T-cell receptor gene therapy in human melanoma-bearing immune-deficient mice: Human but not mouse T cells recapitulate outcome of clinical studies

Human Gene Therapy

Volumn 23, Issue 2, 2012, Pages 187-201

  Straetemans, Trudy ^a   Coccoris, Miriam ^a   Berrevoets, Cor ^a   Treffers Westerlaken, Elike ^a   Scholten, Csilla E V ^a   Schipper, Debby ^a   Ten Hagen, Timo L M ^a   Debets, Reno ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BUSULFAN; CHIMERIC ANTIBODY; CYCLOPHOSPHAMIDE; GLYCOPROTEIN GP 100; GREEN FLUORESCENT PROTEIN; HLA A2 ANTIGEN; INTERLEUKIN 2; RETROVIRUS VECTOR; T LYMPHOCYTE RECEPTOR;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GENE THERAPY; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; GENE TRANSFER; GENETIC ENGINEERING; HUMAN; HUMAN CELL; IN VIVO GENE TRANSFER; LYMPHOCYTE DIFFERENTIATION; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; SCID MOUSE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE RECEPTOR GENE; T LYMPHOCYTE SUBPOPULATION; TRANSGENE; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ANIMALS; CELL DIFFERENTIATION; GENES, REPORTER; GENETIC THERAPY; GENETIC VECTORS; GP100 MELANOMA ANTIGEN; GREEN FLUORESCENT PROTEINS; HLA-A2 ANTIGEN; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MELANOMA; MICE; MICE, SCID; RECEPTORS, ANTIGEN, T-CELL; RETROVIRIDAE; SPECIES SPECIFICITY; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; TRANSGENES;

MUS;

EID: 84856831733     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2010.126     Document Type: Article

References (62)

1. Appay, V., van Lier, R.A., Sallusto, F., and Roederer, M. (2008). Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73, 975-983.
2. Arden, B., Clark, S.P., Kabelitz, D., and Mak, T.W. (1995). Human T-cell receptor variable gene segment families. Immunogenetics 42, 455-500. (Pubitemid 26025063)
3. Berger, C., Jensen, M.C., Lansdorp, P.M., et al. (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.
4. Bobisse, S., Rondina, M., Merlo, A., et al. (2009). Reprogramming T lymphocytes for melanoma adoptive immunotherapy by Tcell receptor gene transfer with lentiviral vectors. Cancer Res. 69, 9385-9394.
5. Brentjens, R.J., Latouche, J.B., Santos, E., et al. (2003). Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat. Med. 9, 279-286. (Pubitemid 36362782)
6. Brentjens, R.J., Santos, E., Nikhamin, Y., et al. (2007). Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts. Clin. Cancer Res. 13, 5426-5435. (Pubitemid 47510370)
7. Butler, M.O., Friedlander, P., Milstein, M.I., et al. (2011). Establishment of antitumor memory in humans using in vitroeducated CD8+ T cells. Sci. Transl. Med. 3, 80ra34.
8. Carpenito, C., Milone, M.C., Hassan, R., et al. (2009). Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc. Natl. Acad. Sci. U.S.A. 106, 3360-3365.
9. Cheadle, E.J., Gilham, D.E., and Hawkins, R.E. (2008). The combination of cyclophosphamide and human T cells genetically engineered to target CD19 can eradicate established B-cell lymphoma. Br. J. Haematol. 142, 65-68. (Pubitemid 351783147)
10. Chekmasova, A.A., Rao, T.D., Nikhamin, Y., et al. (2010). Successful eradication of established peritoneal ovarian tumors in SCID-Beige mice following adoptive transfer of T cells genetically targeted to the MUC16 antigen. Clin. Cancer Res. 16, 3594-3606.
11. Clay, T.M., Custer, M.C., Sachs, J., et al. (1999). Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J. Immunol. 163, 507-513. (Pubitemid 29295880)
12. Craddock, J.A., Lu, A., Bear, A., et al. (2010). Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J. Immunother. 33, 780-788.
13. Darcy, P.K., Haynes, N.M., Snook, M.B., et al. (2000). Redirected perforin-dependent lysis of colon carcinoma by ex vivo genetically engineered CTL. J. Immunol. 164, 3705-3712. (Pubitemid 30169826)
14. de Witte, M.A., Bendle, G.M., van den Boom, M.D., et al. (2008a). TCR gene therapy of spontaneous prostate carcinoma requires in vivo T cell activation. J. Immunol. 181, 2563-2571.
15. de Witte, M.A., Jorritsma, A., Kaiser, A., et al. (2008b). Requirements for effective antitumor responses of TCR transduced T cells. J. Immunol. 181, 5128-5136.
16. Dudley, M.E., Wunderlich, J.R., Yang, J.C., et al. (2005). Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J. Clin. Oncol. 23, 2346-2357. (Pubitemid 46218728)
17. Friedman, T., Shimizu, A., Smith, R.N., et al. (1999). Human CD4+ T cells mediate rejection of porcine xenografts. J. Immunol. 162, 5256-5262. (Pubitemid 29307131)
18. Gade, T.P., Hassen, W., Santos, E., et al. (2005). Targeted elimination of prostate cancer by genetically directed human T lymphocytes. Cancer Res. 65, 9080-9088. (Pubitemid 41377401)
19. Hanson, H.L., Donermeyer, D.L., Ikeda, H., et al. (2000). Eradication of established tumors by CD8 + T cell adoptive immunotherapy. Immunity 13, 265-276.
20. Haynes, N.M., Snook, M.B., Trapani, J.A., et al. (2001). Redirecting mouse CTL against colon carcinoma: superior signaling efficacy of single-chain variable domain chimeras containing TCR-f vs FceRI-c. J. Immunol. 166, 182-187. (Pubitemid 32038431)
21. Haynes, N.M., Trapani, J.A., Teng, M.W., et al. (2002a). Rejection of syngeneic colon carcinoma by CTLs expressing single-chain antibody receptors codelivering CD28 costimulation. J. Immunol. 169, 5780-5786. (Pubitemid 35291680)
22. Haynes, N.M., Trapani, J.A., Teng, M.W., et al. (2002b). Singlechain antigen recognition receptors that costimulate potent rejection of established experimental tumors. Blood 100, 3155-3163. (Pubitemid 35217063)
23. Hinrichs, C.S., Borman, Z.A., Cassard, L., et al. (2009). 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. 106, 17469-17474.
24. Huang, J., Khong, H.T., Dudley, M.E., et al. (2005). Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J. Immunother. 28, 258-267. (Pubitemid 40593992)
25. Hwu, P., Yang, J.C., Cowherd, R., et al. (1995). In vivo antitumor activity of T cells redirected with chimeric antibody/T-cell receptor genes. Cancer Res. 55, 3369-3373.
26. Johnson, L.A., Morgan, R.A., Dudley, M.E., et al. (2009). Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114, 535-546.
27. Kalos, M., Levine, B.L., Porter, D.L., et al. (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.
28. Kaneko, S., Mastaglio, S., Bondanza, A., et al. (2009). IL-7 and IL-15 allow the generation of suicide gene-modified alloreactive self-renewing central memory human T lymphocytes. Blood 113, 1006-1015.
29. Kershaw, M.H., Westwood, J.A., Parker, L.L., et al. (2006). A phase I study on adoptive immunotherapy using genemodified T cells for ovarian cancer. Clin. Cancer Res. 12, 6106-6115. (Pubitemid 44703776)
30. Kessels, H.W., Wolkers, M.C., van den Boom, M.D., et al. (2001). Immunotherapy through TCR gene transfer. Nat. Immunol. 2, 957-961. (Pubitemid 32976169)
31. Kowolik, C.M., Topp, M.S., Gonzalez, S., et al. (2006). CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells. Cancer Res. 66, 10995-11004. (Pubitemid 44876999)
32. Lamers, C.H., Sleijfer, S., Vulto, A.G., et al. (2006a). Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J. Clin. Oncol. 24, e20-e22.
33. Lamers, C.H., Willemsen, R.A., van Elzakker, P., et al. (2006b). Phoenix-ampho outperforms PG13 as retroviral packaging cells to transduce human T cells with tumor-specific receptors: implications for clinical immunogene therapy of cancer. Cancer Gene Ther. 13, 503-509.
34. Milone, M.C., Fish, J.D., Carpenito, C., et al. (2009). Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 17, 1453-1464.
35. Morgan, R.A., Dudley, M.E., Wunderlich, J.R., et al. (2006). Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314, 126-129. (Pubitemid 44547756)
36. Morris, E.C., Tsallios, A., Bendle, G.M., et al. (2005). A critical role of T cell antigen receptor-transduced MHC class Irestricted helper T cells in tumor protection. Proc. Natl. Acad. Sci. U.S.A. 102, 7934-7939. (Pubitemid 40781041)
37. Parkhurst, M.R., Yang, J.C., Langan, R.C., et al. (2011). T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol. Ther. 19, 620-626.
38. Pierson, R.N., 3rd, Winn, H.J., Russell, P.S., and Auchincloss, H., Jr. (1989). Xenogeneic skin graft rejection is especially dependent on CD4+ T cells. J. Exp. Med. 170, 991-996. (Pubitemid 19226679)
39. Pinthus, J.H., Waks, T., Kaufman-Francis, K., et al. (2003). Immuno-gene therapy of established prostate tumors using chimeric receptor-redirected human lymphocytes. Cancer Res. 63, 2470-2476. (Pubitemid 36605185)
40. Pinthus, J.H., Waks, T., Malina, V., et al. (2004). Adoptive immunotherapy of prostate cancer bone lesions using redirected effector lymphocytes. J. Clin. Invest. 114, 1774-1781. (Pubitemid 40385533)
41. Porter, D.L., Levine, B.L., Kalos, M., et al. (2011). Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365, 725-733.
42. Pouw, N., Treffers-Westerlaken, E., Kraan, J., et al. (2010a). Combination of IL-21 and IL-15 enhances tumour-specific cytotoxicity and cytokine production of TCR-transduced primary T cells. Cancer Immunol. Immunother. 59, 921-931.
43. Pouw, N., Treffers-Westerlaken, E., Mondino, A., et al. (2010b). TCR gene-engineered T cell: limited T cell activation and combined use of IL-15 and IL-21 ensure minimal differentiation and maximal antigen-specificity. Mol. Immunol. 47, 1411-1420.
44. Pouw, N.M., Westerlaken, E.J., Willemsen, R.A., and Debets, R. (2007). Gene transfer of human TCR in primary murine T cells is improved by pseudo-typing with amphotropic and ecotropic envelopes. J. Gene Med. 9, 561-570. (Pubitemid 47073988)
45. Robbins, P.F., Dudley, M.E., Wunderlich, J., et al. (2004). Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J. Immunol. 173, 7125-7130. (Pubitemid 39628146)
46. Robbins, P.F., Morgan, R.A., Feldman, S.A., et al. (2011). Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J. Clin. Oncol. 29, 917-924.
47. Savoldo, B., Rooney, C.M., Di Stasi, A., et al. (2007). Epstein Barr virus-specific cytotoxic T lymphocytes expressing the anti-CD30f artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 110, 2620-2630. (Pubitemid 47523186)
48. Schaft, N., Willemsen, R.A., de Vries, J., et al. (2003). Peptide fine specificity of anti-glycoprotein 100 CTL is preserved following transfer of engineered TCRab genes into primary human T lymphocytes. J. Immunol. 170, 2186-2194. (Pubitemid 36197443)
49. Schaft, N., Lankiewicz, B., Drexhage, J., et al. (2006). T cell retargeting to EBV antigens following TCR gene transfer: CD28-containing receptors mediate enhanced antigen-specific IFN-c production. Int. Immunol. 18, 591-601.
50. Seynhaeve, A.L., Hoving, S., Schipper, D., et al. (2007). Tumor necrosis factor a mediates homogeneous distribution of liposomes in murine melanoma that contributes to a better tumor response. Cancer Res. 67, 9455-9462. (Pubitemid 47535935)
51. Shultz, L.D., Lyons, B.L., Burzenski, L.M., et al. (2005). Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2Rcnull mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174, 6477-6489. (Pubitemid 40663843)
52. Smyth, M.J., Kershaw, M.H., and Trapani, J.A. (1997). Xenospecific cytotoxic T lymphocytes: potent lysis in vitro and in vivo. Transplantation 63, 1171-1178. (Pubitemid 27190983)
53. Song, D., Ye, Q., Carpenito, C., et al. (2011). In vivo persistence, tumor localization, and antitumor activity of CAR-engineered T cells is enhanced by costimulatory signaling through CD137 (4-1BB). Cancer Res. 71, 4617-4627.
54. Teng, M.W., Kershaw, M.H., Moeller, M., et al. (2004). Immunotherapy of cancer using systemically delivered genemodified human T lymphocytes. Human Gene Ther. 15, 699-708. (Pubitemid 38925222)
55. Van de Griend, R.J., Van Krimpen, B.A., Bol, S.J., et al. (1984). Rapid expansion of human cytotoxic T cell clones: growth promotion by a heat-labile serum component and by various types of feeder cells. J. Immunol. Methods 66, 285-298. (Pubitemid 14221183)
56. Wang, X., Berger, C., Wong, C.W., et al. (2011). Engraftment of human central memory-derived effector CD8+ T cells in immunodeficient mice. Blood 117, 1888-1898.
57. Westwood, J.A., Smyth, M.J., Teng, M.W., et al. (2005). Adoptive transfer of T cells modified with a humanized chimeric receptor gene inhibits growth of Lewis-Y-expressing tumors in mice. Proc. Natl. Acad. Sci. U.S.A. 102, 19051-19056. (Pubitemid 43049564)
58. Willemsen, R.A., Weijtens, M.E., Ronteltap, C., et al. (2000). Grafting primary human T lymphocytes with cancer-specific chimeric single chain and two chain TCR. Gene Ther. 7, 1369-1377. (Pubitemid 30662242)
59. Xue, S.A., Gao, L., Hart, D., et al. (2005). Elimination of human leukemia cells in NOD/SCID mice by WT1-TCR gene-transduced human T cells. Blood 106, 3062-3067. (Pubitemid 41565901)
60. Xue, S.A., Gao, L., Thomas, S., et al. (2010). Development of a Wilms' tumor antigen-specific T-cell receptor for clinical trials: engineered patient's T cells can eliminate autologous leukemia blasts in NOD/SCID mice. Haematologica 95, 126-134.
61. Zhao, Y., Wang, Q.J., Yang, S., et al. (2009). A herceptin-based chimeric antigen receptor with modified signaling domains leads to enhanced survival of transduced T lymphocytes and antitumor activity. J. Immunol. 183, 5563-5574.
62. Zhao, Y., Moon, E., Carpenito, C., et al. (2010). Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res. 70, 9053-9061.