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Science 13 June 1997:
Vol. 276. no. 5319, pp. 1719 - 1724
DOI: 10.1126/science.276.5319.1719
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Reports

HSV-TK Gene Transfer into Donor Lymphocytes for Control of Allogeneic Graft-Versus-Leukemia

Chiara Bonini, Giuliana Ferrari, Simona Verzeletti, Paolo Servida, Elisabetta Zappone, Luciano Ruggieri, Maurilio Ponzoni, Silvano Rossini, Fulvio Mavilio, Catia Traversari, Claudio Bordignon *

In allogeneic bone marrow transplantation (allo-BMT), donor lymphocytes play a central therapeutic role in both graft-versus-leukemia (GvL) and immune reconstitution. However, their use is limited by the risk of severe graft-versus-host disease (GvHD). Eight patients who relapsed or developed Epstein-Barr virus-induced lymphoma after T cell-depleted BMT were then treated with donor lymphocytes transduced with the herpes simplex virus thymidine kinase (HSV-TK) suicide gene. The transduced lymphocytes survived for up to 12 months, resulting in antitumor activity in five patients. Three patients developed GvHD, which could be effectively controlled by ganciclovir-induced elimination of the transduced cells. These data show that genetic manipulation of donor lymphocytes may increase the efficacy and safety of allo-BMT and expand its application to a larger number of patients.

C. Bonini, G. Ferrari, P. Servida, E. Zappone, L. Ruggieri, S. Rossini, F. Mavilio, C. Traversari, C. Bordignon, Telethon Institute for Gene Therapy (TIGET), Istituto Scientifico H. S. Raffaele, 20132 Milan, Italy.
S. Verzeletti, Molmed S.p.A., 20132 Milan, Italy.
M. Ponzoni, Department of Pathology, Istituto Scientifico H. S. Raffaele, 20132 Milan, Italy.
*   To whom correspondence should be addressed at Istituto Scientifico San Raffaele, Via Olgettina, 60, 20132 Milan, Italy. E-mail: bordigc{at}dibit.hsr.it

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Molecular mechanism for ganciclovir resistance in human T lymphocytes transduced with retroviral vectors carrying the herpes simplex virus thymidine kinase gene.
M. I. Garin, E. Garrett, P. Tiberghien, J. F. Apperley, D. Chalmers, J. V. Melo, and C. Ferrand (2001)
Blood 97, 122-129
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Inducible and irreversible control of gene expression using a single transgene.
E. Fuhrmann-Benzakein, I. Garcia-Gabay, M. S. Pepper, J.-D. Vassalli, and P. L. Herrera (2000)
Nucleic Acids Res. 28, e99
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Design of Retroviral Vectors and Helper Cells for Gene Therapy.
W.-S. Hu and V. K. Pathak (2000)
Pharmacol. Rev. 52, 493-512
   Abstract »    Full Text »    PDF »
Nonmyeloablative Allogeneic Stem Cell Transplantation: Early Promise and Limitations.
N. J. McCarthy and M. R. Bishop (2000)
Oncologist 5, 487-496
   Abstract »    Full Text »
Cancer Immunotherapy with Alloreactive Lymphocytes.
S. Slavin (2000)
N. Engl. J. Med. 343, 802-803
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Rapid, B Lymphoid-Restricted Engraftment Mediated by a Primitive Bone Marrow Subpopulation.
A. E. Searles, S. J. Pohlmann, L. J. Pierce, S. S. Perry, W. B. Slayton, M. P. Mojica, and G. J. Spangrude (2000)
J. Immunol. 165, 67-74
   Abstract »    Full Text »    PDF »
Rapid selection of antigen-specific T lymphocytes by retroviral transduction.
G. Koehne, H. F. Gallardo, M. Sadelain, and R. J. O'Reilly (2000)
Blood 96, 109-117
   Abstract »    Full Text »    PDF »
Acquisition of intact allogeneic human leukocyte antigen molecules by human dendritic cells.
V. Russo, D. Zhou, C. Sartirana, P. Rovere, A. Villa, S. Rossini, C. Traversari, and C. Bordignon (2000)
Blood 95, 3473-3477
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Expression of Herpes Simplex Virus ICP47 and Human Cytomegalovirus US11 Prevents Recognition of Transgene Products by CD8+ Cytotoxic T Lymphocytes.
C. Berger, S. Xuereb, D. C. Johnson, K. S. Watanabe, H.-P. Kiem, P. D. Greenberg, and S. R. Riddell (2000)
J. Virol. 74, 4465-4473
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Herpesvirus saimiri-transformed macaque T cells are tolerated and do not cause lymphoma after autologous reinfusion.
A. Knappe, G. Feldmann, U. Dittmer, E. Meinl, T. Nisslein, S. Wittmann, K. Matz-Rensing, T. Kirchner, W. Bodemer, and H. Fickenscher (2000)
Blood 95, 3256-3261
   Abstract »    Full Text »    PDF »
Immunotherapy of AML: future directions.
M. W Lowdell and M. B C Koh (2000)
J. Clin. Pathol. 53, 49-54
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Managing Indolent Lymphomas in Relapse: Working Our Way Through a Plethora of Options.
F. Cabanillas, S. Horning, M. Kaminski, and R. Champlin (2000)
Hematology 2000, 166-179
   Abstract »    Full Text »    PDF »
Transfusion Medicine: New Clinical Applications of Cellular Immunotherapy.
M. Brenner, C. Rossig, U. Sili, J. W. Young, and E. Goulmy (2000)
Hematology 2000, 356-375
   Abstract »    Full Text »    PDF »
Differential Ganciclovir-mediated Cell Killing by Glutamine 125 Mutants of Herpes Simplex Virus Type 1 Thymidine Kinase.
R. R. Drake, T. N. Wilbert, T. A. Hinds, and K. M. Gilbert (1999)
J. Biol. Chem. 274, 37186-37192
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Substrate Diversity of Herpes Simplex Virus Thymidine Kinase. IMPACT OF THE KINEMATICS OF THE ENZYME.
B. D. Pilger, R. Perozzo, F. Alber, C. Wurth, G. Folkers, and L. Scapozza (1999)
J. Biol. Chem. 274, 31967-31973
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Photochemical Treatment with S-59 Psoralen and Ultraviolet A Light to Control the Fate of Naive or Primed T Lymphocytes In Vivo After Allogeneic Bone Marrow Transplantation.
R. L. Truitt, B. D. Johnson, C. Hanke, S. Talib, and J. E. Hearst (1999)
J. Immunol. 163, 5145-5156
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T-Cell Depletion Plus Salvage Immunotherapy With Donor Leukocyte Infusions as a Strategy to Treat Chronic-Phase Chronic Myelogenous Leukemia Patients Undergoing HLA-Identical Sibling Marrow Transplantation.
W. R. Drobyski, M. J. Hessner, J. P. Klein, C. Kabler-Babbitt, D. H. Vesole, and C. A. Keever-Taylor (1999)
Blood 94, 434-441
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Natural Killer Cell-mediated Lysis of Autologous Cells Modified by Gene Therapy.
C. Liberatore, M. Capanni, N. Albi, I. Volpi, E. Urbani, L. Ruggeri, A. Mencarelli, F. Grignani, and A. Velardi (1999)
J. Exp. Med. 189, 1855-1862
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Design of 5' Untranslated Sequences in Retroviral Vectors Developed for Medical Use.
M. Hildinger, K. L. Abel, W. Ostertag, and C. Baum (1999)
J. Virol. 73, 4083-4089
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Feasibility of Immunotherapy of Relapsed Leukemia With Ex Vivo-Generated Cytotoxic T Lymphocytes Specific for Hematopoietic System-Restricted Minor Histocompatibility Antigens.
T. Mutis, R. Verdijk, E. Schrama, B. Esendam, A. Brand, and E. Goulmy (1999)
Blood 93, 2336-2341
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