CD19-CAR engineered NK-92 cells are sufficient to overcome NK cell resistance in B-cell malignancies

Journal of Cellular and Molecular Medicine

Volumn 20, Issue 7, 2016, Pages 1287-1294

  Romanski, Annette ^a   Uherek, Christoph ^b   Bug, Gesine ^a   Seifried, Erhard ^a   Klingemann, Hans ^c   Wels, Winfried S ^b   Ottmann, Oliver G ^a   Tonn, Torsten ^a,d  

^a GOETHE UNIVERSITY   (Germany)

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

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

CAR; cellular immunotherapy; leukaemia; natural killer cell; NK 92; CD19

Indexed keywords

CD19 ANTIGEN; RETROVIRUS VECTOR;

ACUTE LEUKEMIA; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL CULTURE; CONTROLLED STUDY; CYTOTOXICITY; FLUORESCENCE; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IMMUNOTHERAPY; NATURAL KILLER T CELL; PRIORITY JOURNAL;

EID: 84977497147     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12810     Document Type: Article

References (58)

1. Fiore E, Fusco C, Romero P, et al. Matrix metalloproteinase 9 (MMP-9/gelatinase B) proteolytically cleaves ICAM-1 and participates in tumor cell resistance to natural killer cell-mediated cytotoxicity. Oncogene. 2002; 21: 5213–23.
2. Maki G, Hayes GM, Naji A, et al. NK resistance of tumor cells from multiple myeloma and chronic lymphocytic leukemia patients: implication of HLA-G. Leukemia. 2008; 22: 998–1006.
3. Fernandez-Messina L, Reyburn HT, Vales-Gomez M. Human NKG2D-ligands: cell biology strategies to ensure immune recognition. Front Immunol. 2012; 3: 299.
4. Spear P, Wu MR, Sentman ML, et al. NKG2D ligands as therapeutic targets. Cancer Immun. 2013; 13: 8.
5. Yang F, Shao Y, Yang F, et al. Valproic acid upregulates NKG2D ligand expression and enhances susceptibility of human renal carcinoma cells to NK cell-mediated cytotoxicity. Arch Med Sci. 2013; 9: 323–31.
6. Lanier LL. Missing self, NK cells, and the white album. J Immunol. 2005; 174: 6565.
7. Long EO. Regulation of immune responses through inhibitory receptors. Annu Rev Immunol. 1999; 17: 875–904.
8. De Oliveira SN, Ryan C, Giannoni F, et al. Modification of hematopoietic stem/progenitor cells with CD19-specific chimeric antigen receptors as a novel approach for cancer immunotherapy. Hum Gene Ther. 2013; 24: 824–39.
9. Almasbak H, Walseng E, Kristian A, et al. Inclusion of an IgG1-Fc spacer abrogates efficacy of CD19 CAR T cells in a xenograft mouse model. Gene Ther. 2015; 22: 391–403.
10. Ghorashian S, Pule M, Amrolia P. CD19 chimeric antigen receptor T cell therapy for haematological malignancies. Br J Haematol. 2015; 169: 463–78.
11. Gill S, June CH. Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol Rev. 2015; 263: 68–89.
12. Kebriaei P, Huls H, Jena B, et al. Infusing CD19-directed T cells to augment disease control in patients undergoing autologous hematopoietic stem-cell transplantation for advanced B-lymphoid malignancies. Hum Gene Ther. 2012; 23: 444–50.
13. Klein SC, Boer LH, de Weger RA, et al. Release of cytokines and soluble cell surface molecules by PBMC after activation with the bispecific antibody CD3 x CD19. Scand J Immunol. 1997; 46: 452–8.
14. Kochenderfer JN, Dudley ME, Carpenter RO, et al. Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood. 2013; 122: 4129–39.
15. Roessig C, Scherer SP, Baer A, et al. Targeting CD19 with genetically modified EBV-specific human T lymphocytes. Ann Hematol. 2002; 81: S42–3.
16. Boissel L, Betancur M, Wels WS, et al. Transfection with mRNA for CD19 specific chimeric antigen receptor restores NK cell mediated killing of CLL cells. Leuk Res. 2009; 33: 1255–9.
17. Sutlu T, Nystrom S, Gilljam M, et al. Inhibition of intracellular antiviral defense mechanisms augments lentiviral transduction of human natural killer cells: implications for gene therapy. Hum Gene Ther. 2012; 23: 1090–100.
18. Lapteva N, Durett AG, Sun J, et al. Large-scale ex vivo expansion and characterization of natural killer cells for clinical applications. Cytotherapy. 2012; 14: 1131–43.
19. Siegler U, Meyer-Monard S, Jorger S, et al. Good manufacturing practice-compliant cell sorting and large-scale expansion of single KIR-positive alloreactive human natural killer cells for multiple infusions to leukemia patients. Cytotherapy. 2010; 12: 750–63.
20. Arai S, Meagher R, Swearingen M, et al. Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy. 2008; 10: 625–32.
21. Tonn T, Becker S, Esser R, et al. Cellular immunotherapy of malignancies using the clonal natural killer cell line NK-92. J Hematother Stem Cell Res. 2001; 10: 535–44.
22. 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: 1563–70.
23. Boissel L, Betancur M, Lu W, et al. Comparison of mRNA and lentiviral based transfection of natural killer cells with chimeric antigen receptors recognizing lymphoid antigens. Leuk Lymphoma. 2012; 53: 958–65.
24. Lehner M, Gotz G, Proff J, et al. Redirecting T cells to Ewing's sarcoma family of tumors by a chimeric NKG2D receptor expressed by lentiviral transduction or mRNA transfection. PLoS ONE. 2012; 7: e31210.
25. Klingemann H. Are natural killer cells superior CAR drivers? Oncoimmunology. 2014; 3: e28147.
26. Daldrup-Link HE, Meier R, Rudelius M, et al. In vivo tracking of genetically engineered, anti-HER2/neu directed natural killer cells to HER2/neu positive mammary tumors with magnetic resonance imaging. Eur Radiol. 2005; 15: 4–13.
27. Uherek C, Tonn T, Uherek B, 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: 1265–73.
28. Schonfeld K, Sahm C, Zhang C, et al. Selective inhibition of tumor growth by clonal NK cells expressing an ErbB2/HER2-specific chimeric antigen receptor. Mol Ther. 2015; 23: 330–8.
29. Romanski A, Bug G, Becker S, et al. Mechanisms of resistance to natural killer cell-mediated cytotoxicity in acute lymphoblastic leukemia. Exp Hematol. 2005; 33: 344–52.
30. Tohda S, Sakashita C, Fukuda T, et al. Establishment of a double Philadelphia chromosome-positive acute lymphoblastic leukemia-derived cell line, TMD5: effects of cytokines and differentiation inducers on growth of the cells. Leuk Res. 1999; 23: 255–61.
31. Goselink HM, van Damme J, Hiemstra PS, et al. Colony growth of human hematopoietic progenitor cells in the absence of serum is supported by a proteinase inhibitor identified as antileukoproteinase. J Exp Med. 1996; 184: 1305–12.
32. Nijmeijer BA, Szuhai K, Goselink HM, et al. Long-term culture of primary human lymphoblastic leukemia cells in the absence of serum or hematopoietic growth factors. Exp Hematol. 2009; 37: 376–85.
33. Farag SS, Fehniger TA, Ruggeri L, et al. Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect. Blood. 2002; 100: 1935–47.
34. Tran AC, Zhang D, Byrn R, et al. Chimeric zeta-receptors direct human natural killer (NK) effector function to permit killing of NK-resistant tumor cells and HIV-infected T lymphocytes. J Immunol. 1995; 155: 1000–9.
35. Gerstmayer B, Groner B, Wels W, et al. Stable expression of the ecotropic retrovirus receptor in amphotropic packaging cells facilitates the transfer of recombinant vectors and enhances the yield of retroviral particles. J Virol Methods. 1999; 81: 71–5.
36. Evan GI, Lewis GK, Ramsay G, et al. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol. 1985; 5: 3610–6.
37. Klingemann HG, Wong E, Maki G. A cytotoxic NK-cell line (NK-92) for ex vivo purging of leukemia from blood. Biol Blood Marrow Transplant. 1996; 2: 68–75.
38. Tam YK, Miyagawa B, Ho VC, et al. 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.
39. Yan Y, Steinherz P, Klingemann HG, et al. Antileukemia activity of a natural killer cell line against human leukemias. Clin Cancer Res. 1998; 4: 2859–68.
40. Boissel L, Betancur-Boissel M, Lu W, 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.
41. Abken H, Hombach A, Heuser C. Immune response manipulation: recombinant immunoreceptors endow T-cells with predefined specificity. Curr Pharm Des. 2003; 9: 1992–2001.
42. Bitton N, Debre P, Eshhar Z, et al. T-bodies as antiviral agents. Curr Top Microbiol Immunol. 2001; 260: 271–300.
43. Kershaw MH, Teng MW, Smyth MJ, et al. Supernatural T cells: genetic modification of T cells for cancer therapy. Nat Rev Immunol. 2005; 5: 928–40.
44. Huang G, Yu L, Cooper LJ, et al. Genetically modified T cells targeting interleukin-11 receptor alpha-chain kill human osteosarcoma cells and induce the regression of established osteosarcoma lung metastases. Cancer Res. 2012; 72: 271–81.
45. Zhou X, Li J, Wang Z, et al. Cellular immunotherapy for carcinoma using genetically modified EGFR-specific T lymphocytes. Neoplasia. 2013; 15: 544–53.
46. 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: 376–83.
47. Marin V, Kakuda H, Dander E, et al. Enhancement of the anti-leukemic activity of cytokine induced killer cells with an anti-CD19 chimeric receptor delivering a 4-1BB-zeta activating signal. Exp Hematol. 2007; 35: 1388–97.
48. Muller T, Uherek C, Maki 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. 2008; 57: 411–23.
49. Mihara K, Bhattacharyya J, Kitanaka A, et al. T-cell immunotherapy with a chimeric receptor against CD38 is effective in eliminating myeloma cells. Leukemia. 2012; 26: 365–7.
50. Esser R, Muller T, Stefes 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. 2012; 16: 569–81.
51. Leung K. DiD-Labeled anti-EpCAM-directed NK-92-scFv(MOC31) zeta cells. Molecular Imaging and Contrast Agent Database (MICAD) [Internet] 2004.
52. Tassev DV, Cheng M, Cheung NK. Retargeting NK92 cells using an HLA-A2-restricted, EBNA3C-specific chimeric antigen receptor. Cancer Gene Ther. 2012; 19: 84–100.
53. 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: 917–27.
54. Levine BL. Performance-enhancing drugs: design and production of redirected chimeric antigen receptor (CAR) T cells. Cancer Gene Ther. 2015; 22: 79–84.
55. Maude SL, Shpall EJ, Grupp SA. Chimeric antigen receptor T-cell therapy for ALL. Hematology Am Soc Hematol Educ Program. 2014; 2014: 559–64.
56. Weiland J, Elder A, Forster V, et al. CD19: a multifunctional immunological target molecule and its implications for Blineage acute lymphoblastic leukemia. Pediatr Blood Cancer. 2015; 62(7): 1144–8.
57. Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013; 368: 1509–18.
58. Porter DL, Levine BL, Kalos M, et al. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011; 365: 725–33.