Cytotoxic potential of IL-15-activated cytokine-induced killer cells against human neuroblastoma cells

Pediatric Blood and Cancer

Volumn 63, Issue 12, 2016, Pages 2230-2239

  Cappel, Claudia ^a   Huenecke, Sabine ^a   Suemmerer, Anica ^a   Erben, Stephanie ^a   Rettinger, Eva ^a   Pfirrmann, Verena ^a   Heinze, Annekathrin ^a   Zimmermann, Olga ^a   Klingebiel, Thomas ^a   Ullrich, Evelyn ^a   Bader, Peter ^a   Bremm, Melanie ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

CIK (cytokine induced killer) cells; immunotherapy; neuroblastoma

Indexed keywords

CD3 ANTIGEN; CD56 ANTIGEN; DNAM 1 PROTEIN; EUROPIUM; FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 2; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL KILLER CELL RECEPTOR NKG2D; OKT 3; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR PROTEIN; UNCLASSIFIED DRUG; KLRK1 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K;

ALLOGENEIC STEM CELL TRANSPLANTATION; ARTICLE; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; CYTOKINE INDUCED KILLER CELL; CYTOTOXICITY; EX VIVO STUDY; HIGH RISK PATIENT; HUMAN; HUMAN CELL; IN VITRO STUDY; NATURAL KILLER CELL; NEUROBLASTOMA; NEUROBLASTOMA CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RECEPTOR BINDING ASSAY; RELEASE ASSAY; IMMUNOLOGY; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CYTOKINE-INDUCED KILLER CELLS; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; INTERLEUKIN-15; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; NEUROBLASTOMA; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K;

EID: 84978870825     PISSN: 15455009     EISSN: 15455017     Source Type: Journal    
DOI: 10.1002/pbc.26147     Document Type: Article

References (54)

1. Davidoff AM. Neuroblastoma. Seminars in pediatric surgery. 2012;21(1):2–14.
2. Matthay KK, Reynolds CP, Seeger RC, et al. Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: A children's oncology group study. J Clin Oncol. 2009;27(7):1007–1013.
3. Inoue M, Nakano T, Yoneda A, et al. Graft-versus-tumor effect in a patient with advanced neuroblastoma who received HLA haplo-identical bone marrow transplantation. Bone Marrow Transplant. 2003;32(1):103–106.
4. Kanold J, Paillard C, Tchirkov A, et al. NK cell immunotherapy for high-risk neuroblastoma relapse after haploidentical HSCT. Pediatr Blood Cancer. 2012;59(4):739–742.
5. Lang P, Pfeiffer M, Muller I, et al. Haploidentical stem cell transplantation in patients with pediatric solid tumors: Preliminary results of a pilot study and analysis of graft versus tumor effects. Klinische Padiatrie. 2006;218(6):321–326.
6. Perez-Martinez A, de Prada Vicente I, Fernandez L, et al. Natural killer cells can exert a graft-vs-tumor effect in haploidentical stem cell transplantation for pediatric solid tumors. Exp Hematol. 2012;40(11):882–891, e881.
7. Sung KW, Park JE, Chueh HW, et al. Reduced-intensity allogeneic stem cell transplantation for children with neuroblastoma who failed tandem autologous stem cell transplantation. Pediatr Blood Cancer. 2011;57(4):660–665.
8. Toporski J, Garkavij M, Tennvall J, et al. High-dose iodine-131-metaiodobenzylguanidine with haploidentical stem cell transplantation and posttransplant immunotherapy in children with relapsed/refractory neuroblastoma. Biol Blood Marrow Transplant. 2009;15(9):1077–1085.
9. Brehm C, Huenecke S, Quaiser A, et al. IL-2 stimulated but not unstimulated NK cells induce selective disappearance of peripheral blood cells: Concomitant results to a phase I/II study. PloS ONE. 2011;6(11):e27351.
10. Koehl U, Brehm C, Huenecke S, et al. Clinical grade purification and expansion of NK cell products for an optimized manufacturing protocol. Frontiers Oncol. 2013:3:118.
11. Koehl U, Sorensen J, Esser R, et al. IL-2 activated NK cell immunotherapy of three children after haploidentical stem cell transplantation. Blood Cells Mol Diseases. 2004;33(3):261–266.
12. Passweg JR, Koehl U, Uharek L, Meyer-Monard S, Tichelli A. Natural-killer-cell-based treatment in haematopoietic stem-cell transplantation. Best Pract Res Clin Haematol. 2006;19(4):811–824.
13. Schmidt-Wolf IG, Negrin RS, Kiem HP, Blume KG, Weissman IL. Use of a SCID mouse/human lymphoma model to evaluate cytokine-induced killer cells with potent antitumor cell activity. J Exp Med. 1991;174(1):139–149.
14. Rettinger E, Kuci S, Naumann I, et al. The cytotoxic potential of interleukin-15-stimulated cytokine-induced killer cells against leukemia cells. Cytotherapy. 2012;14(1):91–103.
15. Rettinger E, Meyer V, Kreyenberg H, et al. Cytotoxic Capacity of IL-15-stimulated cytokine-induced killer cells against human acute myeloid leukemia and rhabdomyosarcoma in humanized preclinical mouse models. Frontiers Oncol. 2012:2:32.
16. Schmidt-Wolf IG, Lefterova P, Mehta BA, et al. Phenotypic characterization and identification of effector cells involved in tumor cell recognition of cytokine-induced killer cells. Exp Hematol. 1993;21(13):1673–1679.
17. Lu PH, Negrin RS. A novel population of expanded human CD3+CD56+ cells derived from T cells with potent in vivo antitumor activity in mice with severe combined immunodeficiency. J Immunol. 1994;153(4):1687–1696.
18. Linn YC, Lau SK, Liu BH, et al. Characterization of the recognition and functional heterogeneity exhibited by cytokine-induced killer cell subsets against acute myeloid leukaemia target cell. Immunology. 2009;126(3):423–435.
19. Introna M, Borleri G, Conti E, et al. Repeated infusions of donor-derived cytokine-induced killer cells in patients relapsing after allogeneic stem cell transplantation: A phase I study. Haematologica. 2007;92(7):952–959.
20. Laport GG, Sheehan K, Baker J, et al. Adoptive immunotherapy with cytokine-induced killer cells for patients with relapsed hematologic malignancies after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2011;17(11):1679–1687.
21. Rettinger E, Bonig H, Wehner S, et al. Feasibility of IL-15-activated cytokine-induced killer cell infusions after haploidentical stem cell transplantation. Bone Marrow Transplant. 2013;48(8):1141–1143.
22. Linn YC, Niam M, Chu S, et al. The anti-tumour activity of allogeneic cytokine-induced killer cells in patients who relapse after allogeneic transplant for haematological malignancies. Bone Marrow Transplant. 2012;47(7):957–966.
23. Rettinger E, Huenecke S, Bonig H, et al. Interleukin-15-activated cytokine-induced killer cells may sustain remission in leukemia patients after allogeneic stem cell transplantation: Feasibility, safety and first insights on efficacy. Haematologica. 2016;101(4):e153–156.
24. Rettinger E, Kreyenberg H, Merker M, et al. Immunomagnetic selection or irradiation eliminates alloreactive cells but also reduces anti-tumor potential of cytokine-induced killer cells: Implications for unmanipulated cytokine-induced killer cell infusion. Cytotherapy. 2014;16(6):835–844.
25. Cinatl J, Mainke M, Weissflog A, et al. In vitro differentiation of human neuroblastoma cells induced by sodium phenylacetate. Cancer Lett. 1993:70(1–2):15–24.
26. Cinatl J, Jr, Vogel JU, Cinatl J, et al. Long-term productive human cytomegalovirus infection of a human neuroblastoma cell line. Int J Cancer. 1996;65(1):90–96.
27. Kuci S, Rettinger E, Voss B, et al. Efficient lysis of rhabdomyosarcoma cells by cytokine-induced killer cells: Implications for adoptive immunotherapy after allogeneic stem cell transplantation. Haematologica. 2010;95(9):1579–1586.
28. Pfirrmann V, Oelsner S, Rettinger E, et al. Cytomegalovirus-specific cytokine-induced killer cells: Concurrent targeting of leukemia and cytomegalovirus. Cytotherapy. 2015;17(8):1139–1151.
29. Bochennek K, Fryns E, Wittekindt B, et al. Immune cell subsets at birth may help to predict risk of late-onset sepsis and necrotizing enterocolitis in preterm infants. Early Hum Dev. 2016:93:9–16.
30. Kloess S, Huenecke S, Piechulek D, 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. 2010;40(11):3255–3267.
31. Matthay KK, Villablanca JG, Seeger RC, et al. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group. N Engl J Med. 1999;341(16):1165–1173.
32. Davidoff AM. Neuroblastoma. Semin Pediatr Surg. 2012;21(1):2–14.
33. Passweg JR, Tichelli A, Meyer-Monard S, et al. Purified donor NK-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia. 2004;18(11):1835–1838.
34. Stern M, Passweg JR, Meyer-Monard S, et al. Pre-emptive immunotherapy with purified natural killer cells after haploidentical SCT: A prospective phase II study in two centers. Bone Marrow Transplant. 2013;48(3):433–438.
35. Raffaghello L, Prigione I, Bocca P, et al. Multiple defects of the antigen-processing machinery components in human neuroblastoma: Immunotherapeutic implications. Oncogene. 2005;24(29):4634–4644.
36. Sangiolo D. Cytokine induced killer cells as promising immunotherapy for solid tumors. J Cancer. 2011:2:363–368.
37. Kolb HJ, Schattenberg A, Goldman JM, et al. Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. Blood. 1995;86(5):2041–2050.
38. Tao Q, Chen T, Tao L, et al. IL-15 improves the cytotoxicity of cytokine-induced killer cells against leukemia cells by upregulating CD3+CD56+ cells and downregulating regulatory T cells as well as IL-35. J Immunother. 2013;36(9):462–467.
39. Nishimura R, Baker J, Beilhack A, et al. In vivo trafficking and survival of cytokine-induced killer cells resulting in minimal GVHD with retention of antitumor activity. Blood. 2008;112(6):2563–2574.
40. Distler E, Bloetz A, Albrecht J, et al. Alloreactive and leukemia-reactive T cells are preferentially derived from naive precursors in healthy donors: Implications for immunotherapy with memory T cells. Haematologica. 2011;96(7):1024–1032.
41. Linn YC, Hui KM. Cytokine-induced NK-like T cells: From bench to bedside. J Biomed Biotechnol. 2010:2010:435745.
42. Pende D, Cantoni C, Rivera P, et al. Role of NKG2D in tumor cell lysis mediated by human NK cells: Cooperation with natural cytotoxicity receptors and capability of recognizing tumors of nonepithelial origin. Eur J Immunol. 2001;31(4):1076–1086.
43. Mehta BA, Schmidt-Wolf IG, Weissman IL, Negrin RS. Two pathways of exocytosis of cytoplasmic granule contents and target cell killing by cytokine-induced CD3+ CD56+ killer cells. Blood. 1995;86(9):3493–3499.
44. Pievani A, Borleri G, Pende D, et al. Dual-functional capability of CD3+CD56+ CIK cells, a T-cell subset that acquires NK function and retains TCR-mediated specific cytotoxicity. Blood. 2011;118(12):3301–3310.
45. Franceschetti M, Pievani A, Borleri G, et al. Cytokine-induced killer cells are terminally differentiated activated CD8 cytotoxic T-EMRA lymphocytes. Exp Hematol. 2009;37(5):616–628, e612.
46. Paillard C, Halle P, Tchirkov A, et al. NK cytotoxicity and alloreactivity against neuroblastoma cell lines in vitro: Comparison of Europium fluorometry assay and quantification by RT-PCR. J Immunol Methods. 2012:380(1–2):56–64.
47. Raffaghello L, Prigione I, Airoldi I, et al. Downregulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia. 2004;6(5):558–568.
48. Salih HR, Goehlsdorf D, Steinle A. Release of MICB molecules by tumor cells: Mechanism and soluble MICB in sera of cancer patients. Hum Immunol. 2006;67(3):188–195.
49. Salih HR, Rammensee HG, Steinle A. Cutting edge: Down-regulation of MICA on human tumors by proteolytic shedding. J Immunol. 2002;169(8):4098–4102.
50. Zwirner NW, Fuertes MB, Girart MV, Domaica CI, Rossi LE. Cytokine-driven regulation of NK cell functions in tumor immunity: Role of the MICA–NKG2D system. Cytokine Growth Factor Rev. 2007:18(1–2):159–170.
51. Tettamanti S, Marin V, Pizzitola I, et al. Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor. Br J Haematol. 2013;161(3):389–401.
52. Marten A, Ziske C, Schottker B, et al. Interactions between dendritic cells and cytokine-induced killer cells lead to an activation of both populations. J Immunother. 2001;24(6):502–510.
53. Chan JK, Hamilton CA, Cheung MK, et al. Enhanced killing of primary ovarian cancer by retargeting autologous cytokine-induced killer cells with bispecific antibodies: A preclinical study. Clin Cancer Res. 2006;12(6):1859–1867.
54. Yu AL, Gilman AL, Ozkaynak MF, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med. 2010;363(14):1324–1334.