Cited by 73Immunotherapy and Immune ResponsesSarcoma Diagnosis and TreatmentCAR-T cell therapy research

T-Cell-Based Immunotherapy for Osteosarcoma: Challenges and Opportunities

Open access
Wang, Zhan, Li, Binghao, Ren, Yingqing, Ye, Zhaoming·2016·Frontiers in Immunology

Abstract

Even though combining surgery with chemotherapy has significantly improved the prognosis of osteosarcoma patients, advanced, metastatic, or recurrent osteosarcomas are often non-responsive to chemotherapy, making development of novel efficient therapeutic methods an urgent need. Adoptive immunotherapy has the potential to be a useful non-surgical modality for treatment of osteosarcoma. Recently, alternative strategies, including immunotherapies using naturally occurring or genetically modified T cells, have been found to hold promise in the treatment of hematologic malignancies and solid tumors. In this review, we will discuss possible T-cell-based therapies against osteosarcoma with a special emphasis on combination strategies to improve the effectiveness of adoptive T cell transfer and, thus, to provide a rationale for the clinical development of immunotherapies.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fimmu.2016.00353

Cites

12 of 12 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Native CD8+ T cells play an immunomodulatory role in patients with primary osteosarcoma.

    “Additionally, it has been shown that native CD8+ T cells play an immunomodulatory role, more specifically in patients with primary OS [8,9].”

    From Mesenchymal Stem/Stromal Cells: Immunomodulatory and Bone Regeneration Potential after Tumor Excision in Osteosarcoma Patients (2023) · cites this paper as [9]

    The ‘Unmodified CD8+ T Lymphocytes’ section says evidence suggests cytotoxic CD8+ T cells have a leading role in immune surveillance in patients with osteosarcoma. It does not specifically establish that role in patients with primary osteosarcoma, and its wording is more tentative than ‘has been shown.’ (LLM, conf=0.82)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 146

  1. [1]Jo VY Fletcher CD. WHO classification of soft tissue tumours: an update based on the 2013 (4th) edition. Pathology (2014) 46(2): 95– 104. 10.1097/PAT.0000000000000050 24378391 · DOI
  2. [2]Biermann JS Adkins DR Benjamin RS Brigman B Chow W Conrad EU III Bone cancer. J Natl Compr Canc Netw (2010) 8(6): 688– 712. 20581300
  3. [4]Isakoff MS Bielack SS Meltzer P Gorlick R. Osteosarcoma: current treatment and a collaborative pathway to success. J Clin Oncol (2015) 33(27): 3029– 35. 10.1200/JCO.2014.59.4895 26304877 PMC4979196 · DOI
  4. [5]Roberts SS Chou AJ Cheung NK. Immunotherapy of childhood sarcomas. Front Oncol (2015) 5: 181. 10.3389/fonc.2015.00181 26301204 PMC4528283 · DOI
  5. [6]Kager L Zoubek A Potschger U Kastner U Flege S Kempf-Bielack B Primary metastatic osteosarcoma: presentation and outcome of patients treated on neoadjuvant Cooperative Osteosarcoma Study Group protocols. J Clin Oncol (2003) 21(10): 2011– 8. 10.1200/JCO.2003.08.132 12743156 · DOI · Paper page
  6. [7]Tsuchiya H Kanazawa Y Abdel-Wanis ME Asada N Abe S Isu K Effect of timing of pulmonary metastases identification on prognosis of patients with osteosarcoma: the Japanese Musculoskeletal Oncology Group study. J Clin Oncol (2002) 20(16): 3470– 7. 10.1200/JCO.2002.11.028 12177108 · DOI
  7. [8]Daw NC Chou AJ Jaffe N Rao BN Billups CA Rodriguez-Galindo C Recurrent osteosarcoma with a single pulmonary metastasis: a multi-institutional review. Br J Cancer (2015) 112(2): 278– 82. 10.1038/bjc.2014.585 25422914 PMC4453448 · DOI
  8. [9]Tsukahara T Emori M Murata K Hirano T Muroi N Kyono M Specific targeting of a naturally presented osteosarcoma antigen, papillomavirus binding factor peptide, using an artificial monoclonal antibody. J Biol Chem (2014) 289(32): 22035– 47. 10.1074/jbc.M114.568725 24962571 PMC4139219 · DOI
  9. [10]Wan J Zhang X Liu T Zhang X. Strategies and developments of immunotherapies in osteosarcoma. Oncol Lett (2016) 11(1): 511– 20. 10.3892/ol.2015.3962 26834853 PMC4727173 · DOI
  10. [12]Kawano M Tanaka K Itonaga I Iwasaki T Miyazaki M Ikeda S Dendritic cells combined with anti-GITR antibody produce antitumor effects in osteosarcoma. Oncol Rep (2015) 34(4): 1995– 2001. 10.3892/or.2015.4161 26239052 · DOI · Paper page
  11. [13]He YT Zhang QM Kou QC Tang B. In vitro generation of cytotoxic T lymphocyte response using dendritic cell immunotherapy in osteosarcoma. Oncol Lett (2016) 12(2): 1101– 6. 10.3892/ol.2016.4714 27446401 PMC4950224 · DOI · Paper page
  12. [14]Coley WB The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin Orthop Relat Res (1991) (262): 3– 11. 1984929
  13. [15]Topalian SL Weiner GJ Pardoll DM. Cancer immunotherapy comes of age. J Clin Oncol (2011) 29(36): 4828– 36. 10.1200/JCO.2011.38.0899 22042955 PMC3255990 · DOI
  14. [16]Nauts HC Fowler GA Bogatko FH A review of the influence of bacterial infection and of bacterial products (Coley’s toxins) on malignant tumors in man; a critical analysis of 30 inoperable cases treated by Coley’s mixed toxins, in which diagnosis was confirmed by microscopic examination selected for special study. Acta Med Scand Suppl (1953) 276: 1– 103. 13039964
  15. [17]Yang JC Rosenberg SA. Adoptive T-cell therapy for cancer. Adv Immunol (2016) 130: 279– 94. 10.1016/bs.ai.2015.12.006 26923004 PMC6293459 · DOI
  16. [19]Rosenberg SA Yang JC Sherry RM Kammula US Hughes MS Phan GQ Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res (2011) 17(13): 4550– 7. 10.1158/1078-0432.CCR-11-0116 21498393 PMC3131487 · DOI
  17. [20]Ahmed N Brawley VS Hegde M Robertson C Ghazi A Gerken C 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. 10.1200/JCO.2014.58.0225 25800760 PMC4429176 · DOI · Paper page
  18. [21]Li B Zhu X Sun L Yuan L Zhang J Li H Induction of a specific CD8+ T-cell response to cancer/testis antigens by demethylating pre-treatment against osteosarcoma. Oncotarget (2014) 5(21): 10791– 802. 10.18632/oncotarget.2505 25301731 PMC4279410 · DOI
  19. [22]Li Z Xu Q Peng H Cheng R Sun Z Ye Z IFN-gamma enhances HOS and U2OS cell lines susceptibility to gammadelta T cell-mediated killing through the Fas/Fas ligand pathway. Int Immunopharmacol (2011) 11(4): 496– 503. 10.1016/j.intimp.2011.01.001 21238618 · DOI
  20. [23]Ahmed N Salsman VS Yvon E Louis CU Perlaky L Wels WS Immunotherapy for osteosarcoma: genetic modification of T cells overcomes low levels of tumor antigen expression. Mol Ther (2009) 17(10): 1779– 87. 10.1038/mt.2009.133 19532139 PMC2835000 · DOI · Paper page
  21. [24]Theoleyre S Mori K Cherrier B Passuti N Gouin F Redini F Phenotypic and functional analysis of lymphocytes infiltrating osteolytic tumors: use as a possible therapeutic approach of osteosarcoma. BMC Cancer (2005) 5: 123. 10.1186/1471-2407-5-123 16188028 PMC1262697 · DOI
  22. [25]Morgan DA Ruscetti FW Gallo R. Selective in vitro growth of T lymphocytes from normal human bone marrows. Science (1976) 193(4257): 1007– 8. 10.1126/science.181845 181845 · DOI
  23. [26]Rosenberg SA Cell transfer immunotherapy for metastatic solid cancer – what clinicians need to know. Nat Rev Clin Oncol (2011) 8(10): 577– 85. 10.1038/nrclinonc.2011.116 21808266 PMC6292196 · DOI
  24. [27]Rosenberg SA Restifo NP. Adoptive cell transfer as personalized immunotherapy for human cancer. Science (2015) 348(6230): 62– 8. 10.1126/science.aaa4967 25838374 PMC6295668 · DOI
  25. [28]Davila ML Riviere I Wang X Bartido S Park J Curran K Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med (2014) 6(224): 224ra25. 10.1126/scitranslmed.3008226 24553386 PMC4684949 · DOI
  26. [29]Brentjens RJ Davila ML Riviere I Park J Wang X Cowell LG CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med (2013) 5(177): 177ra38. 10.1126/scitranslmed.3005930 23515080 PMC3742551 · DOI · Paper page
  27. [30]Peng W Ye Y Rabinovich BA Liu C Lou Y Zhang M Transduction of tumor-specific T cells with CXCR2 chemokine receptor improves migration to tumor and antitumor immune responses. Clin Cancer Res (2010) 16(22): 5458– 68. 10.1158/1078-0432.CCR-10-0712 20889916 PMC3476703 · DOI
  28. [31]Junker N Kvistborg P Kollgaard T Straten P Andersen MH Svane IM. Tumor associated antigen specific T-cell populations identified in ex vivo expanded TIL cultures. Cell Immunol (2012) 273(1): 1– 9. 10.1016/j.cellimm.2011.12.004 22230732 · DOI
  29. [32]Adams S Goldstein LJ Sparano JA Demaria S Badve SS. Tumor infiltrating lymphocytes (TILs) improve prognosis in patients with triple negative breast cancer (TNBC). Oncoimmunology (2015) 4(9): e985930. 10.4161/2162402X.2014.985930 26405612 PMC4570112 · DOI
  30. [33]Mina M Boldrini R Citti A Romania P D’Alicandro V De Ioris M Tumor-infiltrating T lymphocytes improve clinical outcome of therapy-resistant neuroblastoma. Oncoimmunology (2015) 4(9): e1019981. 10.1080/2162402X.2015.1019981 26405592 PMC4570119 · DOI
  31. [34]Vassilakopoulou M Avgeris M Velcheti V Kotoula V Rampias T Chatzopoulos K Evaluation of PD-L1 expression and associated tumor-infiltrating lymphocytes in laryngeal squamous cell carcinoma. Clin Cancer Res (2016) 22(3): 704– 13. 10.1158/1078-0432.CCR-15-1543 26408403 · DOI
  32. [35]Muul LM Spiess PJ Director EP Rosenberg SA. Identification of specific cytolytic immune responses against autologous tumor in humans bearing malignant melanoma. J Immunol (1987) 138(3): 989– 95. 3100623
  33. [36]Rosenberg SA Packard BS Aebersold PM Solomon D Topalian SL Toy ST 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. 10.1056/NEJM198812223192527 3264384 · DOI · Paper page
  34. [37]Wu R Forget MA Chacon J Bernatchez C Haymaker C Chen JQ Adoptive T-cell therapy using autologous tumor-infiltrating lymphocytes for metastatic melanoma: current status and future outlook. Cancer J (2012) 18(2): 160– 75. 10.1097/PPO.0b013e31824d4465 22453018 PMC3315690 · DOI
  35. [38]Fousek K Ahmed N The evolution of T-cell therapies for solid malignancies. Clin Cancer Res (2015) 21(15): 3384– 92. 10.1158/1078-0432.CCR-14-2675 26240290 PMC4526112 · DOI
  36. [39]Andersen R Donia M Ellebaek E Borch TH Kongsted P Iversen TZ Long-lasting complete responses in patients with metastatic melanoma after adoptive cell therapy with tumor-infiltrating lymphocytes and an attenuated IL2 regimen. Clin Cancer Res (2016) 22(15): 3734– 45. 10.1158/1078-0432.CCR-15-1879 27006492 · DOI
  37. [40]Berghuis D Santos SJ Baelde HJ Taminiau AH Egeler RM Schilham MW Pro-inflammatory chemokine-chemokine receptor interactions within the Ewing sarcoma microenvironment determine CD8(+) T-lymphocyte infiltration and affect tumour progression. J Pathol (2011) 223(3): 347– 57. 10.1002/path.2819 21171080 · DOI
  38. [41]Kim JR Moon YJ Kwon KS Bae JS Wagle S Kim KM Tumor infiltrating PD1-positive lymphocytes and the expression of PD-L1 predict poor prognosis of soft tissue sarcomas. PLoS One (2013) 8(12): e82870. 10.1371/journal.pone.0082870 24349382 PMC3859621 · DOI
  39. [42]Fujii H Arakawa A Utsumi D Sumiyoshi S Yamamoto Y Kitoh A CD8(+) tumor-infiltrating lymphocytes at primary sites as a possible prognostic factor of cutaneous angiosarcoma. Int J Cancer (2014) 134(10): 2393– 402. 10.1002/ijc.28581 24243586 · DOI
  40. [43]Shen JK Cote GM Choy E Yang P Harmon D Schwab J Programmed cell death ligand 1 expression in osteosarcoma. Cancer Immunol Res (2014) 2(7): 690– 8. 10.1158/2326-6066.CIR-13-0224 24866169 PMC4082476 · DOI
  41. [44]Zheng W Xiao H Liu H Zhou Y. Expression of programmed death 1 is correlated with progression of osteosarcoma. APMIS (2015) 123(2): 102– 7. 10.1111/apm.12311 25257510 · DOI
  42. [45]Schmidt LH Kummel A Gorlich D Mohr M Brockling S Mikesch JH. PD-1 and PD-L1 expression in NSCLC indicate a favorable prognosis in defined subgroups. PLoS One (2015) 10(8): e0136023. 10.1371/journal.pone.0136023 26313362 PMC4552388 · DOI
  43. [46]Cohen CJ Gartner JJ Horovitz-Fried M Shamalov K Trebska-McGowan K Bliskovsky VV Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes. J Clin Invest (2015) 125(10): 3981– 91. 10.1172/JCI82416 26389673 PMC4607110 · DOI
  44. [47]van Rooij N van Buuren MM Philips D Velds A Toebes M Heemskerk B Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J Clin Oncol (2013) 31(32): e439– 42. 10.1200/JCO.2012.47.7521 24043743 PMC3836220 · DOI · Paper page
  45. [48]Heemskerk B Kvistborg P Schumacher TN. The cancer antigenome. EMBO J (2013) 32(2): 194– 203. 10.1038/emboj.2012.333 23258224 PMC3553384 · DOI
  46. [49]Tsukahara T Kawaguchi S Torigoe T Asanuma H Nakazawa E Shimozawa K Prognostic significance of HLA class I expression in osteosarcoma defined by anti-pan HLA class I monoclonal antibody, EMR8-5. Cancer Sci (2006) 97(12): 1374– 80. 10.1111/j.1349-7006.2006.00317.x 16995877 PMC11158095 · DOI · Paper page
  47. [50]Costa FF Le Blanc K Brodin B. Concise review: cancer/testis antigens, stem cells, and cancer. Stem Cells (2007) 25(3): 707– 11. 10.1634/stemcells.2006-0469 17138959 · DOI
  48. [51]Simpson AJ Caballero OL Jungbluth A Chen YT Old LJ. Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer (2005) 5(8): 615– 25. 10.1038/nrc1669 16034368 · DOI
  49. [52]Caballero OL Chen YT Cancer/testis (CT) antigens: potential targets for immunotherapy. Cancer Sci (2009) 100(11): 2014– 21. 10.1111/j.1349-7006.2009.01303.x 19719775 PMC11158245 · DOI
  50. [53]Jacobs JF Brasseur F Hulsbergen-van de Kaa CA van de Rakt MW Figdor CG Adema GJ Cancer-germline gene expression in pediatric solid tumors using quantitative real-time PCR. Int J Cancer (2007) 120(1): 67– 74. 10.1002/ijc.22118 17019710 · DOI
  51. [54]Sudo T Kuramoto T Komiya S Inoue A Itoh K. Expression of MAGE genes in osteosarcoma. J Orthop Res (1997) 15(1): 128– 32. 10.1002/jor.1100150119 9066537 · DOI
  52. [55]Pollack SM Loggers ET Rodler ET Yee C Jones RL Immune-based therapies for sarcoma. Sarcoma (2011) 2011: 438940 10.1155/2011/438940 21331153 PMC3034923 · DOI
  53. [56]Maki RG. Soft tissue sarcoma as a model disease to examine cancer immunotherapy. Curr Opin Oncol (2001) 13(4): 270– 4. 10.1097/00001622-200107000-00010 11429485 · DOI
  54. [57]Vansteenkiste J Zielinski M Linder A Dahabreh J Gonzalez EE Malinowski W Adjuvant MAGE-A3 immunotherapy in resected non-small-cell lung cancer: phase II randomized study results. J Clin Oncol (2013) 31(19): 2396– 403. 10.1200/JCO.2012.43.7103 23715567 · DOI
  55. [58]Kruit WH Suciu S Dreno B Mortier L Robert C Chiarion-Sileni V 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. 10.1200/JCO.2012.43.7111 23715572 · DOI
  56. [59]Robbins PF Morgan RA Feldman SA Yang JC Sherry RM Dudley ME 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. 10.1200/JCO.2010.32.2537 21282551 PMC3068063 · DOI
  57. [60]Friedl P Storim J. Diversity in immune-cell interactions: states and functions of the immunological synapse. Trends Cell Biol (2004) 14(10): 557– 67. 10.1016/j.tcb.2004.09.005 15450978 · DOI
  58. [61]Konkankit VV Kim W Koya RC Eskin A Dam MA Nelson S Decitabine immunosensitizes human gliomas to NY-ESO-1 specific T lymphocyte targeting through the Fas/Fas ligand pathway. J Transl Med (2011) 9: 192. 10.1186/1479-5876-9-192 22060015 PMC3229551 · DOI
  59. [62]Serrano A Tanzarella S Lionello I Mendez R Traversari C Ruiz-Cabello F Rexpression of HLA class I antigens and restoration of antigen-specific CTL response in melanoma cells following 5-aza-2’-deoxycytidine treatment. Int J Cancer (2001) 94(2): 243– 51. 10.1002/ijc.1452 11668505 · DOI
  60. [63]Krishnadas DK Bao L Bai F Chencheri SC Lucas K. Decitabine facilitates immune recognition of sarcoma cells by upregulating CT antigens, MHC molecules, and ICAM-1. Tumour Biol (2014) 35(6): 5753– 62. 10.1007/s13277-014-1764-9 24584817 · DOI
  61. [64]Mesiano G Leuci V Giraudo L Gammaitoni L Carnevale Schianca F Cangemi M Adoptive immunotherapy against sarcomas. Expert Opin Biol Ther (2015) 15(4): 517– 28. 10.1517/14712598.2015.987121 25516119 · DOI
  62. [65]Kato Y Tanaka Y Miyagawa F Yamashita S Minato N. Targeting of tumor cells for human gammadelta T cells by nonpeptide antigens. J Immunol (2001) 167(9): 5092– 8. 10.4049/jimmunol.167.9.5092 11673519 · DOI
  63. [66]Wang H Fang Z Morita CT. Vgamma2Vdelta2 T Cell Receptor recognition of prenyl pyrophosphates is dependent on all CDRs. J Immunol (2010) 184(11): 6209– 22. 10.4049/jimmunol.1000231 20483784 PMC3069129 · DOI
  64. [67]Constant P Davodeau F Peyrat MA Poquet Y Puzo G Bonneville M Stimulation of human gamma delta T cells by nonpeptidic mycobacterial ligands. Science (1994) 264(5156): 267– 70. 10.1126/science.8146660 8146660 · DOI
  65. [68]Caccamo N La Mendola C Orlando V Meraviglia S Todaro M Stassi G Differentiation, phenotype, and function of interleukin-17-producing human Vgamma9Vdelta2 T cells. Blood (2011) 118(1): 129– 38. 10.1182/blood-2011-01-331298 21505189 · DOI
  66. [69]Vermijlen D Ellis P Langford C Klein A Engel R Willimann K Distinct cytokine-driven responses of activated blood gammadelta T cells: insights into unconventional T cell pleiotropy. J Immunol (2007) 178(7): 4304– 14. 10.4049/jimmunol.178.7.4304 17371987 PMC3915340 · DOI
  67. [70]Wesch D Glatzel A Kabelitz D. Differentiation of resting human peripheral blood gamma delta T cells toward Th1- or Th2-phenotype. Cell Immunol (2001) 212(2): 110– 7. 10.1006/cimm.2001.1850 11748927 · DOI
  68. [71]Boissier S Magnetto S Frappart L Cuzin B Ebetino FH Delmas PD Bisphosphonates inhibit prostate and breast carcinoma cell adhesion to unmineralized and mineralized bone extracellular matrices. Cancer Res (1997) 57(18): 3890– 4. 9307266
  69. [72]Boissier S Ferreras M Peyruchaud O Magnetto S Ebetino FH Colombel M Bisphosphonates inhibit breast and prostate carcinoma cell invasion, an early event in the formation of bone metastases. Cancer Res (2000) 60(11): 2949– 54. 10850442
  70. [73]Saad F Gleason DM Murray R Tchekmedyian S Venner P Lacombe L A randomized, placebo-controlled trial of zoledronic acid in patients with hormone-refractory metastatic prostate carcinoma. J Natl Cancer Inst (2002) 94(19): 1458– 68. 10.1093/jnci/94.19.1458 12359855 · DOI
  71. [74]Rosen LS Gordon D Tchekmedyian S Yanagihara R Hirsh V Krzakowski M Zoledronic acid versus placebo in the treatment of skeletal metastases in patients with lung cancer and other solid tumors: a phase III, double-blind, randomized trial – the Zoledronic Acid Lung Cancer and Other Solid Tumors Study Group. J Clin Oncol (2003) 21(16): 3150– 7. 10.1200/JCO.2003.04.105 12915606 · DOI
  72. [75]Muraro M Mereuta OM Carraro F Madon E Fagioli F. Osteosarcoma cell line growth inhibition by zoledronate-stimulated effector cells. Cell Immunol (2007) 249(2): 63– 72. 10.1016/j.cellimm.2007.11.005 18163982 · DOI
  73. [76]Li Z Peng H Xu Q Ye Z Sensitization of human osteosarcoma cells to Vgamma9Vdelta2 T-cell-mediated cytotoxicity by zoledronate. J Orthop Res (2012) 30(5): 824– 30. 10.1002/jor.21579 22025284 · DOI
  74. [77]Liu M Sun LL Li YJ Li HY Zhang J Li BH Trastuzumab enhanced the cytotoxicity of Vgamma9Vdelta2 T cells against zoledronate-sensitized osteosarcoma cells. Int Immunopharmacol (2015) 28(1): 160– 7. 10.1016/j.intimp.2015.06.002 26071219 · DOI
  75. [78]Fournie JJ Sicard H Poupot M Bezombes C Blanc A Romagne F What lessons can be learned from gammadelta T cell-based cancer immunotherapy trials? Cell Mol Immunol (2013) 10(1): 35– 41. 10.1038/cmi.2012.39 23241899 PMC4003170 · DOI
  76. [79]Li Z Tang J Sun L Ye Z [Effect of zoledronate on the cytotoxicity of gammadelta T cells from PBMCs of osteosarcoma patients against osteosarcoma]. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi (2013) 29(1): 6– 9. 23294710
  77. [80]Deniger DC Maiti SN Mi T Switzer KC Ramachandran V Hurton LV Activating and propagating polyclonal gamma delta T cells with broad specificity for malignancies. Clin Cancer Res (2014) 20(22): 5708– 19. 10.1158/1078-0432.CCR-13-3451 24833662 PMC4233015 · DOI
  78. [81]Circosta P Granziero L Follenzi A Vigna E Stella S Vallario A 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(12): 1576– 88. 10.1089/hum.2009.117 19678763 · DOI
  79. [82]Leuci V Mesiano G Gammaitoni L Aglietta M Sangiolo D. Genetically redirected T lymphocytes for adoptive immunotherapy of solid tumors. Curr Gene Ther (2014) 14(1): 52– 62. 10.2174/1566523213666131223130353 24365144 · DOI
  80. [83]Schumacher TN. T-cell-receptor gene therapy. Nat Rev Immunol (2002) 2(7): 512– 9. 10.1038/nri841 12094225 · DOI
  81. [84]Gattinoni L Powell DJ Jr Rosenberg SA Restifo NP. Adoptive immunotherapy for cancer: building on success. Nat Rev Immunol (2006) 6(5): 383– 93. 10.1038/nri1842 16622476 PMC1473162 · DOI
  82. [85]Morgan RA Dudley ME Wunderlich JR Hughes MS Yang JC Sherry RM Cancer regression in patients after transfer of genetically engineered lymphocytes. Science (2006) 314(5796): 126– 9. 10.1126/science.1129003 16946036 PMC2267026 · DOI · Paper page
  83. [86]Thomas S Hart DP Xue SA Cesco-Gaspere M Stauss HJ. T-cell receptor gene therapy for cancer: the progress to date and future objectives. Expert Opin Biol Ther (2007) 7(8): 1207– 18. 10.1517/14712598.7.8.1207 17696819 · DOI
  84. [87]Rosenberg SA Restifo NP Yang JC Morgan RA Dudley ME. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer (2008) 8(4): 299– 308. 10.1038/nrc2355 18354418 PMC2553205 · DOI
  85. [88]Bendle GM Linnemann C Hooijkaas AI Bies L de Witte MA Jorritsma A Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med (2010) 16(5): 565– 70. 1p following 570 10.1038/nm.2128 20400962 · DOI
  86. [89]van Loenen MM de Boer R Amir AL Hagedoorn RS Volbeda GL Willemze R Mixed T cell receptor dimers harbor potentially harmful neoreactivity. Proc Natl Acad Sci U S A (2010) 107(24): 10972– 7. 10.1073/pnas.1005802107 20534461 PMC2890759 · DOI
  87. [90]Cohen CJ Li YF El-Gamil M Robbins PF Rosenberg SA Morgan RA. Enhanced antitumor activity of T cells engineered to express T-cell receptors with a second disulfide bond. Cancer Res (2007) 67(8): 3898– 903. 10.1158/0008-5472.CAN-06-3986 17440104 PMC2147081 · DOI
  88. [91]Kuball J Dossett ML Wolfl M Ho WY Voss RH Fowler C Facilitating matched pairing and expression of TCR chains introduced into human T cells. Blood (2007) 109(6): 2331– 8. 10.1182/blood-2006-05-023069 17082316 PMC1852191 · DOI
  89. [92]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(11): 6223– 31. 10.4049/jimmunol.0902055 20483785 · DOI
  90. [93]van der Veken LT Hagedoorn RS van Loenen MM Willemze R Falkenburg JH Heemskerk MH. Alphabeta T-cell receptor engineered gammadelta T cells mediate effective antileukemic reactivity. Cancer Res (2006) 66(6): 3331– 7. 10.1158/0008-5472.CAN-05-4190 16540688 · DOI
  91. [94]Smith DJ Liu S Ji S Li B McLaughlin J Cheng D Genetic engineering of hematopoietic stem cells to generate invariant natural killer T cells. Proc Natl Acad Sci U S A (2015) 112(5): 1523– 8. 10.1073/pnas.1424877112 25605948 PMC4321292 · DOI
  92. [95]Voss RH Thomas S Pfirschke C Hauptrock B Klobuch S Kuball J Coexpression of the T-cell receptor constant alpha domain triggers tumor reactivity of single-chain TCR-transduced human T cells. Blood (2010) 115(25): 5154– 63. 10.1182/blood-2009-11-254078 20378753 · DOI
  93. [96]Ochi T Fujiwara H Okamoto S An J Nagai K Shirakata T Novel adoptive T-cell immunotherapy using a WT1-specific TCR vector encoding silencers for endogenous TCRs shows marked antileukemia reactivity and safety. Blood (2011) 118(6): 1495– 503. 10.1182/blood-2011-02-337089 21673345 · DOI
  94. [97]Provasi E Genovese P Lombardo A Magnani Z Liu PQ Reik A Editing T cell specificity towards leukemia by zinc finger nucleases and lentiviral gene transfer. Nat Med (2012) 18(5): 807– 15. 10.1038/nm.2700 22466705 PMC5019824 · DOI · Paper page
  95. [98]Johnson LA Morgan RA Dudley ME Cassard L Yang JC Hughes MS 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. 10.1182/blood-2009-03-211714 19451549 PMC2929689 · DOI
  96. [99]Beatty GL O’Hara M. Chimeric antigen receptor-modified T cells for the treatment of solid tumors: defining the challenges and next steps. Pharmacol Ther (2016). 10.1016/j.pharmthera.2016.06.010 27373504 PMC5035606 · DOI
  97. [100]Vitale M Pelusi G Taroni B Gobbi G Micheloni C Rezzani R HLA class I antigen down-regulation in primary ovary carcinoma lesions: association with disease stage. Clin Cancer Res (2005) 11(1): 67– 72. 15671529
  98. [101]Lehner M Gotz G Proff J Schaft N Dorrie J Full F Redirecting T cells to Ewing’s sarcoma family of tumors by a chimeric NKG2D receptor expressed by lentiviral transduction or mRNA transfection. PLoS One (2012) 7(2): e31210. 10.1371/journal.pone.0031210 22355347 PMC3280271 · DOI
  99. [103]Gattenlohner S Marx A Markfort B Pscherer S Landmeier S Juergens H Rhabdomyosarcoma lysis by T cells expressing a human autoantibody-based chimeric receptor targeting the fetal acetylcholine receptor. Cancer Res (2006) 66(1): 24– 8. 10.1158/0008-5472.CAN-05-0542 16397210 · DOI
  100. [104]Abdou AG Kandil M Asaad NY Dawoud MM Shahin AA Abd Eldayem AF. The prognostic role of ezrin and HER2/neu expression in osteosarcoma. Appl Immunohistochem Mol Morphol (2016) 24(5): 355– 63. 10.1097/PAI.000000000000019 26067138 · DOI
  101. [105]Huang MA Krishnadas DK Lucas KG. Cellular and antibody based approaches for pediatric cancer immunotherapy. J Immunol Res (2015) 2015: 675269. 10.1155/2015/675269 26587548 PMC4637498 · DOI
  102. [106]Khalil DN Smith EL Brentjens RJ Wolchok JD. The future of cancer treatment: immunomodulation, CARs and combination immunotherapy. Nat Rev Clin Oncol (2016) 13(5): 273– 90. 10.1038/nrclinonc.2016.25 26977780 PMC5551685 · DOI
  103. [107]Lamers CH Willemsen R van Elzakker P van Steenbergen-Langeveld S Broertjes M Oosterwijk-Wakka J Immune responses to transgene and retroviral vector in patients treated with ex vivo-engineered T cells. Blood (2011) 117(1): 72– 82. 10.1182/blood-2010-07-294520 20889925 · DOI
  104. [108]Cohen CJ Zhao Y Zheng Z Rosenberg SA Morgan RA. 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(17): 8878– 86. 10.1158/0008-5472.CAN-06-1450 16951205 PMC2147082 · DOI
  105. [109]Mata M Gottschalk S Adoptive cell therapy forsarcoma. Immunotherapy (2015) 7(1): 21– 35. 10.2217/imt.14.98 25572477 PMC4331182 · DOI
  106. [110]Old LJ. Cancer vaccines: an overview. Cancer Immun (2008) 8(Suppl 1): 1. 18333603
  107. [111]Baselga J Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer (2009) 9(7): 463– 75. 10.1038/nrc2656 19536107 · DOI
  108. [112]Heinrich PC Behrmann I Muller-Newen G Schaper F Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J (1998) 334(Pt 2): 297– 314. 10.1042/bj3340297 9716487 PMC1219691 · DOI · Paper page
  109. [113]Ernst M Putoczki TL. Molecular pathways: IL11 as a tumor-promoting cytokine-translational implications for cancers. Clin Cancer Res (2014) 20(22): 5579– 88. 10.1158/1078-0432.CCR-13-2492 25074610 · DOI
  110. [114]Zurita AJ Troncoso P Cardo-Vila M Logothetis CJ Pasqualini R Arap W. Combinatorial screenings in patients: the interleukin-11 receptor alpha as a candidate target in the progression of human prostate cancer. Cancer Res (2004) 64(2): 435– 9. 10.1158/0008-5472.CAN-03-2675 14744752 · DOI
  111. [115]Kang Y Siegel PM Shu W Drobnjak M Kakonen SM Cordon-Cardo C A multigenic program mediating breast cancer metastasis to bone. Cancer Cell (2003) 3(6): 537– 49. 10.1016/S1535-6108(03)00132-6 12842083 · DOI
  112. [117]Topalian SL Hodi FS Brahmer JR Gettinger SN Smith DC McDermott DF Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med (2012) 366(26): 2443– 54. 10.1056/NEJMoa1200690 22658127 PMC3544539 · DOI · Paper page
  113. [118]Brahmer JR Tykodi SS Chow LQ Hwu WJ Topalian SL Hwu P Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med (2012) 366(26): 2455– 65. 10.1056/NEJMoa1200694 22658128 PMC3563263 · DOI · Paper page
  114. [119]Villaruz LC Socinski MA The clinical utility of PD-L1 testing in selecting non-small cell lung cancer patients for PD1/PD-L1 directed therapy. Clin Pharmacol Ther (2016) 100(3): 212– 4. 10.1002/cpt.385 27090296 PMC4982801 · DOI
  115. [120]Lussier DM O’Neill L Nieves LM McAfee MS Holechek SA Collins AW Enhanced T-cell immunity to osteosarcoma through antibody blockade of PD-1/PD-L1 interactions. J Immunother (2015) 38(3): 96– 106. 10.1097/CJI.0000000000000065 25751499 PMC6426450 · DOI · Paper page
  116. [121]Boehm U Klamp T Groot M Howard JC Cellular responses to interferon-gamma. Annu Rev Immunol (1997) 15: 749– 95. 10.1146/annurev.immunol.15.1.749 9143706 · DOI · Paper page
  117. [122]Zou W Chen L. Inhibitory B7-family molecules in the tumour microenvironment. Nat Rev Immunol (2008) 8(6): 467– 77. 10.1038/nri2326 18500231 · DOI · Paper page
  118. [123]Dong H Strome SE Salomao DR Tamura H Hirano F Flies DB Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med (2002) 8(8): 793– 800. 10.1038/nm730 12091876 · DOI · Paper page
  119. [124]Taube JM Anders RA Young GD Xu H Sharma R McMiller TL Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med (2012) 4(127): 127ra37. 10.1126/scitranslmed.3003689 22461641 PMC3568523 · DOI · Paper page
  120. [125]Contardi E Palmisano GL Tazzari PL Martelli AM Fala F Fabbi M CTLA-4 is constitutively expressed on tumor cells and can trigger apoptosis upon ligand interaction. Int J Cancer (2005) 117(4): 538– 50. 10.1002/ijc.21155 15912538 · DOI
  121. [126]Leach DR Krummel MF Allison JP Enhancement of antitumor immunity by CTLA-4 blockade. Science (1996) 271(5256): 1734– 6. 10.1126/science.271.5256.1734 8596936 · DOI · Paper page
  122. [127]Yuan J Gnjatic S Li H Powel S Gallardo HF Ritter E CTLA-4 blockade enhances polyfunctional NY-ESO-1 specific T cell responses in metastatic melanoma patients with clinical benefit. Proc Natl Acad Sci U S A (2008) 105(51): 20410– 5. 10.1073/pnas.0810114105 19074257 PMC2629307 · DOI
  123. [128]Eroglu Z Kim DW Wang X Camacho LH Chmielowski B Seja E Long term survival with cytotoxic T lymphocyte-associated antigen 4 blockade using tremelimumab. Eur J Cancer (2015) 51(17): 2689– 97. 10.1016/j.ejca.2015.08.012 26364516 PMC4821004 · DOI
  124. [129]Liu J Wang J Jiang W Tang Y. Effect of cytotoxic T-lymphocyte antigen-4, TNF-alpha polymorphisms on osteosarcoma: evidences from a meta-analysis. Chin J Cancer Res (2013) 25(6): 671– 8. 10.3978/j.issn.1000-9604.2013.11.06 24385694 PMC3872545 · DOI
  125. [130]Yu F Miao J Significant association between cytotoxic T lymphocyte antigen 4 +49G>A polymorphism and risk of malignant bone tumors. Tumour Biol (2013) 34(6): 3371– 5. 10.1007/s13277-013-0908-7 23900675 · DOI
  126. [132]Liu S Geng P Cai X Wang J. Comprehensive evaluation of the cytotoxic T-lymphocyte antigen-4 gene polymorphisms in risk of bone sarcoma. Genet Test Mol Biomarkers (2014) 18(8): 574– 9. 10.1089/gtmb.2014.0023 25000484 · DOI
  127. [134]Kawano M Itonaga I Iwasaki T Tsumura H. Enhancement of antitumor immunity by combining anti-cytotoxic T lymphocyte antigen-4 antibodies and cryotreated tumor lysate-pulsed dendritic cells in murine osteosarcoma. Oncol Rep (2013) 29(3): 1001– 6. 10.3892/or.2013.2224 23291864 · DOI · Paper page
  128. [135]Zhang J Basher F Wu JD. NKG2D ligands in tumor immunity: two sides of a coin. Front Immunol (2015) 6: 97. 10.3389/fimmu.2015.00097 25788898 PMC4349182 · DOI
  129. [136]Groh V Rhinehart R Randolph-Habecker J Topp MS Riddell SR Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol (2001) 2(3): 255– 60. 10.1038/85321 11224526 · DOI
  130. [137]Fernandez L Valentin J Zalacain M Leung W Patino-Garcia A Perez-Martinez A. Activated and expanded natural killer cells target osteosarcoma tumor initiating cells in an NKG2D-NKG2DL dependent manner. Cancer Lett (2015) 368(1): 54– 63. 10.1016/j.canlet.2015.07.042 26276724 · DOI
  131. [139]Lu SM Xiao P Xue L Che LH Yang P Li Y Prevalent expression of MHC class I chain-related molecule A in human osteosarcoma. Neoplasma (2008) 55(3): 266– 72. 18348660
  132. [141]Gan HK Cvrljevic AN Johns TG. The epidermal growth factor receptor variant III (EGFRvIII): where wild things are altered. FEBS J (2013) 280(21): 5350– 70. 10.1111/febs.12393 23777544 · DOI
  133. [142]Kastenhuber ER Huse JT Berman SH Pedraza A Zhang J Suehara Y Quantitative assessment of intragenic receptor tyrosine kinase deletions in primary glioblastomas: their prevalence and molecular correlates. Acta Neuropathol (2014) 127(5): 747– 59. 10.1007/s00401-013-1217-3 24292886 PMC3984672 · DOI
  134. [143]Bartek J Jr Ng K Bartek J Fischer W Carter B Chen CC. Key concepts in glioblastoma therapy. J Neurol Neurosurg Psychiatry (2012) 83(7): 753– 60. 10.1136/jnnp-2011-300709 22396442 · DOI
  135. [144]Morgan RA Johnson LA Davis JL Zheng Z Woolard KD Reap EA Recognition of glioma stem cells by genetically modified T cells targeting EGFRvIII and development of adoptive cell therapy for glioma. Hum Gene Ther (2012) 23(10): 1043– 53. 10.1089/hum.2012.041 22780919 PMC3472555 · DOI
  136. [145]Chu CT Everiss KD Wikstrand CJ Batra SK Kung HJ Bigner DD Receptor dimerization is not a factor in the signalling activity of a transforming variant epidermal growth factor receptor (EGFRvIII). Biochem J (1997) 324(Pt 3): 855– 61. 10.1042/bj3240855 9210410 PMC1218502 · DOI
  137. [146]Freeman SS Allen SW Ganti R Wu J Ma J Su X Copy number gains in EGFR and copy number losses in PTEN are common events in osteosarcoma tumors. Cancer (2008) 113(6): 1453– 61. 10.1002/cncr.23782 18704985 PMC3529469 · DOI
  138. [147]Stephens PJ Greenman CD Fu B Yang F Bignell GR Mudie LJ Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell (2011) 144(1): 27– 40. 10.1016/j.cell.2010.11.055 21215367 PMC3065307 · DOI · Paper page
  139. [149]Salvatore V Teti G Bolzani S Focaroli S Durante S Mazzotti MC Simulating tumor microenvironment: changes in protein expression in an in vitro co-culture system. Cancer Cell Int (2014) 14: 40. 10.1186/1475-2867-14-40 24883044 PMC4038825 · DOI
  140. [151]Rasanen K Vaheri A. Activation of fibroblasts in cancer stroma. Exp Cell Res (2010) 316(17): 2713– 22. 10.1016/j.yexcr.2010.04.032 20451516 · DOI · Paper page
  141. [152]Finocchiaro G Pellegatta S. Novel mechanisms and approaches in immunotherapy for brain tumors. Discov Med (2015) 20(108): 7– 15. 26321082
  142. [153]Leavy O. Therapeutic antibodies: past, present and future. Nat Rev Immunol (2010) 10(5): 297. 10.1038/nri2763 20422787 · DOI
  143. [155]Sharma P Allison JP. The future of immune checkpoint therapy. Science (2015) 348(6230): 56– 61. 10.1126/science.aaa8172 25838373 · DOI · Paper page
  144. [156]Twyman-Saint Victor C Rech AJ Maity A Rengan R Pauken KE Stelekati E Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature (2015) 520(7547): 373– 7. 10.1038/nature14292 25754329 PMC4401634 · DOI · Paper page
  145. [157]Naidoo J Page DB Wolchok JD. Immune modulation for cancer therapy. Br J Cancer (2014) 111(12): 2214– 9. 10.1038/bjc.2014.348 25211661 PMC4264429 · DOI
  146. [158]Tsukahara T Emori M Murata K Mizushima E Shibayama Y Kubo T The future of immunotherapy for sarcoma. Expert Opin Biol Ther (2016) 16(8): 1049– 57. 10.1080/14712598.2016.1188075 27158940 · DOI

Cited by

Sorted by citations

Authors
Wang, Z., Li, B., Ren, Y., & Ye, Z.
Affiliations
Second Affiliated Hospital of Zhejiang University (CN)
Corresponding author
Ye, Zhaoming
Venue
Frontiers in Immunology
Published
2016-09-14
Volume
7
Pages
353-353
ISSN
1664-3224 (ISSN-L)
OpenAlex
W2519623594
Cited by
73
References
12
Citations by year
2026: 2 · 2025: 5 · 2024: 3 · 2023: 9 · 2022: 10 · 2021: 11 · 2020: 10 · 2019: 10 · 2018: 8 · 2017: 4 · 2016: 1
FWCI
0.74
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Immunology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
National Natural Science Foundation of China (Grant nos. 81172547 and 30973444)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Sarcoma Diagnosis and Treatment
  • Health Sciences › Medicine › Oncology › CAR-T cell therapy research
Keywords
osteosarcoma, T cell-based immunotherapy, adoptive T cell therapy, genetically modified T cells, combination immunotherapy, metastatic osteosarcoma, chemoresistance, solid tumor immunotherapy

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review