Continuously expanding CAR NK-92 cells display selective cytotoxicity against B-cell leukemia and lymphoma

Cytotherapy

Volumn 19, Issue 2, 2017, Pages 235-249

  Oelsner, Sarah ^a   Friede, Miriam E ^a   Zhang, Congcong ^a   Wagner, Juliane ^b   Badura, Susanne ^b   Bader, Peter ^b   Ullrich, Evelyn ^b   Ottmann, Oliver G ^c   Klingemann, Hans ^d   Tonn, Torsten ^e   Wels, Winfried S ^a,f  

^a INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^d NantKwest   (United States)

^e DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

adoptive immunotherapy; B cell malignancies; CD19; chimeric antigen receptor; natural killer cells

Indexed keywords

CD137 ANTIGEN; CD19 ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; CYTOKINE; LENTIVIRUS VECTOR; CD3 ANTIGEN, ZETA CHAIN; EPITOPE; HYBRID PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B CELL LEUKEMIA; B CELL LYMPHOMA; CANCER CELL LINE; CANCER INHIBITION; CELL ENGINEERING; CELL EXPANSION; CELL KILLING; CELL TRANSPLANTATION; CONJUGATE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DEGRANULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NATURAL KILLER CELL; NATURAL KILLER CELL 92; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAJI CELL LINE; VIRAL GENE DELIVERY SYSTEM; ADOPTIVE IMMUNOTHERAPY; ANIMAL; B LYMPHOCYTE; CELL PROLIFERATION; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOCYTE ACTIVATION; LYMPHOMA; LYMPHOMA, B-CELL; METABOLISM; NONOBESE DIABETIC MOUSE; PROCEDURES; SCID MOUSE; TRANSPLANTATION; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD137; ANTIGENS, CD19; ANTIGENS, CD3; B-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; HEK293 CELLS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOCYTE ACTIVATION; LYMPHOMA; LYMPHOMA, B-CELL; MALE; MICE; MICE, INBRED NOD; MICE, SCID; RECOMBINANT FUSION PROTEINS;

EID: 85006965240     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2016.10.009     Document Type: Article

References (50)

1. [1] Kalos, M., Levine, B.L., Porter, D.L., Katz, S., Grupp, S.A., Bagg, A., et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med, 3, 2011 95ra73.
2. [2] Grupp, S.A., Kalos, M., Barrett, D., Aplenc, R., Porter, D.L., Rheingold, S.R., et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368 (2013), 1509–1518.
3. [3] Brentjens, R.J., Davila, M.L., Riviere, I., Park, J., Wang, X., Cowell, L.G., et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med, 5, 2013 177ra38.
4. [4] Cruz, C.R., Micklethwaite, K.P., Savoldo, B., Ramos, C.A., Lam, S., Ku, 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.
5. [5] Maude, S.L., Frey, N., Shaw, P.A., Aplenc, R., Barrett, D.M., Bunin, N.J., et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med 371 (2014), 1507–1517.
6. [6] Lee, D.W., Kochenderfer, J.N., Stetler-Stevenson, M., Cui, Y.K., Delbrook, C., Feldman, S.A., 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.
7. [7] Kochenderfer, J.N., Dudley, M.E., Kassim, S.H., Somerville, R.P., Carpenter, R.O., Stetler-Stevenson, M., et al. Chemotherapy-refractory diffuse large B-cell lymphoma and indolent B-cell malignancies can be effectively treated with autologous T cells expressing an anti-CD19 chimeric antigen receptor. J Clin Oncol 33 (2015), 540–549.
8. [8] Suck, G., Novel approaches using natural killer cells in cancer therapy. Semin Cancer Biol 16 (2006), 412–418.
9. [9] Davis, Z.B., Felices, M., Verneris, M.R., Miller, J.S., Natural killer cell adoptive transfer therapy: exploiting the first line of defense against cancer. Cancer J 21 (2015), 486–491.
10. [10] Klingemann, H., Are natural killer cells superior CAR drivers?. Oncoimmunology, 3, 2014, e28147.
11. [11] Vivier, E., Ugolini, S., Blaise, D., Chabannon, C., Brossay, L., Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol 12 (2012), 239–252.
12. [12] Iannello, A., Thompson, T.W., Ardolino, M., Marcus, A., Raulet, D.H., Immunosurveillance and immunotherapy of tumors by innate immune cells. Curr Opin Immunol 38 (2016), 52–58.
13. [13] Koch, J., Steinle, A., Watzl, C., Mandelboim, O., Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol 34 (2013), 182–191.
14. [14] Shifrin, N., Raulet, D.H., Ardolino, M., NK cell self tolerance, responsiveness and missing self recognition. Semin Immunol 26 (2014), 138–144.
15. [15] Velardi, A., Ruggeri, L., Mancusi, A., Aversa, F., Christiansen, F.T., Natural killer cell allorecognition of missing self in allogeneic hematopoietic transplantation: a tool for immunotherapy of leukemia. Curr Opin Immunol 21 (2009), 525–530.
16. [16] Jacoby, E., Yang, Y., Qin, H., Chien, C.D., Kochenderfer, J.N., Fry, T.J., Murine allogeneic CD19 CAR T-cells harbor potent antileukemic activity but have the potential to mediate lethal GVHD. Blood 127:10 (2016), 1361–1370.
17. [17] Suck, G., Odendahl, M., Nowakowska, P., Seidl, C., Wels, W.S., Klingemann, H.G., et al. NK-92: an “off-the-shelf therapeutic” for adoptive natural killer cell-based cancer immunotherapy. Cancer Immunol Immunother 65 (2016), 485–492.
18. [18] Tonn, T., Becker, S., Esser, R., Schwabe, D., Seifried, E., Cellular immunotherapy of malignancies using the clonal natural killer cell line NK-92. J Hematother Stem Cell Res 10 (2001), 535–544.
19. [19] Arai, S., Meagher, R., Swearingen, M., Myint, H., Rich, E., Martinson, J., et al. Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy 10 (2008), 625–632.
20. [20] Tonn, T., Schwabe, D., Klingemann, H.G., Becker, S., Esser, R., Koehl, U., et al. Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy 15 (2013), 1563–1570.
21. [21] 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.
22. [22] 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.
23. [23] 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 15 (2009), 4857–4866.
24. [24] Uherek, C., Tonn, T., Uherek, B., Becker, S., Schnierle, B., Klingemann, H.G., et al. 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.
25. [25] Schönfeld, K., Sahm, C., Zhang, C., Naundorf, S., Brendel, C., Odendahl, M., et al. Selective inhibition of tumor growth by clonal NK cells expressing an ErbB2/HER2-specific chimeric antigen receptor. Mol Ther 23 (2015), 330–338.
26. [26] Zhang, C., Burger, M.C., Jennewein, L., Genßler, S., Schönfeld, K., Zeiner, P., et al. ErbB2/HER2-specific NK cells for targeted therapy of glioblastoma. J Natl Cancer Inst, 108, 2016, djv375.
27. [27] Sutlu, T., Nystrom, S., Gilljam, M., Stellan, B., Applequist, S.E., Alici, E., Inhibition of intracellular antiviral defense mechanisms augments lentiviral transduction of human natural killer cells: implications for gene therapy. Hum Gene Ther 23 (2012), 1090–1100.
28. [28] Boissel, L., Betancur-Boissel, M., Lu, W., Krause, D.S., Van Etten, R.A., Wels, W.S., et al. 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.
29. [29] Romanski, A., Uherek, C., Bug, G., Seifried, E., Klingemann, H., Wels, W.S., et al. 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.
30. [30] Di Stasi, A., Tey, S.K., Dotti, G., Fujita, Y., Kennedy-Nasser, A., Martinez, C., et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med 365 (2011), 1673–1683.
31. [31] Nijmeijer, B.A., Szuhai, K., Goselink, H.M., van Schie, M.L., van der Burg, M., de Jong, D., et al. Long-term culture of primary human lymphoblastic leukemia cells in the absence of serum or hematopoietic growth factors. Exp Hematol 37 (2009), 376–385.
32. [32] Nicholson, I.C., Lenton, K.A., Little, D.J., Decorso, T., Lee, F.T., Scott, A.M., et al. Construction and characterisation of a functional CD19 specific single chain Fv fragment for immunotherapy of B lineage leukaemia and lymphoma. Mol Immunol 34 (1997), 1157–1165.
33. [33] Demaison, C., Parsley, K., Brouns, G., Scherr, M., Battmer, K., Kinnon, C., et al. High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 13 (2002), 803–813.
34. [34] 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.
35. [35] Oberoi, P., Jabulowsky, R.A., Bahr-Mahmud, H., Wels, W.S., EGFR-targeted granzyme B expressed in NK cells enhances natural cytotoxicity and mediates specific killing of tumor cells. PLoS ONE, 8, 2013, e61267.
36. [36] Abel, T., El Filali, E., Waern, J., Schneider, I.C., Yuan, Q., Munch, R.C., et al. Specific gene delivery to liver sinusoidal and artery endothelial cells. Blood 122 (2013), 2030–2038.
37. [37] Genßler, S., Burger, M.C., Zhang, C., Oelsner, S., Mildenberger, I., Wagner, M., et al. 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, 2016, e1119354.
38. [38] 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.
39. [39] Müller, T., Uherek, C., Maki, G., Chow, K.U., Schimpf, A., Klingemann, H.G., 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 57 (2008), 411–423.
40. [40] Esser, R., Müller, T., Stefes, D., Kloess, S., Seidel, D., Gillies, S.D., 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.
41. [41] Chu, J., Deng, Y., Benson, D.M., 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 28 (2014), 917–927.
42. [42] Han, J., Chu, J., Keung Chan, W., Zhang, J., Wang, Y., Cohen, J.B., 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.
43. [43] Tasian, S.K., Gardner, R.A., CD19-redirected chimeric antigen receptor-modified T cells: a promising immunotherapy for children and adults with B-cell acute lymphoblastic leukemia (ALL). Ther Adv Hematol 6 (2015), 228–241.
44. [44] Li, W., Guo, L., Rathi, P., Marinova, E., Gao, X., Wu, M.F., et al. Redirecting T cells to Glypican-3 with 4-1BB.zeta CAR results in Th-1 polarization and potent anti-tumor activity. Hum Gene Ther, 2016, 10.1089/hum.2016.025 in press.
45. [45] Couper, K.N., Blount, D.G., Riley, E.M., IL-10: the master regulator of immunity to infection. J Immunol 180 (2008), 5771–5777.
46. [46] Hombach, A.A., Schildgen, V., Heuser, C., Finnern, R., Gilham, D.E., Abken, H., T cell activation by antibody-like immunoreceptors: the position of the binding epitope within the target molecule determines the efficiency of activation of redirected T cells. J Immunol 178 (2007), 4650–4657.
47. [47] Krenciute, G., Krebs, S., Torres, D., Wu, M.F., Liu, H., Dotti, G., et al. Characterization and functional analysis of scFv-based chimeric antigen receptors to redirect T cells to IL13Ralpha2-positive glioma. Mol Ther 24 (2016), 354–363.
48. [48] Tarazona, R., Sanchez-Correa, B., Casas-Aviles, I., Campos, C., Pera, A., Morgado, S., et al. Immunosenescence: limitations of natural killer cell-based cancer immunotherapy. Cancer Immunol Immunother, 2016, 10.1007/s00262-016-1882-x in press.
49. [49] Glienke, W., Esser, R., Priesner, C., Suerth, J.D., Schambach, A., Wels, W.S., et al. Advantages and applications of CAR-expressing natural killer cells. Front Pharmacol, 6, 2015, 21.
50. [50] Van Elssen, C.H., Oth, T., Germeraad, W.T., Bos, G.M., Vanderlocht, J., Natural killer cells: the secret weapon in dendritic cell vaccination strategies. Clin Cancer Res 20 (2014), 1095–1103.