Progress and prospects for engineered T cell therapies

British Journal of Haematology

Volumn 166, Issue 6, 2014, Pages 818-829

  Qasim, Waseem ^a,b   Thrasher, Adrian J ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

Author keywords

Gene therapy; T cells; Transplantation

Indexed keywords

B LYMPHOCYTE ANTIGEN; BENDAMUSTINE; CD4 ANTIGEN; CD8 ANTIGEN; CYCLOPHOSPHAMIDE; DNA; ETOPOSIDE; FLUDARABINE; IMMUNOGLOBULIN; LENTIVIRUS VECTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MELAN A; METHYLPREDNISOLONE; PENTOSTATIN; RETROVIRUS VECTOR; RNA; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TUMOR ANTIGEN; VIRUS ANTIGEN; VIRUS VECTOR; ZINC FINGER NUCLEASE;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ADOPTIVE TRANSFER; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; B CELL LYMPHOMA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELL SELECTION; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL (TOPIC); COLORECTAL CARCINOMA; CRYOPRESERVATION; CYTOKINE RELEASE SYNDROME; CYTOMEGALOVIRUS INFECTION; DNA MODIFICATION; ENTERITIS; EPSTEIN BARR VIRUS INFECTION; GENETIC ENGINEERING; GENETIC TRANSDUCTION; GRAFT VERSUS HOST REACTION; HEPATITIS B; HIGH THROUGHPUT SEQUENCING; HODGKIN DISEASE; HUMAN; IMMUNOTHERAPY; LYMPHOCYTE TRANSFUSION; LYMPHOPROLIFERATIVE DISEASE; MELANOMA; MOLONEY LEUKEMIA ONCOVIRUS; MYELODYSPLASTIC SYNDROME; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RNA EDITING; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TUMOR ESCAPE; TUMOR REGRESSION; VIRAL GENE DELIVERY SYSTEM;

GENE THERAPY; T CELLS; TRANSPLANTATION;

ANTIGENS, NEOPLASM; CELL- AND TISSUE-BASED THERAPY; CLINICAL TRIALS AS TOPIC; FORECASTING; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HEMATOLOGIC NEOPLASMS; HUMANS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TRANSFECTION;

EID: 84907597699     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12981     Document Type: Review

References (97)

1. Berger, C., Jensen, M.C., Lansdorp, P.M., Gough, M., Elliott, C. & Riddell, S.R. (2008) Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest, 118, 294-305.
2. Bonini, C., Ferrari, G., Verzeletti, S., Servida, P., Zappone, E., Ruggieri, L., Ponzoni, M., Rossini, S., Mavilio, F., Traversari, C. & Bordignon, C. (1997) HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science, 276, 1719-1724.
3. Braun, C.J., Boztug, K., Paruzynski, A., Witzel, M., Schwarzer, A., Rothe, M., Modlich, U., Beier, R., Gohring, G., Steinemann, D., Fronza, R., Ball, C.R., Haemmerle, R., Naundorf, S., Kuhlcke, K., Rose, M., Fraser, C., Mathias, L., Ferrari, R., Abboud, M.R., Al-Herz, W., Kondratenko, I., Marodi, L., Glimm, H., Schlegelberger, B., Schambach, A., Albert, M.H., Schmidt, M., von Kalle, C. & Klein, C. (2014) Gene therapy for wiskott-Aldrich syndrome-long-term efficacy and genotoxicity. Sci Transl Med, 6, 227ra233.
4. Brentjens, R.J., Riviere, I., Park, J.H., Davila, M.L., Wang, X., Stefanski, J., Taylor, C., Yeh, R., Bartido, S., Borquez-Ojeda, O., Olszewska, M., Bernal, Y., Pegram, H., Przybylowski, M., Hollyman, D., Usachenko, Y., Pirraglia, D., Hosey, J., Santos, E., Halton, E., Maslak, P., Scheinberg, D., Jurcic, J., Heaney, M., Heller, G., Frattini, M. & Sadelain, M. (2011) Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood, 118, 4817-4828.
5. Brentjens, R.J., Davila, M.L., Riviere, I., Park, J., Wang, X., Cowell, L.G., Bartido, S., Stefanski, J., Taylor, C., Olszewska, M., Borquez-Ojeda, O., Qu, J., Wasielewska, T., He, Q., Bernal, Y., Rijo, I.V., Hedvat, C., Kobos, R., Curran, K., Steinherz, P., Jurcic, J., Rosenblat, T., Maslak, P., Frattini, M. & Sadelain, M. (2013) CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med, 5, 177ra138.
6. Brewin, J., Mancao, C., Straathof, K., Karlsson, H., Samarasinghe, S., Amrolia, P.J. & Pule, M. (2009) Generation of EBV-specific cytotoxic T cells that are resistant to calcineurin inhibitors for the treatment of posttransplantation lymphoproliferative disease. Blood, 114, 4792-4803.
7. Burt, R.K., Drobyski, W.R., Seregina, T., Traynor, A., Oyama, Y., Keever-Taylor, C., Stefka, J., Kuzel, T.M., Brush, M., Rodriquez, J., Burns, W., Tennant, L. & Link, C. (2003) Herpes simplex thymidine kinase gene-transduced donor lymphocyte infusions. Experimental Hematology, 31, 903-910.
8. Cameron, B.J., Gerry, A.B., Dukes, J., Harper, J.V., Kannan, V., Bianchi, F.C., Grand, F., Brewer, J.E., Gupta, M., Plesa, G., Bossi, G., Vuidepot, A., Powlesland, A.S., Legg, A., Adams, K.J., Bennett, A.D., Pumphrey, N.J., Williams, D.D., Binder-Scholl, G., Kulikovskaya, I., Levine, B.L., Riley, J.L., Varela-Rohena, A., Stadtmauer, E.A., Rapoport, A.P., Linette, G.P., June, C.H., Hassan, N.J., Kalos, M. & Jakobsen, B.K. (2013) Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci Transl Med, 5, 197ra103.
9. Chapuis, A.G., Ragnarsson, G.B., Nguyen, H.N., Chaney, C.N., Pufnock, J.S., Schmitt, T.M., Duerkopp, N., Roberts, I.M., Pogosov, G.L., Ho, W.Y., Ochsenreither, S., Wolfl, M., Bar, M., Radich, J.P., Yee, C. & Greenberg, P.D. (2013) Transferred WT1-reactive CD8+ T cells can mediate antileukemic activity and persist in post-transplant patients. Sci Transl Med, 5, 174ra127.
10. Ciceri, F., Bonini, C., Marktel, S., Zappone, E., Servida, P., Bernardi, M., Pescarollo, A., Bondanza, A., Peccatori, J., Rossini, S., Magnani, Z., Salomoni, M., Benati, C., Ponzoni, M., Callegaro, L., Corradini, P., Bregni, M., Traversari, C. & Bordignon, C. (2007) Antitumor effects of HSV-TK-engineered donor lymphocytes after allogeneic stem-cell transplantation. Blood, 109, 4698-4707.
11. Ciceri, F., Bonini, C., Stanghellini, M.T., Bondanza, A., Traversari, C., Salomoni, M., Turchetto, L., Colombi, S., Bernardi, M., Peccatori, J., Pescarollo, A., Servida, P., Magnani, Z., Perna, S.K., Valtolina, V., Crippa, F., Callegaro, L., Spoldi, E., Crocchiolo, R., Fleischhauer, K., Ponzoni, M., Vago, L., Rossini, S., Santoro, A., Todisco, E., Apperley, J., Olavarria, E., Slavin, S., Weissinger, E.M., Ganser, A., Stadler, M., Yannaki, E., Fassas, A., Anagnostopoulos, A., Bregni, M., Stampino, C.G., Bruzzi, P. & Bordignon, C. (2009) Infusion of suicide-gene-engineered donor lymphocytes after family haploidentical haemopoietic stem-cell transplantation for leukaemia (the TK007 trial): a non-randomised phase I-II study. Lancet Oncol, 10, 489-500.
12. Cobbold, M., Khan, N., Pourgheysari, B., Tauro, S., McDonald, D., Osman, H., Assenmacher, M., Billingham, L., Steward, C., Crawley, C., Olavarria, E., Goldman, J., Chakraverty, R., Mahendra, P., Craddock, C. & Moss, P.A. (2005) Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. Journal of Experimental Medicine, 202, 379-386.
13. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A. & Zhang, F. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-823.
14. Cruz, C.R., Micklethwaite, K.P., Savoldo, B., Ramos, C.A., Lam, S., Ku, S., Diouf, O., Liu, E., Barrett, A.J., Ito, S., Shpall, E.J., Krance, R.A., Kamble, R.T., Carrum, G., Hosing, C.M., Gee, A.P., Mei, Z., Grilley, B.J., Heslop, H.E., Rooney, C.M., Brenner, M.K., Bollard, C.M. & Dotti, G. (2013) 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, 122, 2965-2973.
15. Davila, M.L., Riviere, I., Wang, X., Bartido, S., Park, J., Curran, K., Chung, S.S., Stefanski, J., Borquez-Ojeda, O., Olszewska, M., Qu, J., Wasielewska, T., He, Q., Fink, M., Shinglot, H., Youssif, M., Satter, M., Wang, Y., Hosey, J., Quintanilla, H., Halton, E., Bernal, Y., Bouhassira, D.C., Arcila, M.E., Gonen, M., Roboz, G.J., Maslak, P., Douer, D., Frattini, M.G., Giralt, S., Sadelain, M. & Brentjens, R. (2014) Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med, 6, 224ra225.
16. Demaison, C., Parsley, K., Brouns, G., Scherr, M., Battmer, K., Kinnon, C., Grez, M. & Thrasher, A.J. (2002) High-level transduction and gene expression in hematopoietic repopulating cells using a human imunodeficiency virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Human Gene Therapy, 13, 803-813.
17. Di Stasi, A., Tey, S.K., Dotti, G., Fujita, Y., Kennedy-Nasser, A., Martinez, C., Straathof, K., Liu, E., Durett, A.G., Grilley, B., Liu, H., Cruz, C.R., Savoldo, B., Gee, A.P., Schindler, J., Krance, R.A., Heslop, H.E., Spencer, D.M., Rooney, C.M. & Brenner, M.K. (2011) Inducible apoptosis as a safety switch for adoptive cell therapy. New England Journal of Medicine, 365, 1673-1683.
18. Ding, S., Wu, X., Li, G., Han, M., Zhuang, Y. & Xu, T. (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell, 122, 473-483.
19. Dull, T., Zufferey, R., Kelly, M., Mandel, R.J., Nguyen, M., Trono, D. & Naldini, L. (1998) A third-generation lentivirus vector with a conditional packaging system. The Journal of Virology, 72, 8463-8471.
20. Ferrari, G., Rossini, S., Nobili, N., Maggioni, D., Garofalo, A., Giavazzi, R., Mavilio, F. & Bordignon, C. (1992) Transfer of the ADA gene into human ADA-deficient T lymphocytes reconstitutes specific immune functions. Blood, 80, 1120-1124.
21. Feuchtinger, T., Matthes-Martin, S., Richard, C., Lion, T., Fuhrer, M., Hamprecht, K., Handgretinger, R., Peters, C., Schuster, F.R., Beck, R., Schumm, M., Lotfi, R., Jahn, G. & Lang, P. (2006) Safe adoptive transfer of virus-specific T-cell immunity for the treatment of systemic adenovirus infection after allogeneic stem cell transplantation. British Journal of Haematology, 134, 64-76.
22. Field, A.C., Vink, C., Gabriel, R., Al-Subki, R., Schmidt, M., Goulden, N., Stauss, H., Thrasher, A., Morris, E. & Qasim, W. (2013) Comparison of lentiviral and sleeping beauty mediated alphabeta T cell receptor gene transfer. PLoS ONE, 8, e68201.
23. Gattinoni, L., Lugli, E., Ji, Y., Pos, Z., Paulos, C.M., Quigley, M.F., Almeida, J.R., Gostick, E., Yu, Z., Carpenito, C., Wang, E., Douek, D.C., Price, D.A., June, C.H., Marincola, F.M., Roederer, M. & Restifo, N.P. (2011) A human memory T cell subset with stem cell-like properties. Nature Medicine, 17, 1290-1297.
24. Grupp, S.A., Kalos, M., Barrett, D., Aplenc, R., Porter, D.L., Rheingold, S.R., Teachey, D.T., Chew, A., Hauck, B., Wright, J.F., Milone, M.C., Levine, B.L. & June, C.H. (2013) Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. New England Journal of Medicine, 368, 1509-1518.
25. Hacein-Bey-Abina, S., Von Kalle, C., Schmidt, M., Le Deist, F., Wulffraat, N., McIntyre, E., Radford, I., Villeval, J.L., Fraser, C.C., Cavazzana-Calvo, M. & Fischer, A. (2003) A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. New England Journal of Medicine, 348, 255-256.
26. Hacein-Bey-Abina, S., Garrigue, A., Wang, G.P., Soulier, J., Lim, A., Morillon, E., Clappier, E., Caccavelli, L., Delabesse, E., Beldjord, K., Asnafi, V., Macintyre, E., Dal, C.L., Radford, I., Brousse, N., Sigaux, F., Moshous, D., Hauer, J., Borkhardt, A., Belohradsky, B.H., Wintergerst, U., Velez, M.C., Leiva, L., Sorensen, R., Wulffraat, N., Blanche, S., Bushman, F.D., Fischer, A. & Cavazzana-Calvo, M. (2008) Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest., 118, 3132-3142.
27. Hart, D.P., Xue, S.A., Thomas, S., Cesco-Gaspere, M., Tranter, A., Willcox, B., Lee, S.P., Steven, N., Morris, E.C. & Stauss, H.J. (2008) Retroviral transfer of a dominant TCR prevents surface expression of a large proportion of the endogenous TCR repertoire in human T cells. Gene Therapy, 15, 625-631.
28. Heinrich, T., Rengstl, B., Muik, A., Petkova, M., Schmid, F., Wistinghausen, R., Warner, K., Crispatzu, G., Hansmann, M.L., Herling, M., von Laer, D. & Newrzela, S. (2013) Mature T-cell lymphomagenesis induced by retroviral insertional activation of Janus kinase 1. Molecular Therapy, 21, 1160-1168.
29. Heslop, H.E., Ng, C.Y., Li, C., Smith, C.A., Loftin, S.K., Krance, R.A., Brenner, M.K. & Rooney, C.M. (1996) Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nature Medicine, 2, 551-555.
30. Heslop, H.E., Slobod, K.S., Pule, M.A., Hale, G.A., Rousseau, A., Smith, C.A., Bollard, C.M., Liu, H., Wu, M.F., Rochester, R.J., Amrolia, P.J., Hurwitz, J.L., Brenner, M.K. & Rooney, C.M. (2010) Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood, 115, 925-935.
31. Hinrichs, C.S., Borman, Z.A., Gattinoni, L., Yu, Z., Burns, W.R., Huang, J., Klebanoff, C.A., Johnson, L.A., Kerkar, S.P., Yang, S., Muranski, P., Palmer, D.C., Scott, C.D., Morgan, R.A., Robbins, P.F., Rosenberg, S.A. & Restifo, N.P. (2011) Human effector CD8+ T cells derived from naive rather than memory subsets possess superior traits for adoptive immunotherapy. Blood, 117, 808-814.
32. Ho, V.T. & Soiffer, R.J. (2001) The history and future of T-cell depletion as graft-versus-host disease prophylaxis for allogeneic hematopoietic stem cell transplantation. Blood, 98, 3192-3204.
33. Howe, S.J., Mansour, M.R., Schwarzwaelder, K., Bartholomae, C., Hubank, M., Kempski, H., Brugman, M.H., Pike-Overzet, K., Chatters, S.J., de Ridder, D., Gilmour, K.C., Adams, S., Thornhill, S.I., Parsley, K.L., Staal, F.J., Gale, R.E., Linch, D.C., Bayford, J., Brown, L., Quaye, M., Kinnon, C., Ancliff, P., Webb, D.K., Schmidt, M., Von Kalle, C., Gaspar, H.B. & Thrasher, A.J. (2008) Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest., 118, 3143-3150.
34. Humphries, C. (2013) Adoptive cell therapy: Honing that killer instinct. Nature, 504, S13-S15.
35. Ivics, Z. & Izsvak, Z. (2011) Nonviral gene delivery with the sleeping beauty transposon system. Human Gene Therapy, 22, 1043-1051.
36. Ivics, Z., Hackett, P.B., Plasterk, R.H. & Izsvak, Z. (1997) Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell, 91, 501-510.
37. Jensen, M.C., Popplewell, L., Cooper, L.J., DiGiusto, D., Kalos, M., Ostberg, J.R. & Forman, S.J. (2010) 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, 16, 1245-1256.
38. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A. & Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
39. Johnson, L.A., Morgan, R.A., Dudley, M.E., Cassard, L., Yang, J.C., Hughes, M.S., Kammula, U.S., Royal, R.E., Sherry, R.M., Wunderlich, J.R., Lee, C.C., Restifo, N.P., Schwarz, S.L., Cogdill, A.P., Bishop, R.J., Kim, H., Brewer, C.C., Rudy, S.F., VanWaes, C., Davis, J.L., Mathur, A., Ripley, R.T., Nathan, D.A., Laurencot, C.M. & Rosenberg, S.A. (2009) Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood, 114, 535-546.
40. Kalos, M., Levine, B.L., Porter, D.L., Katz, S., Grupp, S.A., Bagg, A. & June, C.H. (2011) T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med, 3, 95ra73.
41. Katsnelson, A. (2013) Drug development: target practice. Nature, 498, S8-S9.
42. Kershaw, M.H., Westwood, J.A., Parker, L.L., Wang, G., Eshhar, Z., Mavroukakis, S.A., White, D.E., Wunderlich, J.R., Canevari, S., Rogers-Freezer, L., Chen, C.C., Yang, J.C., Rosenberg, S.A. & Hwu, P. (2006) A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clinical Cancer Research, 12, 6106-6115.
43. Kochenderfer, J.N., Wilson, W.H., Janik, J.E., Dudley, M.E., Stetler-Stevenson, M., Feldman, S.A., Maric, I., Raffeld, M., Nathan, D.A., Lanier, B.J., Morgan, R.A. & Rosenberg, S.A. (2010) Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood, 116, 4099-4102.
44. Kochenderfer, J.N., Dudley, M.E., Feldman, S.A., Wilson, W.H., Spaner, D.E., Maric, I., Stetler-Stevenson, M., Phan, G.Q., Hughes, M.S., Sherry, R.M., Yang, J.C., Kammula, U.S., Devillier, L., Carpenter, R., Nathan, D.A., Morgan, R.A., Laurencot, C. & Rosenberg, S.A. (2012) B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood, 119, 2709-2720.
45. Kochenderfer, J.N., Dudley, M.E., Carpenter, R.O., Kassim, S.H., Rose, J.J., Telford, W.G., Hakim, F.T., Halverson, D.C., Fowler, D.H., Hardy, N.M., Mato, A.R., Hickstein, D.D., Gea-Banacloche, J.C., Pavletic, S.Z., Sportes, C., Maric, I., Feldman, S.A., Hansen, B.G., Wilder, J.S., Blacklock-Schuver, B., Jena, B., Bishop, M.R., Gress, R.E. & Rosenberg, S.A. (2013) Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood, 122, 4129-4139.
46. Lamers, C.H., Willemsen, R., van Elzakker, P., van Steenbergen-Langeveld, S., Broertjes, M., Oosterwijk-Wakka, J., Oosterwijk, E., Sleijfer, S., Debets, R. & Gratama, J.W. (2011) Immune responses to transgene and retroviral vector in patients treated with ex vivo-engineered T cells. Blood, 117, 72-82.
47. Lee, D.S.N., Shah, N.N., StelerStevenson, M., Sabatino, M., Delbrook, C., Richards, K., Kockenderfer, J., Rosenberg, S., Stroncek, D., Wayne, A. & Mckall, C. (2013) Anti-CD19 Chimeric Antigen Receptor (CAR) T cells produce complete responses with acceptable toxicity but without chronic B-cell Aplasia in children with relapsed or refractory Acute Lymphoblastic Leukemia (ALL) even after allogeneic Hematopoietic Stem Cell Transplantation (HSCT). Blood, 122, 68.
48. Leen, A.M., Christin, A., Myers, G.D., Liu, H., Cruz, C.R., Hanley, P.J., Kennedy-Nasser, A.A., Leung, K.S., Gee, A.P., Krance, R.A., Brenner, M.K., Heslop, H.E., Rooney, C.M. & Bollard, C.M. (2009) Cytotoxic T lymphocyte therapy with donor T cells prevents and treats adenovirus and Epstein-Barr virus infections after haploidentical and matched unrelated stem cell transplantation. Blood, 114, 4283-4292.
49. Linette, G.P., Stadtmauer, E.A., Maus, M.V., Rapoport, A.P., Levine, B.L., Emery, L., Litzky, L., Bagg, A., Carreno, B.M., Cimino, P.J., Binder-Scholl, G.K., Smethurst, D.P., Gerry, A.B., Pumphrey, N.J., Bennett, A.D., Brewer, J.E., Dukes, J., Harper, J., Tayton-Martin, H.K., Jakobsen, B.K., Hassan, N.J., Kalos, M. & June, C.H. (2013) Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood, 122, 863-871.
50. Lombardo, A., Genovese, P., Beausejour, C.M., Colleoni, S., Lee, Y.L., Kim, K.A., Ando, D., Urnov, F.D., Galli, C., Gregory, P.D., Holmes, M.C. & Naldini, L. (2007) Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nature Biotechnology, 25, 1298-1306.
51. Louis, C.U., Savoldo, B., Dotti, G., Pule, M., Yvon, E., Myers, G.D., Rossig, C., Russell, H.V., Diouf, O., Liu, E., Liu, H., Wu, M.F., Gee, A.P., Mei, Z., Rooney, C.M., Heslop, H.E. & Brenner, M.K. (2011) Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood, 118, 6050-6056.
52. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E. & Church, G.M. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823-826.
53. Mavilio, F., Ferrari, G., Rossini, S., Nobili, N., Bonini, C., Casorati, G., Traversari, C. & Bordignon, C. (1994) Peripheral blood lymphocytes as target cells of retroviral vector- mediated gene transfer. Blood, 83, 1988-1997.
54. Miller, A.D. & Buttimore, C. (1986) Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Molecular and Cellular Biology, 6, 2895-2902.
55. Miller, J.C., Tan, S., Qiao, G., Barlow, K.A., Wang, J., Xia, D.F., Meng, X., Paschon, D.E., Leung, E., Hinkley, S.J., Dulay, G.P., Hua, K.L., Ankoudinova, I., Cost, G.J., Urnov, F.D., Zhang, H.S., Holmes, M.C., Zhang, L., Gregory, P.D. & Rebar, E.J. (2011) A TALE nuclease architecture for efficient genome editing. Nature Biotechnology, 29, 143-148.
56. Milone, M.C., Fish, J.D., Carpenito, C., Carroll, R.G., Binder, G.K., Teachey, D., Samanta, M., Lakhal, M., Gloss, B., Danet-Desnoyers, G., Campana, D., Riley, J.L., Grupp, S.A. & June, C.H. (2009) Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Molecular Therapy, 17, 1453-1464.
57. Montini, E., Cesana, D., Schmidt, M., Sanvito, F., Bartholomae, C.C., Ranzani, M., Benedicenti, F., Sergi, L.S., Ambrosi, A., Ponzoni, M., Doglioni, C., Di, S.C., von, K.C. & Naldini, L. (2009) 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., 119, 964-975.
58. Morgan, R.A., Dudley, M.E., Wunderlich, J.R., Hughes, M.S., Yang, J.C., Sherry, R.M., Royal, R.E., Topalian, S.L., Kammula, U.S., Restifo, N.P., Zheng, Z., Nahvi, A., de Vries, C.R., Rogers-Freezer, L.J., Mavroukakis, S.A. & Rosenberg, S.A. (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science, 314, 126-129.
59. Morgan, R.A., Chinnasamy, N., Abate-Daga, D., Gros, A., Robbins, P.F., Zheng, Z., Dudley, M.E., Feldman, S.A., Yang, J.C., Sherry, R.M., Phan, G.Q., Hughes, M.S., Kammula, U.S., Miller, A.D., Hessman, C.J., Stewart, A.A., Restifo, N.P., Quezado, M.M., Alimchandani, M., Rosenberg, A.Z., Nath, A., Wang, T., Bielekova, B., Wuest, S.C., Akula, N., McMahon, F.J., Wilde, S., Mosetter, B., Schendel, D.J., Laurencot, C.M. & Rosenberg, S.A. (2013) Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. Journal of Immunotherapy, 36, 133-151.
60. Naldini, L., Blomer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F.H., Verma, I.M. & Trono, D. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science, 272, 263-267.
61. Newrzela, S., Cornils, K., Li, Z., Baum, C., Brugman, M.H., Hartmann, M., Meyer, J., Hartmann, S., Hansmann, M.L., Fehse, B. & von Laer, D. (2008) Resistance of mature T cells to oncogene transformation. Blood, 112, 2278-2286.
62. Ochi, T., Fujiwara, H., Okamoto, S., An, J., Nagai, K., Shirakata, T., Mineno, J., Kuzushima, K., Shiku, H. & Yasukawa, M. (2011) Novel adoptive T-cell immunotherapy using a WT1-specific TCR vector encoding silencers for endogenous TCRs shows marked antileukemia reactivity and safety. Blood, 118, 1495-1503.
63. Ott, M.G., Schmidt, M., Schwarzwaelder, K., Stein, S., Siler, U., Koehl, U., Glimm, H., Kuhlcke, K., Schilz, A., Kunkel, H., Naundorf, S., Brinkmann, A., Deichmann, A., Fischer, M., Ball, C., Pilz, I., Dunbar, C., Du, Y., Jenkins, N.A., Copeland, N.G., Luthi, U., Hassan, M., Thrasher, A.J., Hoelzer, D., Von Kalle, C., Seger, R. & Grez, M. (2006) Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nature Medicine, 12, 401-409.
64. Park, J.R., Digiusto, D.L., Slovak, M., Wright, C., Naranjo, A., Wagner, J., Meechoovet, H.B., Bautista, C., Chang, W.C., Ostberg, J.R. & Jensen, M.C. (2007) Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Molecular Therapy, 15, 825-833.
65. Parkhurst, M.R., Yang, J.C., Langan, R.C., Dudley, M.E., Nathan, D.A., Feldman, S.A., Davis, J.L., Morgan, R.A., Merino, M.J., Sherry, R.M., Hughes, M.S., Kammula, U.S., Phan, G.Q., Lim, R.M., Wank, S.A., Restifo, N.P., Robbins, P.F., Laurencot, C.M. & Rosenberg, S.A. (2011) T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Molecular Therapy, 19, 620-626.
66. Peggs, K.S., Verfuerth, S., Pizzey, A., Khan, N., Guiver, M., Moss, P.A. & Mackinnon, S. (2003) Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet, 362, 1375-1377.
67. Peggs, K.S., Thomson, K., Samuel, E., Dyer, G., Armoogum, J., Chakraverty, R., Pang, K., Mackinnon, S. & Lowdell, M.W. (2011) Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stem cell transplantation. Clinical Infectious Diseases, 52, 49-57.
68. Porter, D.L., Levine, B.L., Kalos, M., Bagg, A. & June, C.H. (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. New England Journal of Medicine, 365, 725-733.
69. Provasi, E., Genovese, P., Lombardo, A., Magnani, Z., Liu, P.Q., Reik, A., Chu, V., Paschon, D.E., Zhang, L., Kuball, J., Camisa, B., Bondanza, A., Casorati, G., Ponzoni, M., Ciceri, F., Bordignon, C., Greenberg, P.D., Holmes, M.C., Gregory, P.D., Naldini, L. & Bonini, C. (2012) Editing T cell specificity towards leukemia by zinc finger nucleases and lentiviral gene transfer. Nature Medicine, 18, 807-815.
70. Pule, M.A., Savoldo, B., Myers, G.D., Rossig, C., Russell, H.V., Dotti, G., Huls, M.H., Liu, E., Gee, A.P., Mei, Z., Yvon, E., Weiss, H.L., Liu, H., Rooney, C.M., Heslop, H.E. & Brenner, M.K. (2008) Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nature Medicine, 14, 1264-1270.
71. Qasim, W., Mackey, T., Sinclair, J., Chatziandreou, I., Kinnon, C., Thrasher, A.J. & Gaspar, H.B. (2007) Lentiviral vectors for T-cell suicide gene therapy: preservation of T-cell effector function after cytokine-mediated transduction. Molecular Therapy, 15, 355-360.
72. Qasim, W., Gilmour, K., Zhan, H., Derniame, S., McNicol, A.M., Ip, W., Hiwarkar, P., Veys, P. & Gaspar, H.B. (2013a) Interferon-gamma capture T cell therapy for persistent Adenoviraemia following allogeneic haematopoietic stem cell transplantation. British Journal of Haematology, 161, 449-452.
73. Qasim, W., Brunetto, M., Gehring, A., Xue, S.A., Zhan, H., Ciccorossi, P., Gilmour, K., Cavallone, D., Moriconi, F., Farzhenah, F., Mazzoni, A., Chan, L., Morris, E., Thrasher, A., Maini, M., Bonino, F., Stauss, H. & Bertoletti, A. (2013b) Therapy with T cell receptor gene modified T cells targeting HBsAg-producing HCC metastases. Journal of Hepatology, 58, S107.
74. Recchia, A., Bonini, C., Magnani, Z., Urbinati, F., Sartori, D., Muraro, S., Tagliafico, E., Bondanza, A., Stanghellini, M.T., Bernardi, M., Pescarollo, A., Ciceri, F., Bordignon, C. & Mavilio, F. (2006) Retroviral vector integration deregulates gene expression but has no consequence on the biology and function of transplanted T cells. Proceedings of the National Academy of Sciences of the United States of America, 103, 1457-1462.
75. Ricciardelli, I., Brewin, J., Lugthart, G., Albon, S.J., Pule, M. & Amrolia, P.J. (2013) Rapid generation of EBV-specific cytotoxic T lymphocytes resistant to calcineurin inhibitors for adoptive immunotherapy. American Journal of Transplantation, 13, 3244-3252.
76. Ritchie, D.S., Neeson, P.J., Khot, A., Peinert, S., Tai, T., Tainton, K., Chen, K., Shin, M., Wall, D.M., Honemann, D., Gambell, P., Westerman, D.A., Haurat, J., Westwood, J.A., Scott, A.M., Kravets, L., Dickinson, M., Trapani, J.A., Smyth, M.J., Darcy, P.K., Kershaw, M.H. & Prince, H.M. (2013) Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Molecular Therapy, 21, 2122-2129.
77. Robbins, P.F., Morgan, R.A., Feldman, S.A., Yang, J.C., Sherry, R.M., Dudley, M.E., Wunderlich, J.R., Nahvi, A.V., Helman, L.J., Mackall, C.L., Kammula, U.S., Hughes, M.S., Restifo, N.P., Raffeld, M., Lee, C.C., Levy, C.L., Li, Y.F., El-Gamil, M., Schwarz, S.L., Laurencot, C. & Rosenberg, S.A. (2011) Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. Journal of Clinical Oncology, 29, 917-924.
78. Rosenberg, S.A., Aebersold, P., Cornetta, K., Kasid, A., Morgan, R.A., Moen, R., Karson, E.M., Lotze, M.T., Yang, J.C. & Topalian, S.L. (1990) Gene transfer into humans-immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. New England Journal of Medicine, 323, 570-578.
79. Sadelain, M., Brentjens, R. & Riviere, I. (2013) The basic principles of chimeric antigen receptor design. Cancer Discov, 3, 388-398.
80. Sangiolo, D., Lesnikova, M., Nash, R.A., Jensen, M.C., Nikitine, A., Kiem, H.P. & Georges, G.E. (2007) Lentiviral vector conferring resistance to mycophenolate mofetil and sensitivity to ganciclovir for in vivo T-cell selection. Gene Therapy, 14, 1549-1554.
81. Savoldo, B., Ramos, C.A., Liu, E., Mims, M.P., Keating, M.J., Carrum, G., Kamble, R.T., Bollard, C.M., Gee, A.P., Mei, Z., Liu, H., Grilley, B., Rooney, C.M., Heslop, H.E., Brenner, M.K. & Dotti, G. (2011) CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J. Clin. Invest, 121, 1822-1826.
82. Schmitt, T.M., Aggen, D.H., Stromnes, I.M., Dossett, M.L., Richman, S.A., Kranz, D.M. & Greenberg, P.D. (2013) Enhanced-affinity murine T-cell receptors for tumor/self-antigens can be safe in gene therapy despite surpassing the threshold for thymic selection. Blood, 122, 348-356.
83. Scholler, J., Brady, T.L., Binder-Scholl, G., Hwang, W.T., Plesa, G., Hege, K.M., Vogel, A.N., Kalos, M., Riley, J.L., Deeks, S.G., Mitsuyasu, R.T., Bernstein, W.B., Aronson, N.E., Levine, B.L., Bushman, F.D. & June, C.H. (2012) Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells. Sci Transl Med, 4, 132ra153.
84. Schroder, A.R., Shinn, P., Chen, H., Berry, C., Ecker, J.R. & Bushman, F. (2002) HIV-1 integration in the human genome favors active genes and local hotspots. Cell, 110, 521-529.
85. Singh, H., Huls, H., Kebriaei, P. & Cooper, L.J. (2014) A new approach to gene therapy using Sleeping Beauty to genetically modify clinical-grade T cells to target CD19. Immunological Reviews, 257, 181-190.
86. Tebas, P., Stein, D., Tang, W.W., Frank, I., Wang, S.Q., Lee, G., Spratt, S.K., Surosky, R.T., Giedlin, M.A., Nichol, G., Holmes, M.C., Gregory, P.D., Ando, D.G., Kalos, M., Collman, R.G., Binder-Scholl, G., Plesa, G., Hwang, W.T., Levine, B.L. & June, C.H. (2014) Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. New England Journal of Medicine, 370, 901-910.
87. Tiberghien, P., Ferrand, C., Lioure, B., Milpied, N., Angonin, R., Deconinck, E., Certoux, J.M., Robinet, E., Saas, P., Petracca, B., Juttner, C., Reynolds, C.W., Longo, D.L., Herve, P. & Cahn, J.Y. (2001) Administration of herpes simplex-thymidine kinase-expressing donor T cells with a T-cell-depleted allogeneic marrow graft. Blood, 97, 63-72.
88. Till, B.G., Jensen, M.C., Wang, J., Chen, E.Y., Wood, B.L., Greisman, H.A., Qian, X., James, S.E., Raubitschek, A., Forman, S.J., Gopal, A.K., Pagel, J.M., Lindgren, C.G., Greenberg, P.D., Riddell, S.R. & Press, O.W. (2008) Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood, 112, 2261-2271.
89. Torikai, H., Reik, A., Liu, P.Q., Zhou, Y., Zhang, L., Maiti, S., Huls, H., Miller, J.C., Kebriaei, P., Rabinovitch, B., Lee, D.A., Champlin, R.E., Bonini, C., Naldini, L., Rebar, E.J., Gregory, P.D., Holmes, M.C. & Cooper, L.J. (2012) A foundation for universal T-cell based immunotherapy: T cells engineered to express a CD19-specific chimeric-antigen-receptor and eliminate expression of endogenous TCR. Blood, 119, 5697-5705.
90. Torikai, H., Reik, A., Soldner, F., Warren, E.H., Yuen, C., Zhou, Y., Crossland, D.L., Huls, H., Littman, N., Zhang, Z., Tykodi, S.S., Kebriaei, P., Lee, D.A., Miller, J.C., Rebar, E.J., Holmes, M.C., Jaenisch, R., Champlin, R.E., Gregory, P.D. & Cooper, L.J. (2013) Toward eliminating HLA class I expression to generate universal cells from allogeneic donors. Blood, 122, 1341-1349.
91. Urnov, F.D., Miller, J.C., Lee, Y.L., Beausejour, C.M., Rock, J.M., Augustus, S., Jamieson, A.C., Porteus, M.H., Gregory, P.D. & Holmes, M.C. (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature, 435, 646-651.
92. Walter, E.A., Greenberg, P.D., Gilbert, M.J., Finch, R.J., Watanabe, K.S., Thomas, E.D. & Riddell, S.R. (1995) Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. New England Journal of Medicine, 333, 1038-1044.
93. Xue, S.A., Gao, L., Hart, D., Gillmore, R., Qasim, W., Thrasher, A., Apperley, J., Engels, B., Uckert, W., Morris, E. & Stauss, H.J. (2005) Elimination of human leukemia cells in NOD/SCID mice by WT1-TCR gene transduced human T cells. Blood, 106, 3062-3067.
94. Yam, P., Jensen, M., Akkina, R., Anderson, J., Villacres, M.C., Wu, J., Zaia, J.A. & Yee, J.K. (2006) Ex vivo selection and expansion of cells based on expression of a mutated inosine monophosphate dehydrogenase 2 after HIV vector transduction: effects on lymphocytes, monocytes, and CD34+ stem cells. Molecular Therapy, 14, 236-244.
95. Zhan, H., Gilmour, K., Chan, L., Farzaneh, F., McNicol, A.M., Xu, J.H., Adams, S., Fehse, B., Veys, P., Thrasher, A., Gaspar, H. & Qasim, W. (2013) Production and first-in-man use of T cells engineered to express a HSVTK-CD34 sort-suicide gene. PLoS ONE, 8, e77106.
96. Zhao, Y., Zheng, Z., Cohen, C.J., Gattinoni, L., Palmer, D.C., Restifo, N.P., Rosenberg, S.A. & Morgan, R.A. (2006) High-efficiency transfection of primary human and mouse T lymphocytes using RNA electroporation. Molecular Therapy, 13, 151-159.
97. Zufferey, R., Donello, J.E., Trono, D. & Hope, T.J. (1999) Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. The Journal of Virology, 73, 2886-2892.