Engineering Natural Killer Cells for Cancer Immunotherapy

Molecular Therapy

Volumn 25, Issue 8, 2017, Pages 1769-1781

  Rezvani, Katayoun ^a   Rouce, Rayne ^b   Liu, Enli ^a   Shpall, Elizabeth ^a  

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

^b TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

adoptive therapy; CAR; cellular therapy; chimeric antigen receptors; genetic engineering; immunotherapy; killer immunoglobulin receptor; natural killer cells; NK cells; NK expansion

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; BIOLOGICAL MARKER; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANTIGEN SPECIFICITY; CANCER IMMUNOTHERAPY; CANCER THERAPY; CELL ENGINEERING; CELL THERAPY; CELLULAR IMMUNITY; CLINICAL EFFECTIVENESS; CYTOLOGY; CYTOTOXICITY; DNA MODIFICATION; EVIDENCE BASED PRACTICE; HUMAN; NATURAL KILLER CELL; NONHUMAN; PERSONALIZED MEDICINE; PRECLINICAL STUDY; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TARGET CELL; ANIMAL; BIOLOGICAL THERAPY; DISEASE MODEL; GENETIC ENGINEERING; GENETICS; IMMUNOLOGY; METABOLISM; NEOPLASM; PROCEDURES; TRANSLATIONAL RESEARCH;

ANIMALS; BIOMARKERS; CELL- AND TISSUE-BASED THERAPY; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; GENETIC ENGINEERING; HUMANS; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSLATIONAL MEDICAL RESEARCH;

EID: 85021264864     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1016/j.ymthe.2017.06.012     Document Type: Review

References (142)

1. Maude, S.L., Frey, N., Shaw, P.A., Aplenc, R., Barrett, D.M., Bunin, N.J., Chew, A., Gonzalez, V.E., Zheng, Z., Lacey, S.F., et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 371 (2014), 1507–1517.
2. Davila, M.L., Riviere, I., Wang, X., Bartido, S., Park, J., Curran, K., Chung, S.S., Stefanski, J., Borquez-Ojeda, O., Olszewska, M., et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci. Transl. Med., 6, 2014, 224ra25.
3. Lee, D.W., Kochenderfer, J.N., Stetler-Stevenson, M., Cui, Y.K., Delbrook, C., Feldman, S.A., Fry, T.J., Orentas, R., Sabatino, M., Shah, N.N., 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 385 (2015), 517–528.
4. June, C.H., Riddell, S.R., Schumacher, T.N., Adoptive cellular therapy: a race to the finish line. Sci. Transl. Med., 7, 2015, 280ps7.
5. Sadelain, M., CAR therapy: the CD19 paradigm. J. Clin. Invest. 125 (2015), 3392–3400.
6. Locatelli, F., Moretta, F., Brescia, L., Merli, P., Natural killer cells in the treatment of high-risk leukemia. Semin. Immunol. 26 (2014), 173–179.
7. Farag, S.S., Caligiuri, M.A., Human natural killer cell development and biology. Blood Rev. 20 (2006), 123–137.
8. Moretta, L., Locatelli, F., Pende, D., Marcenaro, E., Mingari, M.C., Moretta, A., Killer Ig-like receptor-mediated control of natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Blood 117 (2011), 764–771.
9. Yoon, S.R., Lee, Y.S., Yang, S.H., Ahn, K.H., Lee, J.H., Lee, J.H., Kim, D.Y., Kang, Y.A., Jeon, M., Seol, M., 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. 45 (2010), 1038–1046.
10. Miller, J.S., Soignier, Y., Panoskaltsis-Mortari, A., McNearney, S.A., Yun, G.H., Fautsch, S.K., McKenna, D., Le, C., Defor, T.E., Burns, L.J., et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105 (2005), 3051–3057.
11. Rubnitz, J.E., Inaba, H., Ribeiro, R.C., Pounds, S., Rooney, B., Bell, T., Pui, C.H., Leung, W., NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J. Clin. Oncol. 28 (2010), 955–959.
12. Sotillo, E., Barrett, D.M., Black, K.L., Bagashev, A., Oldridge, D., Wu, G., Sussman, R., Lanauze, C., Ruella, M., Gazzara, M.R., et al. Convergence of acquired mutations and alternative splicing of CD19 enables resistance to CART-19 immunotherapy. Cancer Discov. 5 (2015), 1282–1295.
13. Kim, S., Poursine-Laurent, J., Truscott, S.M., Lybarger, L., Song, Y.J., Yang, L., French, A.R., Sunwoo, J.B., Lemieux, S., Hansen, T.H., Yokoyama, W.M., Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436 (2005), 709–713.
14. Davies, J.O., Stringaris, K., Barrett, A.J., Rezvani, K., Opportunities and limitations of NK cells as adoptive therapy for malignant disease. Cytotherapy 16 (2014), 1453–1466.
15. Wagner, J.A., Berrien-Elliott, M.M., Rosario, M., Leong, J.W., Jewell, B.A., Schappe, T., Abdel-Latif, S., Fehniger, T.A., Cytokine-induced memory-like differentiation enhances unlicensed natural killer cell antileukemia and FcγRIIIa-triggered responses. Biol. Blood Marrow Transplant 23 (2016), 398–404.
16. Cooper, M.A., Fehniger, T.A., Turner, S.C., Chen, K.S., Ghaheri, B.A., Ghayur, T., Carson, W.E., Caligiuri, M.A., Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 97 (2001), 3146–3151.
17. Campbell, J.J., Qin, S., Unutmaz, D., Soler, D., Murphy, K.E., Hodge, M.R., Wu, L., Butcher, E.C., Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J. Immunol. 166 (2001), 6477–6482.
18. 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. USA 108 (2011), 728–732.
19. Kärre, K., Immunology. A perfect mismatch. Science 295 (2002), 2029–2031.
20. Campbell, K.S., Hasegawa, J., Natural killer cell biology: an update and future directions. J. Allergy Clin. Immunol. 132 (2013), 536–544.
21. Caligiuri, M.A., Human natural killer cells. Blood 112 (2008), 461–469.
22. Bradley, M., Zeytun, A., Rafi-Janajreh, A., Nagarkatti, P.S., 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 92 (1998), 4248–4255.
23. Screpanti, V., Wallin, R.P., Ljunggren, H.G., Grandien, A., A central role for death receptor-mediated apoptosis in the rejection of tumors by NK cells. J. Immunol. 167 (2001), 2068–2073.
24. Kayagaki, N., Yamaguchi, N., Nakayama, M., Takeda, K., Akiba, H., Tsutsui, H., Okamura, H., Nakanishi, K., Okumura, K., Yagita, H., Expression and function of TNF-related apoptosis-inducing ligand on murine activated NK cells. J. Immunol. 163 (1999), 1906–1913.
25. Joncker, N.T., Shifrin, N., Delebecque, F., Raulet, D.H., Mature natural killer cells reset their responsiveness when exposed to an altered MHC environment. J. Exp. Med. 207 (2010), 2065–2072.
26. Lotzová, E., Savary, C.A., Herberman, R.B., Inhibition of clonogenic growth of fresh leukemia cells by unstimulated and IL-2 stimulated NK cells of normal donors. Leuk. Res. 11 (1987), 1059–1066.
27. Stringaris, K., Sekine, T., Khoder, A., Alsuliman, A., Razzaghi, B., Sargeant, R., Pavlu, J., Brisley, G., de Lavallade, H., Sarvaria, A., et al. Leukemia-induced phenotypic and functional defects in natural killer cells predict failure to achieve remission in acute myeloid leukemia. Haematologica 99 (2013), 836–847.
28. Fauriat, C., Just-Landi, S., Mallet, F., Arnoulet, C., Sainty, D., Olive, D., Costello, R.T., Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood 109 (2007), 323–330.
29. Satwani, P., Bavishi, S., Saha, A., Zhao, F., Ayello, J., van de Ven, C., Chu, Y., Cairo, M.S., Upregulation of NKG2D ligands in acute lymphoblastic leukemia and non-Hodgkin lymphoma cells by romidepsin and enhanced in vitro and in vivo natural killer cell cytotoxicity. Cytotherapy 16 (2014), 1431–1440.
30. Jin, F., Lin, H., Gao, S., Hu, Z., Zuo, S., Sun, L., Jin, C., Li, W., Yang, Y., The anti-tumor role of NK cells in vivo pre-activated and restimulated by interleukins in acute lymphoblastic leukemia. Oncotarget, 7, 2016, 79187.
31. Rouce, R.H., Shaim, H., Sekine, T., Weber, G., Ballard, B., Ku, S., Barese, C., Murali, V., Wu, M.F., Liu, H., et al. The TGF-β/SMAD pathway is an important mechanism for NK cell immune evasion in childhood B-acute lymphoblastic leukemia. Leukemia 30 (2016), 800–811.
32. 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. 138 (2007), 97–100.
33. Bachanova, V., Miller, J.S., NK cells in therapy of cancer. Crit. Rev. Oncog. 19 (2014), 133–141.
34. Shah, N., Martin-Antonio, B., Yang, H., Ku, S., Lee, D.A., Cooper, L.J., Decker, W.K., Li, S., Robinson, S.N., Sekine, T., 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, 8, 2013, e76781.
35. El-Sherbiny, Y.M., Meade, J.L., Holmes, T.D., McGonagle, D., Mackie, S.L., Morgan, A.W., Cook, G., Feyler, S., Richards, S.J., Davies, F.E., et al. Requirement for DNAM-1, NKG2D, and NKp46 in the natural killer cell-mediated killing of myeloma cells. Cancer Res. 67 (2007), 8444–8449.
36. Swift, B.E., Williams, B.A., Kosaka, Y., Wang, X.H., Medin, J.A., Viswanathan, S., Martinez-Lopez, J., Keating, A., Natural killer cell lines preferentially kill clonogenic multiple myeloma cells and decrease myeloma engraftment in a bioluminescent xenograft mouse model. Haematologica 97 (2012), 1020–1028.
37. Davies, F.E., Raje, N., Hideshima, T., Lentzsch, S., Young, G., Tai, Y.T., Lin, B., Podar, K., Gupta, D., Chauhan, D., et al. Thalidomide and immunomodulatory derivatives augment natural killer cell cytotoxicity in multiple myeloma. Blood 98 (2001), 210–216.
38. Liu, Y., Wu, H.W., Sheard, M.A., Sposto, R., Somanchi, S.S., Cooper, L.J., Lee, D.A., Seeger, R.C., Growth and activation of natural killer cells ex vivo from children with neuroblastoma for adoptive cell therapy. Clin. Cancer Res. 19 (2013), 2132–2143.
39. Rusakiewicz, S., Semeraro, M., Sarabi, M., Desbois, M., Locher, C., Mendez, R., Vimond, N., Concha, A., Garrido, F., Isambert, N., et al. Immune infiltrates are prognostic factors in localized gastrointestinal stromal tumors. Cancer Res. 73 (2013), 3499–3510.
40. Mamessier, E., Sylvain, A., Thibult, M.L., Houvenaeghel, G., Jacquemier, J., Castellano, R., Gonçalves, A., André, P., Romagné, F., Thibault, G., et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J. Clin. Invest. 121 (2011), 3609–3622.
41. Gras Navarro, A., Björklund, A.T., Chekenya, M., Therapeutic potential and challenges of natural killer cells in treatment of solid tumors. Front. Immunol, 6, 2015, 202.
42. Kailayangiri, S., Altvater, B., Spurny, C., Jamitzky, S., Schelhaas, S., Jacobs, A.H., Wiek, C., Roellecke, K., Hanenberg, H., Hartmann, W., et al. Targeting Ewing sarcoma with activated and GD2-specific chimeric antigen receptor-engineered human NK cells induces upregulation of immune-inhibitory HLA-G. OncoImmunology, 6, 2016, e1250050.
43. Koepsell, S.A., Miller, J.S., McKenna, D.H. Jr., Natural killer cells: a review of manufacturing and clinical utility. Transfusion 53 (2013), 404–410.
44. Leong, J.W., Chase, J.M., Romee, R., Schneider, S.E., Sullivan, R.P., Cooper, M.A., Fehniger, T.A., 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 20 (2014), 463–473.
45. Miller, J.S., Rooney, C.M., Curtsinger, J., McElmurry, R., McCullar, V., Verneris, M.R., Lapteva, N., McKenna, D., Wagner, J.E., Blazar, B.R., Tolar, J., 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. 20 (2014), 1252–1257.
46. Berg, M., Lundqvist, A., McCoy, P. Jr., Samsel, L., Fan, Y., Tawab, A., Childs, R., Berg. 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 11 (2009), 341–355.
47. Rezvani, K., Rouce, R.H., The application of natural killer cell immunotherapy for the treatment of cancer. Front. Immunol., 6, 2015, 578.
48. 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. 209 (2012), 2351–2365.
49. Romain, G., Senyukov, V., Rey-Villamizar, N., Merouane, A., Kelton, W., Liadi, I., Mahendra, A., Charab, W., Georgiou, G., Roysam, B., et al. Antibody Fc engineering improves frequency and promotes kinetic boosting of serial killing mediated by NK cells. Blood 124 (2014), 3241–3249.
50. Kanazawa, T., Hiramatsu, Y., Iwata, S., Siddiquey, M., Sato, Y., Suzuki, M., Ito, Y., Goshima, F., Murata, T., Kimura, H., Anti-CCR4 monoclonal antibody mogamulizumab for the treatment of EBV-associated T- and NK-cell lymphoproliferative diseases. Clin. Cancer Res. 20 (2014), 5075–5084.
51. Lin, W., Voskens, C.J., Zhang, X., Schindler, D.G., Wood, A., Burch, E., Wei, Y., Chen, L., Tian, G., Tamada, K., et al. Fc-dependent expression of CD137 on human NK cells: insights into “agonistic” effects of anti-CD137 monoclonal antibodies. Blood 112 (2008), 699–707.
52. Benson, D.M. Jr., Bakan, C.E., Zhang, S., Collins, S.M., Liang, J., Srivastava, S., Hofmeister, C.C., Efebera, Y., Andre, P., Romagne, F., et al. IPH2101, a novel anti-inhibitory KIR antibody, and lenalidomide combine to enhance the natural killer cell versus multiple myeloma effect. Blood 118 (2011), 6387–6391.
53. Terszowski, G., Klein, C., Stern, M., KIR/HLA interactions negatively affect rituximab- but not GA101 (obinutuzumab)-induced antibody-dependent cellular cytotoxicity. J. Immunol 192 (2014), 5618–5624.
54. Curti, A., Ruggeri, L., D'Addio, A., Bontadini, A., Dan, E., Motta, M.R., Trabanelli, S., Giudice, V., Urbani, E., Martinelli, G., et al. Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood 118 (2011), 3273–3279.
55. Rubnitz, J.E., Inaba, H., Kang, G., Gan, K., Hartford, C., Triplett, B.M., Dallas, M., Shook, D., Gruber, T., Pui, C.H., Leung, W., Natural killer cell therapy in children with relapsed leukemia. Pediatr. Blood Cancer 62 (2015), 1468–1472.
56. Woll, P.S., Grzywacz, B., Tian, X., Marcus, R.K., Knorr, D.A., Verneris, M.R., Kaufman, D.S., Human embryonic stem cells differentiate into a homogeneous population of natural killer cells with potent in vivo antitumor activity. Blood 113 (2009), 6094–6101.
57. Chouaib, S., Pittari, G., Nanbakhsh, A., El Ayoubi, H., Amsellem, S., Bourhis, J.H., Spanholtz, J., Improving the outcome of leukemia by natural killer cell-based immunotherapeutic strategies. Front. Immunol., 5, 2014, 95.
58. Shaim, H., Yvon, E., Cord blood: a promising source of allogeneic natural killer cells for immunotherapy. Cytotherapy 17 (2015), 1–2.
59. Denman, C.J., Senyukov, V.V., Somanchi, S.S., Phatarpekar, P.V., Kopp, L.M., Johnson, J.L., Singh, H., Hurton, L., Maiti, S.N., Huls, M.H., et al. Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PLoS ONE, 7, 2012, e30264.
60. Klingemann, H.G., Wong, E., Maki, G., A cytotoxic NK-cell line (NK-92) for ex vivo purging of leukemia from blood. Biol. Blood Marrow Transplant. 2 (1996), 68–75.
61. Tonn, T., Schwabe, D., Klingemann, H.G., Becker, S., Esser, R., Koehl, U., Suttorp, M., Seifried, E., Ottmann, O.G., Bug, G., Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy 15 (2013), 1563–1570.
62. Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W.D., Tosti, A., Posati, S., Rogaia, D., Frassoni, F., Aversa, F., et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295 (2002), 2097–2100.
63. Olson, J.A., Leveson-Gower, D.B., Gill, S., Baker, J., Beilhack, A., Negrin, R.S., NK cells mediate reduction of GVHD by inhibiting activated, alloreactive T cells while retaining GVT effects. Blood, 115, 2010 4293–4230.
64. Passweg, J.R., Tichelli, A., Meyer-Monard, S., Heim, D., Stern, M., Kühne, T., Favre, G., Gratwohl, A., Purified donor NK-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia 18 (2004), 1835–1838.
65. Koehl, U., Kalberer, C., Spanholtz, J., Lee, D.A., Miller, J.S., Cooley, S., Lowdell, M., Uharek, L., Klingemann, H., Curti, A., et al. Advances in clinical NK cell studies: donor selection, manufacturing and quality control. OncoImmunology, 5, 2015, e1115178.
66. Eshhar, Z., Waks, T., Gross, G., Schindler, D.G., Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc. Natl. Acad. Sci. USA 90 (1993), 720–724.
67. Rouce, R.H., Sharma, S., Huynh, M., Heslop, H.E., Recent advances in T-cell immunotherapy for haematological malignancies. Br. J. Haematol 176 (2017), 688–704.
68. Sadelain, M., Chimeric antigen receptors: driving immunology towards synthetic biology. Curr. Opin. Immunol. 41 (2016), 68–76.
69. Kebriaei, P., Singh, H., Huls, M.H., Figliola, M.J., Bassett, R., Olivares, S., Jena, B., Dawson, M.J., Kumaresan, P.R., Su, S., et al. Phase I trials using sleeping beauty to generate CD19-specific CAR T cells. J. Clin. Invest 126 (2016), 3363–3376.
70. Cruz, C.R., Micklethwaite, K.P., Savoldo, B., Ramos, C.A., Lam, S., Ku, S., Diouf, O., Liu, E., Barrett, A.J., Ito, S., et al. Infusion of donor-derived CD19-redirected virus-specific T cells for B-cell malignancies relapsed after allogeneic stem cell transplant: a phase 1 study. Blood 122 (2013), 2965–2973.
71. Ghosh, A., Smith, M., James, S.E., Davila, M.L., Velardi, E., Argyropoulos, K.V., Gunset, G., Perna, F., Kreines, F.M., Levy, E.R., et al. Donor CD19 CAR T cells exert potent graft-versus-lymphoma activity with diminished graft-versus-host activity. Nat. Med. 23 (2017), 242–249.
72. Ren, J., Liu, X., Fang, C., Jiang, S., June, C.H., Zhao, Y., Multiplex genome editing to generate universal CAR T cells resistant to PD1 inhibition. Clin. Cancer Res. 23 (2017), 2255–2266.
73. Brudno, J.N., Somerville, R.P., Shi, V., Rose, J.J., Halverson, D.C., Fowler, D.H., Gea-Banacloche, J.C., Pavletic, S.Z., Hickstein, D.D., Lu, T.L., et al. Allogeneic T cells that express an anti-CD19 chimeric antigen receptor induce remissions of B-cell malignancies that progress after allogeneic hematopoietic stem-cell transplantation without causing graft-versus-host disease. J. Clin. Oncol 34 (2016), 1112–1121.
74. Geller, M.A., Miller, J.S., Use of allogeneic NK cells for cancer immunotherapy. Immunotherapy 3 (2011), 1445–1459.
75. Cooley, S., Trachtenberg, E., Bergemann, T.L., Saeteurn, K., Klein, J., Le, C.T., Marsh, S.G., Guethlein, L.A., Parham, P., Miller, J.S., Weisdorf, D.J., Donors with group B KIR haplotypes improve relapse-free survival after unrelated hematopoietic cell transplantation for acute myelogenous leukemia. Blood 113 (2009), 726–732.
76. Sekine, T., Marin, D., Cao, K., Li, L., Mehta, P., Shaim, H., Sobieski, C., Jones, R., Oran, B., Hosing, C., et al. Specific combinations of donor and recipient KIR-HLA genotypes predict for large differences in outcome after cord blood transplantation. Blood 128 (2016), 297–312.
77. Bao, X., Wang, M., Zhou, H., Zhang, H., Wu, X., Yuan, X., Li, Y., Wu, D., He, J., Donor killer immunoglobulin-like receptor profile Bx1 imparts a negative effect and centromeric B-specific gene motifs render a positive effect on standard-risk acute myeloid leukemia/myelodysplastic syndrome patient survival after unrelated donor hematopoietic stem cell transplantation. Biol. Blood Marrow Transplant. 22 (2016), 232–239.
78. Oevermann, L., Michaelis, S.U., Mezger, M., Lang, P., Toporski, J., Bertaina, A., Zecca, M., Moretta, L., Locatelli, F., Handgretinger, R., KIR B haplotype donors confer a reduced risk for relapse after haploidentical transplantation in children with ALL. Blood 124 (2014), 2744–2747.
79. Carlsten, M., Childs, R.W., Genetic manipulation of NK cells for cancer immunotherapy: techniques and clinical implications. Front. Immunol., 6, 2015, 266.
80. Glienke, W., Esser, R., Priesner, C., Suerth, J.D., Schambach, A., Wels, W.S., Grez, M., Kloess, S., Arseniev, L., Koehl, U., Advantages and applications of CAR-expressing natural killer cells. Front. Pharmacol., 6, 2015, 21.
81. Tettamanti, S., Marin, V., Pizzitola, I., Magnani, C.F., Giordano Attianese, G.M., Cribioli, E., Maltese, F., Galimberti, S., Lopez, A.F., Biondi, A., et al. Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor. Br. J. Haematol. 161 (2013), 389–401.
82. Liu, E., Tong, Y., Dotti, G., Savoldo, B., Muftuoglu, M., Kondo, K., Mukherjee, M., Orange, J.S., Sobieski, C., Alsuliman, A., et al. Cord blood derived natural killer cells engineered with a chimeric antigen receptor targeting CD19 and expressing IL-15 have long term persistence and exert potent anti-leukemia activity. Blood, 126, 2016, 3091.
83. Kloess, S., Huenecke, S., Piechulek, D., Esser, R., Koch, J., Brehm, C., Soerensen, J., Gardlowski, T., Brinkmann, A., Bader, P., et al. IL-2-activated haploidentical NK cells restore NKG2D-mediated NK-cell cytotoxicity in neuroblastoma patients by scavenging of plasma MICA. Eur. J. Immunol. 40 (2010), 3255–3267.
84. Raffaghello, L., Prigione, I., Airoldi, I., Camoriano, M., Levreri, I., Gambini, C., Pende, D., Steinle, A., Ferrone, S., Pistoia, V., Downregulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia 6 (2004), 558–568.
85. Huenecke, S., Zimmermann, S.Y., Kloess, S., Esser, R., Brinkmann, A., Tramsen, L., Koenig, M., Erben, S., Seidl, C., Tonn, T., et al. IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16- subpopulations and in vivo influence after haploidentical NK cell infusion. J. Immunother. 33 (2010), 200–210.
86. Klingemann, H.G., Cellular therapy of cancer with natural killer cells-where do we stand. Cytotherapy 15 (2013), 1185–1194.
87. Altvater, B., Landmeier, S., Pscherer, S., Temme, J., Schweer, K., Kailayangiri, S., Campana, D., Juergens, H., Pule, M., Rossig, C., 2B4 (CD244) signaling by recombinant antigen-specific chimeric receptors costimulates natural killer cell activation to leukemia and neuroblastoma cells. Clin. Cancer Res. 15 (2009), 4857–4866.
88. Imai, C., Iwamoto, S., Campana, D., Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood 106 (2005), 376–383.
89. Li, L., Liu, L.N., Feller, S., Allen, C., Shivakumar, R., Fratantoni, J., Wolfraim, L.A., Fujisaki, H., Campana, D., Chopas, N., et al. Expression of chimeric antigen receptors in natural killer cells with a regulatory-compliant non-viral method. Cancer Gene Ther. 17 (2010), 147–154.
90. Shimasaki, N., Fujisaki, H., Cho, D., Masselli, M., Lockey, T., Eldridge, P., Leung, W., Campana, D., A clinically adaptable method to enhance the cytotoxicity of natural killer cells against B-cell malignancies. Cytotherapy 14 (2012), 830–840.
91. Chu, Y., Hochberg, J., Yahr, A., Ayello, J., van de Ven, C., Barth, M., Czuczman, M., Cairo, M.S., Targeting CD20+ aggressive B-cell non-Hodgkin lymphoma by anti-CD20 CAR mRNA-modified expanded natural killer cells in vitro and in NSG mice. Cancer Immunol. Res. 3 (2015), 333–344.
92. Kruschinski, A., Moosmann, A., Poschke, I., Norell, H., Chmielewski, M., Seliger, B., Kiessling, R., Blankenstein, T., Abken, H., Charo, J., Engineering antigen-specific primary human NK cells against HER-2 positive carcinomas. Proc. Natl. Acad. Sci. USA 105 (2008), 17481–17486.
93. Romanski, A., Uherek, C., Bug, G., Seifried, E., Klingemann, H., Wels, W.S., Ottmann, O.G., Tonn, T., CD19-CAR engineered NK-92 cells are sufficient to overcome NK cell resistance in B-cell malignancies. J. Cell. Mol. Med. 20 (2016), 1287–1294.
94. Boissel, L., Betancur, M., Wels, W.S., Tuncer, H., Klingemann, H., Transfection with mRNA for CD19 specific chimeric antigen receptor restores NK cell mediated killing of CLL cells. Leuk. Res. 33 (2009), 1255–1259.
95. Boissel, L., Betancur-Boissel, M., Lu, W., Krause, D.S., Van Etten, R.A., Wels, W.S., Klingemann, H., Retargeting NK-92 cells by means of CD19- and CD20-specific chimeric antigen receptors compares favorably with antibody-dependent cellular cytotoxicity. OncoImmunology, 2, 2013, e26527.
96. Müller, T., Uherek, C., Maki, G., Chow, K.U., Schimpf, A., Klingemann, H.G., Tonn, T., Wels, W.S., 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. 57 (2008), 411–423.
97. Jiang, H., Zhang, W., Shang, P., Zhang, H., Fu, W., Ye, F., Zeng, T., Huang, H., Zhang, X., Sun, W., et al. Transfection of chimeric anti-CD138 gene enhances natural killer cell activation and killing of multiple myeloma cells. Mol. Oncol. 8 (2014), 297–310.
98. Esser, R., Müller, T., Stefes, D., Kloess, S., Seidel, D., Gillies, S.D., Aperlo-Iffland, C., Huston, J.S., Uherek, C., Schönfeld, K., 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. 16 (2012), 569–581.
99. Uherek, C., Tonn, T., Uherek, B., Becker, S., Schnierle, B., Klingemann, H.G., Wels, W., Retargeting of natural killer-cell cytolytic activity to ErbB2-expressing cancer cells results in efficient and selective tumor cell destruction. Blood 100 (2002), 1265–1273.
100. Schönfeld, K., Sahm, C., Zhang, C., Naundorf, S., Brendel, C., Odendahl, M., Nowakowska, P., Bönig, H., Köhl, U., Kloess, S., et al. Selective inhibition of tumor growth by clonal NK cells expressing an ErbB2/HER2-specific chimeric antigen receptor. Mol. Ther. 23 (2015), 330–338.
101. Sahm, C., Schönfeld, K., Wels, W.S., Expression of IL-15 in NK cells results in rapid enrichment and selective cytotoxicity of gene-modified effectors that carry a tumor-specific antigen receptor. Cancer Immunol. Immunother 61 (2012), 1451–1461.
102. Zhang, G., Liu, R., Zhu, X., Wang, L., Ma, J., Han, H., Wang, X., Zhang, G., He, W., Wang, W., et al. Retargeting NK-92 for anti-melanoma activity by a TCR-like single-domain antibody. Immunol. Cell Biol. 91 (2013), 615–624.
103. Tagaya, Y., Bamford, R.N., DeFilippis, A.P., Waldmann, T.A., IL-15: a pleiotropic cytokine with diverse receptor/signaling pathways whose expression is controlled at multiple levels. Immunity 4 (1996), 329–336.
104. Di Stasi, A., Tey, S.K., Dotti, G., Fujita, Y., Kennedy-Nasser, A., Martinez, C., Straathof, K., Liu, E., Durett, A.G., Grilley, B., et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 365 (2011), 1673–1683.
105. Suerth, J.D., Morgan, M.A., Kloess, S., Heckl, D., Neudörfl, C., Falk, C.S., Koehl, U., Schambach, A., Efficient generation of gene-modified human natural killer cells via alpharetroviral vectors. J. Mol. Med. (Berl.) 94 (2016), 83–93.
106. Hermanson, D.L., Kaufman, D.S., Utilizing chimeric antigen receptors to direct natural killer cell activity. Front. Immunol., 6, 2015, 195.
107. Yagita, M., Huang, C.L., Umehara, H., Matsuo, Y., Tabata, R., Miyake, M., Konaka, Y., Takatsuki, K., A novel natural killer cell line (KHYG-1) from a patient with aggressive natural killer cell leukemia carrying a p53 point mutation. Leukemia 14 (2000), 922–930.
108. Arai, S., Meagher, R., Swearingen, M., Myint, H., Rich, E., Martinson, J., Klingemann, H., Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy 10 (2008), 625–632.
109. Chu, J., Deng, Y., Benson, D.M., He, S., Hughes, T., Zhang, J., Peng, Y., Mao, H., Yi, L., Ghoshal, K., 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 28 (2014), 917–927.
110. Suck, G., Odendahl, M., Nowakowska, P., Seidl, C., Wels, W.S., Klingemann, H.G., Tonn, T., NK-92: an ‘off-the-shelf therapeutic’ for adoptive natural killer cell-based cancer immunotherapy. Cancer Immunol. Immunother 65 (2016), 485–492.
111. Boissel, L., Klingemann, H., Khan, J., Soon-Shiong, P., Intra-tumor injection of CAR-engineered NK cells induces tumor regression and protection against tumor re-challenge. Blood, 128, 2016, 466.
112. Klingemann, H., Are natural killer cells superior CAR drivers?. OncoImmunology, 3, 2014, e28147.
113. Oelsner, S., Friede, M.E., Zhang, C., Wagner, J., Badura, S., Bader, P., Ullrich, E., Ottmann, O.G., Klingemann, H., Tonn, T., Wels, W.S., Continuously expanding CAR NK-92 cells display selective cytotoxicity against B-cell leukemia and lymphoma. Cytotherapy 19 (2017), 235–249.
114. Chen, X., Han, J., Chu, J., Zhang, L., Zhang, J., Chen, C., Chen, L., Wang, Y., Wang, H., Yi, L., et al. A combinational therapy of EGFR-CAR NK cells and oncolytic herpes simplex virus 1 for breast cancer brain metastases. Oncotarget 7 (2016), 27764–27777.
115. Han, J., Chu, J., Keung Chan, W., Zhang, J., Wang, Y., Cohen, J.B., Victor, A., Meisen, W.H., Kim, S.H., Grandi, P., et al. CAR-engineered NK cells targeting wild-type EGFR and EGFRvIII enhance killing of glioblastoma and patient-derived glioblastoma stem cells. Sci. Rep., 5, 2015, 11483.
116. Genßler, S., Burger, M.C., Zhang, C., Oelsner, S., Mildenberger, I., Wagner, M., Steinbach, J.P., Wels, W.S., Dual targeting of glioblastoma with chimeric antigen receptor-engineered natural killer cells overcomes heterogeneity of target antigen expression and enhances antitumor activity and survival. OncoImmunology, 5, 2015, e1119354.
117. Tassev, D.V., Cheng, M., Cheung, N.K., Retargeting 92 cells using an HLA-A2-restricted, EBNA3C-specific chimeric antigen receptor. Cancer Gene Ther 19 (2012), 84–100.
118. Chen, K.H., Wada, M., Pinz, K.G., Liu, H., Lin, K.W., Jares, A., Firor, A.E., Shuai, X., Salman, H., Golightly, M., et al. Preclinical targeting of aggressive T cell malignancies using anti-CD5 chimeric antigen receptor. Leukemia, 2017, 10.1038/leu.2017.8 Published online February 10, 2017.
119. Uphoff, C.C., Denkmann, S.A., Steube, K.G., Drexler, H.G., Detection of EBV, HBV, HCV, HIV-1, HTLV-I and -II, and SMRV in human and other primate cell lines. J. Biomed. Biotechnol., 2010, 2010, 904767.
120. Maki, G., Klingemann, H.G., Martinson, J.A., Tam, Y.K., Factors regulating the cytotoxic activity of the human natural killer cell line, NK-92. J. Hematother. Stem Cell Res. 10 (2001), 369–383.
121. Weitzman, J., Betancur, M., Boissel, L., Rabinowitz, A.P., Klein, A., Klingemann, H., Variable contribution of monoclonal antibodies to ADCC in patients with chronic lymphocytic leukemia. Leuk. Lymphoma 50 (2009), 1361–1368.
122. Jochems, C., Hodge, J.W., Fantini, M., Fujii, R., Morillon, Y.M. 2nd, Greiner, J.W., Padget, M.R., Tritsch, S.R., Tsang, K.Y., Campbell, K.S., et al. An NK cell line (haNK) expressing high levels of granzyme and engineered to express the high affinity CD16 allele. Oncotarget 7 (2016), 86359–86373.
123. Lowe, E., Truscott, L.C., De Oliveira, S.N., In vitro generation of human NK cells expressing chimeric antigen receptor through differentiation of gene-modified hematopoietic stem cells. Methods Mol. Biol. 1441 (2016), 241–251.
124. Bauer, S., Groh, V., Wu, J., Steinle, A., Phillips, J.H., Lanier, L.L., Spies, T., Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285 (1999), 727–729.
125. Gasser, S., Orsulic, S., Brown, E.J., Raulet, D.H., The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436 (2005), 1186–1190.
126. Chang, Y.H., 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. 73 (2013), 1777–1786.
127. Lindau, D., Gielen, P., Kroesen, M., Wesseling, P., Adema, G.J., The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology 138 (2013), 105–115.
128. Wu, J., Song, Y., Bakker, A.B., Bauer, S., Spies, T., Lanier, L.L., Phillips, J.H., An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285 (1999), 730–732.
129. Upshaw, J.L., Arneson, L.N., Schoon, R.A., Dick, C.J., Billadeau, D.D., Leibson, P.J., NKG2D-mediated signaling requires a DAP10-bound Grb2-Vav1 intermediate and phosphatidylinositol-3-kinase in human natural killer cells. Nat. Immunol. 7 (2006), 524–532.
130. Töpfer, K., Cartellieri, M., Michen, S., Wiedemuth, R., Müller, N., Lindemann, D., Bachmann, M., Füssel, M., Schackert, G., Temme, A., DAP12-based activating chimeric antigen receptor for NK cell tumor immunotherapy. J. Immunol. 194 (2015), 3201–3212.
131. Hassuneh, M.R., Nagarkatti, P.S., Nagarkatti, M., Evidence for the participation of interleukin-2 (IL-2) and IL-4 in the regulation of autonomous growth and tumorigenesis of transformed cells of lymphoid origin. Blood 89 (1997), 610–620.
132. Baum, C., Fehse, B., Mutagenesis by retroviral transgene insertion: risk assessment and potential alternatives. Curr. Opin. Mol. Ther. 5 (2003), 458–462.
133. Wu, C., Dunbar, C.E., Stem cell gene therapy: the risks of insertional mutagenesis and approaches to minimize genotoxicity. Front. Med. 5 (2011), 356–371.
134. Stein, S., Ott, M.G., Schultze-Strasser, S., Jauch, A., Burwinkel, B., Kinner, A., Schmidt, M., Krämer, A., Schwäble, J., Glimm, H., et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat. Med. 16 (2010), 198–204.
135. Braun, C.J., Boztug, K., Paruzynski, A., Witzel, M., Schwarzer, A., Rothe, M., Modlich, U., Beier, R., Göhring, G., Steinemann, D., et al. Gene therapy for Wiskott-Aldrich syndrome–long-term efficacy and genotoxicity. Sci. Transl. Med., 6, 2014, 227ra33.
136. Hacein-Bey-Abina, S., Garrigue, A., Wang, G.P., Soulier, J., Lim, A., Morillon, E., Clappier, E., Caccavelli, L., Delabesse, E., Beldjord, K., et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118 (2008), 3132–3142.
137. Zhao, Y., Moon, E., Carpenito, C., Paulos, C.M., Liu, X., Brennan, A.L., Chew, A., Carroll, R.G., Scholler, J., Levine, B.L., et al. Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res. 70 (2010), 9053–9061.
138. Zhou, X., Dotti, G., Krance, R.A., Martinez, C.A., Naik, S., Kamble, R.T., Durett, A.G., Dakhova, O., Savoldo, B., Di Stasi, A., et al. Inducible caspase-9 suicide gene controls adverse effects from alloreplete T cells after haploidentical stem cell transplantation. Blood 125 (2015), 4103–4113.
139. Kwon, H.J., Kim, N., Kim, H.S., Molecular checkpoints controlling natural killer cell activation and their modulation for cancer immunotherapy. Exp. Mol. Med., 49, 2017, e311.
140. Poirot, L., Philip, B., Schiffer-Mannioui, C., Le Clerre, D., Chion-Sotinel, I., Derniame, S., Potrel, P., Bas, C., Lemaire, L., Galetto, R., et al. Multiplex genome-edited T-cell manufacturing platform for “off-the-shelf” adoptive T-cell immunotherapies. Cancer Res. 75 (2015), 3853–3864.
141. Qasim, W., Zhan, H., Samarasinghe, S., Adams, S., Amrolia, P., Stafford, S., Butler, K., Rivat, C., Wright, G., Somana, K., et al. Molecular remission of infant B-ALL after infusion of universal TALEN gene-edited CAR T cells. Sci. Transl. Med., 9, 2017, eaaj2013.
142. Qasim, W., Amrolia, P.J., Samarasinghe, S., Ghorashian, S., Zhan, H., Stafford, S., Butler, K., Ahsan, G., Gilmour, K., Adams, S., et al. First clinical application of Talen engineered universal CAR19 T cells in B-ALL. Blood, 126, 2015, 2046.