Improving natural killer cell cancer immunotherapy

Current Opinion in Organ Transplantation

Volumn 20, Issue 6, 2015, Pages 671-680

  Berrien Elliott, Melissa M ^a   Romee, Rizwan ^a   Fehniger, Todd A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Immunotherapy; Natural killer cells

Indexed keywords

CARFILZOMIB; CD3 ANTIGEN; CD56 ANTIGEN; CETUXIMAB; GAMMA INTERFERON; INTERLEUKIN 15; LENALIDOMIDE; RITUXIMAB; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; TUMOR NECROSIS FACTOR; UBLITUXIMAB;

ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; CANCER IMMUNOTHERAPY; CANCER PATIENT; CARCINOMA; CELL THERAPY; CHRONIC LYMPHATIC LEUKEMIA; CYTOKINE PRODUCTION; HEMATOLOGIC MALIGNANCY; HODGKIN DISEASE; HUMAN; KIDNEY CARCINOMA; LYMPHOMA; MACROPHAGE; MANTLE CELL LYMPHOMA; MELANOMA; MULTIPLE MYELOMA; MYELODYSPLASTIC SYNDROME; NATURAL KILLER CELL; NONHODGKIN LYMPHOMA; PROSTATE CANCER; REGULATORY T LYMPHOCYTE; REVIEW; WALDENSTROEM MACROGLOBULINEMIA; BIOLOGICAL THERAPY; DISEASE COURSE; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASMS; PATHOLOGY;

ADOPTIVE TRANSFER; CELL- AND TISSUE-BASED THERAPY; DISEASE PROGRESSION; HUMANS; IMMUNOTHERAPY; KILLER CELLS, NATURAL; NEOPLASMS;

EID: 84947129611     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/MOT.0000000000000243     Document Type: Review

References (78)

1. Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012; 12:298-306.
2. Couzin-Frankel J. Breakthrough of the year 2013. Cancer immunotherapy. Science 2013; 342:1432-1433.
3. Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med 2006; 354:1813-1826.
4. Caligiuri MA. Human natural killer cells. Blood 2008; 112:461-469.
5. Vivier E, Tomasello E, Baratin M, et al. Functions of natural killer cells. Nat Immunol 2008; 9:503-510.
6. Mittal D, Gubin MM, Schreiber RD, Smyth MJ. New insights into cancer immunoediting and its three component phases-elimination, equilibrium and escape. Curr Opin Immunol 2014; 27:16-25.
7. Vitale M, Cantoni C, Pietra G, et al. Effect of tumor cells and tumor micro-environment on NK-cell function. Eur J Immunol 2014; 44:1582-1592.
8. Costello RT, Sivori S, Marcenaro E, et al. Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood 2002; 99:3661-3667.
9. Fauriat C, Just-Landi S, Mallet F, et al. Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemic cells in NCRdull phenotype induction. Blood 2006; 109:323-330.
10. Imai K, Matsuyama S, Miyake S, et al. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 2000; 356:1795-1799.
11. Ruggeri L, Capanni M, Urbani E, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002; 295:2097-2100.
12. Velardi A, Ruggeri L, Mancusi A, et al. Natural killer cell allorecognition of missing self in allogeneic hematopoietic transplantation: a tool for immu-notherapy of leukemia. Curr Opin Immunol 2009; 21:525-530.
13. Rubnitz JE, Inaba H, Ribeiro RC, et al. A pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol 2010; 28:955-959.
14. Curti A, Ruggeri L, D'Addio A, 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; 118:3273-3279.
15. Miller JS, Soignier Y, Panoskaltsis-Mortari A, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 2005; 105:3051-3057.
16. Bachanova V, Cooley S, Defor TE, et al. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood 2014; 123:3855-3863.
17. Cooley S, Trachtenberg E, Bergemann TL, et al. Donors with group B KIR haplotypes improve relapse-free survival after unrelated hematopoietic cell transplantation for acute myelogenous leukemia. Blood 2009; 113:726-732.
18. Cooley S, Weisdorf DJ, Guethlein L, et al. Donor selection for natural killer cell receptor genes leads to superior survival after unrelated transplantation for acute myelogenous leukemia. Blood 2010; 116:2411-2419.
19. Venstrom JM, Pittari G, Gooley T, et al. HLA-C-dependent prevention of leukemia relapse by donor activating KIR2DS1. N Engl J Med 2012; 367:805-816.
20. Murphy WJ, Parham P, Miller JS. NK cells: from bench to clinic. Biol Blood Marrow Transplant 2012; 18:S2-S7.
21. Geller MA, Miller JS. Use of allogeneic NK cells for cancer immunotherapy. Immunotherapy 2011; 3:1445-1459.
22. Miller JS. Therapeutic applications: natural killer cells in the clinic. Hematology Am Soc Hematol Educ Program 2013; 2013:247-253.
23. Ljunggren H-G, Malmberg K-J. Prospects for the use of NK cells in immu-notherapy of human cancer. Nat Rev Immunol 2007; 7:329-339.
24. Di Santo JP. Natural killer cells: diversity in search of a niche. Nat Immunol 2008; 9:473-475.
25. Orr MT, Lanier LL. Natural killer cell education and tolerance. Cell 2010; 142:847-856.
26. Lanier LL. NK cell receptors. Annu Rev Immunol 1998; 16:359-393.
27. Jonsson HA, Yokoyama WM. Natural killer cell tolerance licensing and other mechanisms. Adv Immunol 2009; 101:27-79.
28. Horowitz A, Strauss-Albee DM, Leipold M, et al. Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry. Sci Transl Med 2013; 5:208ra145.
29. Nguyen S, Beziat V, Dhedin N, et al. HLA-E upregulation on IFN-gamma-activated AML blasts impairs CD94/NKG2A-dependent NK cytolysis after haplo-mismatched hematopoietic SCT. Bone Marrow Transplant 2009; 43:693-699.
30. Gleason MK, Lenvik TR, Mccullar V, et al. Interferon gamma production in response to galectin-9 Tim-3 is an inducible human natural killer cell receptor that enhances interferon gamma production in response to galectin-9. Blood 2012; 119:3064-3072.
31. Hemon P, Jean-Louis F, Ramgolam K, et al. MHC class II engagement by its ligand LAG-3 (CD223) contributes to melanoma resistance to apoptosis. J Immunol 2011; 186:5173-5183.
32. Chamuleau MED, Souwer Y, Van Ham SM, et al. Class II-associated invariant chain peptide expression on myeloid leukemic blasts predicts poor clinical outcome. Cancer Res 2004; 64:5546-5550.
33. Farnault L, Sanchez C, Baier C, et al. Hematological malignancies escape from NK cell innate immune surveillance: mechanisms and therapeutic implications. Clin Dev Immunol 2012; 2012:1-8.
34. Min-Oo G, Kamimura Y, Hendricks DW, et al. Natural killer cells: walking three paths down memory lane. Trends Immunol 2013; 34:251-258.
35. Berrien-Elliott MM, Wagner JA, Fehniger TA. Human cytokine-induced memory-like natural killer cells. J Innate Immun 2015. [Epub ahead of print]
36. Alnabhan R, Madrigal A, Saudemont A. Differential activation of cord blood and peripheral blood natural killer cells by cytokines. Cytotherapy 2015; 17:73-85.
37. Childs RW, Berg M. Bringing natural killer cells to the clinic: ex vivo manipulation. Hematology Am Soc Hematol Educ Program 2013; 2013:234-246.
38. Zheng X, Wang Y, Wei H, et al. LFA-1 and CD2 synergize for the Erk1/2 activation in the natural killer (NK) cell immunological synapse. J Biol Chem 2009; 284:21280-21287.
39. Tonn T, Schwabe D, Klingemann HG, et al. Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy 2013; 15:1563-1570.
40. Gleason MK, Ross J a, Warlick ED, et al. CD16xCD33 bispecific killer cell engager (BiKE) activates NK cells against primary MDS and MDSC CD33+ targets. Blood 2014; 123:3016-3026.
41. Reusch U, Burkhardt C, Fucek I, et al. A novel tetravalent bispecific TandAb (CD30/CD16A) efficiently recruits NK cells for the lysis of CD30+ tumor cells. MAbs 2014; 6:728-739.
42. Le Garff-Tavernier M, Herbi L, de Romeuf C, et al. Antibody-dependent cellular cytotoxicity of the optimized anti-CD20 monoclonal antibody ublitux-imab on chronic lymphocytic leukemia cells with the 17p deletion. Leukemia 2014; 28:230-233.
43. Le Garff-Tavernier M, Herbi L, de Romeuf C, et al. The optimized anti-CD20 monoclonal antibody ublituximab bypasses natural killer phenotypic features in Waldenström macroglobulinemia. Haematologica 2015; 100:147-151.
44. 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.
45. Topfer K, Cartellieri M, Michen S, et al. DAP12-based activating chimeric antigen receptor for NK cell tumor immunotherapy. J Immunol 2015; 194:3201-3212.
46. Ghosh N, Grunwald M, Fasan O, Bhutani M. Expanding role of lenalidomide in hematologic malignancies. Cancer Manag Res 2015; 7:105-119.
47. Bachanova V, Burns LJ, McKenna DH, et al. Allogeneic natural killer cells for refractory lymphoma. Cancer Immunol Immunother 2010; 59:1739-1744.
48. Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol 2006; 6:595-601.
49. Benson DM, Cohen D, Jagannath S, 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. doi:10.1158/1078-0432.CCR-15-0304.
50. Gleason MK, Verneris MR, Todhunter D, 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; 11:2674-2684.
51. Rothe A, Sasse S, Topp MS, et al. AphaseI study of the bispecific anti-CD30/CD16A antibody construct AFM13 in patients with relapsed or refractory Hodgkin lymphoma. Blood 2015; 125:4024-4031.
52. Junttila TT, Parsons K, Olsson C, et al. Superior in vivo efficacy of a fucosylated trastuzumab in the treatment of HER2-amplified breast cancer. Cancer Res 2010; 70:4481-4489.
53. Srivastava RM, Lee SC, Andrade Filho PA, et al. Cetuximab-activated natural killer and dendritic cells collaborate to trigger tumor antigen-specific T-cell immunity in head and neck cancer patients. Clin Cancer Res 2013; 19:1858-1872.
54. Veeramani S, Wang S-Y, Dahle C, et al. Rituximab infusion induces NK activation in lymphoma patients with the high-affinity CD16 polymorphism. Blood 2011; 118:3347-3349.
55. Boyerinas B, Jochems C, Fantini M, et al. Antibody dependent cellular cytotoxicity (ADCC) activity of a novel anti-PD-L1 antibody, avelumab (MSB0010718C), on human tumor cells. Cancer Immunol Res 2015. doi:10.1158/2326-6066.CIR-15-0059.
56. De Romeuf C, Dutertre CA, Le Garff-Tavernier M, et al. Chronic lymphocytic leukaemia cells are efficiently killed by an anti-CD20 monoclonal antibody selected for improved engagement of FcgRIIIA/CD16. Br J Haematol 2008; 140:635-643.
57. Le Garff-Tavernier M, Herbi L, de Romeuf C, et al. Antibody-dependent cellular cytotoxicity of the optimized anti-CD20 monoclonal antibody ublitux-imab on chronic lymphocytic leukemia cells with the 17p deletion. Leukemia 2014; 28:230-233.
58. Chu J, Deng Y, Benson DM, 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; 28:917-927.
59. Glienke W, Esser R, Priesner C, et al. Advantages and applications of CAR-expressing natural killer cells. Front Pharmacol 2015; 6:1-7.
60. Gill S, Tasian SK, Ruella M, et al. Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood 2014; 123:2343-2354.
61. Kenderian SS, Ruella M, Shestova O, et al. CD33 specific chimeric antigen receptor T cells exhibit potent preclinical activity against human acute myeloid leukemia. Leukemia 2015; 29:1637-1647.
62. Romee R, Leong JW, Fehniger TA. Utilizing cytokines to function-enable human NK cells for the immunotherapy of cancer. Scientifica 2014; 2014:1-18.
63. Fehniger TA, Caligiuri MA. Interleukin 15: biology and relevance to human disease. Blood 2001; 97:14-32.
64. Fehniger TA, Cooper MA, Caligiuri MA. Interleukin-2 and interleukin-15: immunotherapy for cancer. Cytokine Growth Factor Rev 2002; 13:169-183.
65. Conlon KC, Lugli E, Welles HC, 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; 33:74-82.
66. Xu W, Jones M, Liu B, et al. Efficacy and mechanism-of-action of a novel superagonist interleukin-15: interleukin-15 receptor aSu/Fc fusion complex in syngeneic murine models of multiple myeloma. Cancer Res 2013; 73:3075-3086.
67. Long EO, Sik Kim H, Liu D, et al. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol 2013; 31:227-258.
68. Romee R, Schneider SE, Leong JW, et al. Cytokine activation induces human memory-like NK cells. Blood 2012; 120:4751-4760.
69. Leong JW, Chase JM, Romee R, et al. Preactivation with IL-12, IL-15, and IL-18 induces CD25 and a functional high-affinity IL-2 receptor on human cytokine-induced memory-like natural killer cells. Biol Blood Marrow Transplant 2014; 20:463-473.
70. Fehniger TA, Stuart RK, Cooley SA, et al. Preliminary results of a phase 1/2 clinical trial of Cndo-109-activated allogeneic natural killer cells in high risk acute myelogenous leukemia patients in first complete remission. Blood 2014; 124:2320.
71. Epling-Burnette PK, Bai F, Painter JS, et al. Lenalidomide effects on NK function in patients with MDS. Blood 2005; 106:#3437.
72. Kohrt HE, Colevas AD, Houot R, et al. Targeting CD137 enhances the efficacy of cetuximab. J Clin Invest 2014; 124:2668-2682.
73. Pegram HJ, Andrews DM, Smyth MJ, et al. Activating and inhibitory receptors of natural killer cells. Immunol Cell Biol 2011; 89:216-224.
74. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9:162-174.
75. Gasteiger G, Hemmers S, Bos PD, et al. IL-2-dependent adaptive control of NK cell homeostasis. J Exp Med 2013; 210:1179-1187. doi:10.1084/jem.20122571.
76. Da Silva IP, Gallois a, Jimenez-Baranda S, et al. Reversal of NK-cell exhaustion in advanced melanoma by Tim-3 blockade. Cancer Immunol Res 2014; 2:410-422.
77. Vey N, Bourhis J-H, Boissel N, et al. A phase I trial of the anti-inhibitory KIR monoclonal antibody IPH2101 for acute myeloid leukemia (AML) in complete remission. Blood 2012; 120:4317-4323.
78. Benson DM, Hofmeister CC, Padmanabhan S, et al. A phase 1 trial of the anti-KIR antibody IPH2101 in patients with relapsed/refractory multiple myeloma. Blood 2012; 120:4324-4333.