Advertisement

Adoptive Cell Therapy of Gastric Cancer

  • Zhengyun ZouEmail author
  • Lianjun Zhao
  • Yu Ren
  • Shiyao Du
Chapter

Abstract

Tremendous progress has been made in the field of immunotherapy through various research studies and clinical trials. This work has led to significant breakthroughs in the treatment of malignant tumors. Immunotherapy treatment is an additional treatment option to other novel approaches, including immune checkpoint inhibitors and signaling pathway inhibitors; those have demonstrated clear efficacy in the treatment of numerous cancer types. Some examples include malignant melanoma, kidney cancer, lung cancer, and urinary bladder cancer. Adoptive cell therapy (ACT) has also shown clear effects in the treatment of different malignant diseases. ACT is a highly personalized cancer therapy that takes advantage of immune cells that infiltrate tumors for direct anticancer activities. ACT utilizes either natural host cells, such as lymphokine-activated killer cells (LAK), cytokine-induced killer cells (CIK), tumor-infiltrating lymphocytes (TIL), and cytotoxic T lymphocytes (CTL), or host cells that have been genetically engineered to possess antitumor T cell receptors (TCRs) or chimeric antigen receptors (CARs). This chapter profiles ACT in cancer immunotherapy based on reliable data, some of which demonstrates the use of this cell therapy for the treatment of gastric cancer.

Keywords

Gastric Cancer Chimeric Antigen Receptor Cancer Testis Antigen Adoptive Cell Therapy Cytokine Release Syndrome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Schmidt-Wolf IG, Negrin RS, Kiem HP, Blume KG, Weissman IL. Use of a SCID mouse/human lymphoma model to evaluate cytokine-induced killer cells with potent antitumor cell activity. J Exp Med. 1991;174(1):139–49.CrossRefPubMedGoogle Scholar
  2. 2.
    Shi L, Zhou Q, Wu J, Ji M, Li G, Jiang J, et al. Efficacy of adjuvant immunotherapy with cytokine-induced killer cells in patients with locally advanced gastric cancer. Cancer Immunol Immunother. 2012;61(12):2251–9. doi: 10.1007/s00262-012-1289-2.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Liu K, Song G, Hu X, Zhou Y, Li Y, Chen Q, et al. A positive role of cytokine-induced killer cell therapy on gastric cancer therapy in a chinese population: a systematic meta-analysis. Med Sci Monit. 2015;21:3363–70.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Li X, Dai D, Song X, Liu J, Zhu L, Xu W. A meta-analysis of cytokine-induced killer cells therapy in combination with minimally invasive treatment for hepatocellular carcinoma. Clin Res Hepatol Gastroenterol. 2014;38(5):583–91. doi: 10.1016/j.clinre.2014.04.010.CrossRefPubMedGoogle Scholar
  5. 5.
    Wang ZX, Cao JX, Liu ZP, Cui YX, Li CY, Li D, et al. Combination of chemotherapy and immunotherapy for colon cancer in China: a meta-analysis. World J Gastroenterol. 2014;20(4):1095–106. doi: 10.3748/wjg.v20.i4.1095.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Han RX, Liu X, Pan P, Jia YJ, Yu JC. Effectiveness and safety of chemotherapy combined with dendritic cells co-cultured with cytokine-induced killer cells in the treatment of advanced non-small-cell lung cancer: a systematic review and meta-analysis. PLoS One. 2014;9(9):e108958. doi: 10.1371/journal.pone.0108958.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Jiang J, Xu N, Wu C, Deng H, Lu M, Li M, et al. Treatment of advanced gastric cancer by chemotherapy combined with autologous cytokine-induced killer cells. Anticancer Res. 2006;26(3B):2237–42.PubMedGoogle Scholar
  8. 8.
    Rosenberg SA, Spiess P, Lafreniere R. A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science. 1986;233(4770):1318–21.CrossRefPubMedGoogle Scholar
  9. 9.
    Rosenberg SA, Packard BS, Aebersold PM, Solomon D, Topalian SL, Toy ST, et al. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med. 1988;319(25):1676–80. doi: 10.1056/NEJM198812223192527.CrossRefPubMedGoogle Scholar
  10. 10.
    Feldman SA, Assadipour Y, Kriley I, Goff SL, Rosenberg SA. Adoptive cell therapy—tumor-infiltrating lymphocytes, T-cell receptors, and chimeric antigen receptors. Semin Oncol. 2015;42(4):626–39. doi: 10.1053/j.seminoncol.2015.05.005.CrossRefPubMedGoogle Scholar
  11. 11.
    Andersen R, Donia M, Westergaard MC, Pedersen M, Hansen M, Svane IM. Tumor infiltrating lymphocyte therapy for ovarian cancer and renal cell carcinoma. Hum Vaccin Immunother. 2015;11(12):2790–5. doi: 10.1080/21645515.2015.1075106.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Turcotte S, Gros A, Hogan K, Tran E, Hinrichs CS, Wunderlich JR, et al. Phenotype and function of T cells infiltrating visceral metastases from gastrointestinal cancers and melanoma: implications for adoptive cell transfer therapy. J Immunol. 2013;191(5):2217–25. doi: 10.4049/jimmunol.1300538.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Webb JR, Milne K, Watson P, Deleeuw RJ, Nelson BH. Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer. Clin Cancer Res. 2014;20(2):434–44. doi: 10.1158/1078-0432.CCR-13-1877.CrossRefPubMedGoogle Scholar
  14. 14.
    Yannelli JR, Hyatt C, McConnell S, Hines K, Jacknin L, Parker L, et al. Growth of tumor-infiltrating lymphocytes from human solid cancers: summary of a 5-year experience. Int J Cancer. 1996;65(4):413–21. doi:10.1002/(SICI)1097-0215(19960208)65:4<413::AID-IJC3>3.0.CO;2-#.CrossRefPubMedGoogle Scholar
  15. 15.
    Yamaue H, Tanimura H, Tsunoda T, Iwahashi M, Tani M, Inoue M, et al. Clinical application of adoptive immunotherapy by cytotoxic T lymphocytes induced from tumor-infiltrating lymphocytes. Nihon Gan Chiryo Gakkai Shi. 1990;25(5):978–89.PubMedGoogle Scholar
  16. 16.
    Kono K, Takahashi A, Ichihara F, Amemiya H, Iizuka H, Fujii H, et al. Prognostic significance of adoptive immunotherapy with tumor-associated lymphocytes in patients with advanced gastric cancer: a randomized trial. Clin Cancer Res. 2002;8(6):1767–71.PubMedGoogle Scholar
  17. 17.
    Gros A, Robbins PF, Yao X, Li YF, Turcotte S, Tran E, et al. PD-1 identifies the patient-specific CD8(+) tumor-reactive repertoire infiltrating human tumors. J Clin Invest. 2014;124(5):2246–59. doi: 10.1172/JCI73639.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Kerkar SP, Leonardi AJ, van Panhuys N, Zhang L, Yu Z, Crompton JG, et al. Collapse of the tumor stroma is triggered by IL-12 induction of Fas. Mol Ther. 2013;21(7):1369–77. doi: 10.1038/mt.2013.58.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Tran E, Turcotte S, Gros A, Robbins PF, Lu YC, Dudley ME, et al. Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science. 2014;344(6184):641–5. doi: 10.1126/science.1251102.CrossRefPubMedGoogle Scholar
  20. 20.
    Karimi S, Chattopadhyay S, Chakraborty NG. Manipulation of regulatory T cells and antigen-specific cytotoxic T lymphocyte-based tumour immunotherapy. Immunology. 2015;144(2):186–96. doi: 10.1111/imm.12387.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Hoshino T, Seki N, Kikuchi M, Kuramoto T, Iwamoto O, Kodama I, et al. HLA class-I-restricted and tumor-specific CTL in tumor-infiltrating lymphocytes of patients with gastric cancer. Int J Cancer. 1997;70(6):631–8.CrossRefPubMedGoogle Scholar
  22. 22.
    Louis CU, Straathof K, Bollard CM, Gerken C, Huls MH, Gresik MV, et al. Enhancing the in vivo expansion of adoptively transferred EBV-specific CTL with lymphodepleting CD45 monoclonal antibodies in NPC patients. Blood. 2009;113(11):2442–50. doi: 10.1182/blood-2008-05-157222.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Bollard CM, Aguilar L, Straathof KC, Gahn B, Huls MH, Rousseau A, et al. Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin’s disease. J Exp Med. 2004;200(12):1623–33. doi: 10.1084/jem.20040890.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Bae JM, Kim EH. Epstein-Barr Virus and gastric cancer risk: a meta-analysis with meta-regression of case-control studies. J Prev Med Public Health. 2016;49(2):97–107. doi: 10.3961/jpmph.15.068.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Klebanoff CA, Rosenberg SA, Restifo NP. Prospects for gene-engineered T cell immunotherapy for solid cancers. Nat Med. 2016;22(1):26–36. doi: 10.1038/nm.4015.CrossRefPubMedGoogle Scholar
  26. 26.
    Rosenberg SA, Restifo NP. Adoptive cell transfer as personalized immunotherapy for human cancer. Science. 2015;348(6230):62–8. doi: 10.1126/science.aaa4967.CrossRefPubMedGoogle Scholar
  27. 27.
    Zhang L, Morgan RA. Genetic engineering with T cell receptors. Adv Drug Deliv Rev. 2012;64(8):756–62. doi: 10.1016/j.addr.2011.11.009.CrossRefPubMedGoogle Scholar
  28. 28.
    Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science. 2006;314(5796):126–9. doi: 10.1126/science.1129003.
  29. 29.
    Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood. 2009;114(3):535–46. doi: 10.1182/blood-2009-03-211714.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, 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(7):917–24. doi: 10.1200/JCO.2010.32.2537.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Robbins PF, Kassim SH, Tran TL, Crystal JS, Morgan RA, Feldman SA, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res. 2015;21(5):1019–27. doi: 10.1158/1078-0432.CCR-14-2708.CrossRefPubMedGoogle Scholar
  32. 32.
    Rapoport AP, Stadtmauer EA, Binder-Scholl GK, Goloubeva O, Vogl DT, Lacey SF, et al. NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nat Med. 2015;21(8):914–21. doi: 10.1038/nm.3910.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Robbins PF, Li YF, El-Gamil M, Zhao Y, Wargo JA, Zheng Z, et al. Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. J Immunol. 2008;180(9):6116–31.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Morgan RA. Risky business: target choice in adoptive cell therapy. Blood. 2013;122(20):3392–4. doi: 10.1182/blood-2013-09-527622.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Linette GP, Stadtmauer EA, Maus MV, Rapoport AP, Levine BL, Emery L, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood. 2013;122(6):863–71. doi: 10.1182/blood-2013-03-490565.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Tran E, Ahmadzadeh M, Lu YC, Gros A, Turcotte S, Robbins PF, et al. Immunogenicity of somatic mutations in human gastrointestinal cancers. Science. 2015;350(6266):1387–90. doi: 10.1126/science.aad1253.CrossRefPubMedGoogle Scholar
  37. 37.
    Desrichard A, Snyder A, Chan TA. Cancer neoantigens and applications for immunotherapy. Clin Cancer Res. 2016;22(4):807–12. doi: 10.1158/1078-0432.CCR-14-3175.CrossRefPubMedGoogle Scholar
  38. 38.
    Eshhar Z, Waks T, Gross G, Schindler DG. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci U S A. 1993;90(2):720–4.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16):1507–17. doi: 10.1056/NEJMoa1407222.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Gill S, Tasian SK, Ruella M, Shestova O, Li Y, Porter DL, et al. Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood. 2014;123(15):2343–54. doi: 10.1182/blood-2013-09-529537.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5(177):177ra38. doi: 10.1126/scitranslmed.3005930.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Kochenderfer JN, Wilson WH, Janik JE, Dudley ME, Stetler-Stevenson M, Feldman SA, 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;116(20):4099–102. doi: 10.1182/blood-2010-04-281931.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Porter DL, Hwang WT, Frey NV, Lacey SF, Shaw PA, Loren AW, et al. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med. 2015;7(303):303ra139. doi: 10.1126/scitranslmed.aac5415.CrossRefPubMedGoogle Scholar
  44. 44.
    Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365(8):725–33. doi: 10.1056/NEJMoa1103849.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Davila ML, Riviere I, Wang X, Bartido S, Park J, Curran K, et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med. 2014;6(224):224ra25. doi: 10.1126/scitranslmed.3008226.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Lee DW, Kochenderfer JN, Stetler-Stevenson M, Cui YK, Delbrook C, Feldman SA, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet. 2015;385(9967):517–28. doi: 10.1016/S0140-6736(14)61403-3.CrossRefPubMedGoogle Scholar
  47. 47.
    Garfall AL, Maus MV, Hwang WT, Lacey SF, Mahnke YD, Melenhorst JJ, et al. Chimeric antigen receptor T Cells against CD19 for multiple myeloma. N Engl J Med. 2015;373(11):1040–7. doi: 10.1056/NEJMoa1504542.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. 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(4):843–51. doi: 10.1038/mt.2010.24.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Lamers CH, Sleijfer S, van Steenbergen S, van Elzakker P, van Krimpen B, Groot C, et al. Treatment of metastatic renal cell carcinoma with CAIX CAR-engineered T cells: clinical evaluation and management of on-target toxicity. Mol Ther. 2013;21(4):904–12. doi: 10.1038/mt.2013.17.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Louis CU, Savoldo B, Dotti G, Pule M, Yvon E, Myers GD, et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood. 2011;118(23):6050–6. doi: 10.1182/blood-2011-05-354449.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Lee DW, Gardner R, Porter DL, Louis CU, Ahmed N, Jensen M, et al. Current concepts in the diagnosis and management of cytokine release syndrome. Blood. 2014;124(2):188–95. doi: 10.1182/blood-2014-05-552729.
  52. 52.
    Posey Jr AD, Schwab RD, Boesteanu AC, Steentoft C, Mandel U, Engels B, et al. Engineered CAR T cells targeting the cancer-associated Tn-glycoform of the membrane mucin MUC1 control adenocarcinoma. Immunity. 2016;44(6):1444–54. doi: 10.1016/j.immuni.2016.05.014.
  53. 53.
    Yang J, Li ZH, Zhou JJ, Chen RF, Cheng LZ, Zhou QB, et al. Preparation and antitumor effects of nanovaccines with MAGE-3 peptides in transplanted gastric cancer in mice. Chin J Cancer. 2010;29(4):359–64.CrossRefPubMedGoogle Scholar
  54. 54.
    Kono K, Takahashi A, Sugai H, Fujii H, Choudhury AR, Kiessling R, et al. Dendritic cells pulsed with HER-2/neu-derived peptides can induce specific T-cell responses in patients with gastric cancer. Clin Cancer Res. 2002;8(11):3394–400.PubMedGoogle Scholar
  55. 55.
    Amemiya H, Pena A, Chiurillo M, Moscoso J, Useche A, Baffi R. Increased expression of the c-Met receptor mRNA in gastric cancer. Invest Clin. 2013;54(3):284–98.PubMedGoogle Scholar
  56. 56.
    Ajani JA, Hecht JR, Ho L, Baker J, Oortgiesen M, Eduljee A, et al. An open-label, multinational, multicenter study of G17DT vaccination combined with cisplatin and 5-fluorouracil in patients with untreated, advanced gastric or gastroesophageal cancer: the GC4 study. Cancer. 2006;106(9):1908–16. doi: 10.1002/cncr.21814.CrossRefPubMedGoogle Scholar
  57. 57.
    Li ZY, Shan F, Zhang LH, Bu ZD, Wu AW, Wu XJ, et al. Preoperative chemotherapy with a trastuzumab-containing regimen for a patient with gastric cancer and hepatic metastases. Genet Mol Res. 2014;13(4):10952–7. doi: 10.4238/2014.December.19.17.CrossRefPubMedGoogle Scholar
  58. 58.
    Sun M, Shi H, Liu C, Liu J, Liu X, Sun Y. Construction and evaluation of a novel humanized HER2-specific chimeric receptor. Breast Cancer Res. 2014;16(3):R61. doi: 10.1186/bcr3674.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Ahmed N, Brawley VS, Hegde M, Robertson C, Ghazi A, Gerken C, et al. Human epidermal growth factor receptor 2 (HER2)-specific chimeric antigen receptor-modified T cells for the immunotherapy of HER2-positive sarcoma. J Clin Oncol. 2015;33(15):1688–96. doi: 10.1200/JCO.2014.58.0225.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Lee J, van Hummelen P, Go C, Palescandolo E, Jang J, Park HY, et al. High-throughput mutation profiling identifies frequent somatic mutations in advanced gastric adenocarcinoma. PLoS One. 2012;7(6):e38892. doi: 10.1371/journal.pone.0038892.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Wang L, Heng X, Lu Y, Cai Z, Yi Q, Che F. Could B7-H4 serve as a target to activate anti-cancer immunity? Int Immunopharmacol. 2016;38:97–103. doi: 10.1016/j.intimp.2016.05.020.CrossRefPubMedGoogle Scholar
  62. 62.
    Burns WR, Zheng Z, Rosenberg SA, Morgan RA. 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(14):2888–99. doi: 10.1182/blood-2009-01-199216.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Davis JL, Theoret MR, Zheng Z, Lamers CH, Rosenberg SA, Morgan RA. 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(23):5852–61. doi: 10.1158/1078-0432.CCR-10-1280.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan DA, Feldman SA, et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther. 2011;19(3):620–6. doi: 10.1038/mt.2010.272.CrossRefGoogle Scholar
  65. 65.
    Morgan RA, Chinnasamy N, Abate-Daga D, Gros A, Robbins PF, Zheng Z, et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother. 2013;36(2):133–51. doi: 10.1097/CJI.0b013e3182829903.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3(95):95ra73. doi: 10.1126/scitranslmed.3002842.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Kochenderfer JN, Dudley ME, Feldman SA, Wilson WH, Spaner DE, Maric I, 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. 2012;119(12):2709–20. doi: 10.1182/blood-2011-10-384388.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Savoldo B, Ramos CA, Liu E, Mims MP, Keating MJ, Carrum G, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest. 2011;121(5):1822–6. doi: 10.1172/JCI46110.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Till BG, Jensen MC, Wang J, Chen EY, Wood BL, Greisman HA, et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood. 2008;112(6):2261–71. doi: 10.1182/blood-2007-12-128843.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Till BG, Jensen MC, Wang J, Qian X, Gopal AK, Maloney DG, et al. CD20-specific adoptive immunotherapy for lymphoma using a chimeric antigen receptor with both CD28 and 4-1BB domains: pilot clinical trial results. Blood. 2012;119(17):3940–50. doi: 10.1182/blood-2011-10-387969.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Park JR, Digiusto DL, Slovak M, Wright C, Naranjo A, Wagner J, et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther. 2007;15(4):825–33. doi: 10.1038/sj.mt.6300104.CrossRefPubMedGoogle Scholar
  72. 72.
    van Schalkwyk MC, Papa SE, Jeannon JP, Guerrero Urbano T, Spicer JF, Maher J. Design of a phase I clinical trial to evaluate intratumoral delivery of ErbB-targeted chimeric antigen receptor T-cells in locally advanced or recurrent head and neck cancer. Hum Gene Ther Clin Dev. 2013;24(3):134–42. doi: 10.1089/humc.2013.144.CrossRefPubMedGoogle Scholar
  73. 73.
    Ma Q, Gonzalo-Daganzo RM, Junghans RP. Genetically engineered T cells as adoptive immunotherapy of cancer. Cancer Chemother Biol Response Modif. 2002;20:315–41.PubMedGoogle Scholar
  74. 74.
    Katz SC, Burga RA, McCormack E, Wang LJ, Mooring W, Point GR, et al. Phase I hepatic immunotherapy for metastases study of intra-arterial chimeric antigen receptor-modified T-cell therapy for CEA+ liver metastases. Clin Cancer Res. 2015;21(14):3149–59. doi: 10.1158/1078-0432.CCR-14-1421.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Ritchie DS, Neeson PJ, Khot A, Peinert S, Tai T, Tainton K, et al. Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Mol Ther. 2013;21(11):2122–9. doi: 10.1038/mt.2013.154.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Kruit WH, Suciu S, Dreno B, Mortier L, Robert C, Chiarion-Sileni V, et al. Selection of immunostimulant AS15 for active immunization with MAGE-A3 protein: results of a randomized phase II study of the european organisation for research and treatment of cancer melanoma group in metastatic melanoma. J Clin Oncol. 2013;31(19):2413–20. doi: 10.1200/JCO.2012.43.7111.CrossRefPubMedGoogle Scholar
  77. 77.
    Vansteenkiste J, Zielinski M, Linder A, Dahabreh J, Gonzalez EE, Malinowski W, et al. Adjuvant MAGE-A3 immunotherapy in resected non-small-cell lung cancer: phase II randomized study results. J Clin Oncol. 2013;31(19):2396–403. doi: 10.1200/JCO.2012.43.7103.CrossRefPubMedGoogle Scholar
  78. 78.
    Vansteenkiste JF, Cho BC, Vanakesa T, De Pas T, Zielinski M, Kim MS, et al. Efficacy of the MAGE-A3 cancer immunotherapeutic as adjuvant therapy in patients with resected MAGE-A3-positive non-small-cell lung cancer (MAGRIT): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 2016;17(6):822–35. doi: 10.1016/S1470-2045(16)00099-1.CrossRefPubMedGoogle Scholar
  79. 79.
    Gros A, Parkhurst MR, Tran E, Pasetto A, Robbins PF, Ilyas S, et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat Med. 2016;22(4):433–8. doi: 10.1038/nm.4051.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  1. 1.The Comprehensive Cancer Center of Drum Tower HospitalMedical School of Nanjing University and Clinical Cancer Institute of Nanjing UniversityNanjingChina

Personalised recommendations