Efficiency of CD19 chimeric antigen receptor-modified T cells for treatment of B cell malignancies in phase I clinical trials: A meta-analysis

Oncotarget

Volumn 6, Issue 32, 2015, Pages 33961-33971

  Zhang, Tengfei ^a,b   Cao, Ling ^a   Xie, Jing ^c   Shi, Ni ^d   Zhang, Zhen ^a   Luo, Zhenzhen ^a   Yue, Dongli ^a   Zhang, Zimeng ^b   Wang, Liping ^a   Han, Weidong ^e   Xu, Zhongwei ^f   Chen, Hu ^g   Zhang, Yi ^a,h,i  

^a THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d OHIO STATE UNIVERSITY   (United States)

^e CHINESE PLA GENERAL HOSPITAL   (China)

^f PENNSYLVANIA HOSPITAL   (United States)

^g BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^h Biomass Key Laboratory of Henan Province   (China)

ⁱ ZHENGZHOU UNIVERSITY   (China)

Author keywords

B cell malignancies; CD19; Chimeric antigen receptor; Efficiency; Meta analysis

Indexed keywords

CD19 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; CYCLOPHOSPHAMIDE; FLUDARABINE; INTERLEUKIN 2; PENTOSTATIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CELL COUNT; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL EFFECTIVENESS; FOLLICULAR LYMPHOMA; HUMAN; LARGE CELL LYMPHOMA; LYMPHOMA; MANTLE CELL LYMPHOMA; MARGINAL ZONE LYMPHOMA; META ANALYSIS; PHASE 1 CLINICAL TRIAL (TOPIC); PROGRESSION FREE SURVIVAL; SURVIVAL RATE; SYSTEMATIC REVIEW; T LYMPHOCYTE; TREATMENT RESPONSE; ADOPTIVE IMMUNOTHERAPY; CHEMISTRY; DISEASE FREE SURVIVAL; FEMALE; IMMUNOLOGY; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROCEDURES; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; REGRESSION ANALYSIS; REMISSION; TREATMENT OUTCOME;

ANTIGENS, CD19; CLINICAL TRIALS, PHASE I AS TOPIC; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-2; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOMA; MALE; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; RECEPTORS, ANTIGEN, T-CELL; REGRESSION ANALYSIS; REMISSION INDUCTION; T-LYMPHOCYTES; TREATMENT OUTCOME;

EID: 84946040235     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5582     Document Type: Article

References (42)

1. Maus MV, Grupp SA, Porter DL, June CH. Antibodymodified T cells: CARs take the front seat for hematologic malignancies. Blood. 2014;123:2625-35.
2. Kochenderfer JN, Dudley ME, Carpenter RO, Kassim SH, Rose JJ, Telford WG, Hakim FT, Halverson DC, Fowler DH, Hardy NM, Mato AR, Hickstein DD, GeaBanacloche JC, et al. Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood. 2013;122:4129-39.
3. Cruz CR, Micklethwaite KP, Savoldo B, Ramos CA, Lam S, Ku S, Diouf O, Liu E, Barrett AJ, Ito S, Shpall EJ, Krance RA, Kamble RT, et al. Infusion of donorderived 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.
4. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, Teachey DT, Chew A, Hauck B, Wright JF, Milone MC, Levine BL, June CH. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368:1509-18.
5. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365:725-33.
6. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, June CH. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3:95ra73.
7. Kochenderfer JN, Dudley ME, Kassim SH, Somerville RP, Carpenter RO, Stetler-Stevenson M, Yang JC, Phan GQ, Hughes MS, Sherry RM, Raffeld M, Feldman S, Lu L, et al. 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. J Clin Oncol. 2015;33:540-9.
8. Lee DW, Kochenderfer JN, Stetler-Stevenson M, Cui YK, Delbrook C, Feldman SA, Fry TJ, Orentas R, Sabatino M, Shah NN, Steinberg SM, Stroncek D, Tschernia N, 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.
9. Jensen MC, Popplewell L, Cooper LJ, DiGiusto D, Kalos M, Ostberg JR, Forman SJ. 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 2010;16:1245-56.
10. Brentjens RJ, Riviere I, Park JH, Davila ML, Wang X, Stefanski J, Taylor C, Yeh R, Bartido S, Borquez-Ojeda O, Olszewska M, Bernal Y, Pegram H, et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood. 2011;118:4817-28.
11. Kochenderfer JN, Dudley ME, Feldman SA, Wilson WH, Spaner DE, Maric I, Stetler-Stevenson M, Phan GQ, Hughes MS, Sherry RM, Yang JC, Kammula US, Devillier L, 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. 2012;119:2709-20.
12. Kochenderfer JN, Wilson WH, Janik JE, Dudley ME, Stetler-Stevenson M, Feldman SA, Maric I, Raffeld M, Nathan DA, Lanier BJ, Morgan RA, Rosenberg SA. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood. 2010;116:4099-102.
13. Savoldo B, Ramos CA, Liu E, Mims MP, Keating MJ, Carrum G, Kamble RT, Bollard CM, Gee AP, Mei Z, Liu H, Grilley B, Rooney CM, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest. 2011;121:1822-6.
14. Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, Chew A, Gonzalez VE, Zheng Z, Lacey SF, Mahnke YD, Melenhorst JJ, Rheingold SR, et al. Chimeric Antigen Receptor T Cells for Sustained Remissions in Leukemia. New Engl J Med. 2014;371:1507-17.
15. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, Bartido S, Stefanski J, Taylor C, Olszewska M, Borquez-Ojeda O, Qu J, Wasielewska T, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5:177ra38.
16. Davila ML, Riviere I, Wang X, Bartido S, Park J, Curran K, Chung SS, Stefanski J, Borquez-Ojeda O, Olszewska M, Qu J, Wasielewska T, He Q, 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.
17. Uckun FM, Jaszcz W, Ambrus JL, Fauci AS, Gajl-Peczalska K, Song CW, Wick MR, Myers DE, Waddick K, Ledbetter JA. Detailed studies on expression and function of CD19 surface determinant by using B43 monoclonal antibody and the clinical potential of anti-CD19 immunotoxins. Blood. 1988;71:13-29.
18. Xu XJ, Zhao HZ, Tang YM. Efficacy and safety of adoptive immunotherapy using anti-CD19 chimeric antigen receptor transduced T-cells: a systematic review of phase I clinical trials. Leuk Lymphoma. 2013;54:255-60.
19. Forman SJ, Rowe JM. The myth of the second remission of acute leukemia in the adult. Blood. 2013;121:1077-82.
20. Tam CS, O'Brien S, Plunkett W, Wierda W, Ferrajoli A, Wang X, Do KA, Cortes J, Khouri I, Kantarjian H, Lerner S, Keating MJ. Long-term results of first salvage treatment in CLL patients treated initially with FCR (fludarabine, cyclophosphamide, rituximab). Blood. 2014;124:3059-64.
21. Kater AP, Spiering M, Liu RD, Doreen Te Raa G, Slinger E, Tonino SH, Beckers MM, Daenen S, Doorduijn JK, Lankheet NA, Luijks DM, Eldering E, van Oers MH. Dasatinib in combination with fludarabine in patients with refractory chronic lymphocytic leukemia: a multicenter phase 2 study. Leuk Res. 2014;38:34-41.
22. Christopoulos P, Pfeifer D, Bartholome K, Follo M, Timmer J, Fisch P, Veelken H. Definition and characterization of the systemic T-cell dysregulation in untreated indolent B-cell lymphoma and very early CLL. Blood. 2011;117:3836-46.
23. Riches JC, Gribben JG. Understanding the immunodeficiency in chronic lymphocytic leukemia: potential clinical implications. Hematol Oncol Clin North Am. 2013;27:207-35.
24. Burger JA, Ghia P, Rosenwald A, Caligaris-Cappio F. The microenvironment in mature B-cell malignancies: a target for new treatment strategies. Blood. 2009;114:3367-75.
25. Herishanu Y, Perez-Galan P, Liu D, Biancotto A, Pittaluga S, Vire B, Gibellini F, Njuguna N, Lee E, Stennett L, Raghavachari N, Liu P, McCoy JP, et al. The lymph node microenvironment promotes B-cell receptor signaling, NF-kappaB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood. 2011;117:563-74.
26. Stock W. Adolescents and young adults with acute lymphoblastic leukemia. Hematology Am Soc Hematol Educ Program. 2010;2010:21-9.
27. Kohn DB, Dotti G, Brentjens R, Savoldo B, Jensen M, Cooper LJ, June CH, Rosenberg S, Sadelain M, Heslop HE. CARs on track in the clinic. Mol Ther. 2011;19:432-8.
28. Cui Y, Zhang H, Meadors J, Poon R, Guimond M, Mackall CL. Harnessing the physiology of lymphopenia to support adoptive immunotherapy in lymphoreplete hosts. Blood. 2009;114:3831-40.
29. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer. 2008;8:299-308.
30. Sadelain M, Brentjens R, Rivière I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013;3:388-98.
31. Frauwirth KA, Thompson CB. Activation and inhibition of lymphocytes by costimulation. J Clin Invest. 2002;109:295-9.
32. Dai Z, Arakelov A, Wagener M, Konieczny BT, Lakkis FG. The role of the common cytokine receptor gamma-chain in regulating IL-2-dependent, activation-induced CD8+ T cell death. J Immunol. 1999;163:3131-7.
33. Moroz A, Eppolito C, Li Q, Tao J, Clegg CH, Shrikant PA. IL-21 enhances and sustains CD8+ T cell responses to achieve durable tumor immunity: comparative evaluation of IL-2, IL-15, and IL-21. J Immunol. 2004;173:900-9.
34. Li Y, Kurlander RJ. Comparison of anti-CD3 and antiCD28-coated beads with soluble anti-CD3 for expanding human T cells: differing impact on CD8 T cell phenotype and responsiveness to restimulation. J Transl Med. 2010;8:104.
35. Gargett T, Brown MP. The inducible caspase-9 suicide gene system as a "safety switch" to limit on-target, offtumor toxicities of chimeric antigen receptor T cells. Front Pharmaco. 2014;5:235.
36. Kloss CC, Condomines M, Cartellieri M, Bachmann M, Sadelain M. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat Biotechno. 2013;31:71-5.
37. Wang X, Wong CW, Urak R, Mardiros A, Budde LE, Chang WC, Thomas SH, Brown CE, La Rosa C, Diamond DJ, Jensen MC, Nakamura R, Zaia JA, et al. CMVpp65 vaccine enhances the antitumor efficacy of adoptively transferred CD19-redirected CMV-specific T cells. Clin Cancer Res. 2015; 21:2993-3002
38. Pegram HJ, Lee JC, Hayman EG, Imperato GH, Tedder TF, Sadelain M, Brentjens RJ. Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning. Blood. 2012;119:4133-41.
39. Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol. 2013;13:227-42.
40. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252-64.
41. Higgins JPT, Green S (eds). Cochrane handbook for systematic reviews of interventions, 5th edn. The Cochrane Collaboration, 2011.
42. Victoria N, Marc A, Marc A. Metaprop: a Stata command to perform meta-analysis of binomial data. Archives of Public Health. 2014;72:39.