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Expert Opinion on Biological Therapy Volume 9, 2009 - Issue 11
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Reviews

Treatment of lymphoma with adoptively transferred T cells

Brian G Till Research Associate, Acting Instructor, University of Washington, Fred Hutchinson Cancer Research Center, Department of Medicine, 1100 Fairview Ave. N, D3-190, Seattle, WA 98109, USA +1 206 667 7269; +1 206 667 1874; [email protected]
, MD &
Oliver W Press Professor, Member, University of Washington, Fred Hutchinson Cancer Research Center, Department of Medicine, Seattle, WA 98109, USA
, MD PhD
Pages 1407-1425 | Published online: 02 Sep 2009

Bibliography

  • Weiden PL, Flournoy N, Thomas ED, Antileukemic effect of graft-versus-host disease in human recipients of allogeneic-marrow grafts. N Engl J Med 1979;300:1068-73
  • Porter DL, Antin JH. The graft-versus-leukemia effects of allogeneic cell therapy. Annu Rev Med 1999;50:369-86
  • Khouri IF, McLaughlin P, Saliba RM, Eight-year experience with allogeneic stem cell transplantation for relapsed follicular lymphoma after nonmyeloablative conditioning with fludarabine, cyclophosphamide, and rituximab. Blood 2008;111:5530-6
  • Sorror ML, Storer B, Sandmaier BM, Sustained graft-versus-lymphoma effect among patients (pts) with Mantle Cell Lymphoma (MCL) given nonmyeloablative allogeneic Hematopoietic Cell Transplantation (HCT). Blood 2008;112: Abstract 2147
  • Bishop MR, Dean RM, Steinberg SM, Clinical evidence of a graft-versus-lymphoma effect against relapsed diffuse large B-cell lymphoma after allogeneic hematopoietic stem-cell transplantation. Ann Oncol 2008;19:1935-40
  • Mandigers CM, Verdonck LF, Meijerink JP, Graft-versus-lymphoma effect of donor lymphocyte infusion in indolent lymphomas relapsed after allogeneic stem cell transplantation. Bone Marrow Transplant 2003;32:1159-63
  • Marks DI, Lush R, Cavenagh J, The toxicity and efficacy of donor lymphocyte infusions given after reduced-intensity conditioning allogeneic stem cell transplantation. Blood 2002;100:3108-14
  • van Besien KW, de Lima M, Giralt SA, Management of lymphoma recurrence after allogeneic transplantation: the relevance of graft-versus-lymphoma effect. Bone Marrow Transplant 1997;19:977-82
  • Papadopoulos EB, Ladanyi M, Emanuel D, Infusions of donor leukocytes to treat Epstein-Barr virus-associated lymphoproliferative disorders after allogeneic bone marrow transplantation. N Engl J Med 1994;330:1185-91
  • Rezvani AR, Storer B, Maris M, Nonmyeloablative allogeneic hematopoietic cell transplantation in relapsed, refractory, and transformed indolent non-Hodgkin's lymphoma. J Clin Oncol 2008;26:211-7
  • Khanna R, Burrows SR, Moss DJ. Immune regulation in Epstein-Barr virus-associated diseases. Microbiol Rev 1995;59:387-405
  • Riddell SR, Rabin M, Geballe AP, Class I MHC-restricted cytotoxic T lymphocyte recognition of cells infected with human cytomegalovirus does not require endogenous viral gene expression. J Immunol 1991;146:2795-804
  • Riddell SR, Watanabe KS, Goodrich JM, Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 1992;257:238-41
  • Walter EA, Greenberg PD, Gilbert MJ, Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N Engl J Med 1995;333:1038-44
  • Heslop HE, Brenner MK, Rooney C, Administration of neomycin-resistance-gene-marked EBV-specific cytotoxic T lymphocytes to recipients of mismatched-related or phenotypically similar unrelated donor marrow grafts. Hum Gene Ther 1994;5:381-97
  • Rooney CM, Smith CA, Ng CY, Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 1995;345:9-13
  • Gottschalk S, Ng CY, Perez M, An Epstein-Barr virus deletion mutant associated with fatal lymphoproliferative disease unresponsive to therapy with virus-specific CTLs. Blood 2001;97:835-43
  • Heslop HE, Ng CY, Li C, Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat Med 1996;2:551-5
  • Berger C, Jensen MC, Lansdorp PM, Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest 2008;118:294-305
  • Gottschalk S, Rooney CM, Heslop HE. Post-transplant lymphoproliferative disorders. Annu Rev Med 2005;56:29-44
  • Gustafsson A, Levitsky V, Zou JZ, Epstein-Barr virus (EBV) load in bone marrow transplant recipients at risk to develop posttransplant lymphoproliferative disease: prophylactic infusion of EBV-specific cytotoxic T cells. Blood 2000;95:807-14
  • Khanna R, Bell S, Sherritt M, Activation and adoptive transfer of Epstein-Barr virus-specific cytotoxic T cells in solid organ transplant patients with posttransplant lymphoproliferative disease. Proc Natl Acad Sci USA 1999;96:10391-6
  • Haque T, Amlot PL, Helling N, Reconstitution of EBV-specific T cell immunity in solid organ transplant recipients. J Immunol 1998;160:6204-9
  • Comoli P, Labirio M, Basso S, Infusion of autologous Epstein-Barr virus (EBV)-specific cytotoxic T cells for prevention of EBV-related lymphoproliferative disorder in solid organ transplant recipients with evidence of active virus replication. Blood 2002;99:2592-8
  • Savoldo B, Goss JA, Hammer MM, Treatment of solid organ transplant recipients with autologous Epstein Barr virus-specific cytotoxic T lymphocytes (CTLs). Blood 2006;108:2942-9
  • Sherritt MA, Bharadwaj M, Burrows JM, Reconstitution of the latent T-lymphocyte response to Epstein-Barr virus is coincident with long-term recovery from posttransplant lymphoma after adoptive immunotherapy. Transplantation 2003;75:1556-60
  • Haque T, Taylor C, Wilkie GM, Complete regression of posttransplant lymphoproliferative disease using partially HLA-matched Epstein Barr virus-specific cytotoxic T cells. Transplantation 2001;72:1399-402
  • Orentas RJ, Lemas MV, Mullin MJ, Feasibility of cellular adoptive immunotherapy for Epstein-Barr virus-associated lymphomas using haploidentical donors. J Hematother 1998;7:257-61
  • Sun Q, Burton R, Reddy V, Lucas KG. Safety of allogeneic Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes for patients with refractory EBV-related lymphoma. Br J Haematol 2002;118:799-808
  • Wilkie GM, Taylor C, Jones MM, Establishment and characterization of a bank of cytotoxic T lymphocytes for immunotherapy of epstein-barr virus-associated diseases. J Immunother 2004;27:309-16
  • Haque T, Wilkie GM, Taylor C, Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 2002;360:436-42
  • Haque T, Wilkie GM, Jones MM, Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood 2007;110:1123-31
  • Gandhi MK, Wilkie GM, Dua U, Immunity, homing and efficacy of allogeneic adoptive immunotherapy for posttransplant lymphoproliferative disorders. Am J Transplant 2007;7:1293-9
  • Herbst H, Niedobitek G, Kneba M, High incidence of Epstein-Barr virus genomes in Hodgkin's disease. Am J Pathol 1990;137:13-8
  • Lacroix A, Jaccard A, Rouzioux C, HHV-6 and EBV DNA quantitation in lymph nodes of 86 patients with Hodgkin's lymphoma. J Med Virol 2007;79:1349-56
  • Valente G, Secchiero P, Lusso P, Human herpesvirus 6 and Epstein-Barr virus in Hodgkin's disease: a controlled study by polymerase chain reaction and in situ hybridization. Am J Pathol 1996;149:1501-10
  • Bollard CM, Cooper LJ, Heslop HE. Immunotherapy targeting EBV-expressing lymphoproliferative diseases. Best Pract Res Clin Haematol 2008;21:405-20
  • Bollard CM, Aguilar L, Straathof KC, Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin's disease. J Exp Med 2004;200:1623-33
  • Gahn B, Siller-Lopez F, Pirooz AD, Adenoviral gene transfer into dendritic cells efficiently amplifies the immune response to LMP2A antigen: a potential treatment strategy for Epstein-Barr virus–positive Hodgkin's lymphoma. Int J Cancer 2001;93:706-13
  • Sing AP, Ambinder RF, Hong DJ, Isolation of Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes that lyse Reed-Sternberg cells: implications for immune-mediated therapy of EBV+ Hodgkin's disease. Blood 1997;89:1978-86
  • Su Z, Peluso MV, Raffegerst SH, The generation of LMP2a-specific cytotoxic T lymphocytes for the treatment of patients with Epstein-Barr virus-positive Hodgkin disease. Eur J Immunol 2001;31:947-58
  • Bollard CM, Gottschalk S, Leen AM, Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. Blood 2007;110:2838-45
  • Jurgens LA, Khanna R, Weber J, Orentas RJ. Transduction of primary lymphocytes with Epstein-Barr virus (EBV) latent membrane protein-specific T-cell receptor induces lysis of virus-infected cells: a novel strategy for the treatment of Hodgkin's disease and nasopharyngeal carcinoma. J Clin Immunol 2006;26:22-32
  • Orentas RJ, Roskopf SJ, Nolan GP, Nishimura MI. Retroviral transduction of a T cell receptor specific for an Epstein-Barr virus-encoded peptide. Clin Immunol 2001;98:220-8
  • Morgan RA, Dudley ME, Wunderlich JR, Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006;314:126-9
  • Uckert W, Schumacher TN. TCR transgenes and transgene cassettes for TCR gene therapy: status in 2008. Cancer Immunol Immunother 2009;58:809-22
  • Becker ML, Near R, Mudgett-Hunter M, Expression of a hybrid immunoglobulin-T cell receptor protein in transgenic mice. Cell 1989;58:911-21
  • Goverman J, Gomez SM, Segesman KD, Chimeric immunoglobulin-T cell receptor proteins form functional receptors: implications for T cell receptor complex formation and activation. Cell 1990;60:929-39
  • Gross G, Waks T, Eshhar Z. Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci USA 1989;86:10024-8
  • Kuwana Y, Asakura Y, Utsunomiya N, Expression of chimeric receptor composed of immunoglobulin-derived V regions and T-cell receptor-derived C regions. Biochem Biophys Res Commun 1987;149:960-8
  • Bird RE, Hardman KD, Jacobson JW, Single-chain antigen-binding proteins. Science 1988;242:423-6
  • Eshhar Z, Waks T, Gross G, Schindler DG. 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 USA 1993;90:720-4
  • Irving BA, Weiss A. The cytoplasmic domain of the T cell receptor zeta chain is sufficient to couple to receptor-associated signal transduction pathways. Cell 1991;64:891-901
  • Altenschmidt U, Kahl R, Moritz D, Cytolysis of tumor cells expressing the Neu/erbB-2, erbB-3, and erbB-4 receptors by genetically targeted naive T lymphocytes. Clin Cancer Res 1996;2:1001-8
  • Kahlon KS, Brown C, Cooper LJ, Specific recognition and killing of glioblastoma multiforme by interleukin 13-zetakine redirected cytolytic T cells. Cancer Res 2004;64:9160-6
  • Haynes NM, Snook MB, Trapani JA, Redirecting mouse CTL against colon carcinoma: superior signaling efficacy of single-chain variable domain chimeras containing TCR-zeta vs Fc epsilon RI-gamma. J Immunol 2001;166:182-7
  • Hwu P, Shafer GE, Treisman J, Lysis of ovarian cancer cells by human lymphocytes redirected with a chimeric gene composed of an antibody variable region and the Fc receptor gamma chain. J Exp Med 1993;178:361-6
  • Hwu P, Yang JC, Cowherd R, In vivo antitumor activity of T cells redirected with chimeric antibody/T-cell receptor genes. Cancer Res 1995;55:3369-73
  • Altenschmidt U, Klundt E, Groner B. Adoptive transfer of in vitro-targeted, activated T lymphocytes results in total tumor regression. J Immunol 1997;159:5509-15
  • Haynes NM, Trapani JA, Teng MW, Single-chain antigen recognition receptors that costimulate potent rejection of established experimental tumors. Blood 2002;100:3155-63
  • Stancovski I, Schindler DG, Waks T, Targeting of T lymphocytes to Neu/HER2-expressing cells using chimeric single chain Fv receptors. J Immunol 1993;151:6577-82
  • Darcy PK, Kershaw MH, Trapani JA, Smyth MJ. Expression in cytotoxic T lymphocytes of a single-chain anti-carcinoembryonic antigen antibody. Redirected Fas ligand-mediated lysis of colon carcinoma. Eur J Immunol 1998;28:1663-72
  • Haynes NM, Trapani JA, Teng MW, Rejection of syngeneic colon carcinoma by CTLs expressing single-chain antibody receptors codelivering CD28 costimulation. J Immunol 2002;169:5780-6
  • Hombach A, Koch D, Sircar R, A chimeric receptor that selectively targets membrane-bound carcinoembryonic antigen (mCEA) in the presence of soluble CEA. Gene Ther 1999;6:300-4
  • Lamers CH, Langeveld SC, Groot-van Ruijven CM, Gene-modified T cells for adoptive immunotherapy of renal cell cancer maintain transgene-specific immune functions in vivo. Cancer Immunol Immunother 2007;56:1875-83
  • Lamers CH, Sleijfer S, Vulto AG, Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J Clin Oncol 2006;24:e20-2
  • Clay TM, Custer MC, Sachs J, Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J Immunol 1999;163:507-13
  • Willemsen RA, Weijtens ME, Ronteltap C, Grafting primary human T lymphocytes with cancer-specific chimeric single chain and two chain TCR. Gene Ther 2000;7:1369-77
  • Maher J, Brentjens RJ, Gunset G, Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta /CD28 receptor. Nat Biotechnol 2002;20:70-5
  • Ma Q, Safar M, Holmes E, Anti-prostate specific membrane antigen designer T cells for prostate cancer therapy. Prostate 2004;61:12-25
  • Gonzalez S, Naranjo A, Serrano LM, Genetic engineering of cytolytic T lymphocytes for adoptive T-cell therapy of neuroblastoma. J Gene Med 2004;6:704-11
  • Krause A, Guo HF, Latouche JB, Antigen-dependent CD28 signaling selectively enhances survival and proliferation in genetically modified activated human primary T lymphocytes. J Exp Med 1998;188:619-26
  • Rossig C, Bollard CM, Nuchtern JG, Targeting of G(D2)-positive tumor cells by human T lymphocytes engineered to express chimeric T-cell receptor genes. Int J Cancer 2001;94:228-36
  • Finney HM, Lawson AD, Bebbington CR, Weir AN. Chimeric receptors providing both primary and costimulatory signaling in T cells from a single gene product. J Immunol 1998;161:2791-7
  • Press OW, Farr AG, Borroz KI, Endocytosis and degradation of monoclonal antibodies targeting human B-cell malignancies. Cancer Res 1989;49:4906-12
  • Press OW, Howell-Clark J, Anderson S, Bernstein I. Retention of B-cell-specific monoclonal antibodies by human lymphoma cells. Blood 1994;83:1390-7
  • Maloney DG, Davis T, Levy R. In reply (letter). J Clin Oncol 1998;16:1636-37
  • McLaughlin P, Grillo-Lopez AJ, Link BK, Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program. J Clin Oncol 1998;16:2825-33
  • Hainsworth JD, Litchy S, Burris HA, Rituximab as first-line and maintenance therapy for patients with indolent non-Hodgkin's lymphoma. J Clin Oncol 2002;20:4261-7
  • Solal-Celigny P. Rituximab as first-line monotherapy in low-grade follicular lymphoma with a low tumor burden. Anticancer Drugs 2001;12(Suppl 2):S11-4
  • Czuczman MS, Weaver R, Alkuzweny B, Prolonged clinical and molecular remission in patients with low-grade or follicular non-hodgkin's lymphoma treated with rituximab plus CHOP chemotherapy: 9-year follow-up. J Clin Oncol 2004;22:4711-6
  • Hiddemann W, Kneba M, Dreyling M, Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group. Blood 2005;106:3725-32
  • Marcus R, Imrie K, Solal-Celigny P, Phase III study of R-CVP compared with cyclophosphamide, vincristine, and prednisone alone in patients with previously untreated advanced follicular lymphoma. J Clin Oncol 2008;26:4579-86
  • Gopal AK, Rajendran JG, Gooley TA, High-dose [131I]tositumomab (anti-CD20) radioimmunotherapy and autologous hematopoietic stem-cell transplantation for adults > or = 60 years old with relapsed or refractory B-cell lymphoma. J Clin Oncol 2007;25:1396-402
  • Kaminski MS, Tuck M, Estes J, 131I-tositumomab therapy as initial treatment for follicular lymphoma. N Engl J Med 2005;352:441-9
  • Witzig TE, White CA, Wiseman GA, Phase I/II trial of IDEC-Y2B8 radioimmunotherapy for treatment of relapsed or refractory CD20(+) B-cell non-Hodgkin's lymphoma. J Clin Oncol 1999;17:3793-803
  • Jensen M, Tan G, Forman S, CD20 is a molecular target for scFvFc:zeta receptor redirected T cells: implications for cellular immunotherapy of CD20+ malignancy. Biol Blood Marrow Transplant 1998;4:75-83
  • Jensen MC, Clarke P, Tan G, Human T lymphocyte genetic modification with naked DNA. Mol Ther 2000;1:49-55
  • Jensen MC, Cooper LJ, Wu AM, Engineered CD20-specific primary human cytotoxic T lymphocytes for targeting B-cell malignancy. Cytotherapy 2003;5:131-8
  • Wang J, Press OW, Lindgren CG, Cellular immunotherapy for follicular lymphoma using genetically modified CD20-specific CD8+ cytotoxic T lymphocytes. Mol Ther 2004;9:577-86
  • Brentjens RJ, Latouche JB, Santos E, Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat Med 2003;9:279-86
  • Cheadle EJ, Gilham DE, Thistlethwaite FC, Killing of non-Hodgkin lymphoma cells by autologous CD19 engineered T cells. Br J Haematol 2005;129:322-32
  • Cooper LJ, Al-Kadhimi Z, DiGiusto D, Development and application of CD19-specific T cells for adoptive immunotherapy of B cell malignancies. Blood Cells Mol Dis 2004;33:83-9
  • Vera J, Savoldo B, Vigouroux S, T lymphocytes redirected against the kappa light chain of human immunoglobulin efficiently kill mature B lymphocyte-derived malignant cells. Blood 2006;108:3890-7
  • James SE, Greenberg PD, Jensen MC, Antigen sensitivity of CD22-specific chimeric TCR is modulated by target epitope distance from the cell membrane. J Immunol 2008;180:7028-38
  • Hombach A, Heuser C, Sircar R, 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;58:1116-9
  • Hombach A, Heuser C, Sircar R, Characterization of a chimeric T-cell receptor with specificity for the Hodgkin's lymphoma-associated CD30 antigen. J Immunother 1999;22:473-80
  • Savoldo B, Rooney CM, Di Stasi A, Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 2007;110:2620-30
  • Till BG, Jensen MC, Wang J, Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood 2008;112:2261-71
  • Berger C, Flowers ME, Warren EH, Riddell SR. Analysis of transgene-specific immune responses that limit the in vivo persistence of adoptively transferred HSV-TK-modified donor T cells after allogeneic hematopoietic cell transplantation. Blood 2006;107:2294-302
  • Riddell SR, Elliott M, Lewinsohn DA, T-cell mediated rejection of gene-modified HIV-specific cytotoxic T lymphocytes in HIV-infected patients. Nat Med 1996;2:216-23
  • Bluestone JA. New perspectives of CD28-B7-mediated T cell costimulation. Immunity 1995;2:555-9
  • Bretscher P, Cohn M. A theory of self-nonself discrimination. Science 1970;169:1042-9
  • Sharpe AH. Mechanisms of costimulation. Immunol Rev 2009;229:5-11
  • Brocker T, Karjalainen K. Signals through T cell receptor-zeta chain alone are insufficient to prime resting T lymphocytes. J Exp Med 1995;181:1653-9
  • Jenkins MK, Chen CA, Jung G, Inhibition of antigen-specific proliferation of type 1 murine T cell clones after stimulation with immobilized anti-CD3 monoclonal antibody. J Immunol 1990;144:16-22
  • Gimmi CD, Freeman GJ, Gribben JG, Human T-cell clonal anergy is induced by antigen presentation in the absence of B7 costimulation. Proc Natl Acad Sci USA 1993;90:6586-90
  • Topp MS, Riddell SR, Akatsuka Y, Restoration of CD28 expression in CD28- CD8+ memory effector T cells reconstitutes antigen-induced IL-2 production. J Exp Med 2003;198:947-55
  • Maric M, Zheng P, Sarma S, Maturation of cytotoxic T lymphocytes against a B7-transfected nonmetastatic tumor: a critical role for costimulation by B7 on both tumor and host antigen-presenting cells. Cancer Res 1998;58:3376-84
  • Stopeck AT, Gessner A, Miller TP, Loss of B7.2 (CD86) and intracellular adhesion molecule 1 (CD54) expression is associated with decreased tumor-infiltrating T lymphocytes in diffuse B-cell large-cell lymphoma. Clin Cancer Res 2000;6:3904-9
  • Gerstmayer B, Altenschmidt U, Hoffmann M, Wels W. Costimulation of T cell proliferation by a chimeric B7-2 antibody fusion protein specifically targeted to cells expressing the erbB2 proto-oncogene. J Immunol 1997;158:4584-90
  • Li Y, Hellstrom KE, Newby SA, Chen L. Costimulation by CD48 and B7-1 induces immunity against poorly immunogenic tumors. J Exp Med 1996;183:639-44
  • Alvarez-Vallina L, Hawkins RE. Antigen-specific targeting of CD28-mediated T cell co-stimulation using chimeric single-chain antibody variable fragment-CD28 receptors. Eur J Immunol 1996;26:2304-9
  • Finney HM, Akbar AN, Lawson AD. Activation of resting human primary T cells with chimeric receptors: costimulation from CD28, inducible costimulator, CD134, and CD137 in series with signals from the TCR zeta chain. J Immunol 2004;172:104-13
  • Pule MA, Straathof KC, Dotti G, A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol Ther 2005;12:933-41
  • Carpenito C, Milone MC, Hassan R, Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci USA 2009;106:3360-5
  • Geiger TL, Nguyen P, Leitenberg D, Flavell RA. Integrated src kinase and costimulatory activity enhances signal transduction through single-chain chimeric receptors in T lymphocytes. Blood 2001;98:2364-71
  • Hombach A, Wieczarkowiecz A, Marquardt T, Tumor-specific T cell activation by recombinant immunoreceptors: CD3 zeta signaling and CD28 costimulation are simultaneously required for efficient IL-2 secretion and can be integrated into one combined CD28/CD3 zeta signaling receptor molecule. J Immunol 2001;167:6123-31
  • Kowolik CM, Topp MS, Gonzalez S, CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells. Cancer Res 2006;66:10995-1004
  • Imai C, Mihara K, Andreansky M, Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004;18:676-84
  • Loskog A, Giandomenico V, Rossig C, Addition of the CD28 signaling domain to chimeric T-cell receptors enhances chimeric T-cell resistance to T regulatory cells. Leukemia 2006;20:1819-28
  • Wang J, Jensen M, Lin Y, Optimizing adoptive polyclonal T cell immunotherapy of lymphomas, using a chimeric T cell receptor possessing CD28 and CD137 costimulatory domains. Hum Gene Ther 2007;18:712-25
  • Brentjens RJ, Santos E, Nikhamin Y, Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts. Clin Cancer Res 2007;13:5426-35
  • Milone MC, Fish JD, Carpenito C, Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther 2009;17:1453-64
  • Hollyman D, Stefanski J, Przybylowski M, Manufacturing validation of biologically functional T cells targeted to CD19 antigen for autologous adoptive cell therapy. J Immunother 2009;32:169-80
  • Alvarez-Vallina L, Russell SJ. Efficient discrimination between different densities of target antigen by tetracycline-regulatable T bodies. Hum Gene Ther 1999;10:559-63
  • Weijtens ME, Hart EH, Bolhuis RL. Functional balance between T cell chimeric receptor density and tumor associated antigen density: CTL mediated cytolysis and lymphokine production. Gene Ther 2000;7:35-42
  • Choudhuri K, Wiseman D, Brown MH, T-cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature 2005;436:578-82
  • Zhou X, Cui Y, Huang X, Lentivirus-mediated gene transfer and expression in established human tumor antigen-specific cytotoxic T cells and primary unstimulated T cells. Hum Gene Ther 2003;14:1089-105
  • Huang X, Guo H, Kang J, Sleeping Beauty transposon-mediated engineering of human primary T cells for therapy of CD19+ lymphoid malignancies. Mol Ther 2008;16:580-9
  • Singh H, Manuri PR, Olivares S, Redirecting specificity of T-cell populations for CD19 using the Sleeping Beauty system. Cancer Res 2008;68:2961-71
  • Diaz-Montero CM, El Naggar S, Al Khami A, Priming of naive CD8+ T cells in the presence of IL-12 selectively enhances the survival of CD8+CD62Lhi cells and results in superior anti-tumor activity in a tolerogenic murine model. Cancer Immunol Immunother 2008;57:563-72
  • Kaneko S, Mastaglio S, Bondanza A, IL-7 and IL-15 allow the generation of suicide gene-modified alloreactive self-renewing central memory human T lymphocytes. Blood 2009;113:1006-15
  • Hinrichs CS, Gattinoni L, Restifo NP. Programming CD8+ T cells for effective immunotherapy. Curr Opin Immunol 2006;18:363-70
  • Rossig C, Bollard CM, Nuchtern JG, Epstein-Barr virus-specific human T lymphocytes expressing antitumor chimeric T-cell receptors: potential for improved immunotherapy. Blood 2002;99:2009-16
  • Cooper LJ, Al-Kadhimi Z, Serrano LM, Enhanced antilymphoma efficacy of CD19-redirected influenza MP1-specific CTLs by cotransfer of T cells modified to present influenza MP1. Blood 2005;105:1622-31
  • Li Y, Yee C. IL-21 mediated Foxp3 suppression leads to enhanced generation of antigen-specific CD8+ cytotoxic T lymphocytes. Blood 2008;111:229-35
  • Morse MA, Hobeika AC, Osada T, Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines. Blood 2008;112:610-8
  • Kline J, Brown IE, Zha YY, Homeostatic proliferation plus regulatory T-cell depletion promotes potent rejection of B16 melanoma. Clin Cancer Res 2008;14:3156-67
  • Moeller M, Haynes NM, Kershaw MH, Adoptive transfer of gene-engineered CD4+ helper T cells induces potent primary and secondary tumor rejection. Blood 2005;106:2995-3003
  • Antony PA, Piccirillo CA, Akpinarli A, CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J Immunol 2005;174:2591-601
  • Riddell SR, Greenberg PD. The use of anti-CD3 and anti-CD28 monoclonal antibodies to clone and expand human antigen-specific T cells. J Immunol Methods 1990;128:189-201
  • Foster AE, Leen AM, Lee T, Autologous designer antigen-presenting cells by gene modification of T lymphocyte blasts with IL-7 and IL-12. J Immunother 2007;30:506-16
  • Suhoski MM, Golovina TN, Aqui NA, Engineering artificial antigen-presenting cells to express a diverse array of co-stimulatory molecules. Mol Ther 2007;15:981-8
  • Gattinoni L, Klebanoff CA, Palmer DC, Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest 2005;115:1616-26
  • Carrio R, Rolle CE, Malek TR. Non-redundant role for IL-7R signaling for the survival of CD8+ memory T cells. Eur J Immunol 2007;37:3078-88
  • Schluns KS, Kieper WC, Jameson SC, Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 2000;1:426-32
  • Tan JT, Ernst B, Kieper WC, Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8+ cells but are not required for memory phenotype CD4+ cells. J Exp Med 2002;195:1523-32
  • Cavalieri S, Cazzaniga S, Geuna M, Human T lymphocytes transduced by lentiviral vectors in the absence of TCR activation maintain an intact immune competence. Blood 2003;102:497-505
  • Daudt L, Maccario R, Locatelli F, Interleukin-15 favors the expansion of central memory CD8+ T cells in ex vivo generated, antileukemia human cytotoxic T lymphocyte lines. J Immunother 2008;31:385-93
  • Klebanoff CA, Finkelstein SE, Surman DR, IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells. Proc Natl Acad Sci USA 2004;101:1969-74
  • Manjunath N, Shankar P, Wan J, Effector differentiation is not prerequisite for generation of memory cytotoxic T lymphocytes. J Clin Invest 2001;108:871-8
  • Imamichi H, Sereti I, Lane HC. IL-15 acts as a potent inducer of CD4(+)CD25(hi) cells expressing FOXP3. Eur J Immunol 2008;38:1621-30
  • Hinrichs CS, Spolski R, Paulos CM, IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. Blood 2008;111:5326-33
  • Chang J, Cho JH, Lee SW, IL-12 priming during in vitro antigenic stimulation changes properties of CD8 T cells and increases generation of effector and memory cells. J Immunol 2004;172:2818-26
  • Macgregor JN, Li Q, Chang AE, Ex vivo culture with interleukin (IL)-12 improves CD8(+) T-cell adoptive immunotherapy for murine leukemia independent of IL-18 or IFN-gamma but requires perforin. Cancer Res 2006;66:4913-21
  • Surh CD, Boyman O, Purton JF, Sprent J. Homeostasis of memory T cells. Immunol Rev 2006;211:154-63
  • Klebanoff CA, Khong HT, Antony PA, Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends Immunol 2005;26:111-7
  • Gattinoni L, Finkelstein SE, Klebanoff CA, Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 2005;202:907-12
  • Proietti E, Greco G, Garrone B, Importance of cyclophosphamide-induced bystander effect on T cells for a successful tumor eradication in response to adoptive immunotherapy in mice. J Clin Invest 1998;101:429-41
  • Bracci L, Moschella F, Sestili P, Cyclophosphamide enhances the antitumor efficacy of adoptively transferred immune cells through the induction of cytokine expression, B-cell and T-cell homeostatic proliferation, and specific tumor infiltration. Clin Cancer Res 2007;13:644-53
  • Dudley ME, Wunderlich JR, Yang JC, Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005;23:2346-57
  • Wallen H, Thompson JA, Reilly JZ, Fludarabine modulates immune response and extends in vivo survival of adoptively transferred CD8 T cells in patients with metastatic melanoma. PLoS ONE 2009;4:e4749
  • Dudley ME, Yang JC, Sherry R, Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 2008;26:5233-9
  • Saxton ML, Longo DL, Wetzel HE, Adoptive transfer of anti-CD3-activated CD4+ T cells plus cyclophosphamide and liposome-encapsulated interleukin-2 cure murine MC-38 and 3LL tumors and establish tumor-specific immunity. Blood 1997;89:2529-36
  • North RJ. Cyclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells. J Exp Med 1982;155:1063-74
  • Ghiringhelli F, Larmonier N, Schmitt E, CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 2004;34:336-44
  • Berd D, Mastrangelo MJ, Engstrom PF, Augmentation of the human immune response by cyclophosphamide. Cancer Res 1982;42:4862-6
  • Berd D, Mastrangelo MJ. Effect of low dose cyclophosphamide on the immune system of cancer patients: reduction of T-suppressor function without depletion of the CD8+ subset. Cancer Res 1987;47:3317-21
  • Yee C, Thompson JA, Byrd D, Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci USA 2002;99:16168-73
  • Ahmadzadeh M, Rosenberg SA. IL-2 administration increases CD4+ CD25(hi) Foxp3+ regulatory T cells in cancer patients. Blood 2006;107:2409-14
  • Shah MH, Freud AG, Benson DM, A phase I study of ultra low dose interleukin-2 and stem cell factor in patients with HIV infection or HIV and cancer. Clin Cancer Res 2006;12:3993-6
  • Zhang H, Chua KS, Guimond M, Lymphopenia and interleukin-2 therapy alter homeostasis of CD4+CD25+ regulatory T cells. Nat Med 2005;11:1238-43
  • Vera JF, Hoyos V, Savoldo B, Genetic manipulation of tumor-specific cytotoxic T lymphocytes to restore responsiveness to IL-7. Mol Ther 2009;17:880-8
  • Melchionda F, Fry TJ, Milliron MJ, Adjuvant IL-7 or IL-15 overcomes immunodominance and improves survival of the CD8+ memory cell pool. J Clin Invest 2005;115:1177-87
  • Rubinstein MP, Kadima AN, Salem ML, Systemic administration of IL-15 augments the antigen-specific primary CD8+ T cell response following vaccination with peptide-pulsed dendritic cells. J Immunol 2002;169:4928-35
  • Hsu C, Hughes MS, Zheng Z, Primary human T lymphocytes engineered with a codon-optimized IL-15 gene resist cytokine withdrawal-induced apoptosis and persist long-term in the absence of exogenous cytokine. J Immunol 2005;175:7226-34
  • Quintarelli C, Vera JF, Savoldo B, Co-expression of cytokine and suicide genes to enhance the activity and safety of tumor-specific cytotoxic T lymphocytes. Blood 2007;110:2793-802
  • Iuchi T, Teitz-Tennenbaum S, Huang J, Interleukin-21 augments the efficacy of T-cell therapy by eliciting concurrent cellular and humoral responses. Cancer Res 2008;68:4431-41
  • Scheeren FA, Diehl SA, Smit LA, IL-21 is expressed in Hodgkin lymphoma and activates STAT5: evidence that activated STAT5 is required for Hodgkin lymphomagenesis. Blood 2008;111:4706-15
  • Lu Z, Sherr D. A Head-to-Head Comparison between cyclophosphamide and ontak in reducing the influence of tregs on self (Tumor) peptide-specific CTL responses. Blood 2008;112:Abstract #2570
  • Rooney CM, Smith CA, Ng CY, Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 1998;92:1549-55
  • Hacein-Bey-Abina S, Garrigue A, Wang GP, Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest 2008;118:3132-42
  • Corrigan-Curay J. Clonal population of cells detected in a clinical gene transfer study using a lentiviral vector. Office of Biotechnology Activities Memorandum, 10 June 2009
  • Montini E, Cesana D, Schmidt M, The genotoxic potential of retroviral vectors is strongly modulated by vector design and integration site selection in a mouse model of HSC gene therapy. J Clin Invest 2009;119:964-75
  • Introna M, Barbui AM, Bambacioni F, Genetic modification of human T cells with CD20: a strategy to purify and lyse transduced cells with anti-CD20 antibodies. Hum Gene Ther 2000;11:611-20
  • van Meerten T, Claessen MJ, Hagenbeek A, Ebeling SB. The CD20/alphaCD20 ‘suicide’ system: novel vectors with improved safety and expression profiles and efficient elimination of CD20-transgenic T cells. Gene Ther 2006;13:789-97
  • Bonini C, Ferrari G, Verzeletti S, HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science 1997;276:1719-24
  • Thomis DC, Marktel S, Bonini C, A Fas-based suicide switch in human T cells for the treatment of graft-versus-host disease. Blood 2001;97:1249-57
  • Berger C, Blau CA, Huang ML, Pharmacologically regulated Fas-mediated death of adoptively transferred T cells in a nonhuman primate model. Blood 2004;103:1261-9
  • Straathof KC, Pule MA, Yotnda P, An inducible caspase 9 safety switch for T-cell therapy. Blood 2005;105:4247-54
  • Di Stasi A, De Angelis B, Rooney CM, T lymphocytes coexpressing CCR4 and a chimeric antigen receptor have improved homing and antitumor activity in a Hodgkin tumor model. Blood 2009;113:6392-402
  • Bollard CM, Rossig C, Calonge MJ, Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood 2002;99:3179-87

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