A novel method using blinatumomab for efficient, clinical-grade expansion of polyclonal T cells for adoptive immunotherapy

Journal of Immunology

Volumn 193, Issue 9, 2014, Pages 4739-4747

  Golay, Josée ^a   D'Amico, Anna ^a   Borleri, Gianmaria ^b   Bonzi, Michela ^a   Valgardsdottir, Rut ^a   Alzani, Rachele ^c   Cribioli, Sabrina ^c   Albanese, Clara ^c   Pesenti, Enrico ^c   Finazzi, Maria Chiara ^b   Quaresmini, Giulia ^b   Nagorsen, Dirk ^d   Introna, Martino ^a   Rambaldi, Alessandro ^b  

^a Centro di Terapia Cellulare   (Italy)

^b Azienda Ospedaliera Papa Giovanni XXIII   (Italy)

^c NERVIANO MEDICAL SCIENCES   (Italy)

^d AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLINATUMOMAB; CD19 ANTIGEN; CD272 ANTIGEN; LYMPHOCYTE ANTIGEN; PROGRAMMED DEATH 1 RECEPTOR; RECOMBINANT INTERLEUKIN 2; UNCLASSIFIED DRUG; BISPECIFIC ANTIBODY; INTERLEUKIN 2; MEMBRANE ANTIGEN;

ADOPTIVE IMMUNOTHERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; LARGE CELL LYMPHOMA; MEMORY CELL; MOUSE; NOD SCID MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; CULTURE TECHNIQUE; CYTOTOXICITY; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOPHENOTYPING; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; METABOLISM; MORTALITY; PHENOTYPE; T LYMPHOCYTE SUBPOPULATION; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, BISPECIFIC; ANTIGENS, SURFACE; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-2; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MICE; PHENOTYPE; PROGRAMMED CELL DEATH 1 RECEPTOR; T-LYMPHOCYTE SUBSETS;

EID: 84908144124     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401550     Document Type: Article

References (53)

1. Riches, J. C., A. G. Ramsay, and J. G. Gribben. 2012. Immune reconstitution in chronic lymphocytic leukemia. Curr. Hematol. Malig. Rep. 7: 13-20.
2. Lanasa, M. C. 2010. Novel insights into the biology of CLL. Hematology (Am. Soc. Hematol. Educ. Program) 2010: 70-76.
3. Christopoulos, P., D. Pfeifer, K. Bartholomé, M. Follo, J. Timmer, P. Fisch, and H. Veelken. 2011. Definition and characterization of the systemic T-cell dysregulation in untreated indolent B-cell lymphoma and very early CLL. Blood 117: 3836-3846.
4. Bartik, M. M., D. Welker, and N. E. Kay. 1998. Impairments in immune cell function in B cell chronic lymphocytic leukemia. Semin. Oncol. 25: 27-33.
5. Hallek, M. 2013. Signaling the end of chronic lymphocytic leukemia: new frontline treatment strategies. Blood 122: 3723-3734.
6. Melchardt, T., L. Weiss, R. Greil, and A. Egle. 2013. Viral infections and their management in patients with chronic lymphocytic leukemia. Leuk. Lymphoma 54: 1602-1613.
7. Kharfan-Dabaja, M. A., W. G. Wierda, and L. J. Cooper. 2014. Immunotherapy for chronic lymphocytic leukemia in the era of BTK inhibitors. Leukemia 28: 507-517.
8. Restifo, N. P., M. E. Dudley, and S. A. Rosenberg. 2012. Adoptive immuno-therapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12: 269-281.
9. Vacchelli, E., A. Eggermont, W. H. Fridman, J. Galon, E. Tartour, L. Zitvogel, G. Kroemer, and L. Galluzzi. 2013. Trial watch: adoptive cell transfer for anticancer immunotherapy. OncoImmunology 2: e24238.
10. Maus, M. V., S. A. Grupp, D. L. Porter, and C. H. June. 2014. Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood 123: 2625-2635.
11. Hami, L. S., C. Green, N. Leshinsky, E. Markham, K. Miller, and S. Craig. 2004. GMP production and testing of Xcellerated T cells for the treatment of patients with CLL. Cytotherapy 6: 554-562.
12. Thompson, J. A., R. A. Figlin, C. Sifri-Steele, R. J. Berenson, and M. W. Frohlich. 2003. A phase I trial of CD3/CD28-activated T cells (Xcell-erated T cells) and interleukin-2 in patients with metastatic renal cell carcinoma. Clin. Cancer Res. 9: 3562-3570.
13. Nagorsen, D., and P. A. Baeuerle. 2011. Immunomodulatory therapy of cancer with T cell-engaging BiTE antibody blinatumomab. Exp. Cell Res. 317: 1255-1260.
14. Dreier, T., G. Lorenczewski, C. Brandl, P. Hoffmann, U. Syring, F. Hanakam, P. Kufer, G. Riethmuller, R. Bargou, and P. A. Baeuerle. 2002. Extremely potent, rapid and costimulation-independent cytotoxic T-cell response against lymphoma cells catalyzed by a single-chain bispecific antibody. Int. J. Cancer 100: 690-697.
15. Löffler, A., M. Gruen, C. Wuchter, F. Schriever, P. Kufer, T. Dreier, F. Hanakam, P. A. Baeuerle, K. Bommert, L. Karawajew, et al. 2003. Efficient elimination of chronic lymphocytic leukaemia B cells by autologous T cells with a bispecific anti-CD19/anti-CD3 single-chain antibody construct. Leukemia 17: 900-909.
16. Löffler, A., P. Kufer, R. Lutterbüse, F. Zettl, P. T. Daniel, J. M. Schwenkenbecher, G. Riethmüller, B. Dörken, and R. C. Bargou. 2000. A recombinant bispecific single-chain antibody, CD19 × CD3, induces rapid and high lymphoma-directed cytotoxicity by unstimulated T lymphocytes. Blood 95: 2098-2103.
17. d'Argouges, S., S. Wissing, C. Brandl, N. Prang, R. Lutterbuese, A. Kozhich, J. Suzich, M. Locher, P. Kiener, P. Kufer, et al. 2009. Combination of rituximab with blinatumomab (MT103/MEDI-538), a T cell-engaging CD19-/CD3-bispecific antibody, for highly efficient lysis of human B lymphoma cells. Leuk. Res. 33: 465-473.
18. Wong, R., C. Pepper, P. Brennan, D. Nagorsen, S. Man, and C. Fegan. 2013. Blinatumomab induces autologous T-cell killing of chronic lymphocytic leukemia cells. Haematologica 98: 1930-1938.
19. Alzani, R., O. Pedrini, C. Albanese, R. Ceruti, A. Casolaro, V. Patton, F. Colotta, A. Rambaldi, M. Introna, E. Pesenti, et al. 2010. Therapeutic efficacy of the pan-cdk inhibitor PHA-793887 in vitro and in vivo in engraftment and high-burden leukemia models. Exp. Hematol. 38: 259-269.e2.
20. Amann, M., K. Brischwein, P. Lutterbuese, L. Parr, L. Petersen, G. Lorenczewski, E. Krinner, S. Bruckmeier, S. Lippold, R. Kischel, et al. 2008. Therapeutic window of MuS110, a single-chain antibody construct bispecific for murine EpCAM and murine CD3. Cancer Res. 68: 143-151.
21. Ramsay, A. G., A. J. Johnson, A. M. Lee, G. Gorgün, R. Le Dieu, W. Blum, J. C. Byrd, and J. G. Gribben. 2008. Chronic lymphocytic leukemia T cells show impaired immunological synapse formation that can be reversed with an immunomodulating drug. J. Clin. Invest. 118: 2427-2437.
22. Ramsay, A. G., A. J. Clear, R. Fatah, and J. G. Gribben. 2012. Multiple inhibitory ligands induce impaired T-cell immunologic synapse function in chronic lymphocytic leukemia that can be blocked with lenalidomide: establishing a reversible immune evasion mechanism in human cancer. Blood 120: 1412-1421.
23. Gerdemann, U., J. M. Keirnan, U. L. Katari, R. Yanagisawa, A. S. Christin, L. E. Huye, S. K. Perna, S. Ennamuri, S. Gottschalk, M. K. Brenner, et al. 2012. Rapidly generated multivirus-specific cytotoxic T lymphocytes for the prophylaxis and treatment of viral infections. Mol. Ther. 20: 1622-1632.
24. Rapoport, A. P., N. A. Aqui, E. A. Stadtmauer, D. T. Vogl, H. B. Fang, L. Cai, S. Janofsky, A. Chew, J. Storek, G. Akpek, et al. 2011. Combination immuno-therapy using adoptive T-cell transfer and tumor antigen vaccination on the basis of hTERT and survivin after ASCT for myeloma. Blood 117: 788-797.
25. Rapoport, A. P., E. A. Stadtmauer, N. Aqui, A. Badros, J. Cotte, L. Chrisley, E. Veloso, Z. Zheng, S. Westphal, R. Mair, et al. 2005. Restoration of immunity in lymphopenic individuals with cancer by vaccination and adoptive T-cell transfer. Nat. Med. 11: 1230-1237.
26. Laport, G. G., B. L. Levine, E. A. Stadtmauer, S. J. Schuster, S. M. Luger, S. Grupp, N. Bunin, F. J. Strobl, J. Cotte, Z. Zheng, et al. 2003. Adoptive transfer of costimulated T cells induces lymphocytosis in patients with relapsed/refractory non-Hodgkin lymphoma following CD34+-selected hematopoietic cell transplantation. Blood 102: 2004-2013.
27. Rezvany, M. R., M. Jeddi-Tehrani, A. Osterborg, E. Kimby, H. Wigzell, and H. Mellstedt. 1999. Oligoclonal TCRBV gene usage in B-cell chronic lymphocytic leukemia: major perturbations are preferentially seen within the CD4 T-cell subset. Blood 94: 1063-1069.
28. Serrano, D., J. Monteiro, S. L. Allen, J. Kolitz, P. Schulman, S. M. Lichtman, A. Buchbinder, V. P. Vinciguerra, N. Chiorazzi, and P. K. Gregersen. 1997. Clonal expansion within the CD4+CD57+ and CD8+CD57+ T cell subsets in chronic lymphocytic leukemia. J. Immunol. 158: 1482-1489.
29. Antony, P. A., C. A. Piccirillo, A. Akpinarli, S. E. Finkelstein, P. J. Speiss, D. R. Surman, D. C. Palmer, C. C. Chan, C. A. Klebanoff, W. W. Overwijk, et al. 2005. CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J. Immunol. 174: 2591-2601.
30. Burrell, B. E., Y. Nakayama, J. Xu, C. C. Brinkman, and J. S. Bromberg. 2012. Regulatory T cell induction, migration, and function in transplantation. J. Immunol. 189: 4705-4711.
31. Bargou, R., E. Leo, G. Zugmaier, M. Klinger, M. Goebeler, S. Knop, R. Noppeney, A. Viardot, G. Hess, M. Schuler, et al. 2008. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 321: 974-977.
32. Klinger, M., C. Brandl, G. Zugmaier, Y. Hijazi, R. C. Bargou, M. S. Topp, N. Gökbuget, S. Neumann, M. Goebeler, A. Viardot, et al. 2012. Immuno-pharmacologic response of patients with B-lineage acute lymphoblastic leukemia to continuous infusion of T cell-engaging CD19/CD3-bispecific BiTE antibody blinatumomab. Blood 119: 6226-6233.
33. Dong, H., N. A. Franklin, D. J. Roberts, H. Yagita, M. J. Glennie, and T. N. Bullock. 2012. CD27 stimulation promotes the frequency of IL-7 receptor-expressing memory precursors and prevents IL-12-mediated loss of CD8(+) T cell memory in the absence of CD4(+) T cell help. J. Immunol. 188: 3829-3838.
34. Denoeud, J., and M. Moser. 2011. Role of CD27/CD70 pathway of activation in immunity and tolerance. J. Leukoc. Biol. 89: 195-203.
35. Rosenberg, S. A., J. C. Yang, R. M. Sherry, U. S. Kammula, M. S. Hughes, G. Q. Phan, D. E. Citrin, N. P. Restifo, P. F. Robbins, J. R. Wunderlich, et al. 2011. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 17: 4550-4557.
36. Li, Y., S. Liu, J. Hernandez, L. Vence, P. Hwu, and L. Radvanyi. 2010. MART-1-specific melanoma tumor-infiltrating lymphocytes maintaining CD28 expression have improved survival and expansion capability following antigenic restimulation in vitro. J. Immunol. 184: 452-465.
37. Kowolik, C. M., M. S. Topp, S. Gonzalez, T. Pfeiffer, S. Olivares, N. Gonzalez, D. D. Smith, S. J. Forman, M. C. Jensen, and L. J. Cooper. 2006. CD28 co-stimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells. Cancer Res. 66: 10995-11004.
38. Powell, D. J., Jr., M. E. Dudley, P. F. Robbins, and S. A. Rosenberg. 2005. Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105: 241-250.
39. Riley, J. L., and C. H. June. 2005. The CD28 family: a T-cell rheostat for therapeutic control of T-cell activation. Blood 105: 13-21.
40. Berger, C., M. C. Jensen, P. M. Lansdorp, M. Gough, C. Elliott, and S. R. Riddell. 2008. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 118: 294-305.
41. Klebanoff, C. A., L. Gattinoni, and N. P. Restifo. 2012. Sorting through subsets: which T-cell populations mediate highly effective adoptive immunotherapy? J. Immunother. 35: 651-660.
42. Riches, J. C., J. K. Davies, F. McClanahan, R. Fatah, S. Iqbal, S. Agrawal, A. G. Ramsay, and J. G. Gribben. 2013. T cells from CLL patients exhibit features of T-cell exhaustion but retain capacity for cytokine production. Blood 121: 1612-1621.
43. Ramsay, A. G., R. Evans, S. Kiaii, L. Svensson, N. Hogg, and J. G. Gribben. 2013. Chronic lymphocytic leukemia cells induce defective LFA-1-directed T-cell motility by altering Rho GTPase signaling that is reversible with lenalidomide. Blood 121: 2704-2714.
44. Grzywnowicz, M., J. Zaleska, D. Mertens, W. Tomczak, P. Wlasiuk, K. Kosior, A. Piechnik, A. Bojarska-Junak, A. Dmoszynska, and K. Giannopoulos. 2012. Programmed death-1 and its ligand are novel immunotolerant molecules expressed on leukemic B cells in chronic lymphocytic leukemia. PLoS One 7: e35178.
45. Orsini, E., A. Guarini, S. Chiaretti, F. R. Mauro, and R. Foa. 2003. The circulating dendritic cell compartment in patients with chronic lymphocytic leukemia is severely defective and unable to stimulate an effective T-cell response. Cancer Res. 63: 4497-4506.
46. Dazzi, F., E. D'Andrea, G. Biasi, G. De Silvestro, G. Gaidano, M. Schena, T. Tison, F. Vianello, A. Girolami, and F. Caligaris-Cappio. 1995. Failure of B cells of chronic lymphocytic leukemia in presenting soluble and alloantigens. Clin. Immunol. Immunopathol. 75: 26-32.
47. Riella, L. V., A. M. Paterson, A. H. Sharpe, and A. Chandraker. 2012. Role of the PD-1 pathway in the immune response. Am. J. Transplant. 12: 2575-2587.
48. Derré, L., J. P. Rivals, C. Jandus, S. Pastor, D. Rimoldi, P. Romero, O. Michielin, D. Olive, and D. E. Speiser. 2010. BTLA mediates inhibition of human tumor-specific CD8+ T cells that can be partially reversed by vaccination. J. Clin. Invest. 120: 157-167.
49. Pasero, C., D. E. Speiser, L. Derré, and D. Olive. 2012. The HVEM network: new directions in targeting novel costimulatory/co-inhibitory molecules for cancer therapy. Curr. Opin. Pharmacol. 12: 478-485.
50. Drake, C. G. 2012. Combination immunotherapy approaches. Ann. Oncol. 23 (Suppl. 8): viii41-46.
51. Wolchok, J. D., H. Kluger, M. K. Callahan, M. A. Postow, N. A. Rizvi, A. M. Lesokhin, N. H. Segal, C. E. Ariyan, R. A. Gordon, K. Reed, et al. 2013. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 369: 122-133.
52. Hamid, O., C. Robert, A. Daud, F. S. Hodi, W. J. Hwu, R. Kefford, J. D. Wolchok, P. Hersey, R. W. Joseph, J. S. Weber, et al. 2013. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N. Engl. J. Med. 369: 134-144.
53. Lucchini, G., and P. Bader. 2014. Hematopoietic stem cell transplantation and immunotherapy for pediatric acute myeloid leukemia: an open challenge. Expert Rev. Hematol. 7: 291-300.