Selective inhibition of tumor growth by clonal NK cells expressing an ErbB2/HER2-specific chimeric antigen receptor

Molecular Therapy

Volumn 23, Issue 2, 2015, Pages 330-338

  Schönfeld, Kurt ^a   Sahm, Christiane ^a   Zhang, Congcong ^a   Naundorf, Sonja ^b   Brendel, Christian ^a   Odendahl, Marcus ^c   Nowakowska, Paulina ^d   Bönig, Halvard ^d   Köhl, Ulrike ^e   Kloess, Stephan ^e   Köhler, Sylvia ^a   Holtgreve Grez, Heidi ^f   Jauch, Anna ^f   Schmidt, Manfred ^g   Schubert, Ralf ^h   Kühlcke, Klaus ^b   Seifried, Erhard ^d   Klingemann, Hans G ⁱ   Rieger, Michael A ^a,g,h   Tonn, Torsten ^c   Grez, Manuel ^a   Wels, Winfried S ^a,g   more..

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

^b BIONTECH AG   (Germany)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d GOETHE UNIVERSITY   (Germany)

^e HANNOVER MEDICAL SCHOOL   (Germany)

^f UNIVERSITY OF HEIDELBERG   (Germany)

^g GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^h UNIVERSITY HOSPITAL FRANKFURT   (Germany)

ⁱ Conkwest Inc ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPITOPE; HYBRID PROTEIN; IMMUNOGLOBULIN RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BIOLOGICAL ACTIVITY; BREAST CARCINOMA; CANCER INHIBITION; CELL ENGINEERING; CELL THERAPY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOLYSIS; FEMALE; GAMMA RADIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CARCINOMA; LUNG METASTASIS; MOUSE; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; TUMOR XENOGRAFT; ANIMAL; BREAST NEOPLASMS; CLONAL EVOLUTION; CYTOTOXICITY; DISEASE MODEL; DRUG SCREENING; GENE EXPRESSION; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; IMMUNOTHERAPY; LENTIVIRINAE; METABOLISM; MIXED LYMPHOCYTE CULTURE; NEOPLASMS; PATHOLOGY; PHENOTYPE; TRANSFORMED CELL LINE; TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CLONAL EVOLUTION; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; EPITOPES, T-LYMPHOCYTE; FEMALE; GENE EXPRESSION; GENETIC VECTORS; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY; KILLER CELLS, NATURAL; LENTIVIRUS; LYMPHOCYTE CULTURE TEST, MIXED; NEOPLASMS; PHENOTYPE; RECEPTOR, ERBB-2; RECEPTORS, IMMUNOLOGIC; RECOMBINANT FUSION PROTEINS; TRANSDUCTION, GENETIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84922257867     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.219     Document Type: Article

References (49)

1. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A., et al. (2011). T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 3: 95ra73
2. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR., et al. (2013). Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368: 1509-1518
3. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG., et al. (2013). CD19- targeted T cells rapidly induce molecular remissions in adults with chemotherapyrefractory acute lymphoblastic leukemia. Sci Transl Med 5: 177ra38
4. Kochenderfer JN, Dudley ME, Carpenter RO, Kassim SH, Rose JJ, Telford WG., et al. (2013). Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood 122: 4129-4139
5. Kalos M and June CH. (2013). Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology. Immunity 39: 49-60
6. Imai K, Matsuyama S, Miyake S, Suga K and Nakachi K. (2000). Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356: 1795-1799
7. Vesely MD, Kershaw MH, Schreiber RD and Smyth MJ. (2011). Natural innate and adaptive immunity to cancer. Annu Rev Immunol 29: 235-271
8. Vivier E, Ugolini S, Blaise D, Chabannon C and Brossay L. (2012). Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol 12: 239-252
9. Suck G. (2006). Novel approaches using natural killer cells in cancer therapy. Semin Cancer Biol 16: 412-418
10. Geller MA and Miller JS. (2011). Use of allogeneic NK cells for cancer immunotherapy. Immunotherapy 3: 1445-1459
11. Klingemann HG. (2013). Cellular therapy of cancer with natural killer cells-where do we stand?. Cytotherapy 15: 1185-1194
12. Orange JS. (2008). Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol 8: 713-725
13. Koch J, Steinle A, Watzl C and Mandelboim O. (2013). Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol 34: 182-191
14. Imai C, Iwamoto S and Campana D. (2005). Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood 106: 376-383
15. Müller T, Uherek C, Maki G, Chow KU, Schimpf A, Klingemann HG., et al. (2008). 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: 411-423
16. Boissel L, Betancur M, Wels WS, Tuncer H and Klingemann H. (2009). Transfection with mRNA for CD19 specific chimeric antigen receptor restores NK cell mediated killing of CLL cells. Leuk Res 33: 1255-1259
17. Chu J, Deng Y, Benson DM Jr, He, S, Hughes T, Zhang J., et al. (2013). CS1-specific chimeric antigen receptor (CAR)-engineered natural killer cells enhance in vitro and in vivo anti-tumor activity against human multiple myeloma. Leukemia 28: 917-927
18. Uherek C, Tonn T, Uherek B, Becker S, Schnierle B, Klingemann HG., et al. (2002). Retargeting of natural killer-cell cytolytic activity to ErbB2-expressing cancer cells results in efficient and selective tumor cell destruction. Blood 100: 1265-1273
19. Altvater B, Landmeier S, Pscherer S, Temme J, Schweer K, Kailayangiri S., et al. (2009). 2B4 (CD244) signaling by recombinant antigen-specific chimeric receptors costimulates natural killer cell activation to leukemia and neuroblastoma cells. Clin Cancer Res 15: 4857-4866
20. Esser R, Müller T, Stefes D, Kloess S, Seidel D, Gillies SD., et al. (2012). 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: 569-581
21. Sahm C, Schönfeld K and Wels WS. (2012). 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: 1451-1461
22. Sutlu T, Nyström S, Gilljam M, Stellan B, Applequist SE and Alici E. (2012). Inhibition of intracellular antiviral defense mechanisms augments lentiviral transduction of human natural killer cells: implications for gene therapy. Hum Gene Ther 23: 1090-1100
23. Arai S, Meagher R, Swearingen M, Myint H, Rich E, Martinson J., et al. (2008). Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy 10: 625-632
24. Tonn T, Schwabe D, Klingemann HG, Becker S, Esser R, Koehl U., et al. (2013). Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy 15: 1563-1570
25. Hynes NE and Lane HA. (2005). ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 5: 341-354
26. Wels W, Harwerth IM, Zwickl M, Hardman N, Groner B and Hynes NE. (1992). Construction bacterial expression and characterization of a bifunctional singlechain antibody-phosphatase fusion protein targeted to the human erbB-2 receptor. Biotechnology (NY) 10: 1128-1132
27. Moritz D, Wels W, Mattern J and Groner B. (1994). Cytotoxic T lymphocytes with a grafted recognition specificity for ERBB2-expressing tumor cells. Proc Natl Acad Sci USA 91: 4318-4322
28. Bhat R and Watzl C. (2007). Serial killing of tumor cells by human natural killer cells-enhancement by therapeutic antibodies. PLoS ONE 2: e326
29. Couper KN, Blount DG and Riley EM. (2008). IL-10: the master regulator of immunity to infection. J Immunol 180: 5771-5777
30. Maki G, Klingemann HG, Martinson JA and Tam YK. (2001). Factors regulating the cytotoxic activity of the human natural killer cell line NK-92. J Hematother Stem Cell Res 10: 369-383
31. Davies JK, Singh H, Huls H, Yuk D, Lee DA, Kebriaei P., et al. (2010). Combining CD19 redirection and alloanergization to generate tumor-specific human T cells for allogeneic cell therapy of B-cell malignancies. Cancer Res 70: 3915-3924
32. Oberoi P and Wels WS. (2013). Arming NK cells with enhanced antitumor activity: CARs and beyond. Oncoimmunology 2: e25220
33. Klingemann H. (2014). Are natural killer cells superior CAR drivers?. Oncoimmunology 3: e28147
34. Press MF, Cordon-Cardo C and Slamon DJ. (1990). Expression of the HER-2/neu proto-oncogene in normal human adult and fetal tissues. Oncogene 5: 953-962
35. Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM and Rosenberg SA. (2010). Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 18: 843-851
36. Hombach AA, Schildgen V, Heuser C, Finnern R, Gilham DE and Abken H. (2007). 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: 4650-4657
37. James SE, Greenberg PD, Jensen MC, Lin Y, Wang J, Till BG., et al. (2008). Antigen sensitivity of CD22-specific chimeric TCR is modulated by target epitope distance from the cell membrane. J Immunol 180: 7028-7038
38. Cho HS, Mason K, Ramyar KX, Stanley AM, Gabelli SB, Denney DW Jr., et al. (2003). Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab. Nature 421: 756-760
39. Gerstmayer B, Altenschmidt U, Hoffmann M and Wels W. (1997). Costimulation of T cell proliferation by a chimeric B7-2 antibody fusion protein specifically targeted to cells expressing the erbB2 proto-oncogene. J Immunol 158: 4584-4590
40. Grada Z, Hegde M, Byrd T, Shaffer DR, Ghazi A, Brawley VS., et al. (2013). TanCAR: A Novel Bispecific Chimeric Antigen Receptor for Cancer Immunotherapy. Mol Ther Nucleic Acids 2: e105
41. Di Cosimo S. (2011). Heart to heart with trastuzumab: a review on cardiac toxicity. Target Oncol 6: 189-195
42. von Minckwitz G, Harder S, Hövelmann S, Jäger E, Al-Batran SE, Loibl S., et al. (2005). Phase I clinical study of the recombinant antibody toxin scFv(FRP5)-ETA specific for the ErbB2/HER2 receptor in patients with advanced solid malignomas. Breast Cancer Res 7: R617-R626
43. Houghton AN, Real FX, Davis LJ, Cordon-Cardo C and Old LJ. (1987). Phenotypic heterogeneity of melanoma. Relation to the differentiation program of melanoma cells. J Exp Med 165: 812-829
44. Maurer-Gebhard M, Schmidt M, Azemar M, Altenschmidt U, Stöcklin E, Wels W., et al. (1998). Systemic treatment with a recombinant erbB-2 receptor-specific tumor toxin efficiently reduces pulmonary metastases in mice injected with genetically modified carcinoma cells. Cancer Res 58: 2661-2666
45. Demaison C, Parsley K, Brouns G, Scherr M, Battmer K, Kinnon C., et al. (2002). High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency [correction of imunodeficiency] virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 13: 803-813
46. Schambach A, Bohne J, Baum C, Hermann FG, Egerer L, von Laer D., et al. (2006). Woodchuck hepatitis virus post-transcriptional regulatory element deleted from X protein and promoter sequences enhances retroviral vector titer and expression. Gene Ther 13: 641-645
47. Schmidt M, Carbonaro DA, Speckmann C, Wissler M, Bohnsack J, Elder M., et al. (2003). Clonality analysis after retroviral-mediated gene transfer to CD34+ cells from the cord blood of ADA-deficient SCID neonates. Nat Med 9: 463-468
48. Klöss S, Bochennek K, Huenecke S, Zimmermann SY, Kuçi S, Müller T., et al. (2007). A novel five-colour flow cytometric assay to determine NK cell cytotoxicity against neuroblastoma and other adherent tumour cells. J Immunol Methods 325: 140-147
49. Tavri S, Jha P, Meier R, Henning TD, Müller T, Hostetter D., et al. (2009). Optical imaging of cellular immunotherapy against prostate cancer. Mol Imaging 8: 15-26