ErbB2/HER2-Specific NK Cells for Targeted Therapy of Glioblastoma

Journal of the National Cancer Institute

Volumn 108, Issue 5, 2016, Pages

  Zhang, Congcong ^a,b   Burger, Michael C ^b,c   Jennewein, Lukas ^c   Genßler, Sabrina ^a   Schönfeld, Kurt ^a   Zeiner, Pia ^c   Hattingen, Elke ^c   Harter, Patrick N ^c   Mittelbronn, Michel ^c   Tonn, Torsten ^d   Steinbach, Joachim P ^b,c   Wels, Winfried S ^a,b  

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

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c GOETHE UNIVERSITY   (Germany)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL KILLING; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; FLOW CYTOMETRY; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BRAIN NEOPLASMS; C57BL MOUSE; DRUG SCREENING; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; MOLECULARLY TARGETED THERAPY; NONOBESE DIABETIC MOUSE; PROCEDURES; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; MOLECULAR TARGETED THERAPY; RECEPTOR, ERBB-2; RECEPTORS, ANTIGEN, T-CELL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84968761575     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djv375     Document Type: Article

References (52)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma. N Engl J Med. 2005;352(10):987-996.
2. Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459-466.
3. Bähr O, Herrlinger U, Weller M, et al. Very late relapses in glioblastoma longterm survivors. J Neurol. 2009;256(10):1756-1758.
4. Omuro A, DeAngelis LM. Glioblastoma and other malignant gliomas: A clinical review. JAMA. 2013;310(17):1842-1850.
5. Dix AR, Brooks WH, Roszman TL, et al. Immune defects observed in patients with primary malignant brain tumors. J Neuroimmunol. 1999;100(1-2):216-232.
6. Vaquero J, Coca S, Oya S, et al. Presence and significance of NK cells in glioblastomas. J Neurosurg. 1989;70(5):728-731.
7. Kuppner MC, Hamou MF, Bodmer S, et al. The glioblastoma-derived T-cell suppressor factor/transforming growth factor beta 2 inhibits the generation of lymphokine-activated killer (LAK) cells. Int J Cancer. 1988;42(4):562-567.
8. Roth P, Mittelbronn M, Wick W, et al. Malignant glioma cells counteract antitumor immune responses through expression of lectin-like transcript-1. Cancer Res. 2007;67(8):3540-3544.
9. Crane CA, Han SJ, Barry JJ, et al. TGF-beta downregulates the activating receptor NKG2D on NK cells and CD8+ T cells in glioma patients. Neuro Oncol. 2010;12(1):7-13.
10. Crane CA, Austgen K, Haberthur K, et al. Immune evasion mediated by tumor-derived lactate dehydrogenase induction of NKG2D ligands on myeloid cells in glioblastoma patients. Proc Natl Acad Sci U S A. 2014;111(35):12823-12828.
11. Castriconi R, Daga A, Dondero A, et al. NK cells recognize and kill human glioblastoma cells with stem cell-like properties. J Immunol. 2009;182(6):3530-3539.
12. Avril T, Vauleon E, Hamlat A, et al. Human glioblastoma stem-like cells are more sensitive to allogeneic NK and T cell-mediated killing compared with serum-cultured glioblastoma cells. Brain Pathol. 2012;22(2):159-174.
13. Hayes RL, Koslow M, Hiesiger EM, et al. Improved long term survival after intracavitary interleukin-2 and lymphokine-activated killer cells for adults with recurrent malignant glioma. Cancer. 1995;76(5):840-852.
14. Dillman RO, Duma CM, Schiltz PM, et al. Intracavitary placement of autologous lymphokine-activated killer (LAK) cells after resection of recurrent glioblastoma. J Immunother. 2004;27(5):398-404.
15. Geller MA, Miller JS. Use of allogeneic NK cells for cancer immunotherapy. Immunotherapy. 2011;3(12):1445-1459.
16. 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(4):535-544.
17. 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(6):625-632.
18. 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(12):1563-1570.
19. 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(4):1265-1273.
20. Müller 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(3):411-423.
21. Sahm C, Schönfeld K, Wels WS. 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. 2012;61(9):1451-1461.
22. Esser R, Müller T, Stefes D, et al. NK cells engineered to express a GD(2) -specific antigen receptor display built-in ADCC-like activity against tumour cells of neuroectodermal origin. J Cell Mol Med. 2012;16(3):569-581.
23. 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(10):e26527.
24. 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(1):376-383.
25. Ahmed N, Salsman VS, Kew Y, et al. HER2-specific T cells target primary glioblastoma stem cells and induce regression of autologous experimental tumors. Clin Cancer Res. 2010;16(2):474-485.
26. Schlegel J, Stumm G, Brandle K, et al. Amplification and differential expression of members of the erbB-gene family in human glioblastoma. J Neurooncol. 1994;22(3):201-207.
27. Koka V, Potti A, Forseen SE, et al. Role of Her-2/neu overexpression and clinical determinants of early mortality in glioblastoma multiforme. Am J Clin Oncol. 2003;26(4):332-335.
28. Liu G, Ying H, Zeng G, et al. HER-2, gp100, and MAGE-1 are expressed in human glioblastoma and recognized by cytotoxic T cells. Cancer Res. 2004;64(14):4980-4986.
29. Andersson U, Guo D, Malmer B, et al. Epidermal growth factor receptor family (EGFR, ErbB2-4) in gliomas and meningiomas. Acta Neuropathol. 2004;108(2):135-142.
30. Schönfeld 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(2):330-338.
31. Harwerth IM, Wels W, Marte BM, et al. Monoclonal antibodies against the extracellular domain of the erbB-2 receptor function as partial ligand agonists. J Biol Chem. 1992;267(21):15160-15167.
32. Baumgarten P, Harter PN, Tonjes M, et al. Loss of FUBP1 expression in gliomas predicts FUBP1 mutation and is associated with oligodendroglial differentiation, IDH1 mutation and 1p/19q loss of heterozygosity. Neuropathol Appl Neurobiol. 2014;40(2):205-216.
33. Lee J, Kotliarova S, Kotliarov Y, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9(5):391-403.
34. Ausman JI, Shapiro WR, Rall DP. Studies on the chemotherapy of experimental brain tumors: development of an experimental model. Cancer Res. 1970;30(9):2394-2400.
35. Szatmari T, Lumniczky K, Desaknai S, et al. Detailed characterization of the mouse glioma 261 tumor model for experimental glioblastoma therapy. Cancer Sci. 2006;97(6):546-553.
36. Hynes NE, Lane HA. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer. 2005;5(5):341-354.
37. Baselga J, Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer. 2009;9(7):463-475.
38. Press MF, Cordon-Cardo C, Slamon DJ. Expression of the HER-2/neu proto-oncogene in normal human adult and fetal tissues. Oncogene. 1990;5(7):953-962.
39. Slamon DJ, Clark GM, Wong SG, et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 1987;235(4785):177-182.
40. Alkins RD, Burgess A, Ganguly M, et al. Focused ultrasound delivers targeted immune cells to metastatic brain tumors. Cancer Res. 2013;73(6):1892-1899.
41. Chamberlain MC. Radiographic patterns of relapse in glioblastoma. J Neurooncol. 2011;101(2):319-323.
42. Kalos M, Levine BL, Porter DL, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3(95):95ra73.
43. Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368(16):1509-1518.
44. Brentjens RJ, Davila ML, Riviere I, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5(177):177ra38.
45. 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(25):4129-4139.
46. Hunn MK, Farrand KJ, Broadley KW, et al. Vaccination with irradiated tumor cells pulsed with an adjuvant that stimulates NKT cells is an effective treatment for glioma. Clin Cancer Res. 2012;18(23):6446-6459.
47. Eberstal S, Sanden E, Fritzell S, et al. Intratumoral COX-2 inhibition enhances GM-CSF immunotherapy against established mouse GL261 brain tumors. Int J Cancer. 2014;134(11):2748-2753.
48. Kalinski P, Mailliard RB, Giermasz A, et al. Natural killer-dendritic cell crosstalk in cancer immunotherapy. Expert Opin Biol Ther. 2005;5(10):1303-1315.
49. Walzer T, Dalod M, Robbins SH, et al. Natural-killer cells and dendritic cells: "l'union fait la force". Blood. 2005;106(7):2252-2258.
50. Parsons DW, Jones S, Zhang X, et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008;321(5897):1807-1812.
51. Vogelstein B, Papadopoulos N, Velculescu VE, et al. Cancer genome landscapes. Science. 2013;339(6127):1546-1558.
52. Johnson BE, Mazor T, Hong C, et al. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science. 2014;343(6167):189-193.