Chimeric antigen receptor-engineered cytokine-induced killer cells overcome treatment resistance of pre-B-cell acute lymphoblastic leukemia and enhance survival

International Journal of Cancer

Volumn 139, Issue 8, 2016, Pages 1799-1809

  Oelsner, Sarah ^a,b   Wagner, Juliane ^b   Friede, Miriam E ^a   Pfirrmann, Verena ^b   Genßler, Sabrina ^a   Rettinger, Eva ^b   Buchholz, Christian J ^c,d   Pfeifer, Heike ^b   Schubert, Ralf ^b   Ottmann, Oliver G ^e   Ullrich, Evelyn ^b   Bader, Peter ^b   Wels, Winfried S ^a,d  

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

^b GOETHE UNIVERSITY   (Germany)

^c PAUL EHRLICH INSTITUT   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

adoptive immunotherapy; B ALL; CD19; chimeric antigen receptor; cytokine induced killer cells

Indexed keywords

CD19 ANTIGEN; CD3 ANTIBODY; CD3 ANTIGEN; CD56 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 2; LENTIVIRUS VECTOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B CELL LEUKEMIA; CANCER IMMUNOTHERAPY; CANCER REGRESSION; CANCER SURVIVAL; CELL KILLING; CELL POPULATION; CONTROLLED STUDY; CYTOKINE INDUCED KILLER CELL; CYTOTOXICITY; DONOR LYMPHOCYTE INFUSION; EX VIVO STUDY; GRAFT VERSUS HOST REACTION; HIGH RISK PATIENT; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KILLER CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MINIMAL RESIDUAL DISEASE; MOUSE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RISK REDUCTION; T LYMPHOCYTE; TUMOR XENOGRAFT;

EID: 84981285594     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.30217     Document Type: Article

References (46)

1. Loghavi S, Kutok JL, Jorgensen JL. B-acute lymphoblastic leukemia/lymphoblastic lymphoma. Am J Clin Pathol 2015;144:393–410.
2. Pulsipher MA, Bader P, Klingebiel T, et al. Allogeneic transplantation for pediatric acute lymphoblastic leukemia: the emerging role of peritransplantation minimal residual disease/chimerism monitoring and novel chemotherapeutic, molecular, and immune approaches aimed at preventing relapse. Biol Blood Marrow Transplant 2009;15:62–71.
3. Peters C, Schrappe M, von Stackelberg A, et al. Stem-cell transplantation in children with acute lymphoblastic leukemia: a prospective international multicenter trial comparing sibling donors with matched unrelated donors-The ALL-SCT-BFM-2003 trial. J Clin Oncol 2015;33:1265–74.
4. Kolb HJ. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 2008;112:4371–83.
5. Feuchtinger T, Opherk K, Bethge WA, et al. Adoptive transfer of pp65-specific T cells for the treatment of chemorefractory cytomegalovirus disease or reactivation after haploidentical and matched unrelated stem cell transplantation. Blood 2010;116:4360–7.
6. Sangiolo D, Mesiano G, Carnevale-Schianca F, et al. Cytokine induced killer cells as adoptive immunotherapy strategy to augment graft versus tumor after hematopoietic cell transplantation. Expert Opin Biol Ther 2009;9:831–40.
7. Rettinger E, Kuci S, Naumann I, et al. The cytotoxic potential of interleukin-15-stimulated cytokine-induced killer cells against leukemia cells. Cytotherapy 2012;14:91–103.
8. Rettinger E, Huenecke S, Bönig H, et al. IL-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:e153–e156.
9. Schmidt-Wolf IG, Negrin RS, Kiem HP, et al. Use of a SCID mouse/human lymphoma model to evaluate cytokine-induced killer cells with potent antitumor cell activity. J Exp Med 1991;174:139–49.
10. Verneris MR, Baker J, Edinger M, et al. Studies of ex vivo activated and expanded CD8+ NK-T cells in humans and mice. J Clin Immunol 2002;22:131–6.
11. Pfirrmann V, Oelsner S, Rettinger E, et al. Cytomegalovirus-specific cytokine-induced killer cells: concurrent targeting of leukemia and cytomegalovirus. Cytotherapy 2015;17:1139–51.
12. Schmeel LC, Schmeel FC, Coch C, et al. Cytokine-induced killer (CIK) cells in cancer immunotherapy: report of the international registry on CIK cells (IRCC). J Cancer Res Clin Oncol 2015;141:839–49.
13. 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.
14. 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;5:177ra38.
15. Cruz CR, Micklethwaite KP, Savoldo B, 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 2013;122:2965–73.
16. Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med 2014;371:1507–17.
17. Lee DW, Kochenderfer JN, Stetler-Stevenson M, 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 2015;385:517–28.
18. Zola H, MacArdle PJ, Bradford T, et al. Preparation and characterization of a chimeric CD19 monoclonal antibody. Immunol Cell Biol 1991;69:411–22.
19. Nicholson IC, Lenton KA, Little DJ, et al. Construction and characterisation of a functional CD19 specific single chain Fv fragment for immunotherapy of B lineage leukaemia and lymphoma. Mol Immunol 1997;34:1157–65.
20. 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;61:1451–61.
21. 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;23:330–8.
22. Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med 2011;365:1673–83.
23. Müller N, Hartmann C, Genssler S, et al. A bispecific transmembrane antibody simultaneously targeting intra- and extracellular epitopes of the epidermal growth factor receptor inhibits receptor activation and tumor cell growth. Int J Cancer 2014;134:2547–59.
24. 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.
25. Demaison C, Parsley K, Brouns G, 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 2002;13:803–13.
26. Zufferey R, Nagy D, Mandel RJ, et al. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 1997;15:871–5.
27. Abel T, El Filali E, Waern J, et al. Specific gene delivery to liver sinusoidal and artery endothelial cells. Blood 2013;122:2030–8.
28. Gabert J, Beillard E, van der Velden VH, et al. Standardization and quality control studies of 'real-time' quantitative reverse transcriptase polymerase chain reaction of fusion gene transcripts for residual disease detection in leukemia—a Europe Against Cancer program. Leukemia 2003;17:2318–57.
29. 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;95:1579–86.
30. Schmidt-Wolf IG, Finke S, Trojaneck B, et al. Phase I clinical study applying autologous immunological effector cells transfected with the interleukin-2 gene in patients with metastatic renal cancer, colorectal cancer and lymphoma. Br J Cancer 1999;81:1009–16.
31. Olioso P, Giancola R, Di Riti M, et al. Immunotherapy with cytokine induced killer cells in solid and hematopoietic tumours: a pilot clinical trial. Hematol Oncol 2009;27:130–9.
32. Zhang Y, Wang J, Wang Y, et al. Autologous CIK cell immunotherapy in patients with renal cell carcinoma after radical nephrectomy. Clin Dev Immunol 2013;2013:195691.
33. Jakel CE, Vogt A, Gonzalez-Carmona MA, et al. Clinical studies applying cytokine-induced killer cells for the treatment of gastrointestinal tumors. J Immunol Res 2014;2014:897214.
34. 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;92:952–9.
35. 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;17:1679–87.
36. Yang B, Lu XC, Yu RL, et al. Repeated transfusions of autologous cytokine-induced killer cells for treatment of haematological malignancies in elderly patients: a pilot clinical trial. Hematol Oncol 2012;30:115–22.
37. 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;36:462–7.
38. 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;153:1687–96.
39. 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;16:835–44.
40. Marin V, Dander E, Biagi E, et al. Characterization of in vitro migratory properties of anti-CD19 chimeric receptor-redirected CIK cells for their potential use in B-ALL immunotherapy. Exp Hematol 2006;34:1219–29.
41. 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.
42. Schlimper C, Hombach AA, Abken H, et al. Improved activation toward primary colorectal cancer cells by antigen-specific targeting autologous cytokine-induced killer cells. Clin Dev Immunol 2012;2012:238924.
43. Hombach AA, Rappl G, Abken H. Arming cytokine-induced killer cells with chimeric antigen receptors: CD28 outperforms combined CD28-OX40 “super-stimulation”. Mol Ther 2013;21:2268–77.
44. Trapani JA, Davis J, Sutton VR, et al. Proapoptotic functions of cytotoxic lymphocyte granule constituents in vitro and in vivo. Curr Opin Immunol 2000;12:323–9.
45. Maude SL, Barrett D, Teachey DT, et al. Managing cytokine release syndrome associated with novel T cell-engaging therapies. Cancer J 2014;20:119–22.
46. Verneris MR, Karimi M, Baker J, et al. Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells. Blood 2004;103:3065–72.