Clinical and immunological responses after CD30-specific chimeric antigen receptor-redirected lymphocytes

Journal of Clinical Investigation

Volumn 127, Issue 9, 2017, Pages 3462-3471

  Ramos, Carlos A ^a,b   Ballard, Brandon ^a   Zhang, Huimin ^a   Dakhova, Olga ^a   Gee, Adrian P ^a   Mei, Zhuyong ^a   Bilgi, Mrinalini ^a   Wu, Meng Fen ^c   Liu, Hao ^b,c   Grilley, Bambi ^a,d   Bollard, Catherine M ^a,b,d   Chang, Bill H ^e   Rooney, Cliona M ^a,f   Brenner, Malcolm K ^a,b,d   Heslop, Helen E ^a,b,d   Dotti, Gianpietro ^a,b   Savoldo, Barbara ^a,d  

^a CENTER FOR CELL AND GENE THERAPY   (United States)

^b Department of Medicine ^*  (United States)

^c Dan L Duncan Cancer Center   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^f BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRENTUXIMAB VEDOTIN; CD30 ANTIGEN; CELL THERAPY AGENT; CHIMERIC ANTIGEN RECEPTOR; RETROVIRUS VECTOR; ANTIBODY CONJUGATE; ANTINEOPLASTIC AGENT; CD28 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADULT; AGED; ANAPLASTIC LARGE CELL LYMPHOMA; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOTRANSPLANTATION; CANCER RECURRENCE; CELL THERAPY; CLINICAL ARTICLE; CLINICAL EFFECTIVENESS; CLINICAL OUTCOME; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DIFFUSE LARGE B CELL LYMPHOMA; DISEASE COURSE; FEASIBILITY STUDY; FEMALE; HODGKIN DISEASE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MALE; MIDDLE AGED; PATIENT SAFETY; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; T LYMPHOCYTE; TREATMENT OUTCOME; TREATMENT RESPONSE; CHEMISTRY; CLINICAL TRIAL; CYTOLOGY; DOSE RESPONSE; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOMA, LARGE-CELL, ANAPLASTIC; METABOLISM; MOLECULARLY TARGETED THERAPY; TRANSPLANTATION CONDITIONING; TUMOR RECURRENCE; YOUNG ADULT;

ADULT; ANTIGENS, CD28; ANTIGENS, CD30; ANTINEOPLASTIC AGENTS; DISEASE PROGRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HODGKIN DISEASE; HUMANS; IMMUNOCONJUGATES; IMMUNOPHENOTYPING; LYMPHOMA, LARGE-CELL, ANAPLASTIC; MALE; MIDDLE AGED; MOLECULAR TARGETED THERAPY; NEOPLASM RECURRENCE, LOCAL; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TRANSPLANTATION CONDITIONING; TREATMENT OUTCOME; YOUNG ADULT;

EID: 85028909387     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI94306     Document Type: Article

References (43)

1. Dotti G, Gottschalk S, Savoldo B, Brenner MK. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev. 2014;257(1):107-126.
2. Maude SL, Teachey DT, Porter DL, Grupp SA. CD19-targeted chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Blood. 2015;125(26):4017-4023.
3. Kochenderfer JN, 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(6):540-549.
4. Lee DW, 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(9967):517-528.
5. Brentjens RJ, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5(177):177ra38.
6. Turtle CJ, et al. Immunotherapy of non-Hodgkin's lymphoma with a defined ratio of CD8+ and CD4+ CD19-specific chimeric antigen receptor-modified T cells. Sci Transl Med. 2016;8(355):355ra116.
7. Savoldo B, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest. 2011;121(5):1822-1826.
8. Ramos CA, et al. Clinical responses with T lymphocytes targeting malignancy-associated κ light chains. J Clin Invest. 2016;126(7):2588-2596.
9. Porter DL, et al. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med. 2015;7(303):303ra139.
10. Wang X, et al. Phase 1 studies of central memory-derived CD19 CAR T-cell therapy following autologous HSCT in patients with B-cell NHL. Blood. 2016;127(24):2980-2990.
11. Maude SL, Barrett D, Teachey DT, Grupp SA. Managing cytokine release syndrome associated with novel T cell-engaging therapies. Cancer J. 2014;20(2):119-122.
12. Lee DW, et al. Current concepts in the diagnosis and management of cytokine release syndrome. Blood. 2014;124(2):188-195.
13. Davila ML, et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med. 2014;6(224):224ra25.
14. Falini B, et al. CD30 (Ki-1) molecule: a new cytokine receptor of the tumor necrosis factor receptor superfamily as a tool for diagnosis and immunotherapy. Blood. 1995;85(1):1-14.
15. Younes A, Ansell SM. Novel agents in the treatment of Hodgkin lymphoma: Biological basis and clinical results. Semin Hematol. 2016;53(3):186-189.
16. Forero-Torres A, et al. A phase II study of SGN-30(anti-CD30 mAb) in Hodgkin lymphoma or systemic anaplastic large cell lymphoma. Br J Haematol. 2009;146(2):171-179.
17. Younes A, et al. Brentuximab vedotin (SGN-35) for relapsed CD30-positive lymphomas. N Engl J Med. 2010;363(19):1812-1821.
18. Moskowitz CH, et al. Brentuximab vedotin as consolidation therapy after autologous stemcell transplantation in patients with Hodgkin's lymphoma at risk of relapse or progression (AETHERA): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2015;385(9980):1853-1862.
19. Bollard CM, et al. Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin's disease. J Exp Med. 2004;200(12):1623-1633.
20. Bollard CM, et al. Sustained complete responses in patients with lymphoma receiving autologous cytotoxic T lymphocytes targeting Epstein-Barr virus latent membrane proteins. J Clin Oncol. 2014;32(8):798-808.
21. Roskrow MA, et al. Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes for the treatment of patients with EBV-positive relapsed Hodgkin's disease. Blood. 1998;91(8):2925-2934.
22. Younes A, et al. Nivolumab for classical Hodgkin's lymphoma after failure of both autologous stem-cell transplantation and brentuximab vedotin: a multicentre, multicohort, single-arm phase 2 trial. Lancet Oncol. 2016;17(9):1283-1294.
23. Ansell SM, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med. 2015;372(4):311-319.
24. Armand P, et al. Programmed death-1 blockade with pembrolizumab in patients with classical hodgkin lymphoma after brentuximab vedotin failure. J Clin Oncol. 2016;34(31):3733-3739.
25. Wang CM, et al. Autologous T cells expressing CD30 chimeric antigen receptors for relapsed or refractory Hodgkin lymphoma: an open-label phase I trial. Clin Cancer Res. 2017;23(5):1156-1166.
26. Savoldo B, et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30ζ artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood. 2007;110(7):2620-2630.
27. Di Stasi A, et al. T lymphocytes coexpressing CCR4 and a chimeric antigen receptor targeting CD30 have improved homing and antitumor activity in a Hodgkin tumor model. Blood. 2009;113(25):6392-6402.
28. Croft M. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat Rev Immunol. 2003;3(8):609-620.
29. Arber C, et al. The immunogenicity of virusderived 2A sequences in immunocompetent individuals. Gene Ther. 2013;20(9):958-962.
30. Zanotti R, et al. Serum levels of soluble CD30 improve International Prognostic Score in predicting the outcome of advanced Hodgkin's lymphoma. Ann Oncol. 2002;13(12):1908-1914.
31. Hombach A, et al. An anti-CD30 chimeric receptor that mediates CD3-zeta-independent T-cell activation against Hodgkin's lymphoma cells in the presence of soluble CD30. Cancer Res. 1998;58(6):1116-1119.
32. Aldinucci D, Gloghini A, Pinto A, De Filippi R, Carbone A. The classical Hodgkin's lymphoma microenvironment and its role in promoting tumour growth and immune escape. J Pathol. 2010;221(3):248-263.
33. Turtle CJ, et al. CD19 CAR-T cells of defined CD4+:CD8+ composition in adult B cell ALL patients. J Clin Invest. 2016;126(6):2123-2138.
34. Maude SL, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16):1507-1517.
35. Kochenderfer JN, et al. B-cell depletion and remissions of malignancy along with cytokineassociated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood. 2012;119(12):2709-2720.
36. Klebanoff CA, Khong HT, Antony PA, Palmer DC, Restifo NP. Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends Immunol. 2005;26(2):111-117.
37. Slivnick DJ, Ellis TM, Nawrocki JF, Fisher RI. The impact of Hodgkin's disease on the immune system. Semin Oncol. 1990;17(6):673-682.
38. Bollard CM, et al. Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. Blood. 2007;110(8):2838-2845.
39. Jensen MC, et al. 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(9):1245-1256.
40. Hudecek M, et al. The nonsignaling extracellular spacer domain of chimeric antigen receptors is decisive for in vivo antitumor activity. Cancer Immunol Res. 2015;3(2):125-135.
41. Reichel J, et al. Flow sorting and exome sequencing reveal the oncogenome of primary Hodgkin and Reed-Sternberg cells. Blood. 2015;125(7):1061-1072.
42. Cheson BD, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007;25(5):579-586.
43. Xu Y, et al. Closely related T-memory stem cells correlate with in vivo expansion of CAR.CD19-T cells and are preserved by IL-7 and IL-15. Blood. 2014;123(24):3750-3759.