Functional human antigen-specific T cells produced in vitro using retroviral T cell receptor transfer into hematopoietic progenitors

Journal of Immunology

Volumn 179, Issue 8, 2007, Pages 4959-4968

  Van Lent, Anja U ^a   Nagasawa, Maho ^a   Van Loenen, Marleen M ^b   Schotte, Remko ^c   Schumacher, Ton N M ^c   Heemskerk, Mirjam H M ^b   Spits, Hergen ^a,d   Legrand, Nicolas ^a,e  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d GENENTECH INC   (United States)

^e ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MELAN A; MINOR HISTOCOMPATIBILITY ANTIGEN; RETROVIRUS VECTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; EPITOPE; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE TRANSFER; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE; LYMPHOCYTE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; STROMA CELL; T LYMPHOCYTE; THYMUS; UMBILICAL CORD BLOOD; CELL DIFFERENTIATION; CELL LINE; COCULTURE; CYTOLOGY; GENETIC TRANSDUCTION; GENETICS; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PRESCHOOL CHILD; RETROVIRUS; T LYMPHOCYTE SUBPOPULATION;

CELL DIFFERENTIATION; CELL LINE; CHILD, PRESCHOOL; COCULTURE TECHNIQUES; EPITOPES, T-LYMPHOCYTE; GENE TRANSFER TECHNIQUES; HEMATOPOIETIC STEM CELLS; HUMANS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RETROVIRIDAE; T-LYMPHOCYTE SUBSETS; TRANSDUCTION, GENETIC;

EID: 36549043268     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.8.4959     Document Type: Article

References (53)

1. Douek, D. C., L. J. Picker, and R. A. Koup. 2003. T cell dynamics in HIV-1 infection. Annu. Rev. Immunol. 21: 265-304.
2. van den Brink, M. R., O. Alpdogan, and R. L. Boyd. 2004. Strategies to enhance T-cell reconstitution in immunocompromised patients. Nat. Rev. Immunol. 4: 856-867.
3. Moss, P., and A. Rickinson. 2005. Cellular immunotherapy for viral infection after HSC transplantation. Nat. Rev. Immunol. 5: 9-20.
4. Riddell, S. R., K. S. Watanabe, J. M. Goodrich, C. R. Li, M. E. Agha, and P. D. Greenberg. 1992. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257: 238-241.
5. Rooney, C. M., C. A. Smith, C. Y. Ng, S. K. Loftin, J. W. Sixbey, Y. Gan, D. K. Srivastava, L. C. Bowman, R. A. Krance, M. K. Brenner, and H. E. Heslop. 1998. Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 92: 1549-1555.
6. Haque, T., G. M. Wilkie, C. Taylor, P. L. Amlot, P. Murad, A. Iley, D. Dombagoda, K. M. Britton, A. J. Swerdlow, and D. H. Crawford. 2002. Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 360: 436-442.
7. Peggs, K. S., S. Verfuerth, A. Pizzey, N. Khan, M. Guiver, P. A. Moss, and S. Mackinnon. 2003. Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 362: 1375-1377.
8. Kershaw, M. H., M. W. Teng, M. J. Smyth, and P. K. Darcy. 2005. Supernatural T cells: genetic modification of T cells for cancer therapy. Nat. Rev. Immunol. 5: 928-940.
9. Kessels, H. W., M. C. Wolkers, M. D. van den Boom, M. A. van der Valk, and T. N. Schumacher. 2001. Immunotherapy through TCR gene transfer. Nat. Immunol. 2: 957-961.
10. Heemskerk, M. H., M. Hoogeboom, R. A. de Paus, M. G. Kester, M. A. van der Hoorn, E. Goulmy, R. Willemze, and J. H. Falkenburg. 2003. 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 α joining region. Blood 102: 3530-3540.
11. Heemskerk, M. H., M. Hoogeboom, R. Hagedoorn, M. G. Kester, R. Willemze, and J. H. Falkenburg. 2004. Reprogramming of virus-specific T cells into leukemia-reactive T cells using T cell receptor gene transfer. J. Exp. Med. 199: 885-894.
12. Zhao, Y., Z. Zheng, P. F. Robbins, H. T. Khong, S. A. Rosenberg, and R. A. Morgan. 2005. Primary human lymphocytes transduced with NY-ESO-1 antigen-specific TCR genes recognize and kill diverse human tumor cell lines. J. Immunol. 174: 4415-4423.
13. Morgan, R. A., M. E. Dudley, J. R. Wunderlich, M. S. Hughes, J. C. Yang, R. M. Sherry, R. E. Royal, S. L. Topalian, U. S. Kammula, N. P. Restifo, et al. 2006. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129.
14. Arnold, P. Y., A. R. Burton, and D. A. Vignali. 2004. Diabetes incidence is unaltered in glutamate decarboxylase 65-specific TCR retrogenic nonobese diabetic mice: generation by retroviral-mediated stem cell gene transfer. J. Immunol. 173: 3103-3111.
15. Yang, L., and D. Baltimore. 2005. Long-term in vivo provision of antigen-specific T cell immunity by programming hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 102: 4518-4523.
16. Holst, J., K. M. Vignali, A. R. Burton, and D. A. Vignali. 2006. Rapid analysis of T-cell selection in vivo using T cell-receptor retrogenic mice. Nat. Methods 3: 191-197.
17. Ceredig, R., E. J. Jenkinson, H. R. MacDonald, and J. J. Owen. 1982. Development of cytolytic T lymphocyte precursors in organ-cultured mouse embryonic thymus rudiments. J. Exp. Med. 155: 617-622.
18. Res, P., B. Blom, T. Hori, K. Weijer, and H. Spits. 1997. Downregulation of CD1 marks acquisition of functional maturation of human thymocytes and defines a control point in late stages of human T cell development. J. Exp. Med. 185: 141-151.
19. Collins, L. S., and K. Dorshkind. 1987. A stromal cell line from myeloid long-term bone marrow cultures can support myelopoiesis and B lymphopoiesis. J. Immunol. 138: 1082-1087.
20. Suzuki, J., J. Fujita, S. Taniguchi, K. Sugimoto, and K. J. Mori. 1992. Characterization of murine hemopoietic-supportive (MS-1 and MS-5) and non-supportive (MS-K) cell lines. Leukemia 6: 452-458.
21. Wiktor-Jedrzejczak, W., A. Bartocci, A. W. Ferrante, Jr., A. Ahmed-Ansari, K. W. Sell, J. W. Pollard, and E. R. Stanley. 1990. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc. Natl. Acad. Sci. USA 87: 4828-4832.
22. Yoshida, H., S. Hayashi, T. Kunisada, M. Ogawa, S. Nishikawa, H. Okamura, T. Sudo, and L. D. Shultz. 1990. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345: 442-444.
23. Nakano, T., H. Kodama, and T. Honjo. 1994. Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science 265: 1098-1101.
24. Schmitt, T. M., and J. C. Zuniga-Pflucker. 2002. Induction of T cell development from hematopoietic progenitor cells by δ-like-1 in vitro. Immunity 17: 749-756.
25. Schmitt, T. M., and J. C. Zuniga-Pflucker. 2006. T-cell development, doing it in a dish. Immunol. Rev. 209: 95-102.
26. + progenitor cells mature to T cells on OP9-DL1 stromal cell line without thymus microenvironment. Blood Cells Mol. Dis. 33: 227-232.
27. Haddad, R., P. Guardiola, B. Izac, C. Thibault, J. Radich, A. L. Delezoide, C. Baillou, F. M. Lemoine, J. C. Gluckman, F. Pflumio, and B. Canque. 2004. Molecular characterization of early human T/NK and B-lymphoid progenitor cells in umbilical cord blood. Blood 104: 3918-3926.
28. La Motte-Mohs, R. N., E. Herer, and J. C. Zuniga-Pflucker. 2005. Induction of T-cell development from human cord blood hematopoietic stem cells by δ-like 1 in vitro. Blood 105: 1431-1439.
29. Dontje, W., R. Schotte, T. Cupedo, M. Nagasawa, F. Scheeren, R. Gimeno, H. Spits, and B. Blom. 2006. δ-like1-induced Notch1 signaling regulates the human plasmacytoid dendritic cell versus T-cell lineage decision through control of GATA-3 and Spi-B. Blood 107: 2446-2452.
30. Spits, H. 2002. Development of αβ T cells in the human thymus. Nat. Rev. Immunol. 2: 760-772.
31. Heemskerk, M. H., R. S. Hagedoorn, M. A. van der Hoorn, L. T. van der Veken, M. Hoogeboom, M. G. Kester, R. Willemze, and J. H. Falkenburg. 2007. 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 109: 235-243.
32. Dudley, M. E., J. R. Wunderlich, P. F. Robbins, J. C. Yang, P. Hwu, D. J. Schwartzentruber, S. L. Topalian, R. Sherry, N. P. Restifo, A. M. Hubicki, et al. 2002. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854.
33. Jaleco, A. C., A. P. Stegmann, M. H. Heemskerk, F. Couwenberg, A. Q. Bakker, K. Weijer, and H. Spits. 1999. Genetic modification of human B-cell development: B-cell development is inhibited by the dominant negative helix loop helix factor Id3. Blood 94: 2637-2646.
34. Heemskerk, M. H., B. Blom, G. Nolan, A. P. Stegmann, A. Q. Bakker, K. Weijer, P. C. Res, and H. Spits. 1997. Inhibition of T cell and promotion of natural killer cell development by the dominant negative helix loop helix factor Id3. J. Exp. Med. 186: 1597-1602.
35. Kinsella, T. M., and G. P. Nolan. 1996. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7: 1405-1413.
36. Yssel, H., J. E. De Vries, M. Koken, W. Van Blitterswijk, and H. Spits. 1984. Serum-free medium for generation and propagation of functional human cytotoxic and helper T cell clones. J. Immunol. Methods 72: 219-227.
37. Spits, H., and H. Yssel. 1996. Cloning of human T and natural killer cells. Methods 9: 416-421.
38. Jarriault, S., C. Brou, F. Logeat, E. H. Schroeter, R. Kopan, and A. Israel. 1995. Signalling downstream of activated mammalian Notch. Nature 377: 355-358.
39. Deftos, M. L., E. Huang, E. W. Ojala, K. A. Forbush, and M. J. Bevan. 2000. Notch1 signaling promotes the maturation of CD4 and CD8 SP thymocytes. Immunity 13: 73-84.
40. Aifantis, I., M. Mandal, K. Sawai, A. Ferrando, and T. Vilimas. 2006. Regulation of T-cell progenitor survival and cell-cycle entry by the pre-T-cell receptor. Immunol. Rev. 209: 159-169.
41. Garbe, A. I., A. Krueger, F. Gounari, J. C. Zuniga-Pflucker, and H. von Boehmer. 2006. Differential synergy of Notch and T cell receptor signaling determines αβ versus γδ lineage fate. J. Exp. Med. 203: 1579-1590.
42. Guidos, C. J. 2006. Synergy between the pre-T cell receptor and Notch: cementing the αβ lineage choice. J. Exp. Med. 203: 2233-2237.
43. Garbe, A. I., and H. von Boehmer. 2007. TCR and Notch synergize in αβ versus γδ lineage choice. Trends Immunol. 28: 124-131.
44. von Boehmer, H. 1990. Developmental biology of T cells in T cell-receptor transgenic mice. Annu. Rev. Immunol. 8: 531-556.
45. + T cells. J. Clin. Invest. 115: 1616-1626.
46. Willemsen, R. A., M. E. Weijtens, C. Ronteltap, Z. Eshhar, J. W. Gratama, P. Chames, and R. L. Bolhuis. 2000. Grafting primary human T lymphocytes with cancer-specific chimeric single chain and two chain TCR. Gene Ther. 7: 1369-1377.
47. Schumacher, T. N. 2002. T-cell-receptor gene therapy. Nat. Rev. Immunol. 2: 512-519.
48. Kuball, J., M. L. Dossett, M. Wolfl, W. Y. Ho, R. H. Voss, C. Fowler, and P. D. Greenberg. 2007. Facilitating matched pairing and expression of TCR chains introduced into human T cells. Blood 109: 2331-2338.
49. Ho, W. Y., J. N. Blattman, M. L. Dossett, C. Yee, and P. D. Greenberg. 2003. Adoptive immunotherapy: engineering T cell responses as biologic weapons for tumor mass destruction. Cancer Cells 3: 431-437.
50. Zhao, Y., M. R. Parkhurst, Z. Zheng, C. J. Cohen, J. P. Riley, L. Gattinoni, N. P. Restifo, S. A. Rosenberg, and R. A. Morgan. 2007. Extrathymic generation of tumor-specific T cells from genetically engineered human hematopoietic stem cells via Notch signaling. Cancer Res. 67: 2425-2429.
51. Mayor, S. 2007. World's first public-private cord blood bank launched in UK. BMJ 334: 277.
52. Shizuru, J. A., R. S. Negrin, and I. L. Weissman. 2005. Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. Annu. Rev. Med. 56: 509-538.
53. Wilson, A., and A. Trumpp. 2006. Bone-marrow haematopoietic-stem-cell niches. Nat. Rev. Immunol. 6: 93-106.