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Journal of Immunology Research
Volume 2014, Article ID 525913, 9 pages
http://dx.doi.org/10.1155/2014/525913
Review Article

Cell Transfer Therapy for Cancer: Past, Present, and Future

Department of Medical Oncology, Institute of Clinical Science, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, China

Received 23 September 2013; Accepted 26 December 2013; Published 9 January 2014

Academic Editor: Steven Eric Finkelstein

Copyright © 2014 Xiaoling Qian et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. B. Coley, “The treatment of malignant tumors by repeated inoculations of erysipelas: with a report of ten original cases,” Clinical Orthopaedics and Related Research, no. 262, pp. 3–11, 1991. View at Google Scholar · View at Scopus
  2. W. B. Coley, “The treatment of inoperable sarcoma by bacterial toxins (the mixed toxins of the Streptococcus erysipelas and the Bacillus prodigiosus),” Proceedings of the Royal Society of Medicine, vol. 3, pp. 1–48, 1910. View at Google Scholar
  3. M. T. Lotze, Y. L. Matory, and A. A. Rayner, “Clinical effects and toxicity of interleukin-2 in patients with cancer,” Cancer, vol. 58, no. 12, pp. 2764–2772, 1986. View at Google Scholar · View at Scopus
  4. R. M. Steinman and Z. A. Cohn, “Pillars article: identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J. Exp. Med.1973. 137: 1142–1162,” Journal of Immunology, vol. 178, no. 1, pp. 5–25, 2007. View at Google Scholar · View at Scopus
  5. K. Palucka and J. Banchereau, “Cancer immunotherapy via dendritic cells,” Nature Reviews Cancer, vol. 12, no. 4, pp. 265–277, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. R. So-Rosillo and E. J. Small, “Sipuleucel-T (APC8015) for prostate cancer,” Expert Review of Anticancer Therapy, vol. 6, no. 9, pp. 1163–1167, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. P. W. Kantoff, C. S. Higano, N. D. Shore et al., “Sipuleucel-T immunotherapy for castration-resistant prostate cancer,” The New England Journal of Medicine, vol. 363, no. 5, pp. 411–422, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. C. S. Higano, P. F. Schellhammer, E. J. Small et al., “Integrated data from 2 randomized, double-blind, placebo-controlled, phase 3 trials of active cellular immunotherapy with sipuleucel-T in advanced prostate cancer,” Cancer, vol. 115, no. 16, pp. 3670–3679, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. E. J. Small, P. F. Schellhammer, C. S. Higano et al., “Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer,” Journal of Clinical Oncology, vol. 24, no. 19, pp. 3089–3094, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Paczesny, J. Banchereau, K. M. Wittkowski, G. Saracino, J. Fay, and A. K. Palucka, “Expansion of melanoma-specific cytolytic CD8+ T cell precursors in patients with metastatic melanoma vaccinated with CD34+ progenitor-derived dendritic cells,” Journal of Experimental Medicine, vol. 199, no. 11, pp. 1503–1511, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. M. J. P. Welters, G. G. Kenter, P. J. de Vos van Steenwijk et al., “Success or failure of vaccination for HPV16-positive vulvar lesions correlates with kinetics and phenotype of induced T-cell responses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 26, pp. 11895–11899, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. J. R. Cubillos-Ruiz, J. R. Baird, A. J. Tesone et al., “Reprogramming tumor-associated dendritic cells in vivo using miRNA mimetics triggers protective immunity against ovarian cancer,” Cancer Research, vol. 72, no. 7, pp. 1683–1693, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Miwa, H. Nishida, Y. Tanzawa et al., “TNF-α and tumor lysate promote the maturation of dendritic cells for immunotherapy for advanced malignant bone and soft tissue tumors,” PLoS ONE, vol. 7, no. 12, Article ID e52926, 2012. View at Publisher · View at Google Scholar
  14. M. Sugiyama, Y. Kakeji, S. Tsujitani et al., “Antagonism of VEGF by genetically engineered dendritic cells is essential to induce antitumor immunity against malignant ascites,” Molecular Cancer Therapeutics, vol. 10, no. 3, pp. 540–549, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Oertli, M. Heberer, G. C. Spagnoli et al., “Rapid induction of specific cytotoxic T lymphocytes against melanoma-associated antigens by a recombinant vaccinia virus vector expressing multiple immunodominant epitopes and costimulatory molecules in vivo,” Human Gene Therapy, vol. 13, no. 4, pp. 569–575, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Adamina, R. Rosenthal, W. P. Weber et al., “Intranodal immunization with a vaccinia virus encoding multiple antigenic epitopes and costimulatory molecules in metastatic melanoma,” Molecular Therapy, vol. 18, no. 3, pp. 651–659, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Tatsumi, T. Takehara, S. Yamaguchi et al., “Injection of IL-12 gene-transduced dendritic cells into mouse liver tumor lesions activates both innate and acquired immunity,” Gene Therapy, vol. 14, no. 11, pp. 863–871, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. X. Zheng, J. Koropatnick, D. Chen et al., “Silencing IDO in dendritic cells: a novel approach to enhance cancer immunotherapy in a murine breast cancer model,” International Journal of Cancer, vol. 132, no. 4, pp. 967–977, 2013. View at Publisher · View at Google Scholar
  19. A. Saha and S. K. Chatterjee, “Combination of CTL-associated antigen-4 blockade and depletion of CD25+ regulatory T cells enhance tumour immunity of dendritic cell-based vaccine in a mouse model of colon cancer,” Scandinavian Journal of Immunology, vol. 71, no. 2, pp. 70–82, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. J. C. Roder and H. F. Pross, “The biology of the human natural killer cell,” Journal of Clinical Immunology, vol. 2, no. 4, pp. 249–263, 1982. View at Google Scholar · View at Scopus
  21. J. S. Miller, “The biology of natural killer cells in cancer, infection, and pregnancy,” Experimental Hematology, vol. 29, no. 10, pp. 1157–1168, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Cerwenka and L. L. Lanier, “Natural killer cells, viruses and cancer,” Nature Reviews Immunology, vol. 1, no. 1, pp. 41–49, 2001. View at Google Scholar · View at Scopus
  23. M. Cheng, Y. Chen, W. Xiao, R. Sun, and Z. Tian, “NK cell-based immunotherapy for malignant diseases,” Cellular and Molecular Immunology, vol. 10, no. 3, pp. 230–252, 2013. View at Publisher · View at Google Scholar
  24. H. G. Ljunggren and K. Karre, “In search of the “missing self”: MHC molecules and NK cell recognition,” Immunology Today, vol. 11, no. 7, pp. 237–244, 1990. View at Google Scholar · View at Scopus
  25. S. Bauer, V. Groh, J. Wu et al., “Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA,” Science, vol. 285, no. 5428, pp. 727–729, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. L. Binyamin, R. K. Alpaugh, T. L. Hughes, C. T. Lutz, K. S. Campbell, and L. M. Weiner, “Blocking NK cell inhibitory self-recognition promotes antibody-dependent cellular cytotoxicity in a model of anti-lymphoma therapy,” Journal of Immunology, vol. 180, no. 9, pp. 6392–6401, 2008. View at Google Scholar · View at Scopus
  27. C. Figueiredo, A. Seltsam, and R. Blasczyk, “Permanent silencing of NKG2A expression for cell-based therapeutics,” Journal of Molecular Medicine, vol. 87, no. 2, pp. 199–210, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Spear, M. R. Wu, M. L. Sentman, and C. L. Sentman, “NKG2D ligands as therapeutic targets,” Cancer Immunity, vol. 13, article 8, 2013. View at Google Scholar
  29. M. J. Besser, T. Shoham, O. Harari-Steinberg et al., “Development of allogeneic NK cell adoptive transfer therapy in metastatic melanoma patients: in vitro preclinical optimization studies,” PLoS ONE, vol. 8, no. 3, Article ID e57922, 2013. View at Publisher · View at Google Scholar
  30. E. A. Grimm, A. Mazumder, H. Z. Zhang, and S. A. Rosenberg, “Lymphokine-activated killer cell phenomenon. Lysis of natural killer-resistant fresh solid tumor cells by interleukin 2-activated autologous human peripheral blood lymphocytes,” Journal of Experimental Medicine, vol. 155, no. 6, pp. 1823–1841, 1982. View at Google Scholar · View at Scopus
  31. S. A. Rosenberg, “Immunotherapy of cancer by systemic administration of lymphoid cells plus interleukin-2,” Journal of Biological Response Modifiers, vol. 3, no. 5, pp. 501–511, 1984. View at Google Scholar · View at Scopus
  32. T. M. Law, R. J. Motzer, M. Mazumdar et al., “Phase III randomized trial of interleukin-2 with or without lymphokine-activated killer cells in the treatment of patients with advanced renal cell carcinoma,” Cancer, vol. 76, no. 5, pp. 824–832, 1995. View at Publisher · View at Google Scholar
  33. M. Terme, E. Ullrich, N. F. Delahaye, N. Chaput, and L. Zitvogel, “Natural killer cell-directed therapies: moving from unexpected results to successful strategies,” Nature Immunology, vol. 9, no. 5, pp. 486–494, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Ruggeri, M. Capanni, E. Urbani et al., “Effectiveness of donor natural killer cell aloreactivity in mismatched hematopoietic transplants,” Science, vol. 295, no. 5562, pp. 2097–2100, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Ruggeri, A. Mancusi, K. Perruccio, E. Burchielli, M. F. Martelli, and A. Velardi, “Natural killer cell alloreactivity for leukemia therapy,” Journal of Immunotherapy, vol. 28, no. 3, pp. 175–182, 2005. View at Google Scholar · View at Scopus
  36. J. S. Miller, Y. Soignier, A. Panoskaltsis-Mortari et al., “Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer,” Blood, vol. 105, no. 8, pp. 3051–3057, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Re, C. Staudacher, L. Zamai, V. Vecchio, and M. Bregni, “Killer cell Ig-like receptors ligand-mismatched, alloreactive natural killer cells lyse primary solid tumors,” Cancer, vol. 107, no. 3, pp. 640–648, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. E. G. Iliopoulou, P. Kountourakis, M. V. Karamouzis et al., “A phase I trial of adoptive transfer of allogeneic natural killer cells in patients with advanced non-small cell lung cancer,” Cancer Immunology, Immunotherapy, vol. 59, no. 12, pp. 1781–1789, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Lundqvist, J. P. McCoy, L. Samsel, and R. Childs, “Reduction of GVHD and enhanced antitumor effects after adoptive infusion of alloreactive Ly49-mismatched NK cells from MHC-matched donors,” Blood, vol. 109, no. 8, pp. 3603–3606, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. H. G. Ljunggren and K. J. Malmberg, “Prospects for the use of NK cells in immunotherapy of human cancer,” Nature Reviews Immunology, vol. 7, no. 5, pp. 329–339, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Tonn, S. Becker, R. Esser, D. Schwabe, and E. Seifried, “Cellular immunotherapy of malignancies using the clonal natural killer cell line NK-92,” Journal of Hematotherapy and Stem Cell Research, vol. 10, no. 4, pp. 535–544, 2001. View at Google Scholar · View at Scopus
  42. H. G. Klingemann, “Natural killer cell-based immunotherapeutic strategies,” Cytotherapy, vol. 7, no. 1, pp. 16–22, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. K. J. Malmberg, Y. T. Bryceson, M. Carlsten et al., “NK cell-mediated targeting of human cancer and possibilities for new means of immunotherapy,” Cancer Immunology, Immunotherapy, vol. 57, no. 10, pp. 1541–1552, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Suck, D. R. Branch, M. J. Smyth et al., “KHYG-1, a model for the study of enhanced natural killer cell cytotoxicity,” Experimental Hematology, vol. 33, no. 10, pp. 1160–1171, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Zhang, J. Zhang, J. Niu, J. Zhang, and Z. Tian, “Interleukin-15 improves cytotoxicity of natural killer cells via up-regulating NKG2D and cytotoxic effector molecule expression as well as STAT1 and ERK1/2 phosphorylation,” Cytokine, vol. 42, no. 1, pp. 128–136, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. F. D. Shi, H. G. Ljunggren, A. la Cava, and L. van Kaer, “Organ-specific features of natural killer cells,” Nature Reviews Immunology, vol. 11, no. 10, pp. 658–671, 2011. View at Publisher · View at Google Scholar
  47. J. J. Subleski, R. H. Wiltrout, and J. M. Weiss, “Application of tissue-specific NK and NKT cell activity for tumor immunotherapy,” Journal of Autoimmunity, vol. 33, no. 3-4, pp. 275–281, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. M. R. Parkhurst, J. P. Riley, M. E. Dudley, and S. A. Rosenberg, “Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression,” Clinical Cancer Research, vol. 17, no. 19, pp. 6287–6297, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Curti, L. Ruggeri, A. D'Addio et al., “Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients,” Blood, vol. 118, no. 12, pp. 3273–3279, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Ni, M. Miller, A. Stojanovic, and A. Cerwenka, “Toward the next generation of NK cell-based adoptive cancer immunotherapy,” Oncoimmunology, vol. 2, no. 4, Article ID e23811, 2013. View at Google Scholar
  51. J. Jiang, C. Wu, and B. Lu, “Cytokine-induced killer cells promote antitumor immunity,” Journal of Translational Medicine, vol. 11, article 83, 2013. View at Publisher · View at Google Scholar
  52. P. Olioso, R. Giancola, M. Di Riti, A. Contento, P. Accorsi, and A. Iacone, “Immunotherapy with cytokine induced killer cells in solid and hematopoietic tumours: a pilot clinical trial,” Hematological Oncology, vol. 27, no. 3, pp. 130–139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Jiang, N. Xu, C. Wu et al., “Treatment of advanced gastric cancer by chemotherapy combined with autologous cytokine-induced killer cells,” Anticancer Research, vol. 26, no. 3 B, pp. 2237–2242, 2006. View at Google Scholar · View at Scopus
  54. C. Wu, J. Jiang, L. Shi, and N. Xu, “Prospective study of chemotherapy in combination with cytokine-induced killer cells in patients suffering from advanced non-small cell lung cancer,” Anticancer Research, vol. 28, no. 6 B, pp. 3997–4002, 2008. View at Google Scholar · View at Scopus
  55. D. S. Weng, J. Zhou, Q. Zhou et al., “Minimally invasive treatment combined with cytokine-induced killer cells therapy lower the short-term recurrence rates of hepatocellular carcinomas,” Journal of Immunotherapy, vol. 31, no. 1, pp. 63–71, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. F. Tita-Nwa, G. Moldenhauer, M. Herbst, C. Kleist, A. D. Ho, and M. Kornacker, “Cytokine-induced killer cells targeted by the novel bispecific antibody CD19×CD5 (HD37×T5.16) efficiently lyse B-lymphoma cells,” Cancer Immunology, Immunotherapy, vol. 56, no. 12, pp. 1911–1920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. V. Marin, H. Kakuda, E. Dander et al., “Enhancement of the anti-leukemic activity of cytokine induced killer cells with an anti-CD19 chimeric receptor delivering a 4-1BB-ζ activating signal,” Experimental Hematology, vol. 35, no. 9, pp. 1388–1397, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. S. H. Yoon, J. M. Lee, S. Woo et al., “Transfer of Her-2/neu specificity into cytokine-induced killer (CIK) cells with RNA encoding chimeric immune receptor (CIR),” Journal of Clinical Immunology, vol. 29, no. 6, pp. 806–814, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. I. G. H. Schmidt-Wolf, S. Finke, B. Trojaneck et al., “Phase I clinical study applying autologous immunological effector cells transfected with the interleukin-1 gene in patients with metastatic renal cancer, colorectal cancer and lymphoma,” The British Journal of Cancer, vol. 81, no. 6, pp. 1009–1016, 1999. View at Publisher · View at Google Scholar · View at Scopus
  60. S. A. Rosenberg, B. S. Packard, P. M. Aebersold et al., “Use of tumor-infiltrating lymphocyts and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report,” The New England Journal of Medicine, vol. 319, no. 25, pp. 1676–1680, 1988. View at Google Scholar · View at Scopus
  61. S. A. Rosenberg, J. C. Yang, R. M. Sherry et al., “Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy,” Clinical Cancer Research, vol. 17, no. 13, pp. 4550–4557, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. C. A. Klebanoff, S. E. Finkelstein, D. R. Surman et al., “IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 7, pp. 1969–1974, 2004. View at Google Scholar
  63. L. Gattinoni, S. E. Finkelstein, C. A. Klebanoff et al., “Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells,” Journal of Experimental Medicine, vol. 202, no. 7, pp. 907–912, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. A. M. Wolf, D. Wolf, M. Steurer, G. Gastl, E. Gunsilius, and B. Grubeck-Loebenstein, “Increase of regulatory T cells in the peripheral blood of cancer patients,” Clinical Cancer Research, vol. 9, no. 2, pp. 606–612, 2003. View at Google Scholar · View at Scopus
  65. R. A. Morgan, M. E. Dudley, Y. Y. L. Yu et al., “High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens,” Journal of Immunology, vol. 171, no. 6, pp. 3287–3295, 2003. View at Google Scholar · View at Scopus
  66. M. E. Dudley, J. R. Wunderlich, T. E. Shelton, J. Even, and S. A. Rosenberg, “Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients,” Journal of Immunotherapy, vol. 26, no. 4, pp. 332–342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. L. A. Johnson, R. A. Morgan, M. E. Dudley et al., “Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen,” Blood, vol. 114, no. 3, pp. 535–546, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Kaneko, S. Mastaglio, A. Bondanza et al., “IL-7 and IL-15 allow the generation of suicide gene modified alloreactive self-renewing central memory human T lymphocytes,” Blood, vol. 113, no. 5, pp. 1006–1015, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. T. N. Golovina and R. H. Vonderheide, “Regulatory T cells overcoming suppression of t-cell immunity,” Cancer Journal, vol. 16, no. 4, pp. 342–347, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. R. Morita, Y. Hirohashi, and N. Sato, “Depletion of Tregs in vivo: a promising approach to enhance antitumor immunity without autoimmunity,” Immunotherapy, vol. 4, no. 11, pp. 1103–1105, 2012. View at Publisher · View at Google Scholar
  71. S. Amarnath and D. H. Fowler, “Harnessing autophagy for adoptive T-cell therapy,” Immunotherapy, vol. 4, no. 1, pp. 1–4, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. G. Dotti, B. Savoldo, M. Pule et al., “Human cytotoxic T lymphocytes with reduced sensitivity to Fas-induced apoptosis,” Blood, vol. 105, no. 12, pp. 4677–4684, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. X. Y. Lei, Y. Xu, T. Wang et al., “Knockdown of human bid gene expression enhances survival of CD8+ T cells,” Immunology Letters, vol. 122, no. 1, pp. 30–36, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. D. Eaton, D. E. Gilham, A. O'Neill, and R. E. Hawkins, “Retroviral transduction of human peripheral blood lymphocytes with bcl-XL promotes in vitro lymphocyte survival in pro-apoptotic conditions,” Gene Therapy, vol. 9, no. 8, pp. 527–535, 2002. View at Publisher · View at Google Scholar · View at Scopus
  75. J. Charo, S. E. Finkelstein, N. Grewal, N. P. Restifo, P. F. Robbins, and S. A. Rosenberg, “Bcl-2 overexpression enhances tumor-specific T-cell survival,” Cancer Research, vol. 65, no. 5, pp. 2001–2008, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. J. H. Shin, H. B. Park, Y. M. Oh et al., “Positive conversion of negative signaling of CTLA4 potentiates antitumor efficacy of adoptive T-cell therapy in murine tumor models,” Blood, vol. 119, no. 24, pp. 5678–5687, 2012. View at Publisher · View at Google Scholar
  77. A. S. Y. Lo, J. R. Taylor, F. Farzaneh, D. M. Kemeny, N. J. Dibb, and J. Maher, “Harnessing the tumour-derived cytokine, CSF-1, to co-stimulate T-cell growth and activation,” Molecular Immunology, vol. 45, no. 5, pp. 1276–1287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. M. H. Kershaw, P. Hwu, G. Wang et al., “Redirecting migration of T cells to chemokine secreted from tumors by genetic modification with CXCR2,” Human Gene Therapy, vol. 13, no. 16, pp. 1971–1980, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. M. E. Prosser, C. E. Brown, A. F. Shami, S. J. Forman, and M. C. Jensen, “Tumor PD-L1 co-stimulates primary human CD8+ cytotoxic T cells modified to express a PD1:CD28 chimeric receptor,” Molecular Immunology, vol. 51, no. 3-4, pp. 263–272, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. F. Ito and A. E. Chang, “Cancer immunotherapy: current status and future directions,” Surgical Oncology Clinics of North America, vol. 22, no. 4, pp. 765–783, 2013. View at Publisher · View at Google Scholar
  81. M. R. Parkhurst, J. C. Yang, R. C. Langan et al., “T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis,” Molecular Therapy, vol. 19, no. 3, pp. 620–626, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Zhao, A. D. Bennett, Z. Zheng et al., “High-affinity TCRs generated by phage display provide CD4+ T cells with the ability to recognize and kill tumor cell lines,” Journal of Immunology, vol. 179, no. 9, pp. 5845–5854, 2007. View at Google Scholar · View at Scopus
  83. R. A. Morgan, M. E. Dudley, J. R. Wunderlich et al., “Cancer regression in patients after transfer of genetically engineered lymphocytes,” Science, vol. 314, no. 5796, pp. 126–129, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. P. F. Robbins, R. A. Morgan, S. A. Feldman et al., “Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1,” Journal of Clinical Oncology, vol. 29, no. 7, pp. 917–924, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. K. Hanada, Q. J. Wang, T. Inozume, and J. C. Yang, “Molecular identification of an MHC-independent ligand recognized by a human α/β T-cell receptor,” Blood, vol. 117, no. 18, pp. 4816–4825, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. G. P. Linette, E. A. Stadtmauer, M. V. Maus et al., “Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma,” Blood, vol. 122, no. 6, pp. 863–871, 2013. View at Publisher · View at Google Scholar
  87. S. Okamoto, J. Mineno, H. Ikeda et al., “Improved expression and reactivity of transduced tumor-specific TCRs in human lymphocytes by specific silencing of endogenous TCR,” Cancer Research, vol. 69, no. 23, pp. 9003–9011, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. E. Provasi, P. Genovese, A. Lombardo et al., “Editing T cell specificity towards leukemia by zinc finger nucleases and lentiviral gene transfer,” Nature Medicine, vol. 18, no. 5, pp. 807–815, 2012. View at Publisher · View at Google Scholar
  89. N. P. Restifo, F. M. Marincola, Y. Kawakami, J. Taubenberger, J. R. Yannelli, and S. A. Rosenberg, “Loss of functional β2-microglobulin in metastatic melanomas from five patients receiving immunotherapy,” Journal of the National Cancer Institute, vol. 88, no. 2, pp. 100–108, 1996. View at Publisher · View at Google Scholar · View at Scopus
  90. C. E. Brown, R. Starr, B. Aguilar et al., “Stem-like tumor-initiating cells isolated from IL13Rα2 expressing gliomas are targeted and killed by IL13-zetakine-redirected T cells,” Clinical Cancer Research, vol. 18, no. 8, pp. 2199–2209, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. S. Lucas and P. G. Coulie, “About human tumor antigens to be used in immunotherapy,” Seminars in Immunology, vol. 20, no. 5, pp. 301–307, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. A. M. Scott, D. Geleick, M. Rubira et al., “Construction, production, and characterization of humanized anti-Lewis Y monoclonal antibody 3S193 for targeted immunotherapy of solid tumors,” Cancer Research, vol. 60, no. 12, pp. 3254–3261, 2000. View at Google Scholar · View at Scopus
  93. C. Imai, S. Iwamoto, and D. Campana, “Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells,” Blood, vol. 106, no. 1, pp. 376–383, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. Q. Ma, R. M. Gonzalo-Daganzo, and R. P. Junghans, “Genetically engineered T cells as adoptive immunotherapy of cancer,” Cancer Chemotherapy and Biological Response Modifiers, vol. 20, pp. 315–341, 2002. View at Google Scholar · View at Scopus
  95. H. M. Finney, A. N. Akbar, and A. D. G. Lawson, “Activation of resting human primary T cells with chimeric receptors: costimulation from CD28, inducible costimulator, CD134, and CD137 in series with signals from the TCRζ chain,” Journal of Immunology, vol. 172, no. 1, pp. 104–113, 2004. View at Google Scholar · View at Scopus
  96. M. H. Kershaw, J. A. Westwood, and P. K. Darcy, “Gene-engineered T cells for cancer therapy,” Nature Reviews Cancer, vol. 13, no. 8, pp. 525–541, 2013. View at Publisher · View at Google Scholar
  97. R. J. Brentjens, E. Santos, Y. Nikhamin et al., “Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts,” Clinical Cancer Research, vol. 13, no. 18, part 1, pp. 5426–5435, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. M. C. Milone, J. D. Fish, C. Carpenito et al., “Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo,” Molecular Therapy, vol. 17, no. 8, pp. 1453–1464, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. C. Carpenito, M. C. Milone, R. Hassan et al., “Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 9, pp. 3360–3365, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. P. C. R. Emtage, A. S. Y. Lo, E. M. Gomes, D. L. Liu, R. M. Gonzalo-Daganzo, and R. P. Junghans, “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,” Clinical Cancer Research, vol. 14, no. 24, pp. 8112–8122, 2008. View at Publisher · View at Google Scholar · View at Scopus
  101. B. Savoldo, C. A. Ramos, E. Liu et al., “CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients,” Journal of Clinical Investigation, vol. 121, no. 5, pp. 1822–1826, 2011. View at Publisher · View at Google Scholar · View at Scopus
  102. D. G. Song, Q. Ye, M. Poussin, G. M. Harms, M. Figini, and D. J. Powell Jr., “CD27 costimulation augments the survival and antitumor activity of redirected human T cells in vivo,” Blood, vol. 119, no. 3, pp. 696–706, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. X. S. Zhong, M. Matsushita, J. Plotkin, I. Riviere, and M. Sadelain, “Chimeric antigen receptors combining 4-1BB and CD28 signaling domains augment PI 3 kinase/AKT/Bcl-X L activation and CD8 T cell-mediated tumor eradication,” Molecular Therapy, vol. 18, no. 2, pp. 413–420, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. M. A. Pulè, K. C. Straathof, G. Dotti, H. E. Heslop, C. M. Rooney, and M. K. Brenner, “A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells,” Molecular Therapy, vol. 12, no. 5, pp. 933–941, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. M. A. Pule, B. Savoldo, G. D. Myers et al., “Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma,” Nature Medicine, vol. 14, no. 11, pp. 1264–1270, 2008. View at Publisher · View at Google Scholar · View at Scopus
  106. F. M. Uckun, W. Jaszcz, J. L. Ambrus et al., “Detailed studies on expression and function of CD19 surface determinant by using B43 monoclonal antibody and the clinical potential of anti-CD19 immunotoxins,” Blood, vol. 71, no. 1, pp. 13–29, 1988. View at Google Scholar · View at Scopus
  107. H. Harada, M. M. Kawano, N. Huang et al., “Phenotypic difference of normal plasma cells from mature myeloma cells,” Blood, vol. 81, no. 10, pp. 2658–2663, 1993. View at Google Scholar · View at Scopus
  108. J. N. Kochenderfer, W. H. Wilson, J. E. Janik 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, vol. 116, no. 20, pp. 4099–4102, 2010. View at Publisher · View at Google Scholar · View at Scopus
  109. J. N. Kochenderfer, M. E. Dudley, S. A. Feldman et al., “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, vol. 119, no. 12, pp. 2709–2720, 2012. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Kalos, B. L. Levine, D. L. Porter et al., “T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia,” Science Translational Medicine, vol. 3, no. 95, Article ID 95ra73, 2011. View at Publisher · View at Google Scholar · View at Scopus
  111. S. A. Grupp, M. Kalos, D. Barrett et al., “Chimeric antigen receptor-modified T cells for acute lymphoid leukemia,” The New England Journal of Medicine, vol. 368, no. 16, pp. 1509–1518, 2013. View at Publisher · View at Google Scholar
  112. D. S. Ritchie, P. J. Neeson, A. Khot et al., “Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia,” Molecular Therapy, 2013. View at Publisher · View at Google Scholar
  113. C. H. J. Lamers, R. Willemsen, P. van Elzakker et al., “Immune responses to transgene and retroviral vector in patients treated with ex vivo-engineered T cells,” Blood, vol. 117, no. 1, pp. 72–82, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. M. H. Kershaw, J. A. Westwood, L. L. Parker et al., “A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer,” Clinical Cancer Research, vol. 12, no. 20, pp. 6106–6115, 2006. View at Publisher · View at Google Scholar · View at Scopus
  115. R. A. Morgan, J. C. Yang, M. Kitano, M. E. Dudley, C. M. Laurencot, and S. A. Rosenberg, “Case report of a serious adverse event following the administration of t cells transduced with a chimeric antigen receptor recognizing ERBB2,” Molecular Therapy, vol. 18, no. 4, pp. 843–851, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. L. Gattinoni, E. Lugli, Y. Ji et al., “A human memory T cell subset with stem cell-like properties,” Nature Medicine, vol. 17, no. 10, pp. 1290–1297, 2011. View at Publisher · View at Google Scholar · View at Scopus
  117. C. A. Klebanoff, L. Gattinoni, D. C. Palmer et al., “Determinants of successful CD8+ T-cell adoptive immunotherapy for large established tumors in mice,” Clinical Cancer Research, vol. 17, no. 16, pp. 5343–5352, 2011. View at Publisher · View at Google Scholar · View at Scopus
  118. D. N. Vatakis, R. C. Koya, C. C. Nixon et al., “Antitumor activity from antigen-specific CD8 T cells generated in vivo from genetically engineered human hematopoietic stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 51, pp. E1408–E1416, 2011. View at Publisher · View at Google Scholar · View at Scopus
  119. S. Teitz-Tennenbaum, Q. Li, M. A. Davis et al., “Radiotherapy combined with intratumoral dendritic cell vaccination enhances the therapeutic efficacy of adoptive T-cell transfer,” Journal of Immunotherapy, vol. 32, no. 6, pp. 602–612, 2009. View at Publisher · View at Google Scholar · View at Scopus
  120. D. J. Schwartzentruber, D. H. Lawson, J. M. Richards et al., “gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma,” The New England Journal of Medicine, vol. 364, no. 22, pp. 2119–2127, 2011. View at Publisher · View at Google Scholar
  121. S. Wada, K. Yoshimura, E. L. Hipkiss et al., “Cyclophosphamide augments antitumor immunity: studies in an autochthonous prostate cancer model,” Cancer Research, vol. 69, no. 10, pp. 4309–4318, 2009. View at Publisher · View at Google Scholar · View at Scopus
  122. C. Robert, L. Thomas, I. Bondarenko et al., “Ipilimumab plus dacarbazine for previously untreated metastatic melanoma,” The New England Journal of Medicine, vol. 364, no. 26, pp. 2517–2526, 2011. View at Publisher · View at Google Scholar · View at Scopus