarlariello D, Thomas B, Zhang X, et al. TGF-beta utilizes SMAD3 to inhibit CD16-mediated IFN-gamma production and antibody-dependent cellular cytotoxicity in human NK cells. J Immunol 2008; 181: 3784-3792.
51. Seimetz D, Lindhofer H, Bokemeyer C. Development and approval of the trifunctional antibody catumaxomab (anti-EpCAM x anti-CD3) as a targeted cancer immunotherapy. Cancer Treat Rev 2010; 36: 458-467.
52. Fayette J, Wirth L, Oprean C, Udrea A, Jimeno A, Rischin D, et al. Randomized phase II study of duligotuzumab (MEHD7945A) vs. cetuximab in squamous cell carcinoma of the head and neck (MEHGAN Study). Front Oncol 2016; 6: 232.
53. Glorius P, Baerenwaldt A, Kellner C, Staudinger M, Dechant M, Stauch M, et al. The novel tribody [(CD20)(2) x CD16] efficiently triggers effector cell-mediated lysis of malignant B cells. Leukemia 2013; 27: 190-201.
54. Schmohl JU, Felices M, Taras E, Miller JS, Vallera DA. Enhanced ADCC and NK cell activation of an anticarcinoma bispecific antibody by genetic insertion of a modified IL-15 cross-linker. Mol Ther 2016; 24: 1312-1322.
55. Kono K, Takahashi A, Ichihara F, Sugai H, Fujii H, Matsumoto Y. Impaired antibodydependent cellular cytotoxicity mediated by herceptin in patients with gastric cancer. Cancer Res 2002; 62: 5813-5817.
56. 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: 1485-1492.
57. West WH, Tauer KW, Yannelli JR, Marshall GD, Orr DW, Thurman GB, et al. Constantinfusion recombinant interleukin-2 in adoptive immunotherapy of advanced cancer. N Engl J Med 1987; 316: 898-905.
58. 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: 3051-3057.
59. Friedberg JW, Neuberg D, Gribben JG, Fisher DC, Canning C, Koval M, et al. Combination immunotherapy with rituximab and interleukin 2 in patients with relapsed or refractory follicular non-Hodgkin's lymphoma. Br J Haematol 2002; 117: 828-834.
60. Khan KD, Emmanouilides C, Benson DM Jr, Hurst D, Garcia P, Michelson G, et al. A phase 2 study of rituximab in combination with recombinant interleukin-2 for rituximab-refractory indolent non-Hodgkin's lymphoma. Clin Cancer Res 2006; 12: 7046-7053.
61. Mitra S, Ring AM, Amarnath S, Spangler JB, Li P, Ju W, et al. Interleukin-2 activity can be fine tuned with engineered receptor signaling clamps. Immunity 2015; 42: 826-838.
62. Parihar R, Nadella P, Lewis A, Jensen R, De Hoff C, Dierksheide JE, et al. A phase I study of interleukin 12 with trastuzumab in patients with human epidermal growth factor receptor-2-overexpressing malignancies: analysis of sustained interferon gamma production in a subset of patients. Clin Cancer Res 2004; 10: 5027-5037.
63. McMichael EL, Jaime-Ramirez AC, Guenterberg KD, Luedke E, Atwal LS, Campbell AR et al. IL-21 enhances natural killer cell response to cetuximab-coated pancreatic tumor cells. Clin Cancer Res 2016; 23: 489-502.
64. Steele N, Anthony A, Saunders M, Esmarck B, Ehrnrooth E, Kristjansen PE, et al. A phase 1 trial of recombinant human IL-21 in combination with cetuximab in patients with metastatic colorectal cancer. Br J Cancer 2012; 106: 793-798.
65. Croce M, Rigo V, Ferrini S. IL-21: a pleiotropic cytokine with potential applications in oncology. J Immunol Res 2015; 2015: 696578.
66. Han KP, Zhu X, Liu B, Jeng E, Kong L, Yovandich JL, et al. IL-15:IL-15 receptor alpha superagonist complex: high-level co-expression in recombinant mammalian cells, purification and characterization. Cytokine 2011; 56: 804-810.
67. 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: 596-608.
68. Ochoa MC, Fioravanti J, Rodriguez I, Hervas-Stubbs S, Azpilikueta A, Mazzolini G, et al. Antitumor immunotherapeutic and toxic properties of an HDL-conjugated chimeric IL-15 fusion protein. Cancer Res 2013; 73: 139-149.
69. McWilliams EM, Mele JM, Cheney C, Timmerman EA, Fiazuddin F, Strattan EJ, et al. Therapeutic CD94/NKG2A blockade improves natural killer cell dysfunction in chronic lymphocytic leukemia. Oncoimmunology 2016; 5: e1226720.
70. Kohrt HE, Thielens A, Marabelle A, Sagiv-Barfi I, Sola C, Chanuc F, et al. Anti-KIR antibody enhancement of anti-lymphoma activity of natural killer cells as monotherapy and in combination with anti-CD20 antibodies. Blood 2014; 123: 678-686.
71. 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: 2423-2432.
72. Pickup M, Novitskiy S, Moses HL. The roles of TGFbeta in the tumour microenvironment. Nat Rev Cancer 2013; 13: 788-799.
73. Donatelli SS, Zhou JM, Gilvary DL, Eksioglu EA, Chen X, Cress WD, et al. TGF-betainducible microRNA-183 silences tumor-Associated natural killer cells. Proc Natl Acad Sci USA 2014; 111: 4203-4208.
74. Bedi A, Chang X, Noonan K, Pham V, Bedi R, Fertig EJ, et al. Inhibition of TGF-beta enhances the in vivo antitumor efficacy of EGF receptor-Targeted therapy. Mol Cancer Ther 2012; 11: 2429-2439.
75. Sivori S, Falco M, Della Chiesa M, Carlomagno S, Vitale M, Moretta L, et al. CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc Natl Acad Sci USA 2004; 101: 10116-10121.
76. Ming Lim C, Stephenson R, Salazar AM, Ferris RL. TLR3 agonists improve the immunostimulatory potential of cetuximab against EGFR+ head and neck cancer cells. Oncoimmunology 2013; 2: e24677.
77. Charlebois R, Allard B, Allard D, Buisseret L, Turcotte M, Pommey S, et al. PolyI: C and CpG synergize with anti-ErbB2 mAb for treatment of breast tumors resistant to immune checkpoint inhibitors. Cancer Res 2016; 77: 312-319.
78. Chow LQ, Morishima C, Eaton KD, Baik CS, Goulart BH, Anderson LN, et al. Phase 1b trial of the toll-like receptor 8 agonist, motolimod (VTX-2337), combined with cetuximab in patients with recurrent or metastatic SCCHN. Clin Cancer Res (e-pub ahead of print 3 November 2016; doi:10.1158/1078-0432.CCR-16-1934
79. Lu H, Yang Y, Gad E, Inatsuka C, Wenner CA, Disis ML, et al. TLR2 agonist PSK activates human NK cells and enhances the antitumor effect of HER2-Targeted monoclonal antibody therapy. Clin Cancer Res 2011; 17: 6742-6753.
80. Bowles JA, Wang SY, Link BK, Allan B, Beuerlein G, Campbell MA, et al. Anti-CD20 monoclonal antibody with enhanced affinity for CD16 activates NK cells at lower concentrations and more effectively than rituximab. Blood 2006; 108: 2648-2654.
81. 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: 6392-6401.
82. Carlsten M, Levy E, Karambelkar A, Li L, Reger R, Berg M, et al. Efficient mRNA-Based Genetic Engineering of Human NK Cells with High-Affinity CD16 and CCR7 Augments Rituximab-Induced ADCC against Lymphoma and Targets NK Cell Migration toward the Lymph Node-Associated Chemokine CCL19. Front Immunol 2016; 7: 105.
83. Muller T, Uherek C, Maki G, Chow KU, Schimpf A, Klingemann HG, et al. Expression of a CD20-specific chimeric antigen receptor enhances cytotoxic activity of NK cells and overcomes NK-resistance of lymphoma and leukemia cells. Cancer Immunol Immunother 2008; 57: 411-423.
84. 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: e26527.
85. Schirrmann T, Pecher G. Specific targeting of CD33(+) leukemia cells by a natural killer cell line modified with a chimeric receptor. Leuk Res 2005; 29: 301-306.
86. Uherek C, Tonn T, Uherek B, Becker S, Schnierle B, Klingemann HG, et al. Retargeting of natural killer-cell cytolytic activity to ErbB2-expressing cancer cells results in efficient and selective tumor cell destruction. Blood 2002; 100: 1265-1273.
87. 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: 376-383.
88. Voskens CJ, Watanabe R, Rollins S, Campana D, Hasumi K, Mann DL. Ex-vivo expanded human NK cells express activating receptors that mediate cytotoxicity of allogeneic and autologous cancer cell lines by direct recognition and antibody directed cellular cytotoxicity. J Exp Clin Cancer Res 2010; 29: 1-13.
89. Deng X, Terunuma H, Nieda M, Xiao W, Nicol A. Synergistic cytotoxicity of ex vivo expanded natural killer cells in combination with monoclonal antibody drugs against cancer cells. Int Immunopharmacol 2012; 14: 593-605.
90. Romee R, Rosario M, Berrien-Elliott MM, Wagner JA, Jewell BA, Schappe T, et al. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci Transl Med 2016; 8: 357ra123.
91. Chavez JC, Piris-Villaespesa M, Dalia S, Powers J, Turba E, Nodzon L, et al. Results of a phase II study of lenalidomide and rituximab for refractory/relapsed chronic lymphocytic leukemia. Leuk Res 2016; 47: 78-83.
92. Reddy NM, Greer JP, Morgan DS, Chen H, Park SI, Richards KL. A phase II randomized study of lenalidomide or lenalidomide and rituximab as maintenance therapy following standard chemotherapy for patients with high/high-intermediate risk diffuse large B-cell lymphoma. Leukemia 2016; 31: 241-244.
93. Lundqvist A, Abrams SI, Schrump DS, Alvarez G, Suffredini D, Berg M, et al. Bortezomib and depsipeptide sensitize tumors to tumor necrosis factor-related apoptosis-inducing ligand: a novel method to potentiate natural killer cell tumor cytotoxicity. Cancer Res 2006; 66: 7317-7325.
94. Kohrt HE, Tumeh PC, Benson D, Bhardwaj N, Brody J, Formenti S, et al. Immunodynamics: a cancer immunotherapy trials network review of immune monitoring in immuno-oncology clinical trials. J Immunother Cancer 2016; 4: 15.
95. Boyerinas B, Jochems C, Fantini M, Heery CR, Gulley JL, Tsang KY, et al. Antibodydependent cellular cytotoxicity activity of a novel anti-PD-L1 antibody avelumab (MSB0010718C) on human tumor cells. Cancer Immunol Res 2015; 3: 1148-1157.