CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia

Science Translational Medicine

Volumn 5, Issue 177, 2013, Pages

  Brentjens, Renier J ^a   Davila, Marco L ^a   Riviere, Isabelle ^a   Park, Jae ^a   Wang, Xiuyan ^a   Cowell, Lindsay G ^b   Bartido, Shirley ^a   Stefanski, Jolanta ^a   Taylor, Clare ^a   Olszewska, Malgorzata ^a   Borquez Ojeda, Oriana ^a   Qu, Jinrong ^a   Wasielewska, Teresa ^a   He, Qing ^a   Bernal, Yvette ^a   Rijo, Ivelise V ^a   Hedvat, Cyrus ^a   Kobos, Rachel ^a   Curran, Kevin ^a   Steinherz, Peter ^a   Jurcic, Joseph ^a   Rosenblat, Todd ^a   Maslak, Peter ^a   Frattini, Mark ^a   Sadelain, Michel ^a   more..

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UT Southwestern ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINASE; CD19 ANTIGEN; CYCLOPHOSPHAMIDE; CYTARABINE; DEXAMETHASONE; DOXORUBICIN; ETOPOSIDE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN HEAVY CHAIN; INOTUZUMAB OZOGAMICIN; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; MERCAPTOPURINE; METHOTREXATE; MITOXANTRONE; PREDNISONE; STEROID; T LYMPHOCYTE RECEPTOR; VINCRISTINE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADULT; AGED; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ARTICLE; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CELL THERAPY; CLINICAL ARTICLE; CLINICAL TRIAL; CYTOKINE RELEASE; DRUG DOSE REDUCTION; DRUG MEGADOSE; FEMALE; FOLLOW UP; GENE REARRANGEMENT; HEMATOPOIESIS; HUMAN; LEUKEMIA CELL; LEUKEMIA RELAPSE; LEUKEMIA REMISSION; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEROID THERAPY; T LYMPHOCYTE;

ADULT; AGED; ANTIGENS, CD19; CELLS, CULTURED; FEMALE; HUMANS; IMMUNOTHERAPY; MALE; MIDDLE AGED; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; T-LYMPHOCYTES; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84876005284     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3005930     Document Type: Article

References (25)

1. A. K. Fielding, S. M. Richards, R. Chopra, H. M. Lazarus, M. R. Litzow, G. Buck, I. J. Durrant, S. M. Luger, D. I. Marks, I. M. Franklin, A. K. McMillan, M. S. Tallman, J. M. Rowe, A. H. Goldstone; Medical Research Council of the United Kingdom Adult ALL Working Party; Eastern Cooperative Oncology Group, Outcome of 609 adults after relapse of acute lymphoblastic leukemia (ALL); an MRC UKALL12/ECOG 2993 study. Blood 109, 944-950 (2007).
2. N. Gökbuget, D. Stanze, J. Beck, H. Diedrich, H. A. Horst, A. Hüttmann, G. Kobbe, K. A. Kreuzer, L. Leimer, A. Reichle, M. Schaich, S. Schwartz, H. Serve, M. Starck, M. Stelljes, R. Stuhlmann, A. Viardot, K. Wendelin, M. Freund, D. Hoelzer; German Multicenter Study Group for Adult Acute Lymphoblastic Leukemia, Outcome of relapsed adult lymphoblastic leukemia depends on response to salvage chemotherapy, prognostic factors, and performance of stem cell transplantation. Blood 120, 2032-2041 (2012).
3. R. Bassan, O. Spinelli, E. Oldani, T. Intermesoli, M. Tosi, B. Peruta, G. Rossi, E. Borlenghi, E. M. Pogliani, E. Terruzzi, P. Fabris, V. Cassibba, G. Lambertenghi-Deliliers, A. Cortelezzi, A. Bosi, G. Gianfaldoni, F. Ciceri, M. Bernardi, A. Gallamini, D. Mattei, E. Di Bona, C. Romani, A. M. Scattolin, T. Barbui, A. Rambaldi, Improved risk classification for risk-specific therapy based on the molecular study of minimal residual disease (MRD) in adult acute lymphoblastic leukemia (ALL). Blood 113, 4153-4162 (2009).
4. R. J. Brentjens, J. B. Latouche, E. Santos, F. Marti, M. C. Gong, C. Lyddane, P. D. King, S. Larson, M. Weiss, I. Rivière, M. Sadelain, Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat. Med. 9, 279-286 (2003).
5. L. J. Cooper, M. S. Topp, L. M. Serrano, S. Gonzalez, W. C. Chang, A. Naranjo, C. Wright, L. Popplewell, A. Raubitschek, S. J. Forman, M. C. Jensen, T-cell clones can be rendered specific for CD19: Toward the selective augmentation of the graft-versus-B-lineage leukemia effect. Blood 101, 1637-1644 (2003).
6. J. N. Kochenderfer, Z. Yu, D. Frasheri, N. P. Restifo, S. A. Rosenberg, Adoptive transfer of syngeneic T cells transduced with a chimeric antigen receptor that recognizes murine CD19 can eradicate lymphoma and normal B cells. Blood 116, 3875-3886 (2010).
7. M. C. Milone, J. D. Fish, C. Carpenito, R. G. Carroll, G. K. Binder, D. Teachey, M. Samanta, M. Lakhal, B. Gloss, G. Danet-Desnoyers, D. Campana, J. L. Riley, S. A. Grupp, C. H. June, Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 17, 1453-1464 (2009).
8. R. J. Brentjens, I. Rivière, J. H. Park, M. L. Davila, X. Wang, J. Stefanski, C. Taylor, R. Yeh, S. Bartido, O. Borquez-Ojeda, M. Olszewska, Y. Bernal, H. Pegram, M. Przybylowski, D. Hollyman, Y. Usachenko, D. Pirraglia, J. Hosey, E. Santos, E. Halton, P. Maslak, D. Scheinberg, J. Jurcic, M. Heaney, G. Heller, M. Frattini, M. Sadelain, Safety and persistence of adoptively transferred autologous CD19- targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood 118, 4817-4828 (2011).
9. M. Kalos, B. L. Levine, D. L. Porter, S. Katz, S. A. Grupp, A. Bagg, C. H. June, T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 3, 95ra73 (2011).
10. J. N. Kochenderfer, M. E. Dudley, S. A. Feldman, W. H. Wilson, D. E. Spaner, I. Maric, M. Stetler-Stevenson, G. Q. Phan, M. S. Hughes, R. M. Sherry, J. C. Yang, U. S. Kammula, L. Devillier, R. Carpenter, D. A. Nathan, R. A. Morgan, C. Laurencot, S. A. Rosenberg, B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood 119, 2709-2720 (2012).
11. J. N. Kochenderfer, W. H. Wilson, J. E. Janik, M. E. Dudley, M. Stetler-Stevenson, S. A. Feldman, I. Maric, M. Raffeld, D. A. Nathan, B. J. Lanier, R. A. Morgan, S. A. Rosenberg, Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood 116, 4099-4102 (2010).
12. D. L. Porter, B. L. Levine, M. Kalos, A. Bagg, C. H. June, Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365, 725-733 (2011).
13. D. Hollyman, J. Stefanski, M. Przybylowski, S. Bartido, O. Borquez-Ojeda, C. Taylor, R. Yeh, V. Capacio, M. Olszewska, J. Hosey, M. Sadelain, R. J. Brentjens, I. Rivière, Manufacturing validation of biologically functional T cells targeted to CD19 antigen for autologous adoptive cell therapy. J. Immunother. 32, 169-180 (2009).
14. M. C. Jensen, L. Popplewell, L. J. Cooper, D. DiGiusto, M. Kalos, J. R. Ostberg, S. J. Forman, Antitransgene rejection responses contribute to attenuated persistence of adoptively transferred CD20/CD19-specific chimeric antigen receptor redirected T cells in humans. Biol. Blood Marrow Transplant. 16, 1245-1256 (2010).
15. B. Savoldo, C. A. Ramos, E. Liu, M. P. Mims, M. J. Keating, G. Carrum, R. T. Kamble, C. M. Bollard, A. P. Gee, Z. Mei, H. Liu, B. Grilley, C. M. Rooney, H. E. Heslop, M. K. Brenner, G. Dotti, CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J. Clin. Invest. 121, 1822-1826 (2011).
16. M. L. Davila, R. Brentjens, X. Wang, I. Rivière, M. Sadelain, How do CARs work?: Early insights from recent clinical studies targeting CD19. Oncoimmunology 1, 1577-1583 (2012).
17. C. Imai, K. Mihara, M. Andreansky, I. C. Nicholson, C. H. Pui, T. L. Geiger, D. Campana, Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 18, 676-684 (2004).
18. R. J. Brentjens, E. Santos, Y. Nikhamin, R. Yeh, M. Matsushita, K. La Perle, A. Quintás-Cardama, S. M. Larson, M. Sadelain, Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts. Clin. Cancer Res. 13, 5426-5435 (2007).
19. X. S. Zhong, M. Matsushita, J. Plotkin, I. Riviere, M. Sadelain, Chimeric antigen receptors combining 4-1BB and CD28 signaling domains augment PI3kinase/AKT/Bcl-XL activation and CD8+ T cell-mediated tumor eradication. Mol. Ther. 18, 413-420 (2010).
20. J. D. Goldberg, A. Linker, D. Kuk, R. Ratan, J. Jurcic, J. N. Barker, H. Castro-Malaspina, S. Giralt, K. Hsu, A. A. Jakubowski, R. Jenq, G. Koehne, E. B. Papadopoulos, M. R. van den Brink, J. W. Young, F. Boulad, N. A. Kernan, R. J. O'Reilly, S. E. Prockop, J. Yahalom, G. Heller, M. A. Perales, T cell-depleted stem cell transplantation for adults with high-risk acute lymphoblastic leukemia: Long-term survival for patients in first complete remission with a decreased risk of graft-versus-host disease. Biol. Blood Marrow Transplant. 19, 208-213 (2013).
21. A. K. Fielding, J. M. Rowe, S. M. Richards, G. Buck, A. V. Moorman, I. J. Durrant, D. I. Marks, A. K. McMillan, M. R. Litzow, H. M. Lazarus, L. Foroni, G. Dewald, I. M. Franklin, S. M. Luger, E. Paietta, P. H. Wiernik, M. S. Tallman, A. H. Goldstone, Prospective outcome data on 267 unselected adult patients with Philadelphia chromosome-positive acute lymphoblastic leukemia confirms superiority of allogeneic transplantation over chemotherapy in the pre-imatinib era: Results from the International ALL Trial MRC UKALLXII/ECOG2993. Blood 113, 4489-4496 (2009).
22. H. M. Kantarjian, S. O'Brien, T. L. Smith, J. Cortes, F. J. Giles, M. Beran, S. Pierce, Y. Huh, M. Andreeff, C. Koller, C. S. Ha, M. J. Keating, S. Murphy, E. J. Freireich, Results of treatment with hyper-CVAD, a dose-intensive regimen, in adult acute lymphocytic leukemia. J. Clin. Oncol. 18, 547-561 (2000).
23. H. Kantarjian, D. Thomas, J. Jorgensen, E. Jabbour, P. Kebriaei, M. Rytting, S. York, F. Ravandi, M. Kwari, S. Faderl, M. B. Rios, J. Cortes, L. Fayad, R. Tarnai, S. A. Wang, R. Champlin, A. Advani, S. O'Brien, Inotuzumab ozogamicin, an anti-CD22-calecheamicin conjugate, for refractory and relapsed acute lymphocytic leukaemia: A phase 2 study. Lancet Oncol. 13, 403-411 (2012).
24. J. M. Rowe, G. Buck, A. K. Burnett, R. Chopra, P. H. Wiernik, S. M. Richards, H. M. Lazarus, I. M. Franklin, M. R. Litzow, N. Ciobanu, H. G. Prentice, J. Durrant, M. S. Tallman, A. H. Goldstone; ECOG; MRC/NCRI Adult Leukemia Working Party, Induction therapy for adults with acute lymphoblastic leukemia: Results of more than 1500 patients from the international ALL trial: MRC UKALL XII/ECOG E2993. Blood 106, 3760-3767 (2005).
25. P. G. Steinherz, A. Redner, L. Steinherz, P. Meyers, C. Tan, G. Heller, Development of a new intensive therapy for acute lymphoblastic leukemia in children at increased risk of early relapse. The Memorial Sloan-Kettering-New York-II protocol. Cancer 72, 3120-3130 (1993).