Chemotherapy-refractory diffuse large B-cell lymphoma and indolent B-cell malignancies can be effectively treated with autologous T cells expressing an anti-CD19 chimeric antigen receptor

Journal of Clinical Oncology

Volumn 33, Issue 6, 2015, Pages 540-549

  Kochenderfer, James N ^a   Dudley, Mark E ^a   Kassim, Sadik H ^a   Somerville, Robert P T ^a   Carpenter, Robert O ^a   Maryalice, Stetler Stevenson ^a   Yang, James C ^a   Phan, Giao Q ^a   Hughes, Marybeth S ^a   Sherry, Richard M ^a   Raffeld, Mark ^a   Feldman, Steven ^a   Lu, Lily ^a   Li, Yong F ^a   Ngo, Lien T ^a   Goy, Andre ^b   Feldman, Tatyana ^b   Spaner, David E ^c   Wang, Michael L ^d   Chen, Clara C ^a   Kranick, Sarah M ^a   Nath, Avindra ^a   Nathan, Debbie Ann N ^a   Morton, Kathleen E ^a   Toomey, Mary Ann ^a   Rosenberg, Steven A ^a   more..

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b HACKENSACK UNIVERSITY MEDICAL CENTER   (United States)

^c DEPARTMENT OF RADIATION ONCOLOGY   (Canada)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOPLATIN; CD19 ANTIBODY; CHIMERIC ANTIGEN RECEPTOR; CISPLATIN; CREATININE; CYCLOPHOSPHAMIDE; CYTARABINE; DEXAMETHASONE; DOXORUBICIN; ETOPOSIDE; FLUDARABINE; GEMCITABINE; IFOSFAMIDE; METHOTREXATE; METHYLPREDNISOLONE; PREDNISONE; RITUXIMAB; VINCRISTINE; ANTINEOPLASTIC AGENT; CD19 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; VIDARABINE;

ACUTE KIDNEY FAILURE; ACUTE TOXICITY; ADULT; ADVANCED CANCER; AGED; APHASIA; ARTICLE; AUTOTRANSPLANTATION; B CELL LYMPHOMA; BACTEREMIA; BRAIN DISEASE; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER REGRESSION; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; CONFUSION; DELIRIUM; DONOR LYMPHOCYTE INFUSION; DRUG MEGADOSE; DYSPNEA; FACIAL NERVE PARALYSIS; FATIGUE; FEASIBILITY STUDY; FEMALE; FEVER; GAIT DISORDER; HEADACHE; HUMAN; HUMAN CELL; HYPOTENSION; HYPOXIA; INFLUENZA; LARGE CELL LYMPHOMA; MALAISE; MALE; MIDDLE AGED; MULTIPLE CYCLE TREATMENT; MYOCLONUS; NAUSEA; NEUROPATHY; NEUROTOXICITY; PNEUMONIA; PRIORITY JOURNAL; SIDE EFFECT; T LYMPHOCYTE; TACHYCARDIA; TREATMENT DURATION; UPPER EXTREMITY DEEP VEIN THROMBOSIS; URINARY TRACT INFECTION; VASCULAR DISEASE; ADOPTIVE IMMUNOTHERAPY; ANALOGS AND DERIVATIVES; CLINICAL TRIAL; IMMUNOLOGY; LYMPHOMA, B-CELL; LYMPHOMA, LARGE B-CELL, DIFFUSE; MULTIMODALITY CANCER THERAPY; PROCEDURES; TRANSPLANTATION; TRANSPLANTATION CONDITIONING;

ADULT; AGED; ANTIGENS, CD19; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; COMBINED MODALITY THERAPY; CYCLOPHOSPHAMIDE; FEMALE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LYMPHOMA, B-CELL; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; MIDDLE AGED; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TRANSPLANTATION CONDITIONING; VIDARABINE;

EID: 84923118622     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2014.56.2025     Document Type: Article

References (46)

1. Elstrom RL, Martin P, Ostrow K, et al: Response to second-line therapy defines the potential for cure in patients with recurrent diffuse large B-cell lymphoma: Implications for the development of novel therapeutic strategies. Clin Lymphoma Myeloma Leuk 10:192-196, 2010
2. Friedberg JW: Relapsed/refractory diffuse large B-cell lymphoma. Hematology Am Soc Hematol Educ Program 2011:498-505, 2011
3. Moore S, Kayani I, Peggs K, et al: Mini-BEAM is effective as a bridge to transplantation in patients with refractory or relapsed Hodgkin lymphoma who have failed to respond to previous lines of salvage chemotherapy but not in patients with salvage-refractory DLBCL. Br J Haematol 157:543-552, 2012
4. Nagle SJ, Woo K, Schuster SJ, et al: Outcomes of patients with relapsed/refractory diffuse large B-cell lymphoma with progression of lymphoma after autologous stem cell transplantation in the rituximab era. Am J Hematol 88:890-894, 2013
5. Rivera-Rodriguez N, Cabanillas F: Recent advances in the management of mantle cell lymphoma. Curr Opin Oncol 25:716-721, 2013
6. Martelli M, Ferreri AJM, Agostinelli C, et al: Diffuse large B-cell lymphoma. Crit Rev Oncol Hematol 87:146-171, 2013
7. Laport GG: Changing role of stem cell transplantation in follicular lymphoma. Hematology Am Soc Hematol Educ Program 2012:417-425, 2012
8. Vose JM, Bierman PJ, Anderson JR, et al: Progressive disease after high-dose therapy and autologous transplantation for lymphoid malignancy: Clinical course and patient follow-up. Blood 80:2142-2148, 1992
9. Uckun FM, Jaszcz W, Ambrus JL, et al: Detailed studies on expression and function of CD19 surface determinant by using B43 monoclonal antibody and the clinical potential of anti-CD19 immunotoxins. Blood 71:13-29, 1988
10. Eshhar Z, Waks T, Gross G, et al: Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci U S A 90:720-724, 1993
11. Kochenderfer JN, Rosenberg SA: Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors. Nat Rev Clin Oncol 10:267-276, 2013
12. Dotti G, Gottschalk S, Savoldo B, et al: Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev 257: 107-126, 2014
13. Kershaw MH, Westwood JA, Darcy PK: Gene-engineered T cells for cancer therapy. Nat Rev Cancer 13:525-541, 2013
14. Sadelain M, Brentjens R, Rivière I: The basic principles of chimeric antigen receptor design. Cancer Discov 3:388-398, 2013
15. Brentjens RJ, Latouche JB, Santos E, et al: 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
16. Cooper LJ, Topp MS, Serrano LM, et al: 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
17. Milone MC, Fish JD, Carpenito C, et al: 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
18. Wang X, Naranjo A, Brown CE, et al: Phenotypic and functional attributes of lentivirus-modified CD19-specific Human CD8+ central memory T cells manufactured at clinical scale. J Immunother 35: 689-701, 2012
19. Savoldo B, Ramos CA, Liu E, et al: CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest 121:1822-1826, 2011
20. Kochenderfer JN, Yu Z, Frasheri D, et al: 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
21. Kochenderfer JN, Feldman SA, Zhao Y, et al: Construction and preclinical evaluation of an anti-CD19 chimeric antigen receptor. J Immunother 32: 689-702, 2009
22. Kochenderfer JN, Wilson WH, Janik JE, et al: 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
23. Kochenderfer JN, Dudley ME, Feldman SA, et al: 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
24. 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 122:4129-4139, 2013
25. 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 3:95ra73, 2011
26. Porter DL, Levine BL, Kalos M, et al: Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365:725-733, 2011
27. Grupp SA, Kalos M, Barrett D, et al: Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368:1509-1518, 2013
28. Brentjens RJ, Rivière I, Park JH, et al: 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
29. 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 5:177ra38, 2013
30. Cruz CRY, Micklethwaite KP, Savoldo B, et al: Infusion of donor-derived CD19-redirected virusspecific T cells for B-cell malignancies relapsed after allogeneic stem cell transplant: A phase 1 study. Blood 122:2956-2973, 2013
31. Davila ML, Riviere I, Wang X, et al: Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med 6:224ra25, 2014
32. Carpenter RO, Evbuomwan MO, Pittaluga S, et al: B-cell maturation antigen is a promising target for adoptive T-cell therapy of multiple myeloma. Clin Cancer Res 19:2048-2060, 2013
33. Jena B, Maiti S, Huls H, et al: Chimeric antigen receptor (CAR)-specific monoclonal antibody to detect CD19-specific T cells in clinical trials. PLoS One 8:e57838, 2013
34. Gattinoni L, Finkelstein SE, Klebanoff CA, et al: Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 202:907-912, 2005
35. North RJ: Cyclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells. J Exp Med 155:1063-1074, 1982
36. Montero AJ, Diaz-Montero CM, Kyriakopoulos CE, et al: Myeloid-derived suppressor cells in cancer patients: A clinical perspective. J Immunother 35:107-115, 2012
37. Talmadge JE, Gabrilovich DI: History of myeloid-derived suppressor cells. Nat Rev Cancer 13:739-752, 2013
38. Cheson BD, Pfistner B, Juweid ME, et al: Revised response criteria for malignant lymphoma. J Clin Oncol 25:579-586, 2007
39. Hallek M, Cheson BD, Catovsky D, et al: Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: A report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute Working Group 1996 guidelines. Blood 111:5446-5456, 2008
40. Sallusto F, Lenig D, Förster R, et al: Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-712, 1999
41. Rubio V, Stuge TB, Singh N, et al: Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat Med 9:1377-1382, 2003
42. Rosenberg SA, Lotze MT, Yang JC, et al: Experience with the use of high-dose interleukin-2 in the treatment of 652 cancer patients. Ann Surg 210:474-485, 1989
43. Brenchley JM, Karandikar NJ, Betts MR, et al: Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8+ T cells. Blood 101:2711-2720, 2003
44. Focosi D, Bestagno M, Burrone O, et al: CD57+ T lymphocytes and functional immune deficiency. J Leukoc Biol 87:107-116, 2010
45. Sallusto F, Geginat J, Lanzavecchia A: Central memory and effector memory T cell subsets: Function, generation, and maintenance. Annu Rev Immunol 22:745-763, 2004
46. Nagorsen D, Baeuerle PA: Immunomodulatory therapy of cancer with T cell-engaging BiTE antibody blinatumomab. Exp Cell Res 317:1255-1260, 2011