Genetically modulating T-cell function to target cancer

Seminars in Cancer Biology

Volumn 22, Issue 1, 2012, Pages 14-22

  Merhavi Shoham, Efrat ^a   Haga Friedman, Astar ^a   Cohen, Cyrille J ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Genetic immune modulation; TCR; TCR gene transfer; Tumor antigens

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; LENTIVIRUS VECTOR; LYMPHOCYTE ANTIGEN RECEPTOR; MESSENGER RNA; RETROVIRUS VECTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIGEN SPECIFICITY; CANCER RESEARCH; CELL SELECTION; CLINICAL EFFECTIVENESS; DNA MODIFICATION; DNA POLYMORPHISM; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENE TRANSFER; GENETIC ENGINEERING; HUMAN; IMMUNOMODULATION; IMMUNOREACTIVITY; NEOPLASM; NONHUMAN; PATIENT SAFETY; REVIEW; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE RECEPTOR ALPHA CHAIN GENE; T LYMPHOCYTE RECEPTOR BETA CHAIN GENE; T LYMPHOCYTE RECEPTOR GENE; T LYMPHOCYTE SUBPOPULATION; TARGET CELL; TRANSGENE;

GENE REARRANGEMENT; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENES, T-CELL RECEPTOR; GENETIC VECTORS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84857141254     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2011.12.006     Document Type: Review

References (143)

1. Rosenberg S.A., Restifo N.P., Yang J.C., Morgan R.A., Dudley M.E. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008, 8:299-308.
2. Hawkins R.E., Gilham D.E., Debets R., Eshhar Z., Taylor N., Abken H., et al. Development of adoptive cell therapy for cancer: a clinical perspective. Hum Gene Ther 2010, 21:665-672.
3. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ et al. Durable Complete Responses in Heavily Pretreated Patients with Metastatic Melanoma Using T Cell Transfer Immunotherapy. Clin Cancer Res., doi:10.1158/1078-0432.CCR-11-0116.
4. Dembic Z., Haas W., Weiss S., McCubrey J., Kiefer H., von Boehmer H., et al. Transfer of specificity by murine alpha and beta T-cell receptor genes. Nature 1986, 320:232-238.
5. Clay T.M., Custer M.C., Sachs J., Hwu P., Rosenberg S.A., Nishimura M.I. Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J Immunol 1999, 163:507-513.
6. Kessels H.W., Wolkers M.C., van dB, van der Valk M.A., Schumacher T.N. Immunotherapy through TCR gene transfer. Nat Immunol 2001, 2:957-961.
7. Schmitt T.M., Ragnarsson G.B., Greenberg P.D. T cell receptor gene therapy for cancer. Hum Gene Ther 2009, 20:1240-1248.
8. Udyavar A., Geiger T.L. Rebalancing immune specificity and function in cancer by T-cell receptor gene therapy. Arch Immunol Ther Exp (Warsz) 2010, 58:335-346.
9. Thomas S., Stauss H.J., Morris E.C. Molecular immunology lessons from therapeutic T-cell receptor gene transfer. Immunology 2010, 129:170-177.
10. Morgan R.A., Dudley M.E., Wunderlich J.R., Hughes M.S., Yang J.C., Sherry R.M., et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006, 314:126-129.
11. Johnson L.A., Heemskerk B., Powell D.J., Cohen C.J., Morgan R.A., Dudley M.E., et al. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J Immunol 2006, 177:6548-6559.
12. Johnson L.A., Morgan R.A., Dudley M.E., Cassard L., Yang J.C., Hughes M.S., et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009, 114:535-546.
13. Parkhurst M.R., Yang J.C., Langan R.C., Dudley M.E., Nathan D.A., Feldman S.A., et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 2011, 19:620-626.
14. Davis J.L., Theoret M.R., Zheng Z., Lamers C.H., Rosenberg S.A., Morgan R.A. Development of human anti-murine T-cell receptor antibodies in both responding and nonresponding patients enrolled in TCR gene therapy trials. Clin Cancer Res 2010, 16:5852-5861.
15. Robbins P.F., Morgan R.A., Feldman S.A., Yang J.C., Sherry R.M., Dudley M.E., et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 2011, 29:917-924.
16. Park T.S., Rosenberg S.A., Morgan R.A. Treating cancer with genetically engineered T cells. Trends Biotechnol 2011, 29:550-557.
17. Uckert W., Schumacher T.N. TCR transgenes and transgene cassettes for TCR gene therapy: status in 2008. Cancer Immunol Immunother 2009, 58:809-822.
18. Hinrichs C.S., Borman Z.A., Gattinoni L., Yu Z., Burns W.R., Huang J., et al. Human effector CD8+ T cells derived from naive rather than memory subsets possess superior traits for adoptive immunotherapy. Blood 2011, 117:808-814.
19. Burns W.R., Zheng Z., Rosenberg S.A., Morgan R.A. Lack of specific gamma-retroviral vector long terminal repeat promoter silencing in patients receiving genetically engineered lymphocytes and activation upon lymphocyte restimulation. Blood 2009, 114:2888-2899.
20. van Loenen M.M., Hagedoorn R.S., de Boer R., van Egmond E.H., Falkenburg J.H., Heemskerk M.H. Rapid re-expression of retrovirally introduced versus endogenous TCRs in engineered T cells after antigen-specific stimulation. J Immunother 2011, 34:165-174.
21. Tsuji T., Yasukawa M., Matsuzaki J., Ohkuri T., Chamoto K., Wakita D., et al. Generation of tumor-specific, HLA class I-restricted human Th1 and Tc1 cells by cell engineering with tumor peptide-specific T-cell receptor genes. Blood 2005, 106:470-476.
22. Yang S., Cohen C.J., Peng P.D., Zhao Y., Cassard L., Yu Z., et al. Development of optimal bicistronic lentiviral vectors facilitates high-level TCR gene expression and robust tumor cell recognition. Gene Ther 2008, 15:1411-1423.
23. Jones S., Peng P.D., Yang S., Hsu C., Cohen C.J., Zhao Y., et al. Lentiviral vector design for optimal T cell receptor gene expression in the transduction of peripheral blood lymphocytes and tumor-infiltrating lymphocytes. Hum Gene Ther 2009, 20:630-640.
24. Circosta P., Granziero L., Follenzi A., Vigna E., Stella S., Vallario A., et al. T cell receptor (TCR) gene transfer with lentiviral vectors allows efficient redirection of tumor specificity in naive and memory T cells without prior stimulation of endogenous TCR. Hum Gene Ther 2009, 20:1576-1588.
25. Frecha C., Levy C., Cosset F.L., Verhoeyen E. Advances in the field of lentivector-based transduction of T and B lymphocytes for gene therapy. Mol Ther 2010, 18:1748-1757.
26. Levine B.L., Humeau L.M., Boyer J., MacGregor R.R., Rebello T., Lu X., et al. Gene transfer in humans using a conditionally replicating lentiviral vector. Proc Natl Acad Sci U S A 2006, 103:17372-17377.
27. Cavalieri S., Cazzaniga S., Geuna M., Magnani Z., Bordignon C., Naldini L., et al. Human T lymphocytes transduced by lentiviral vectors in the absence of TCR activation maintain an intact immune competence. Blood 2003, 102:497-505.
28. Perro M., Tsang J., Xue S.A., Escors D., Cesco-Gaspere M., Pospori C., et al. Generation of multi-functional antigen-specific human T-cells by lentiviral TCR gene transfer. Gene Ther 2010, 17:721-732.
29. Kerkar S.P., Sanchez-Perez L., Yang S., Borman Z.A., Muranski P., Ji Y., et al. Genetic engineering of murine CD8(+) and CD4(+) T cells for preclinical adoptive immunotherapy studies. J Immunother 2011, 34:343-352.
30. Peng P.D., Cohen C.J., Yang S., Hsu C., Jones S., Zhao Y., et al. Efficient nonviral sleeping beauty transposon-based TCR gene transfer to peripheral blood lymphocytes confers antigen-specific antitumor reactivity. Gene Ther 2009, 16:1042-1049.
31. Till B.G., Jensen M.C., Wang J., Chen E.Y., Wood B.L., Greisman H.A., et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood 2008, 112:2261-2271.
32. Zhao Y., Zheng Z., Cohen C.J., Gattinoni L., Palmer D.C., Restifo N.P., et al. High-efficiency transfection of primary human and mouse T lymphocytes using RNA electroporation. Mol Ther 2006, 13:151-159.
33. Schaft N., Dorrie J., Muller I., Beck V., Baumann S., Schunder T., et al. A new way to generate cytolytic tumor-specific T cells: electroporation of RNA coding for a T cell receptor into T lymphocytes. Cancer Immunol Immunother 2005, 1-10.
34. Rubinstein M.P., Salem M.L., Kadima A.N., Nguyen C.L., Gillanders W.E., Nishimura M.I., et al. Loss of T cell-mediated antitumor immunity after construct-specific downregulation of retrovirally encoded T-cell receptor expression in vivo. Cancer Gene Ther 2009, 16:171-183.
35. Dossett M.L., Teague R.M., Schmitt T.M., Tan X., Cooper L.J., Pinzon C., et al. Adoptive immunotherapy of disseminated leukemia with TCR-transduced, CD8+ T cells expressing a known endogenous TCR. Mol Ther 2009, 17:742-749.
36. Mizuguchi H., Xu Z., Ishii-Watabe A., Uchida E., Hayakawa T. IRES-dependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol Ther 2000, 1:376-382.
37. Szymczak A.L., Vignali D.A. Development of 2A peptide-based strategies in the design of multicistronic vectors. Expert Opin Biol Ther 2005, 5:627-638.
38. Leisegang M., Engels B., Meyerhuber P., Kieback E., Sommermeyer D., Xue S.A., et al. Enhanced functionality of T cell receptor-redirected T cells is defined by the transgene cassette. J Mol Med 2008, 86:573-583.
39. Govers C., Sebestyen Z., Coccoris M., Willemsen R.A., Debets R. T cell receptor gene therapy: strategies for optimizing transgenic TCR pairing. Trends Mol Med 2010, 16:77-87.
40. van Loenen M.M., de Boer R., Amir A.L., Hagedoorn R.S., Volbeda G.L., Willemze R., et al. Mixed T cell receptor dimers harbor potentially harmful neoreactivity. Proc Natl Acad Sci U S A 2010, 107:10972-10977.
41. Bendle G.M., Linnemann C., Hooijkaas A.I., Bies L., de Witte M.A., Jorritsma A., et al. Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med 2010, 16:565-570. 1p.
42. Stanislawski T., Voss R.H., Lotz C., Sadovnikova E., Willemsen R.A., Kuball J., et al. Circumventing tolerance to a human MDM2-derived tumor antigen by TCR gene transfer. Nat Immunol 2001, 2:962-970.
43. Cohen C.J., Zhao Y., Zheng Z., Rosenberg S.A., Morgan R.A. Enhanced antitumor activity of murine-human hybrid T-Cell Receptor (TCR) in human lymphocytes is associated with improved pairing and TCR/CD3 stability. Cancer Res 2006, 66:8878-8886.
44. Voss R.H., Kuball J., Engel R., Guillaume P., Romero P., Huber C., et al. Redirection of T cells by delivering a transgenic mouse-derived MDM2 tumor antigen-specific TCR and its humanized derivative is governed by the CD8 coreceptor and affects natural human TCR expression. Immunol Res 2006, 34:67-87.
45. Thomas S., Xue S.A., Cesco-Gaspere M., San Jose E., Hart D.P., Wong V., et al. Targeting the Wilms tumor antigen 1 by TCR gene transfer: TCR variants improve tetramer binding but not the function of gene modified human T cells. J Immunol 2007, 179:5803-5810.
46. Bialer G., Horovitz-Fried M., Ya'acobi S., Morgan R.A., Cohen C.J. Selected murine residues endow human TCR with enhanced tumor recognition. J Immunol 2010, 184:6232-6241.
47. Sommermeyer D., Uckert W. Minimal amino acid exchange in human TCR constant regions fosters improved function of TCR gene-modified T cells. J Immunol 2010, 184:6223-6231.
48. Boulter J.M., Glick M., Todorov P.T., Baston E., Sami M., Rizkallah P., et al. Stable, soluble T-cell receptor molecules for crystallization and therapeutics. Protein Eng 2003, 16:707-711.
49. Cohen C.J., Li Y.F., El Gamil M., Robbins P.F., Rosenberg S.A., Morgan R.A. Enhanced antitumor activity of T cells engineered to express T-cell receptors with a second disulfide bond. Cancer Res 2007, 67:3898-3903.
50. Kuball J., Dossett M.L., Wolfl M., Ho W.Y., Voss R.H., Fowler C., et al. Facilitating matched pairing and expression of TCR chains introduced into human T cells. Blood 2007, 109:2331-2338.
51. Voss R.H., Willemsen R.A., Kuball J., Grabowski M., Engel R., Intan R.S., et al. Molecular design of the Calphabeta interface favors specific pairing of introduced TCR alphabeta in human T cells. J Immunol 2008, 180:391-401.
52. Sebestyen Z., Schooten E., Sals T., Zaldivar I., San Jose E., Alarcon B., et al. Human TCR That Incorporate CD3{zeta} induce highly preferred pairing between TCR{alpha} and {beta} chains following gene transfer. J Immunol 2008, 180:7736-7746.
53. Chung S., Wucherpfennig K.W., Friedman S.M., Hafler D.A., Strominger J.L. Functional three-domain single-chain T-cell receptors. Proc Natl Acad Sci U S A 1994, 91:12654-12658.
54. Zhang T., He X., Tsang T.C., Harris D.T., Transgenic TCR expression: comparison of single chain with full-length receptor constructs for T-cell function. Cancer Gene Ther 2004, 11:487-496.
55. Voss R.H., Thomas S., Pfirschke C., Hauptrock B., Klobuch S., Kuball J., et al. Coexpression of the T-cell receptor constant alpha domain triggers tumor reactivity of single-chain TCR-transduced human T cells. Blood 2010, 115:5154-5163.
56. Saito T., Hochstenbach F., Marusic-Galesic S., Kruisbeek A.M., Brenner M., Germain R.N. Surface expression of only gamma delta and/or alpha beta T cell receptor heterodimers by cells with four (alpha, beta, gamma, delta) functional receptor chains. J Exp Med 1988, 168:1003-1020.
57. van der Veken L.T., Hagedoorn R.S., van Loenen M.M., Willemze R., Falkenburg J.H., Heemskerk M.H. Alphabeta T-cell receptor engineered gammadelta T cells mediate effective antileukemic reactivity. Cancer Res 2006, 66:3331-3337.
58. Okamoto S., Mineno J., Ikeda H., Fujiwara H., Yasukawa M., Shiku H., et al. Improved expression and reactivity of transduced tumor-specific TCRs in human lymphocytes by specific silencing of endogenous TCR. Cancer Res 2009, 69:9003-9011.
59. Cohen C.J., Zheng Z., Bray R., Zhao Y., Sherman L.A., Rosenberg S.A., et al. Recognition of fresh human tumor by human peripheral blood lymphocytes transduced with a bicistronic retroviral vector encoding a murine anti-p53 TCR. J Immunol 2005, 175:5799-5808.
60. Kuball J., Schmitz F.W., Voss R.H., Ferreira E.A., Engel R., Guillaume P., et al. Cooperation of human tumor-reactive CD4+ and CD8+ T cells after redirection of their specificity by a high-affinity p53A2.1-specific TCR. Immunity 2005, 22:117-129.
61. Udyavar A., Alli R., Nguyen P., Baker L., Geiger T.L. Subtle affinity-enhancing mutations in a myelin oligodendrocyte glycoprotein-specific TCR alter specificity and generate new self-reactivity. J Immunol 2009, 182:4439-4447.
62. Daniels M.A., Hogquist K.A., Jameson S.C. Sweet 'n' sour: the impact of differential glycosylation on T cell responses. Nat Immunol 2002, 3:903-910.
63. Kuball J., Hauptrock B., Malina V., Antunes E., Voss R.H., Wolfl M., et al. Increasing functional avidity of TCR-redirected T cells by removing defined N-glycosylation sites in the TCR constant domain. J Exp Med 2009, 206:463-475.
64. Chlewicki L.K., Holler P.D., Monti B.C., Clutter M.R., Kranz D.M. High-affinity, peptide-specific T cell receptors can be generated by mutations in CDR1, CDR2 or CDR3. J Mol Biol 2005, 346:223-239.
65. Holler P.D., Holman P.O., Shusta E.V., O'Herrin S., Wittrup K.D., Kranz D.M. In vitro evolution of a T cell receptor with high affinity for peptide/MHC. Proc Natl Acad Sci U S A 2000, 97:5387-5392.
66. Li Y., Moysey R., Molloy P.E., Vuidepot A.L., Mahon T., Baston E., et al. Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat Biotechnol 2005, 23:349-354.
67. Varela-Rohena A., Molloy P.E., Dunn S.M., Li Y., Suhoski M.M., Carroll R.G., et al. Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med 2008, 14:1390-1395.
68. Zhao Y., Bennett A.D., Zheng Z., Wang Q.J., Robbins P.F., Yu L.Y., et al. High-affinity TCRs generated by phage display provide CD4+ T cells with the ability to recognize and kill tumor cell lines. J Immunol 2007, 179:5845-5854.
69. Thoams S, Xue SA, Bangham C, Jakobsen BK, Morris E, Stauss HJ. Human T cells expressing affinity matured TCR display accelerated responses but fail to recognise low density of MHC/peptide antigen. Blood., doi:10.1182/blood-2010-12-326736.
70. Alli R., Zhang Z.M., Nguyen P., Zheng J.J., Geiger T.L. Rational design of T cell receptors with enhanced sensitivity for antigen. PLoS One 2011, 6:e18027.
71. Robbins P.F., Li Y.F., El Gamil M., Zhao Y., Wargo J.A., Zheng Z., et al. Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. J Immunol 2008, 180:6116-6131.
72. Sadovnikova E., Stauss H.J. Peptide-specific cytotoxic T lymphocytes restricted by nonself major histocompatibility complex class I molecules: reagents for tumor immunotherapy. Proc Natl Acad Sci U S A 1996, 93:13114-13118.
73. Theobald M., Biggs J., Dittmer D., Levine A.J., Sherman L.A. Targeting p53 as a general tumor antigen. Proc Natl Acad Sci U S A 1995, 92:11993-11997.
74. Li L.P., Lampert J.C., Chen X., Leitao C., Popovic J., Muller W., et al. Transgenic mice with a diverse human T cell antigen receptor repertoire. Nat Med 2010, 16:1029-1034.
75. Sherman L.A., Hesse S.V., Irwin M.J., La Face D., Peterson P. Selecting T cell receptors with high affinity for self-MHC by decreasing the contribution of CD8. Science 1992, 258:815-818.
76. Sommermeyer D., Neudorfer J., Weinhold M., Leisegang M., Engels B., Noessner E., et al. Designer T cells by T cell receptor replacement. Eur J Immunol 2006, 36:3052-3059.
77. Heemskerk M.H., Hagedoorn R.S., van der Hoorn M.A., van der Veken L.T., Hoogeboom M., Kester M.G., et al. Efficiency of T-cell receptor expression in dual-specific T cells is controlled by the intrinsic qualities of the TCR chains within the TCR-CD3 complex. Blood 2007, 109:235-243.
78. Scholten K.B., Kramer D., Kueter E.W., Graf M., Schoedl T., Meijer C.J., et al. Codon modification of T cell receptors allows enhanced functional expression in transgenic human T cells. Clin Immunol 2006, 119:135-145.
79. Jorritsma A., Gomez-Eerland R., Dokter M., van de K.W., Zoet Y.M., Doxiadis I.I., et al. Selecting highly affine and well-expressed TCRs for gene therapy of melanoma. Blood 2007, 110:3564-3572.
80. Robbins P.F., Dudley M.E., Wunderlich J., El Gamil M., Li Y.F., Zhou J., et al. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J Immunol 2004, 173:7125-7130.
81. Turtle C.J., Riddell S.R. Genetically retargeting CD8+ lymphocyte subsets for cancer immunotherapy. Curr Opin Immunol 2011, 23:299-305.
82. Yang L., Baltimore D. Long-term in vivo provision of antigen-specific T cell immunity by programming hematopoietic stem cells. Proc Natl Acad Sci U S A 2005, 102:4518-4523.
83. Alajez N.M., Schmielau J., Alter M.D., Cascio M., Finn O.J. Therapeutic potential of a tumor-specific, MHC-unrestricted T-cell receptor expressed on effector cells of the innate and the adaptive immune system through bone marrow transduction and immune reconstitution. Blood 2005, 105:4583-4589.
84. Ha S.P., Klemen N.D., Kinnebrew G.H., Brandmaier A.G., Marsh J., Hangoc G., et al. Transplantation of mouse HSCs genetically modified to express a CD4-restricted TCR results in long-term immunity that destroys tumors and initiates spontaneous autoimmunity. J Clin Invest 2010, 120:4273-4288.
85. Zhao Y., Parkhurst M.R., Zheng Z., Cohen C.J., Riley J.P., Gattinoni L., et al. Extrathymic generation of tumor-specific T cells from genetically engineered human hematopoietic stem cells via Notch signaling. Cancer Res 2007, 67:2425-2429.
86. van Lent A.U., Nagasawa M., van Loenen M.M., Schotte R., Schumacher T.N., Heemskerk M.H., et al. Functional human antigen-specific T cells produced in vitro using retroviral T cell receptor transfer into hematopoietic progenitors. J Immunol 2007, 179:4959-4968.
87. Hacein-Bey-Abina S., von Kalle C., Schmidt M., Le Deist F., Wulffraat N., McIntyre E., et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2003, 348:255-256.
88. Duval L., Schmidt H., Kaltoft K., Fode K., Jensen J.J., Sorensen S.M., et al. Adoptive transfer of allogeneic cytotoxic T lymphocytes equipped with a HLA-A2 restricted MART-1 T-cell receptor: a phase I trial in metastatic melanoma. Clin Cancer Res 2006, 12:1229-1236.
89. Heemskerk M.H., Hoogeboom M., Hagedoorn R., Kester M.G., Willemze R., Falkenburg J.H. Reprogramming of virus-specific T cells into leukemia-reactive T cells using T cell receptor gene transfer. J Exp Med 2004, 199:885-894.
90. Pule M.A., Savoldo B., Myers G.D., Rossig C., Russell H.V., Dotti G., et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 2008, 14:1264-1270.
91. van der Veken L.T., Coccoris M., Swart E., Falkenburg J.H., Schumacher T.N., Heemskerk M.H. Alpha beta T cell receptor transfer to gamma delta T cells generates functional effector cells without mixed TCR dimers in vivo. J Immunol 2009, 182:164-170.
92. Berger C., Jensen M.C., Lansdorp P.M., Gough M., Elliott C., Riddell S.R. 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.
93. Yang S., Luca G., Liu F., Ji Y., Yu Z., Restifo N.P., et al. In vitro generated anti-tumor T lymphocytes exhibit distinct subsets mimicking in vivo antigen-experienced cells. Cancer Immunol Immunother 2011, 60:739-749.
94. Hinrichs C.S., Borman Z.A., Cassard L., Gattinoni L., Spolski R., Yu Z., et al. Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci U S A 2009, 106:17469-17474.
95. Bonini C., Bondanza A., Perna S.K., Kaneko S., Traversari C., Ciceri F., et al. The suicide gene therapy challenge: how to improve a successful gene therapy approach. Mol Ther 2007, 15:1248-1252.
96. Introna M., Barbui A.M., Bambacioni F., Casati C., Gaipa G., Borleri G., et al. Genetic modification of human T cells with CD20: a strategy to purify and lyse transduced cells with anti-CD20 antibodies. Hum Gene Ther 2000, 11:611-620.
97. Straathof K.C., Pule M.A., Yotnda P., Dotti G., Vanin E.F., Brenner M.K., et al. An inducible caspase 9 safety switch for T-cell therapy. Blood 2005, 105:4247-4254.
98. de Witte M.A., Jorritsma A., Swart E., Straathof K.C., de Punder K., Haanen J.B., et al. An inducible caspase 9 safety switch can halt cell therapy-induced autoimmune disease. J Immunol 2008, 180:6365-6373.
99. Kieback E., Charo J., Sommermeyer D., Blankenstein T., Uckert W. A safeguard eliminates T cell receptor gene-modified autoreactive T cells after adoptive transfer. Proc Natl Acad Sci U S A 2008, 105:623-628.
100. Recchia A., Bonini C., Magnani Z., Urbinati F., Sartori D., Muraro S., et al. Retroviral vector integration deregulates gene expression but has no consequence on the biology and function of transplanted T cells. Proc Natl Acad Sci U S A 2006, 103:1457-1462.
101. Fujio K., Misaki Y., Setoguchi K., Morita S., Kawahata K., Kato I., et al. Functional reconstitution of class II MHC-restricted T cell immunity mediated by retroviral transfer of the alpha beta TCR complex. J Immunol 2000, 165:528-532.
102. Zhao Y., Zheng Z., Khong H.T., Rosenberg S.A., Morgan R.A. Transduction of an HLA-DP4-restricted NY-ESO-1-specific TCR into primary human CD4+ lymphocytes. J Immunother 2006, 29:398-406.
103. Heemskerk M.H., Hoogeboom M., de Paus R.A., Kester M.G., van der Hoorn M.A., Goulmy E., et al. Redirection of antileukemic reactivity of peripheral T lymphocytes using gene transfer of minor histocompatibility antigen HA-2-specific T-cell receptor complexes expressing a conserved alpha joining region. Blood 2003, 102:3530-3540.
104. Mommaas B., van Halteren A.G., Pool J., van d V., Wieles B., Heemskerk M.H., et al. Adult and cord blood T cells can acquire HA-1 specificity through HA-1 T-cell receptor gene transfer. Haematologica 2005, 90:1415-1421.
105. Marcu-Malina V., Heijhuurs S., van Buuren M., Hartkamp L., Strand S., Sebestyen Z., et al. Redirecting {alpha}{beta}T cells against cancer cells by transfer of a broadly tumor-reactive {gamma}{delta}T-cell receptor. Blood 2011, 118:50-59.
106. 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 U S A 1989, 86:10024-10028.
107. Sadelain M., Brentjens R., Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol 2009, 21:215-223.
108. Jena B., Dotti G., Cooper L.J. Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor. Blood 2010, 116:1035-1044.
109. Emtage P.C., Lo A.S., Gomes E.M., Liu D.L., Gonzalo-Daganzo R.M., Junghans R.P. Second-generation anti-carcinoembryonic antigen designer T cells resist activation-induced cell death, proliferate on tumor contact, secrete cytokines, and exhibit superior antitumor activity in vivo: a preclinical evaluation. Clin Cancer Res 2008, 14:8112-8122.
110. Pule M.A., Straathof K.C., Dotti G., Heslop H.E., Rooney C.M., Brenner M.K. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol Ther 2005, 12:933-941.
111. Zhong X.S., Matsushita M., Plotkin J., Riviere I., Sadelain M. Chimeric antigen receptors combining 4-1BB and CD28 signaling domains augment PI3kinase/AKT/Bcl-XL activation and CD8+ T cell-mediated tumor eradication. Mol Ther 2010, 18:413-420.
112. Kohn D.B., Dotti G., Brentjens R., Savoldo B., Jensen M., Cooper L.J., et al. CARs on track in the clinic. Mol Ther 2011, 19:432-438.
113. Lamers C.H., Sleijfer S., Vulto A.G., Kruit W.H., Kliffen M., Debets R., et al. 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-e22.
114. Kochenderfer J.N., Wilson W.H., Janik J.E., Dudley M.E., Stetler-Stevenson M., Feldman S.A., et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood 2010.
115. Brentjens R., Yeh R., Bernal Y., Riviere I., Sadelain M. Treatment of chronic lymphocytic leukemia with genetically targeted autologous T cells: case report of an unforeseen adverse event in a phase I clinical trial. Mol Ther 2010, 18:666-668.
116. Morgan R.A., Yang J.C., Kitano M., Dudley M.E., Laurencot C.M., Rosenberg S.A. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010, 18:843-851.
117. Barber A., Meehan K.R., Sentman C.L. Treatment of multiple myeloma with adoptively transferred chimeric NKG2D receptor-expressing T cells. Gene Ther 2011, 18:509-516.
118. Cohen C.J., Denkberg G., Lev A., Epel M., Reiter Y. Recombinant antibodies with MHC-restricted, peptide-specific, T-cell receptor-like specificity: new tools to study antigen presentation and TCR-peptide-MHC interactions. J Mol Recognit 2003, 16:324-332.
119. Willemsen R., Chames P., Schooten E., Gratama J.W., Debets R. Selection of human antibody fragments directed against tumor T-cell epitopes for adoptive T-cell therapy. Cytometry A 2008, 73:1093-1099.
120. Willemsen R.A., Debets R., Hart E., Hoogenboom H.R., Bolhuis R.L., Chames P. A phage display selected fab fragment with MHC class I-restricted specificity for MAGE-A1 allows for retargeting of primary human T lymphocytes. Gene Ther 2001, 8:1601-1608.
121. Kershaw M.H., Wang G., Westwood J.A., Pachynski R.K., Tiffany H.L., Marincola F.M., et al. Redirecting migration of T cells to chemokine secreted from tumors by genetic modification with CXCR2. Hum Gene Ther 2002, 13:1971-1980.
122. Di Stasi A., De Angelis B., Rooney C.M., Zhang L., Mahendravada A., Foster A.E., et al. T lymphocytes coexpressing CCR4 and a chimeric antigen receptor targeting CD30 have improved homing and antitumor activity in a Hodgkin tumor model. Blood 2009, 113:6392-6402.
123. Craddock J.A., Lu A., Bear A., Pule M., Brenner M.K., Rooney C.M., et al. Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J Immunother 2010, 33:780-788.
124. Eaton D., Gilham D.E., O'Neill A., Hawkins R.E. Retroviral transduction of human peripheral blood lymphocytes with Bcl-X(L) promotes in vitro lymphocyte survival in pro-apoptotic conditions. Gene Ther 2002, 9:527-535.
125. Charo J., Finkelstein S.E., Grewal N., Restifo N.P., Robbins P.F., Rosenberg S.A. Bcl-2 overexpression enhances tumor-specific T-cell survival. Cancer Res 2005, 65:2001-2008.
126. Dotti G., Savoldo B., Pule M., Straathof K.C., Biagi E., Yvon E., et al. Human cytotoxic T lymphocytes with reduced sensitivity to Fas-induced apoptosis. Blood 2005, 105:4677-4684.
127. Lei X.Y., Xu Y.M., Wang T., Xie Q.S., Jia L.T., Wang L.F., et al. Knockdown of human bid gene expression enhances survival of CD8+ T cells. Immunol Lett 2009, 122:30-36.
128. Topp M.S., Riddell S.R., Akatsuka Y., Jensen M.C., Blattman J.N., Greenberg P.D. Restoration of CD28 expression in CD28- CD8+ memory effector T cells reconstitutes antigen-induced IL-2 production. J Exp Med 2003, 198:947-955.
129. Stephan M.T., Ponomarev V., Brentjens R.J., Chang A.H., Dobrenkov K.V., Heller G., et al. T cell-encoded CD80 and 4-1BBL induce auto- and transcostimulation, resulting in potent tumor rejection. Nat Med 2007, 13:1440-1449.
130. Borkner L., Kaiser A., van de K.W., Andreesen R., Mackensen A., Haanen J.B., et al. RNA interference targeting programmed death receptor-1 improves immune functions of tumor-specific T cells. Cancer Immunol Immunother 2010, 59:1173-1183.
131. Hwu P., Yannelli J., Kriegler M., Anderson W.F., Perez C., Chiang Y., et al. Functional and molecular characterization of tumor-infiltrating lymphocytes transduced with tumor necrosis factor-alpha cDNA for the gene therapy of cancer in humans. J Immunol 1993, 150:4104-4115.
132. Heemskerk B., Liu K., Dudley M.E., Johnson L.A., Kaiser A., Downey S., et al. Adoptive cell therapy for patients with melanoma, using tumor-infiltrating lymphocytes genetically engineered to secrete interleukin-2. Hum Gene Ther 2008, 19:496-510.
133. Hsu C., Hughes M.S., Zheng Z., Bray R.B., Rosenberg S.A., Morgan R.A. 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, 175:7226-7234.
134. Wagner H.J., Bollard C.M., Vigouroux S., Huls M.H., Anderson R., Prentice H.G., et al. A strategy for treatment of Epstein-Barr virus-positive Hodgkin's disease by targeting interleukin 12 to the tumor environment using tumor antigen-specific T cells. Cancer Gene Ther 2004, 11:81-91.
135. Kerkar S.P., Muranski P., Kaiser A., Boni A., Sanchez-Perez L., Yu Z., et al. Tumor-specific CD8+ T cells expressing interleukin-12 eradicate established cancers in lymphodepleted hosts. Cancer Res 2010, 70:6725-6734.
136. Zhang L., Kerkar S.P., Yu Z., Zheng Z., Yang S., Restifo N.P., et al. Improving adoptive T cell therapy by targeting and controlling IL-12 expression to the tumor environment. Mol Ther 2011, 19:751-759.
137. Bollard C.M., Rossig C., Calonge M.J., Huls M.H., Wagner H.J., Massague J., et al. Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood 2002, 99:3179-3187.
138. Lo A.S., Taylor J.R., Farzaneh F., Kemeny D.M., Dibb N.J., Maher J. Harnessing the tumour-derived cytokine, CSF-1, to co-stimulate T-cell growth and activation. Mol Immunol 2008, 45:1276-1287.
139. Stromnes I.M., Blattman J.N., Tan X., Jeevanjee S., Gu H., Greenberg P.D. Abrogating Cbl-b in effector CD8(+) T cells improves the efficacy of adoptive therapy of leukemia in mice. J Clin Invest 2010, 120:3722-3734.
140. Sun J., Dotti G., Huye L.E., Foster A.E., Savoldo B., Gramatges M.M., et al. T cells expressing constitutively active Akt resist multiple tumor-associated inhibitory mechanisms. Mol Ther 2010, 18:2006-2017.
141. Stauss H.J., Cesco-Gaspere M., Thomas S., Hart D.P., Xue S.A., Holler A., et al. Monoclonal T-cell receptors: new reagents for cancer therapy. Mol Ther 2007, 15:1744-1750.
142. Pouw N., Treffers-Westerlaken E., Kraan J., Wittink F., ten Hagen T., Verweij J., et al. Combination of IL-21 and IL-15 enhances tumour-specific cytotoxicity and cytokine production of TCR-transduced primary T cells. Cancer Immunol Immunother 2010, 59:921-931.
143. Marrack P., Scott-Browne J.P., Dai S., Gapin L., Kappler J.W. Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu Rev Immunol 2008, 26:171-203.