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

Volumn 122, Issue 17, 2013, Pages 2956-2973

  Cruz, Conrad Russell Y ^a   Micklethwaite, Kenneth P ^a   Savoldo, Barbara ^a   Ramos, Carlos A ^a   Lam, Sharon ^a   Ku, Stephanie ^a   Diouf, Oumar ^a   Liu, Enli ^a   Barrett, A John ^b   Ito, Sawa ^b   Shpall, Elizabeth J ^c   Krance, Robert A ^a,d   Kamble, Rammurti T ^a,d   Carrum, George ^a,d   Hosing, Chitra M ^c   Gee, Adrian P ^a   Mei, Zhuyong ^a   Grilley, Bambi J ^a   Heslop, Helen E ^a,d   Rooney, Cliona M ^a   Brenner, Malcolm K ^a,d   Bollard, Catherine M ^a,d   Dotti, Gianpietro ^a   more..

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

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

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

^d HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 SPECIFIC CHIMERIC ANTIGEN RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 6; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CD19 ANTIGEN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADULT; ALLOGENEIC STEM CELL TRANSPLANTATION; ANTINEOPLASTIC ACTIVITY; AREA UNDER THE CURVE; ARTICLE; B CELL LEUKEMIA; CANCER CHEMOTHERAPY; CANCER REGRESSION; CHILD; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHADENOPATHY; MALE; OUTCOME ASSESSMENT; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; T LYMPHOCYTE; TREATMENT RESPONSE; VIREMIA; VIRUS LOAD; VIRUS REACTIVATION; VIRUS SPECIFIC T LYMPHOCYTE; ADENOVIRIDAE; ALLOTRANSPLANTATION; B LYMPHOCYTE; CLINICAL TRIAL; CYTOMEGALOVIRUS; EPSTEIN BARR VIRUS; GENE EXPRESSION; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MIDDLE AGED; PATHOLOGY; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN ENGINEERING; RECURRENT DISEASE; TRANSPLANTATION; VIROLOGY;

ADENOVIRIDAE; ADULT; ANTIGENS, CD19; ANTINEOPLASTIC AGENTS; B-LYMPHOCYTES; CHILD; CYTOMEGALOVIRUS; FEMALE; GENE EXPRESSION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HERPESVIRUS 4, HUMAN; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MIDDLE AGED; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN ENGINEERING; RECURRENCE; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 84887821770     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-06-506741     Document Type: Article

References (40)

1. Martin TG, Gajewski JL. Allogeneic stem cell transplantation for acute lymphocytic leukemia in adults. Hematol Oncol Clin North Am. 2001;15(1):97-120.
2. Kumar P, Defor TE, Brunstein C, et al. Allogeneic hematopoietic stem cell transplantation in adult acute lymphocytic leukemia: impact of donor source on survival. Biol Blood Marrow Transplant. 2008;14(12):1394-1400.
3. Aricò M, Valsecchi MG, Camitta B, et al. Outcome of treatment in children with Philadelphia chromosome-positive acute lymphoblastic leukemia. N Engl J Med. 2000;342(14):998-1006.
4. Tomblyn M, Chiller T, Einsele H, et al; Center for International Blood and Marrow Research; National Marrow Donor program; European Blood and MarrowTransplant Group; American Society of Blood and Marrow Transplantation; Canadian Blood and Marrow Transplant Group; Infectious Diseases Society of America; Society for Healthcare Epidemiology of America; Association of Medical Microbiology and Infectious Disease Canada; Centers for Disease Control and Prevention. Guidelines for preventing infectious complications among hematopoietic cell transplantation recipients: a global perspective. Biol Blood Marrow Transpl. 2009;15(10):1143-1238.
5. Wingard JR, Hsu J, Hiemenz JW. Hematopoietic stem cell transplantation: an overview of infection risks and epidemiology. Hematol Oncol Clin North Am. 2011;25(1):101-116.
6. Forman SJ, Rowe JM. The myth of the second remission of acute leukemia in the adult. Blood. 2013;121(7):1077-1082.
7. Doubrovina E, Oflaz-Sozmen B, Prockop SE, et al. Adoptive immunotherapy with unselected or EBV-specific T cells for biopsy-proven EBV1 lymphomas after allogeneic hematopoietic cell transplantation. Blood. 2012;119(11):2644-2656.
8. Frey NV, Porter DL. Graft-versus-host disease after donor leukocyte infusions: presentation and management. Best Pract Res Clin Haematol. 2008;21(2):205-222.
9. Tallen G, Ratei R, Mann G, et al. Long-term outcome in children with relapsed acute lymphoblastic leukemia after time-point and siteof-relapse stratification and intensified shortcourse multidrug chemotherapy: results of trial ALL-REZ BFM 90. J Clin Oncol. 2010;28(14):2339-2347.
10. Ringdén O, Pavletic SZ, Anasetti C, et al. The graft-versus-leukemia effect using matched unrelated donors is not superior to HLA-identical siblings for hematopoietic stem cell transplantation. Blood. 2009;113(13):3110-3118.
11. Rooney CM, Smith CA, Ng CY, et al. Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood. 1998;92(5):1549-1555.
12. Peggs KS, Verfuerth S, Pizzey A, et al. Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet. 2003;362(9393):1375-1377.
13. Leen AM, Myers GD, Sili U, et al. Monoculturederived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat Med. 2006;12(10):1160-1166.
14. Heslop HE, Slobod KS, Pule MA, et al. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood. 2010;115(5):925-935.
15. Warren EH, Fujii N, Akatsuka Y, et al. Therapy of relapsed leukemia after allogeneic hematopoietic cell transplantation with T cells specific for minor histocompatibility antigens. Blood. 2010;115(19):3869-3878.
16. 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. 2011;3(95):95ra73.
17. Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368(16):1509-1518.
18. 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(177):177ra138.
19. Kochenderfer JN, Yu Z, Frasheri D, Restifo NP, Rosenberg SA. Adoptive transfer of syngeneic T cells transduced with a chimeric antigen receptor that recognizes murine CD19 can eradicate lymphoma and normal B cells. Blood. 2010;116(19):3875-3886.
20. 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. 2011;121(5):1822-1826.
21. Micklethwaite KP, Savoldo B, Hanley PJ, et al. Derivation of human T lymphocytes from cord blood and peripheral blood with antiviral and antileukemic specificity from a single culture as protection against infection and relapse after stem cell transplantation. Blood. 2010;115(13):2695-2703.
22. Smith CA, Ng CY, Heslop HE, et al. Production of genetically modified Epstein-Barr virus-specific cytotoxic T cells for adoptive transfer to patients at high risk of EBV-associated lymphoproliferative disease. J Hematother. 1995;4(2):73-79.
23. Schade AE, Schieven GL, Townsend R, et al. Dasatinib, a small-molecule protein tyrosine kinase inhibitor, inhibits T-cell activation and proliferation. Blood. 2008;111(3):1366-1377.
24. Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med. 2011;365(18):1673-1683.
25. Cwynarski K, Ainsworth J, Cobbold M, et al. Direct visualization of cytomegalovirus-specific T-cell reconstitution after allogeneic stem cell transplantation. Blood. 2001;97(5):1232-1240.
26. Myers GD, Bollard CM, Wu MF, et al. Reconstitution of adenovirus-specific cellmediated immunity in pediatric patients after hematopoietic stem cell transplantation. Bone Marrow Transplant. 2007;39(11):677-686.
27. 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. 2011;118(18):4817-4828.
28. 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. 2010;116(20):4099-4102.
29. Till BG, Jensen MC, Wang J, et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood. 2008;112(6):2261-2271.
30. Melenhorst JJ, Leen AM, Bollard CM, et al. Allogeneic virus-specific T cells with HLA alloreactivity do not produce GVHD in human subjects. Blood. 2010;116(22):4700-4702.
31. Pule MA, Savoldo B, Myers GD, et al. Virusspecific T cells engineered to coexpress tumorspecific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med. 2008;14(11):1264-1270.
32. Rossig C, Bollard CM, Nuchtern JG, Rooney CM, Brenner MK. Epstein-Barr virus-specific human T lymphocytes expressing antitumor chimeric T-cell receptors: potential for improved immunotherapy. Blood. 2002;99(6):2009-2016.
33. Savoldo B, Rooney CM, Di Stasi A, et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood. 2007;110(7):2620-2630.
34. Guerrero A, Riddell SR, Storek J, et al. Cytomegalovirus viral load and virus-specific immune reconstitution after peripheral blood stem cell versus bone marrow transplantation. Biol Blood Marrow Transplant. 2012;18(1):66-75.
35. Guimond M, Fry TJ, Mackall CL. Cytokine signals in T-cell homeostasis. J Immunother. 2005;28(4):289-294.
36. Gerdemann U, Keirnan JM, Katari UL, et al. Rapidly generated multivirus-specific cytotoxic T lymphocytes for the prophylaxis and treatment of viral infections. Mol Ther. 2012;20(8):1622-1632.
37. Louis CU, Savoldo B, Dotti G, et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood. 2011;118(23):6050-6056.
38. Savoldo B, Goss JA, Hammer MM, et al. Treatment of solid organ transplant recipients with autologous Epstein Barr virus-specific cytotoxic T lymphocytes (CTLs). Blood. 2006;108(9):2942-2949.
39. Roback JD. Vaccine-enhanced donor lymphocyte infusion (veDLI). Hematology (Am Soc Hematol Educ Program). 2006;486-491, 513.
40. Petsch B, Schnee M, Vogel AB, et al. Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nat Biotechnol. 2012;30(12):1210-1216.