The suicide gene therapy challenge: How to improve a successful gene therapy approach

Molecular Therapy

Volumn 15, Issue 7, 2007, Pages 1248-1252

  Bonini, Chiara ^a,b   Bondanza, Attilio ^a,b   Perna, Serena Kimi ^a,b   Kaneko, Shin ^a   Traversari, Catia ^c   Ciceri, Fabio ^a,b   Bordignon, Claudio ^b,c  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c MOLMED S P A   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AP 1903; AP 20187; CASPASE 9; CD20 ANTIBODY; CD20 ANTIGEN; CD34 ANTIGEN; FAS ANTIGEN; FK 506 BINDING PROTEIN; GANCICLOVIR; HYBRID PROTEIN; IMMUNOSUPPRESSIVE AGENT; LENTIVIRUS VECTOR; MONOCLONAL ANTIBODY; PRODRUG; RETROVIRUS VECTOR; STEROID; THYMIDINE KINASE; UNCLASSIFIED DRUG;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ALLOIMMUNITY; ALTERNATIVE RNA SPLICING; APOPTOSIS; CANCER RECURRENCE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL SELECTION; CLINICAL TRIAL; DIMERIZATION; DRUG EFFICACY; DRUG SAFETY; GENE DIRECTED ENZYME PRODRUG THERAPY; GENE TRANSFER; GENETIC TRANSDUCTION; GRAFT VERSUS HOST REACTION; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE DEPLETION; META ANALYSIS; REVIEW; SUICIDE GENE THERAPY; SYSTEMATIC REVIEW; T LYMPHOCYTE ACTIVATION;

ANIMALS; GENE THERAPY; GENES, TRANSGENIC, SUICIDE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; PRODRUGS; T-LYMPHOCYTES; TREATMENT OUTCOME;

EID: 34250718593     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/sj.mt.6300190     Document Type: Review

References (65)

1. Bonini, C, Ferrari, G, Verzeletti, S, Servida, P, Zappone, E., Ruggieri, L et al. (1997). HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science 276: 1719-1724.
2. Tiberghien, P, Ferrand, C, Lioure, B, Milpied, N, Angonin, R, Deconinck, E et al. (2001). Administration of herpes simplex-thymidine kinase-expressing donor T cells with a T-cell depleted allogeneic marrow graft. Blood 97: 63-72.
3. Munshi, NC, Tricot, G, Jagannath, S, Metha, J, Desikan, K, Siegle, S et al. (1997). Clinical results of thymidine kinase (TK) gene transduced donor lymphocyte infusion following allogeneic transplantation in myeloma. Blood 90: 11a.
4. Champlin, R, Besinger, W, Henslee-Downey, J, Cornetta, K, Parker, P, Carabasi, M et al. (1999). Phase I/II study of thymidine kinase (TK)-transduced donor lymphocyte infusions (DLI) in patients with hematologic malignanicies. Blood 94: 1448a.
5. Burt, RK, Drobyski, WR, Seregina, T, Traynor, A, Oyama, Y, Keever-Taylor, C et al. (2003). Herpes simplex thymidine kinase gene-transduced donor lymphocyte infusion. Exp Hematol 10: 903-910.
6. + -enriched blood stem cells. Blood 104: 3408-3409.
7. Onodera, M, Kaneko, S, Otsu, M, Kojima, H, Sumazaki, R, Toma, S et al. (2006). Gene therapy clinical trials for relapsed leukemia with infusion of the suicide-gene transduced donor lymphocytes in Japan. Mol Ther 13: 1107a.
8. Weissinger, EM, Silvani, A, Radrizzani, M, Benati, C, Dammann, E, Gallo Stampino, C et al. (2003). The fate of gene modified T-cells can be followed in 2 patients without immunosuppression after allogeneic stem cell transplantation. Blood 102: 5735a.
9. Ciceri, F, Bonini, C, Marktel, S, Zappone, E, Servida, P, Bemardi, M et al. (2007). Anti-tumor effects of HSV-TK engineered donor lymphocytes after allogeneic stem cell transplantation. Blood (epub ahead of print).
10. Bonini, C, Ciceri, F, Lupo Stangheltini, MT, Bondanza, A, Magnani, Z, Perna, S et al. (2006). Rapid and wide immunereconstitution Obtained with HSV-TK engineered donor lymphocyte add-backs permits long-term survival after haplo-HSCT. Session type: Oral session. Blood 108: 307a.
11. Appelbaum, FR (2001). Haematopoietic cell transplantation as immunotherapy. Nature 411: 385-389.
12. Robinet, E, Fehse, B, Ebeling, S, Sauce, D, Ferrand, C and Tiberghien, P (2005). Improving the ex vivo retroviral-mediated suicide-gene transfer process in T lymphocytes to preserve immune function. Cytotherapy 7: 150-157.
13. Bondanza, A, Ciceri, F and Bonini, C (2005). Application of donor lymphocytes expressing a suicide gene for early GVL induction and later control of GVH reactions after bone-marrow transplantation. Methods Mol Med 109: 475-486.
14. Tiberghien, P (1998). "Suicide" gene for the control of graft-versus-host disease. Curr Opin Hematol 5: 478-482.
15. Ciceri, F, Bonini, C, Gallo-Stampino, C and Bordignon, C (2005). Modulation of GvHD by suicide-gene transduced donor T lymphocytes: clinical applications in mismatched transplantation. Cytotherapy 7: 144-149.
16. Bonini, C, Grez, M, Traversari, C, Ciceri, F, Marktel, S, Ferrari, G et al. (2003). Safety of retroviral gene marking with a truncated NGF receptor. Nat Med 9: 367-369.
17. Recchia, A, Bonini, C, Magnani, Z, Urbinati, F, Sartori, D, Muraro, S et al. (2006). Retroviral vector integration deregulates gene expression but has no consequence on the biology and function of transplanted T cells. Proc Natl Acad Sci USA 103: 1457-1462.
18. Giordano, FA, Fehse, B, Hotz-Wagenblatt, A, Jonnakuty, S, del Val, C, Appelt, JU et al. (2006). Retroviral vector insertions in T-lymphocytes used for suicide gene therapy occur in gene groups with specific molecular functions. Bone Marrow Transplant 38: 229-235.
19. Lamana, ML, Segovia, JC, Guenechea, G and Bueren, JA (2001). Systematic analysis of clinically applicable conditions leading to a high efficiency of transduction and transgene expression in human T cells. J Gene Med 3: 32-41.
20. Weijtens, MEM, Van Spronsen, AM, Martens, ACM and Hagenbeek, A (2000). Reduced graft-versus-host inducing potential of thymidine kinase transduced, selected and expanded T cells: Studies in a rat model. Mol Ther 1: S270.
21. Marini, FC 3rd and Komblau, SM (1999). Production and culture of HSVtk transduced suicidal lymphocytes induces variable changes in the lymphocyte subset composition. Bone Marrow Transplant 23: 907-915.
22. Sauce, D, Mercier, P, Battini, JL, Ferrand, C, Certoux, JM, Manel, N et al. (2004). Preferential retroviral-mediated transduction of EBV- and CMV-specific T cells after polyclonal T-cell activation. Gene Ther 11: 1019-1022.
23. Sauce, D, Bodinier, M, Garin, M, Petracca, B, Tonnelier, N, Duperrier, A et al. (2002). Retrovirus-mediated gene transfer in primary T lymphocytes impairs their anti-Epstein-Barr virus potential through both culture-dependent and selection process-dependent mechanisms. Blood 99: 1165-1173.
24. + T cells do not induce graft-versus-host disease. J Clin Invest 112: 101-108.
25. Chen, BJ, Cui, X, Sempowski, GD, Liu, C and Chao, NJ (2004). Transfer of allogeneic CD62L- memory T cells without graft-versus-host disease. Blood 103: 1534-1541.
26. Bondanza, A, Valtolina, V, Magnani, Z, Ponzoni, M, Fleischhauer, K, Bonyhadi, M et al. (2006). Suicide gene therapy of graft-versus-host disease induced by central memory human T lymphocytes. Blood 107: 1828-1836.
27. Ferrand, C, Robinet, E, Contassot E, Certoux, JM, Lim, A, Herve, P et al. (2000). Retrovirus-mediated gene transfer in primary T lymphocytes: Influence of the transduction/selection process and of ex vivo expansion on the T cell receptor beta chain hypervariable region repertoire. Hum Gene Ther 11: 1151-1164.
28. Berger, C, Blau, CA Clackson, T, Riddell, SR and Heimfeld, S (2003). CD28 costimulation and immunoaffinity-based selection efficiently generate primary gene-modified T cells for adoptive immunotherapy. Blood 101: 476-484.
29. Rettig, MP, Ritchey, JK, Meyerrose, TE, Haug, JS and Dipersio, JF (2003). Transduction and selection of human T cells with novel CD34/ thymidine kinase chimeric suicide genes for the treatment of graft-versus-host disease. Mol Ther 8: 29-41.
30. Bukrinsky, MI, Sharova, N, Dempsey, MP, Stanwick, TL, Bukrinskaya, AG, Haggerty, S et al. (1992). Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc Natl Acad Sci USA 89: 6580-6584.
31. Korin, YD and Zack, JA (1998). Progression to the G1b phase of the cell cycle is required for completion of human immunodeficiency virus type 1 reverse transcription in T cells. J Virol 72: 3161-3168.
32. + T cells. Proc Natl Acad Sci USA 98: 9277-9282.
33. Unutmaz, D, Kewalramani, VN, Marmon, S and Littman, DR (1999). Cytokine signals are sufficient for HIV-1 infection of resting human T lymphocytes. J Exp Med 189: 1735-1746.
34. Verhoeyen, E, Dardalhon, V, Ducrey-Rundquist, O, Trono, D, Taylor, N and Cosset, FL (2003). IL-7 surface-engineered lentiviral vectors promote survival and efficient gene transfer in resting primary T lymphocytes. Blood 101: 2167-2174.
35. Cavalieri, S, Cazzaniga, S, Geuna, M, Magnani, Z, Bordignon, C, Naldini, L et al. (2003). Human T lymphocytes transduced by lentiviral vectors in the absence of TCR activation maintain an intact immune competence. Blood 102: 497-505.
36. Dupre, L, Trifari, S, Follenzi, A, Marangoni, F, Lain de Lera, T, Bernad, A et al. (2004). Lentiviral vector-mediated gene transfer in T cells from Wiskott-Aldrich syndrome patients leads to functional correction. Mol Ther 10: 903-915.
37. Schroder, AR, Shinn, P, Chen, H, Berry, C, Ecker, JR and Bushman, F (2002). HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110: 521-529.
38. Wu, X, Li, Y, Crise, B and Burgess, SM (2003). Transcription start regions in the human genome are favored targets for MLV integration. Science 300: 1749-1751.
39. De Palma, M, Montini, E, Santoni de Sio, FR, Benedicenti, F, Gentile, A, Medico, E et al. (2005). Promoter trapping reveals significant differences in integration site selection between MLV and HIV vectors in primary hematopoietic cells. Blood 105: 2307-2315.
40. Qasim, W, Mackey, T, Sinclair, J, Chatziandreou, I, Kinnon, C, Thrasher, AJ et al. (2007). Lentiviral vectors for T-cell suicide gene therapy: Preservation of T-cell effector function after cytokine-mediated transduction. Mol Ther 15: 355-360.
41. Mavilio, F, Ferrari, G, Rossini, S, Nobili, N, Bonini, C, Casorati, G et al. (1994). Peripheral blood lymphocytes as target cells of retroviral vector-mediated gene transfer. Blood 83: 1988-1997.
42. Introna, M, Barbui, AM, Bambacioni, F, Casati, C, Gaipa, G, Borleri, G et al. (2000). Genetic modification of human T cells with CD20: A strategy to purify and lyse transduced cells with anti-CD20 antibodies. Hum Gene Ther 11: 611-620.
43. Fehse, B, Richters, A, Putimtseva-Scharf, K, Klump, H, Li, Z, Ostertag, W et al. (2000). CD34 splice variant: An attractive marker for selection of gene-modified cells. Mol Ther 1: 448-456.
44. Serafini, M, Manganini, M, Borleri, G, Bonamino, M, Imberti, L, Biondi, A et al. (2004). Characterization of CD20-transduced T lymphocytes as an alternative suicide gene therapy approach for the treatment of graft-versus-host disease. Hum Gene Ther 15: 63-76.
45. Maloney, DG (2005). Immunotherapy for non-Hodgkin's lymphoma: Monoclonal antibodies and vaccines. J Clin Oncol 23: 6421-6428.
46. Junker, K, Koehl, U, Zimmerman, S, Stein, S, Schwabe, D, Klingebiel, T et al. (2003). Kinetics of cell death in T lymphocytes genetically modified with two novel suicide fusion genes. Gene Ther 10: 1189-1197.
47. Rettig, MP, Ritchey, JK, Prior, JL, Haug, JS, Piwnica-Worms, D and Dipersio, JF (2004). Kinetics of in vivo elimination of suicide gene-expressing T cells affects engraftment graft-versus-host disease, and graft-versus-leukemia after allogeneic bone marrow transplantation. J Immunol 173: 3620-3630.
48. Aints, A, Belusa, R, Andersson, RM, Guven, H and Dilber, MS (2002). Enhanced ouabain resistance gene as a eukaryotic selection marker. Hum Gene Ther 13: 969-977.
49. Tiberghien, P, Reynolds, CW, Keller, J, Spence, S, Deschaseaux, M, Certoux, JM et al. (1994). Ganciclovir treatment of herpes simplex thymidine kinase-transduced primary T lymphocytes: An approach for specific in vivo donor T-cell depletion after bone marrow transplantation? Blood 84: 1333-1341.
50. Cohen, JL, Boyer, O, Thomas-Vaslin, V and Klatzmann, D (1999). Suicide gene-mediated modulation of graft-versus-host disease. Leuk Lymphoma 34: 473-480.
51. Cohen, JL, Boyer, O, Salomon, B, Onclercq, R, Charlotte, F, Bruel, S et al. (1997). Prevention of graft-versus-host Disease in mice using a suicide gene expressed in T lymphocytes. Blood 89: 4636-4645.
52. Garin, MI, Garrett, E, Tiberghien, P, Apperley, JF, Chalmers, D, Melo, JV et al. (2001). Molecular mechanism for ganciclovir resistance in human T lymphocytes transduced with retroviral vectors carrying the herpes simplex virus thymidine kinase gene. Blood 97: 122-129.
53. Chalmers, D, Ferrand, C, Apperley, JF, Melo, JV, Ebeling, S, Newton, I et al. (2001). Elimination of the truncated message from the herpes simplex virus thymidine kinase suicide gene. Mol Ther 4 146-148.
54. Qasim, W, Thrasher, AJ, Buddle, I, Kinnon, C, Black ME and Gaspar, HB (2002). T cell transduction and suicide with an enhanced mutant thymidine kinase. Gene Ther 9: 824-827.
55. Riddell, SR, Elliott, M, Lewinsohn, DA, Gilbert, MJ, Wilson, L, Manley, SA et al. (1996). T-cell mediated rejection of gene-modified HIV-specific cytotoxic T lymphocytes in HIV infected patients. Nat Med 2: 216-223.
56. Berger, C, Flowers, ME, Warren, EH and Riddell, SR (2006). 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 107 2294-2302.
57. Thomis, DC, Marktel, S, Bonini, C, Traversari, C, Gilman, M, Bordignon, C et al. (2001). A Fas-based suicide switch in human T cells for the treatment of graft-versus-host disease. Blood 97: 1249-1257.
58. Straathof, KC, Pule, MA, Yotnda, P, Dotti, G, Vanin, EF, Brenner, MK et al. (2005). An inducible caspase 9 safety switch for T-cell therapy. Blood 105: 4247-4254.
59. Berger, C, Blau, CA, Huang, ML, Iuliucci, JD, Dalgamo, DC, Gaschet, J et al. (2004). Pharmacologically regulated Fas-mediated death of adoptively transferred T cells in a nonhuman primate model. Blood 103: 1261-1269.
60. Van Meerten, T, Claessen, MJ, Hagenbeek, A and Ebeling, SB (2006). The CD20/alphaCD20 'suicide' system: Novel vectors with improved safety and expression profiles and efficient elimination of CD20-transgenic T cells. Gene Ther 13: 789-797.
61. Serafini, M, Bonamino, M, Golay, J and Introna, M (2004). Elongation factor 1 (EF1alpha) promoter in a lentiviral backbone improves expression of the CD20 suicide gene in primary T lymphocytes allowing efficient rituximab-mediated lysis. Haematologica 89: 86-95.
62. Iuliucci, JD, Oliver, SD, Morley S, Ward, C, Ward, J, Dalgamo, D et al. (2001). Intravenous safety and pharmacokinetics of a novel dimerizer drug, AP1903, in healthy volunteers. J Clin Pharmacol 41: 870-879.
63. Traversari, C, Marktel, S, Magnani, Z, Mangia, P, Russo, V, Ciceri, F et al. (2007). The potential immunogenicity of the TK-suicide gene does not prevent full clinical benefit associated with the use of TK-transduced donor lymphocytes in HSCT for hematologic malignancies. Blood (epub ahead of print).
64. Bonini, C, Ciceri, F, Marktel, S, Magnani, Z, Cazzaniga, S, Zappone, E et al. (2002). Abrogation of GvHD and early immune reconstitution after infusion of HSV-TK engineered donor lymphocytes after haplo-identical hemtopoietic stem cell transplantation. Blood 100: 115a.
65. Ciceri, F, Bonini, C, Lupo Stanghellini, MT, Bondanza, A, Magnani, Z, Perna, S et al. (2005). HSV-TK engineered donor lymphocytes add-backs reduce late mortality and improve survival of high risk acute leukemia after haplo-HSCT: Results of a phase II multicenter trial. Blood 106: 133a.