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Review

Emerging biological therapies to treat acute lymphoblastic leukemia

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Pages 107-121 | Received 22 Jul 2016, Accepted 02 Nov 2016, Published online: 25 Dec 2016

References

  • Biological therapies for cancer. [cited 2016 Oct 25]. Available from: https://www.cancer.gov/about-cancer/treatment/types/immunotherapy/bio-therapies-fact-sheet
  • Targeted cancer therapies. [cited 2016 Oct 25]. Available from: https://www.cancer.gov/about-cancer/treatment/types/targeted-therapies/fact-sheet
  • Arber DA, Orazi A, Hasserjian R, et al. The 2016 revision of the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016;127:2391–2405.
  • Pui C-H, Mullighan CG, Evans WE, et al. Pediatric acute lymphoblastic leukemia: where are we going and how do we get there? Blood. 2012;120(6):1165–1174.
  • Bassan R, Hoelzer D. Modern therapy of acute lymphoblastic leukemia. J Clin Oncol. 2011;29:532–543.
  • Mullighan CG. Molecular genetics of B-precursor acute lymphoblastic leukemia. J Clin Invest. 2012 Oct 1;122(10):3407–3415.
  • Chiaretti S, Gianfelici V, O’Brien SM, et al. Advances in the genetics and therapy of acute lymphoblastic leukemia. Am Soc Clin Oncol Educ Book. 2016;35:e314–e322.
  • Beldjord K, Chevret S, Asnafi V, et al. Oncogenetics and minimal residual disease are independent outcome predictors in adult patients with acute lymphoblastic leukemia. Blood. 2014;123:3739–3749.
  • Egler RA, Ahuja SP, Matloub Y. L-asparaginase in the treatment of patients with acute lymphoblastic leukemia. J Pharmacol Pharmacother. 2016;7:62–7110.
  • Chalandon Y, Thomas X, Hayette S, et al. Randomized study of reduced-intensity chemotherapy combined with imatinib in adults with Ph-positive acute lymphoblastic leukemia. Blood. 2015;125:3711–3719.
  • Drugs approved for leukemia. [cited 2016 Oct 25]. Available from: https://www.cancer.gov/about-cancer/treatment/drugs/leukemia
  • Jones L, Carol H, Evans K, et al. A review of new agents evaluated against pediatric acute lymphoblastic leukemia by the pediatric preclinical testing program. Leuk Advance. [Online publication 2016 Aug 12]. DOI:10.1038/leu.2016.192
  • Peirs S, Matthijssens F, Goossens S, et al. ABT-199 mediated inhibition of BCL-2 as a novel therapeutic strategy in T-cell acute lymphoblastic leukemia. Blood. 2014;124:3738–3747.
  • Khaw SL, Suryani S, Evans K, et al. Venetoclax responses of pediatric ALL xenografts reveal sensitivity of MLL-rearranged leukemia. Blood. 2016;128:1382–1395.
  • Leonard JT, Rowley JS, Eide CA, et al. Targeting BCL-2 and ABL/LYN in Philadelphia chromosome-positive acute lymphoblastic leukemia. Sci Transl Med. 2016;8(354):354ra114.
  • Dhédin N, Huynh A, Maury S, et al. Role of allogeneic stem cell transplantation in adult patients with Ph-negative acute lymphoblastic leukemia. Blood. 2015;125:2486–2496.
  • Ruggeri A, Labopin M, Sanz G, et al. Comparison of outcomes after unrelated cord blood and unmanipulated haploidentical stem cell transplantation in adults with acute. Leukemia. 2015;29(9):1891–1900.
  • Graça M. Dores, Susan S. Devesa, Curtis Re, et al. Acute leukemia incidence and patient survival among children and adults in the United States, 2001-2007. Blood. 2012;119:34–43.
  • Rae C, Furlong W, Jankovic M, et al. Economic evaluation of treatment for acute lymphoblastic leukaemia in childhood. Eur J Cancer Care (Engl). 2014;23(6):779–785.
  • Kaul S, Korgenski EK, Ying J, et al. A retrospective analysis of treatment-related hospitalization costs of pediatric, adolescent, and young adult acute lymphoblastic leukemia. Cancer Med. 2016;5:221–229.
  • Van Litsenburg RR, Uyl-de Groot CA, Raat H, et al. Cost-effectiveness of treatment of childhood acute lymphoblastic leukemia with chemotherapy only: the influence of new medication and diagnostic technology. Pediatr Blood Cancer. 2011;57:1005–1010.
  • Dombret H, Thomas X, Chevallier P, et al. Healthcare burden and reimbursement of hospitalization during chemotherapy for adults with Ph-negative relapsed or refractory B-cell precursor acute lymphoblastic leukemia in France: a retrospective chart review. J Med Econ. 2016;19:1034–1039.
  • Bene MC, Castoldi G, Knapp W, et al. Proposals for the immunological classification of acute leukemias. European Group for the Immunological Characterization of Leukemias (EGIL). Leukemia. 1995;9:1783–1786.
  • Jabbour E, O’Brien S, Ravandi F, et al. Monoclonal antibodies in acute lymphoblastic leukemia. Blood. 2015;125:4010–4016.
  • Thomas DA, O’Brien S, Faderl S, et al. Chemoimmunotherapy with a modified hyper-CVAD and rituximab regimen improves outcome in de novo Philadelphia chromosome-negative precursor B-lineage acute lymphoblastic leukemia. J Clin Oncol. 2010;28:3880–3889.
  • Hoelzer D, Huettmann A, Kaul F, et al. Immunochemotherapy with rituximab improves molecular CR rate and outcome in CD20+ B-lineage standard and high risk patients; results of 263 CD20+ patients studied prospectively in GMALL study 07/2003. Blood. 2011;116:77–78.
  • Maury S, Chevret S, Thomas X, et al. Addition of rituximab improves the outcome of adult patients with CD20-positive, Ph-negative, B-cell precursor acute lymphoblastic leukemia (BCP-ALL): results of the randomized GRAALL-R 2005 study. Blood. 2015;126:1.
  • Stolz C, Hess G, Hähnel PS, et al. Targeting Bcl-2 family proteins modulates the sensitivity of B-cell lymphoma to rituximab-induced apoptosis. Blood. 2008;112:3312–3321.
  • Romaguera JE, Fayad LE, McLaughlin P, et al. Phase I trial of bortezomib in combination with rituximab-HyperCVAD alternating with rituximab, methotrexate and cytarabine for untreated aggressive mantle cell lymphoma. Br J Haematol. 2010;151:47–53.
  • Rahmé R, Benayoun E, Pautas C, et al. Treatment with 5-azacytidin upregulates the expression of CD20 in CD20-negative B cell acute lymphoblastic leukemia: a case report. Exp Hematol. 2013;41(6):505–507.
  • Jabbour E, Kantarjian H, Thomas D, et al. Phase II study of the hyper-CVAD regimen in combination with ofatumumab as frontline therapy for adults with CD-20 positive acute lymphoblastic leukemia (ALL). Blood. 2013;122:2664.
  • Awasthi A, Ayello J, Van De Ven C, et al. Comparative study of obinutuzumab (GA101) vs. rituximab against CD20+ rituximab-sensitive and -resistant burkitt (BL) and acute lymphoblastic leukemia (B-ALL): potential targeted therapy in patients with high risk BL and pre-B-ALL. Blood. 2014;124:2251.
  • Kantarjian HM, Lioure B, Kim SK, et al. A phase II study of coltuximab ravtansine (SAR3419) monotherapy in patients with relapsed or refractory acute lymphoblastic leukemia. Clin Lymphoma Myeloma Leuk. 2016;1:139–145.
  • Fathi AT, Borate U, DeAngelo DJ, et al. A phase 1 study of denintuzumab mafodotin (SGN-CD19A) in adults with relapsed or refractory B-lineage acute leukemia (B-ALL) and highly aggressive lymphoma. Blood. 2015;126:1328.
  • Anja Löffler A, Peter Kufer P, Ralf Lutterbüse R, et al. A recombinant bispecific single-chain antibody, CD19 × CD3, induces rapid and high lymphoma-directed cytotoxicity by unstimulated T lymphocytes. Blood. 2000;95:2098–2103.
  • Klinger M, Brandl C, Zugmaier G, et al. Immunopharmacologic response of patients with B-lineage acute lymphoblastic leukemia to continuous infusion of T cell-engaging CD19/CD3-bispecific BiTE antibody blinatumomab. Blood. 2012 Jun 28;119(26):6226–6233.
  • Topp MS, Gökbuget N, Zugmaier G, et al. Phase II trial of the anti-CD19 bispecific T cell-engager blinatumomab shows hematologic and molecular remissions in patients with relapsed or refractory B-precursor acute lymphoblastic leukemia. J Clin Oncol. 2014;32:4134–4140.
  • Zugmaier G, Gökbuget N, Klinger M, et al. Long-term survival and T-cell kinetics in relapsed/refractory ALL patients who achieved MRD response after blinatumomab treatment. Blood. 2015;126:2578–2584.
  • Topp MS, Gökbuget N, Stein AS, et al. Safety and activity of blinatumomab for adult patients with relapsed or refractory B-precursor acute lymphoblastic leukaemia: a multicentre, single-arm, phase 2 study. Lancet Oncol. 2015;16:57–66.
  • Goekbuget N, Kantarjian H, Brüggemann M, et al. An evaluation of molecular response in a phase 2 open-label, multicenter confirmatory study in patients (pts) with relapsed/refractory b-precursor acute lymphoblastic leukemia (R/R ALL) receiving treatment with the BiTE® antibody construct blinatumomab. Blood. 2014;124:3704.
  • Martinelli G, Dombret H, Chevallier P, et al. Complete molecular and hematologic response in adult patients with relapsed/refractory (R/R) Philadelphia chromosome-positive B-precursor acute lymphoblastic leukemia (ALL) following treatment with blinatumomab: results from a phase 2 single-arm, multicenter study (ALCANTARA). Blood. 2015;126:679.
  • Topp MS, Stein A, Gökbuget N. Blinatumomab improved overall survival in patients with relapsed or refractory Philadelphia negative B-cell precursor acute lymphoblastic leukemia in a randomized, open-label phase 3 study (TOWER). Haematologica. 2016;101(s1):22.
  • Topp MS, Kufer P, Gökbuget N, et al. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy-refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. J Clin Oncol. 2011;29:2493–2498.
  • Topp MS, Gökbuget N, Zugmaier G, et al. Long-term follow-up of hematologic relapse-free survival in a phase 2 study of blinatumomab in patients with MRD in B-lineage ALL. Blood. 2012;120:5185–5187.
  • Zugmaier G, Goekbuget N, Viardot A, et al. Long-term survival in adult patients with relapsed/refractory B-precursor acute lymphoblastic leukemia (ALL) who achieved minimal residual disease (MRD) response following anti-CD19 BiTE® blinatumomab. Blood. 2014;124:2287.
  • Gökbuget N, Dombret H, Bonifacio M, et al. Long-term outcomes after blinatumomab treatment: follow-up of a phase 2 study in patients (Pts) with minimal residual disease (MRD) positive B-cell precursor acute lymphoblastic leukemia (ALL). Blood. 2015;126:680.
  • Stein A, Topp MS, Goekbuget N, et al. Allogeneic hematopoietic stem cell transplantation following anti-CD19 BiTE® blinatumomab in adult patients with relapsed/refractory B-precursor acute lymphoblastic leukemia (ALL). Blood. 2014;124:965.
  • Topp MS, Gökbuget N, O’Brien S, et al. Influence of baseline factors on outcomes in patients (pts) with relapsed/refractory B-precursor acute lymphoblastic leukemia (R/R ALL) treated with blinatumomab. Haematologica. 2015;100(s1):30.
  • Zugmaier G, Gökbuget N, Klinger M, et al. Long-term survival and T-cell kinetics in relapsed/refractory ALL patients who achieved MRD response after blinatumomab treatment. Blood. 2015;126:2578–2584.
  • Teachey DT, Rheingold SR, Maude SL, et al. Cytokine release syndrome after blinatumomab treatment related to abnormal macrophage activation and ameliorated with cytokine-directed therapy. Blood. 2013;121:5154–5157.
  • Zugmaier G, Topp MS, Alekar S, et al. Long-term follow-up of serum immunoglobulin levels in blinatumomab-treated patients with minimal residual disease-positive B-precursor acute lymphoblastic leukemia. Blood Cancer J. 2014;4:244.
  • Kantarjian HM, Stein AS, Bargou RC, et al. Safety and activity of blinatumomab for older patients (pts) with relapsed/refractory (R/R) B-precursor acute lymphoblastic leukemia (ALL) in two phase 2 studies. J Clin Oncol. 2015;33:7043.
  • Kantarjian HM, Stein AS, Bargou RC, et al. Blinatumomab treatment of older adults with relapsed/refractory B-precursor acute lymphoblastic leukemia: results from two phase 2 studies. Cancer. 2016;122:2178–2185.
  • Thomas X. Blinatumomab: a new era of treatment for adult ALL? Lancet Oncol. 2015;16:6–7.
  • Topp MS, Stelljes M, Zugmaier G, et al. Retreatment with blinatumomab after CD19-positive relapse: experience from 3 trials in patients with relapsed/refractory B-precursor acute lymphoblastic leukemia (R/R ALL). Haematologica. 2015;100(s1):31–32.
  • Sokolov A, Parovichnikova E, Troitskay V, et al. Combined blinatumomab + dasatinib/ibrutinib therapy of relapsed acute lymphoblastic leukemia patients. Antileukemic effect on the T-helper and T-regulatory cells reduction background. Haematologica. 2016;101(s1):354.
  • Przepiorka D, Ko C-W, Deisseroth A, et al. FDA approval: blinatumomab. Clin Cancer Res. 2015;21:4035–4039.
  • Sanford M. Blinatumomab: first global approval. Drugs. 2015;75:321–327.
  • Schlegel P, Lang P, Zugmaier G, et al. Pediatric posttransplant relapsed/refractory B-precursor acute lymphoblastic leukemia shows durable remission by therapy with the T-cell engaging bispecific antibody blinatumomab. Haematologica. 2014;99:1212.
  • Zugmaier G, Handgretinger R, Locatelli F, et al. A phase 1/2 study of blinatumomab in pediatric patients with relapsed/refractory B-cell precursor acute lymphoblastic leukemia. Blood. 2013;122:70.
  • Gore L, Locatelli F, Zugmaier G, et al. Initial results from a phase 2 study of blinatumomab in pediatric patients with relapsed/refractory B-cell precursor acute lymphoblastic leukemia. Blood. 2014;124:3703.
  • Meany HJ, Seibel NL, Krailo MJ, et al. Feasability study of a novel experimental induction protocol combining B43-PAP (anti-CD19) immunotoxin with standard induction chemotherapy in children and adolescents with relapsed B-lineage ALL: a report from the Children’s Oncology Group. Immunother. 2015;38:299–305.
  • Raetz EA, Cairo MS, Borowitz MJ, et al. Re-induction chemoimmunotherapy with epratuzumab in relapsed acute lymphoblastic leukemia (ALL): phase ii results from Children’s Oncology Group (COG) study ADVL04P2.Pediatr. Pediatr Blood Cancer. 2015;62:1171–1175.
  • Advani AS, McDonough S, Coutre S, et al. SWOG S0910: A phase 2 trial of clofarabine/cytarabine/epratuzumab for relapsed/refractory acute lymphocytic leukaemia. Br J Haematol. 2014;165:504–509.
  • Chevallier P, Huguet F, Raffoux E, et al. Vincristine, dexamethasone and epratuzumab for older relapsed/refractory CD22+ B-acute lymphoblastic leukemia patients: a phase II study. Haematologica. 2015;100:e128–e131.
  • Chevallier P, Eugene T, Robillard N, et al. (90)Y-labelled anti-CD22 epratuzumab tetraxetan in adults with refractory or relapsed CD22-positive B-cell acute lymphoblastic leukaemia: a phase 1 dose-escalation study. Lancet Haematol. 2015;2:e108–e117.
  • Chevallier P, Bodet-Milin C, Robillard N, et al. BCR-ABL1 molecular remission after 90Y-epratuzumab tetraxetan radioimmunotherapy in CD22+ Ph+ B-ALL: proof of principle. Eur J Haematol. 2013;91:552–556.
  • De Vries JF, Zwaan CM, De Bie M, et al. The novel calicheamicin-conjugated CD22 antibody inotuzumab ozogamicin (CMC-544) effectively kills primary pediatric acute lymphoblastic leukemia cells. Leukemia. 2012;26:255–264.
  • DeAngelo DJ, Stock W, Shustov AR, et al. Weekly inotuzumab ozogamicin (Ino) in adult patients with relapsed or refractory CD22-positive acute lymphoblastic leukemia (ALL). Blood. 2013;122:3906.
  • Kantarjian H, Thomas D, Jorgensen J, et al. Inotuzumab ozogamicin, an anti-CD22-calecheamicin conjugate, for refractory and relapsed acute lymphocytic leukaemia: a phase 2 study. Lancet Oncol. 2012;13(4):403–411.
  • Kantarjian H, Thomas D, Jorgensen J, et al. Results of inotuzumab ozogamicin, a CD22 monoclonal antibody in refractory and relapsed acute lymphocytic leukemia. Cancer. 2013;119:2728–2736.
  • Sasaki K, Kantarjian HM, O’Brien S, et al. 3721 salvage chemotherapy with inotuzumab ozogamicin (INO) combined with mini-hyper-CVD for adult patients with relapsed/refractory (R/R) acute lymphoblastic leukemia (ALL). Blood. 2015;126:3721.
  • Elias Jabbour E, Susan O’Brien S, Koji Sasaki K, et al. Frontline inotuzumab ozogamicin in combination with low-intensity chemotherapy (mini-hyper-CVD) for older patients with acute lymphoblastic leukemia (ALL). Blood. 2015;126:83.
  • Jabbour EJ, Advani AS, Stelljes M, et al. Efficacy and safety of inotuzumab ozogamicin in older patients with relapsed/refractory acute lymphoblastic leukemia enrolled in the global phase 3 randomized controlled INO-VATE trial. Haematologica. 2016;101(s1):32.
  • DeAngelo DJ, Jabbour EJ, Stelljes M, et al. Inotuzumab ozogamicin for relapsed/refractory acute lymphoblastic leukemia in the global phase 3 randomized controlled INO-VATE trial: efficacy and safety by prior therapy. Haematologica. 2016;101(s1):184.
  • Kantarjian HM, DeAngelo DJ, Advani AS, et al. Overall survival in relapsed/refractory B-cell acute lymphoblastic leukemia patients receiving inotuzumab ozogamicin vs standard care in the phase 3 INO-VATE study. Kantarjian HM, DeAngelo DJ, Advani AS, et al. Haematologica. 2016;101(s1):339.
  • Kantarjian HM, Su Y, Bhattacharyya H, et al. Patient-reported outcomes from a global phase 3 randomized controlled trial of inotuzumab ozogamicin versus standard care for relapsed/refractory acute lymphoblastic leukemia. Haematologica. 2016;101(s1):202.
  • Kantarjian HM, DeAngelo DJ, Stelljes M, et al. Inotuzumab ozogamicin versus standard therapy for acute lymphoblastic leukemia. N Engl J Med. 2016. [Published online 12 Jun 2016]. DOI:10.1056/NEJMoa1509277
  • Kebriaei P, Wilhelm K, Ravandi F, et al. Feasibility of allografting in patients with advanced acute lymphoblastic leukemia after salvage therapy with inotuzumab ozogamicin. Clin Lymphoma Myeloma Leuk. 2013;13:296–301.
  • Wayne AS, Kreitman RJ, Findley HW, et al. Anti-CD22 immunotoxin RFB4(dsFv)-PE38 (BL22) for CD22-positive hematologic malignancies of childhood: preclinical studies and phase I clinical trial. Clin Cancer Res. 2010;16:1894–1903.
  • Wayne AS, Bhojwani D, Silverman LB, et al. A novel anti-CD22 immunotoxin, moxetumomab pasudotox: phase I study in pediatric acute lymphoblastic leukemia (ALL). Blood. 2011;118:248.
  • Ravandi F, Cortes J, Thomas D, et al. Phase I Istudy of moxetumomab pasudotox in adult patients with relapsed or refractory acute lymphoblastic leukemia. Haematologica. 2016;101(s1):351.
  • Herrera L, Bostrom B, Gore L, et al. A phase 1 study of combotox in pediatric patients with refractory B-lineage acute lymphoblastic leukemia. J Pediatr Hematol Oncol. 2009;31:936–941.
  • Schindler J, Gajavelli S, Ravandi F, et al. A phase I study of a combination of anti-CD19 and anti-CD22 immunotoxins (combotox) in adult patients with refractory B-lineage acute lymphoblastic leukaemia. Br J Haematol. 2011;154:471–476.
  • Tibes R, Keating MJ, Ferrajoli A, et al. Activity of alemtuzumab in patients with CD52-positive acute leukemia. Cancer. 2006;106:2645–2651.
  • Gorin NC, Isnard F, Garderet L, et al. Administration of alemtuzumab and G-CSF to adults with relapsed or refractory acute lymphoblastic leukemia: results of a phase II study. Eur J Haematol. 2013;91:315–321.
  • Stock W, Sanford B, Lozanski G, et al. Alemtuzumab can be incorporated into front-line therapy of adult acute lymphoblastic leukemia (ALL): final phase I results of a Cancer and Leukemia Group B study (CALGB 10102). Blood. 2009;114:838.
  • Papayannidis C, Derenzini E, Iacobucci I, et al. Successful combination treatment of clofarabine, cytarabine, and gemtuzumab-ozogamicin in adult refractory B-acute lymphoblastic leukemia. Am J Hematol. 2009;84:849–850.
  • Chevallier P, Mahe B, Garand R. Combination of chemotherapy and gemtuzumab ozogamicin in adult Philadelphia positive acute lymphoblastic leukemia patient harboring CD33 expression. Int J Hematol. 2008;88:209–211.
  • Balduzzi A, Rossi V, Corral L, et al. Molecular remission induced by gemtuzumab ozogamicin associated with donor lymphocyte infusions in t(4;11) acute lymphoblastic leukemia relapsed after transplantation. Leukemia. 2003;17:2247–2248.
  • Strickland SA, Glenn M, Zheng W, et al. SAR650984, a CD38 monoclonal antibody in patients with selected CD38+ hematological malignancies – data from a dose-escalation phase I study. Blood. 2013; 122:284.
  • Chevallier P, Robillard N, Wuilleme-Toumi S, et al. Overexpression of Her2/neu is observed in one third of adult acute lymphoblastic leukaemia patients and is associated with chemoresistance in these patients. Haematologica. 2004;89(11):1399–1401.
  • Chevallier P, Robillard N, Charbonnier A, et al. Trastuzumab for treatment of refractory/relapsed HER2-positive adult B-ALL: results of a phase 2 GRAALL study. Blood. 2012;119(11):2474–2477.
  • National Cancer Institute. CAR-T cell therapy: engineering patients’immune cells to treat their cancers. [cited 2016 Jun 20] Available from: http://www.cancer.gov/about-cancer/treatment/research/car-t-cells
  • Maude SL, Shpall EJ, Grupp SA. Chimeric antigen receptor T-cell therapy for ALL. ASH Education Book. 2014;2014:559–564.
  • Lee D, Kochenderfer J, 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;385:517–528.
  • Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor–modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368:1509–1518.
  • Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371:1507–1517.
  • Grupp SA, Maude SL, Shaw PA, et al. Durable remissions in children with relapsed/refractory ALL treated with T cells engineered with a CD19-targeted chimeric antigen receptor (CTL019). Grupp SA, Maude SL, Shaw PA, et al. Blood. 2015;126:681.
  • Maude S, Teachey D, Rheingold S, et al. Durable remissions after monotherapy with CD19-specific chimeric antigen receptor (CAR)-modified T cells in children and young adults with relapsed/refractory ALL. Haematologica. 2016;01(s1):183–184.
  • Turtle C, Sommermeyer D, Berger C, et al. Therapy of B cell malignancies with CD19-specific chimeric antigen receptor-modified T cells of defined subset composition. Blood. 2014;124:384.
  • Turtle CJ, Hanafi L-A, Berger C, et al. Rate of durable complete response in ALL, NHL, and CLL after immunotherapy with optimized lymphodepletion and defined composition CD19 CAR-T cells. J Clin Oncol. 2016;34:102.
  • 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.
  • 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. 2014;6:224ra25.
  • Park JH, Riviere I, Wang X, et al. Implications of minimal residual disease negative complete remission (MRD-CR) and allogeneic stem cell transplant on safety and clinical outcome of CD19-targeted 19-28z CAR modified t cells in adult patients with relapsed, refractory B-cell ALL. Blood. 2015;126:682.
  • Kebriaei P, Huls H, Singh H, et al. Adoptive therapy using sleeping beauty gene transfer system and artificial antigen presenting cells to manufacture T cells expressing CD19-specific chimeric antigen receptor. Blood. 2014;124:311.
  • Kebriaei P, Ciurea SO, Huls MH, et al. Pre-emptive donor lymphocyte infusion with CD19-directed, CAR-modified T cells infused after allogeneic hematopoietic cell transplantation for patients with advanced CD19+ malignancies. Blood. 2015;126:862.
  • Maude SL, Barrett DM, Rheingold SR, et al. Efficacy of humanized CD19-targeted chimeric antigen receptor (CAR)-modified T cells in children with relapsed ALL. J Clin Oncol. 2016;34:3007.
  • Lee DW, Stetler-Stevenson M, Yuan CM, et al. Safety and response of incorporating CD19 chimeric antigen receptor T cell therapy in typical salvage regimens for children and young adults with acute lymphoblastic leukemia. Blood. 2015;126:684.
  • Frey NV, Shaw PA, Hexner EO, et al. Optimizing chimeric antigen receptor (CAR) T cell therapy for adult patients with relapsed or refractory (r/r) acute lymphoblastic leukemia (ALL).J. Clin Oncol. 2016;34:7002.
  • Dunbar CE. Blood’s 70th anniversary: CARs on the blood highway. Blood. 2016;128:1–3.
  • Couzin-Frankel J. Breakthrough of the year 2013. Cancer immunotherapy. Science. 2013;342:1432–1433.
  • Garber HR, Mirza A, Mittendorf EA, et al. Adoptive T-cell therapy for leukemia. Mol Cell Ther. 2014;2:25.
  • Haso W, Lee DW, Shah NN, et al. Anti-CD22-chimeric antigen receptors targeting B-cell precursor acute lymphoblastic leukemia. Blood. 2013;121:1165–1174.
  • Torikai H, Reik A, Liu PQ, et al. A foundation for universal T-cell based immunotherapy: T cells engineered to express a CD19-specific chimeric-antigen-receptor and eliminate expression of endogenous TCR. Blood. 2012;119:5697–5705.
  • Qasim W, Amrolia PJ, Samarasinghe S, et al. First clinical application of talen engineered universal CAR19 T cells in B-ALL. Blood. 2015;126:2046.
  • Huls H, Kebriaei P, Cooper LJ. A new approach to gene therapy using Sleeping Beauty to genetically modify clinical-grade T cells to target CD19. Immunol Rev. 2014;257:181–190.
  • Pegram HJ, Lee JC, Hayman EG, et al. Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning. Blood. 2012;119:4133–4141.
  • Maus MV, June CH. Making better chimeric antigen receptors for adoptive T-cell therapy. Marcela V. Maus, Carl H. June. Clin Cancer Res. 2016;22:1875–1884.
  • Cruz CRY, 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;122:2965–2973.
  • Gleason MK, Verneris MR, Todhunter DA, et al. Bispecific and trispecific killer cell engagers directly activate human NK cells through CD16 signaling and induce cytotoxicity and cytokine production. Mol Cancer Ther. 2012;11:2674–2684.
  • Orentas RJ, Nordlund J, He J, et al. Bioinformatic description of immunotherapy targets for pediatric T-cell leukemia and the impact of normal gene sets used for comparison. Front Oncol. 2014;4:134.
  • Shalabi H, Angiolillo A, Fry TJ. Beyond CD19: opportunities for future development of targeted immunotherapy in pediatric relapsed-refractory acute leukemia. Front Pediatr. 2015;3:80.
  • Stauss HJ. Engineered T cells can fight malignant T cells. Blood. 2015;126:927–928.
  • Mamonkin M, Rouce RH, Tashiro H, et al. A T-cell–directed chimeric antigen receptor for the selective treatment of T-cell malignancies. Blood. 2015;126:983–992.
  • Suryadevara CM, Gedeon PC, Sanchez-Perez L, et al. BiTEs the “missing link” in cancer therapy? Oncoimmunology. 2015;4:e1008339.

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