Browse > Article
http://dx.doi.org/10.4062/biomolther.2021.180

Strategies for Manipulating T Cells in Cancer Immunotherapy  

Lee, Hyang-Mi (College of Pharmacy, Dongduk Women's University)
Publication Information
Biomolecules & Therapeutics / v.30, no.4, 2022 , pp. 299-308 More about this Journal
Abstract
T cells are attractive targets for the development of immunotherapy to treat cancer due to their biological features, capacity of cytotoxicity, and antigen-specific binding of receptors. Novel strategies that can modulate T cell functions or receptor reactivity provide effective therapies, including checkpoint inhibitor, bispecific antibody, and adoptive transfer of T cells transduced with tumor antigen-specific receptors. T cell-based therapies have presented successful pre-clinical/clinical outcomes despite their common immune-related adverse effects. Ongoing studies will allow us to advance current T cell therapies and develop innovative personalized T cell therapies. This review summarizes immunotherapeutic approaches with a focus on T cells. Anti-cancer T cell therapies are also discussed regarding their biological perspectives, efficacy, toxicity, challenges, and opportunities.
Keywords
Cancer immunotherapy; Checkpoint inhibitor; Bispecific antibody; Adoptive T cell transfer; Tumor-specific T cells;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Kuwana, Y., Asakura, Y., Utsunomiya, N., Nakanishi, M., Arata, Y., Itoh, S., Nagase, F. and Kurosawa, Y. (1987) Expression of chimeric receptor composed of immunoglobulin-derived V regions and T-cell receptor-derived C regions. Biochem. Biophys. Res. Commun. 149, 960-968.   DOI
2 Leach, D. R., Krummel, M. F. and Allison, J. P. (1996) Enhancement of antitumor immunity by CTLA-4 blockade. Science 271, 1734-1736.   DOI
3 Lee, L., Wang, R. F., Wang, X., Mixon, A., Johnson, B. E., Rosenberg, S. A. and Schrump, D. S. (1999) NY-ESO-1 may be a potential target for lung cancer immunotherapy. Cancer J. Sci. Am. 5, 20-25.
4 Liu, Y. and Zheng, P. (2020) Preserving the CTLA-4 checkpoint for safer and more effective cancer immunotherapy. Trends Pharmacol. Sci. 41, 4-12.   DOI
5 Maher, J., Brentjens, R. J., Gunset, G., Riviere, I. and Sadelain, M. (2002) Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta /CD28 receptor. Nat. Biotechnol. 20, 70-75.   DOI
6 Majzner, R. G., Theruvath, J. L., Nellan, A., Heitzeneder, S., Cui, Y., Mount, C. W., Rietberg, S. P., Linde, M. H., Xu, P., Rota, C., Sotillo, E., Labanieh, L., Lee, D. W., Orentas, R. J., Dimitrov, D. S., Zhu, Z., Croix, B. S., Delaidelli, A., Sekunova, A., Bonvini, E., Mitra, S. S., Quezado, M. M., Majeti, R., Monje, M., Sorensen, P. H. B., Maris, J. M. and Mackall, C. L. (2019) CAR T cells targeting B7-H3, a pan-cancer antigen, demonstrate potent preclinical activity against pediatric solid tumors and brain tumors. Clin. Cancer Res. 25, 2560-2574.   DOI
7 Huang, L. Q., Brasseur, F., Serrano, A., De Plaen, E., van der Bruggen, P., Boon, T. and Van Pel, A. (1999) Cytolytic T lymphocytes recognize an antigen encoded by MAGE-A10 on a human melanoma. J. Immunol. 162, 6849-6854.   DOI
8 Hung, C. F., Xu, X., Li, L., Ma, Y., Jin, Q., Viley, A., Allen, C., Natarajan, P., Shivakumar, R., Peshwa, M. V. and Emens, L. A. (2018) Development of anti-human mesothelin-targeted chimeric antigen receptor messenger RNA-transfected peripheral blood lymphocytes for ovarian cancer therapy. Hum. Gene Ther. 29, 614-625.   DOI
9 Iwai, Y., Ishida, M., Tanaka, Y., Okazaki, T., Honjo, T. and Minato, N. (2002) Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. U.S.A. 99, 12293-12297.   DOI
10 Ansell, S. M., Lesokhin, A. M., Borrello, I., Halwani, A., Scott, E. C., Gutierrez, M., Schuster, S. J., Millenson, M. M., Cattry, D., Freeman, G. J., Rodig, S. J., Chapuy, B., Ligon, A. H., Zhu, L., Grosso, J. F., Kim, S. Y., Timmerman, J. M., Shipp, M. A. and Armand, P. (2015) PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N. Engl. J. Med. 372, 311-319.   DOI
11 Aung, P. P., Liu, Y. C., Ballester, L. Y., Robbins, P. F., Rosenberg, S. A. and Lee, C. C. (2014) Expression of New York esophageal squamous cell carcinoma-1 in primary and metastatic melanoma. Hum. Pathol. 45, 259-267.   DOI
12 Bielamowicz, K., Fousek, K., Byrd, T. T., Samaha, H., Mukherjee, M., Aware, N., Wu, M. F., Orange, J. S., Sumazin, P., Man, T. K., Joseph, S. K., Hegde, M. and Ahmed, N. (2018) Trivalent CAR T cells overcome interpatient antigenic variability in glioblastoma. NeuroOncol. 20, 506-518.
13 Rosenthal, M. A., Balana, C., van Linde, M. E., Sayehli, C., Fiedler, W. M., Wermke, M., Massard, C., Mellinghoff, I. K., Khasraw, M., Ang, A., Rasmussen, E., Kast, J., Stienen, S. and Cloughesy, T. F. (2019) ATIM-49 (LTBK-01). AMG 596, a novel anti-EGFRvIII bispecific T cell engager (BITE(®)) molecule for the treatment of glioblastoma (GBM): planned interim analysis in recurrent GBM (RGBM). Neuro-Oncol. 21, vi283.
14 Ghorashian, S., Kramer, A. M., Onuoha, S., Wright, G., Bartram, J., Richardson, R., Albon, S. J., Casanovas-Company, J., Castro, F., Popova, B., Villanueva, K., Yeung, J., Vetharoy, W., Guvenel, A., Wawrzyniecka, P. A., Mekkaoui, L., Cheung, G. W., Pinner, D., Chu, J., Lucchini, G., Silva, J., Ciocarlie, O., Lazareva, A., Inglott, S., Gilmour, K. C., Ahsan, G., Ferrari, M., Manzoor, S., Champion, K., Brooks, T., Lopes, A., Hackshaw, A., Farzaneh, F., Chiesa, R., Rao, K., Bonney, D., Samarasinghe, S., Goulden, N., Vora, A., Veys, P., Hough, R., Wynn, R., Pule, M. A. and Amrolia, P. J. (2019) Enhanced CAR T cell expansion and prolonged persistence in pediatric patients with ALL treated with a low-affinity CD19 CAR. Nat. Med. 25, 1408-1414.   DOI
15 Rosenberg, S. A., Yang, J. C., Sherry, R. M., Kammula, U. S., Hughes, M. S., Phan, G. Q., Citrin, D. E., Restifo, N. P., Robbins, P. F., Wunderlich, J. R., Morton, K. E., Laurencot, C. M., Steinberg, S. M., White, D. E. and Dudley, M. E. (2011) Durable complete responses in heavily pretreated patients with metastatic melanoma using Tcell transfer immunotherapy. Clin. Cancer Res. 17, 4550-4557.   DOI
16 Twyman-Saint Victor, C., Rech, A. J., Maity, A., Rengan, R., Pauken, K. E., Stelekati, E., Benci, J. L., Xu, B., Dada, H., Odorizzi, P. M., Herati, R. S., Mansfield, K. D., Patsch, D., Amaravadi, R. K., Schuchter, L. M., Ishwaran, H., Mick, R., Pryma, D. A., Xu, X., Feldman, M. D., Gangadhar, T. C., Hahn, S. M., Wherry, E. J., Vonderheide, R. H. and Minn, A. J. (2015) Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 520, 373-377.   DOI
17 Rapoport, A. P., Stadtmauer, E. A., Binder-Scholl, G. K., Goloubeva, O., Vogl, D. T., Lacey, S. F., Badros, A. Z., Garfall, A., Weiss, B., Finklestein, J., Kulikovskaya, I., Sinha, S. K., Kronsberg, S., Gupta, M., Bond, S., Melchiori, L., Brewer, J. E., Bennett, A. D., Gerry, A. B., Pumphrey, N. J., Williams, D., Tayton-Martin, H. K., Ribeiro, L., Holdich, T., Yanovich, S., Hardy, N., Yared, J., Kerr, N., Philip, S., Westphal, S., Siegel, D. L., Levine, B. L., Jakobsen, B. K., Kalos, M. and June, C. H. (2015) NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nat. Med. 21, 914-921.   DOI
18 Riley, R. S., June, C. H., Langer, R. and Mitchell, M. J. (2019) Delivery technologies for cancer immunotherapy. Nat. Rev. Drug Discov. 18, 175-196.   DOI
19 Robbins, P. F., Kassim, S. H., Tran, T. L., Crystal, J. S., Morgan, R. A., Feldman, S. A., Yang, J. C., Dudley, M. E., Wunderlich, J. R., Sherry, R. M., Kammula, U. S., Hughes, M. S., Restifo, N. P., Raffeld, M., Lee, C. C., Li, Y. F., El-Gamil, M. and Rosenberg, S. A. (2015) A pilot trial using lymphocytes genetically engineered with an NYESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin. Cancer Res. 21, 1019-1027.   DOI
20 Rosenberg, S. A., Packard, B. S., Aebersold, P. M., Solomon, D., Topalian, S. L., Toy, S. T., Simon, P., Lotze, M. T., Yang, J. C. and Seipp, C. A. (1988) Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N. Engl. J. Med. 319, 1676-1680.   DOI
21 Porter, D. L., Kalos, M., Zheng, Z., Levine, B. and June, C. (2011a) Chimeric antigen receptor therapy for B-cell malignancies. J. Cancer 2, 331-332.   DOI
22 Weber, J., Mandala, M., Del Vecchio, M., Gogas, H. J., Arance, A. M., Cowey, C. L., Dalle, S., Schenker, M., Chiarion-Sileni, V., Marquez-Rodas, I., Grob, J. J., Butler, M. O., Middleton, M. R., Maio, M., Atkinson, V., Queirolo, P., Gonzalez, R., Kudchadkar, R. R., Smylie, M., Meyer, N., Mortier, L., Atkins, M. B., Long, G. V., Bhatia, S., Lebbe, C., Rutkowski, P., Yokota, K., Yamazaki, N., Kim, T. M., de Pril, V., Sabater, J., Qureshi, A., Larkin, J. and Ascierto, P. A.; CheckMate 238 Collaborators (2017) Adjuvant nivolumab versus ipilimumab in resected stage III or IV melanoma. N. Engl. J. Med. 377, 1824-1835.   DOI
23 Ott, P. A., Hu, Z., Keskin, D. B., Shukla, S. A., Sun, J., Bozym, D. J., Zhang, W., Luoma, A., Giobbie-Hurder, A., Peter, L., Chen, C., Olive, O., Carter, T. A., Li, S., Lieb, D. J., Eisenhaure, T., Gjini, E., Stevens, J., Lane, W. J., Javeri, I., Nellaiappan, K., Salazar, A. M., Daley, H., Seaman, M., Buchbinder, E. I., Yoon, C. H., Harden, M., Lennon, N., Gabriel, S., Rodig, S. J., Barouch, D. H., Aster, J. C., Getz, G., Wucherpfennig, K., Neuberg, D., Ritz, J., Lander, E. S., Fritsch, E. F., Hacohen, N. and Wu, C. J. (2017) An immunogenic personal neoantigen vaccine for patients with melanoma. Nature 547, 217-221.   DOI
24 Palmer, D. C., Guittard, G. C., Franco, Z., Crompton, J. G., Eil, R. L., Patel, S. J., Ji, Y., Van Panhuys, N., Klebanoff, C. A., Sukumar, M., Clever, D., Chichura, A., Roychoudhuri, R., Varma, R., Wang, E., Gattinoni, L., Marincola, F. M., Balagopalan, L., Samelson, L. E. and Restifo, N. P. (2015) Cish actively silences TCR signaling in CD8+ T cells to maintain tumor tolerance. J. Exp. Med. 212, 2095-2113.   DOI
25 Klinger, M., Benjamin, J., Kischel, R., Stienen, S. and Zugmaier, G. (2016) Harnessing T cells to fight cancer with BiTE(R) antibody constructs--past developments and future directions. Immunol. Rev. 270, 193-208.   DOI
26 Wolchok, J. D., Chiarion-Sileni, V., Gonzalez, R., Rutkowski, P., Grob, J. J., Cowey, C. L., Lao, C. D., Wagstaff, J., Schadendorf, D., Ferrucci, P. F., Smylie, M., Dummer, R., Hill, A., Hogg, D., Haanen, J., Carlino, M. S., Bechter, O., Maio, M., Marquez-Rodas, I., Guidoboni, M., McArthur, G., Lebbe, C., Ascierto, P. A., Long, G. V., Cebon, J., Sosman, J., Postow, M. A., Callahan, M. K., Walker, D., Rollin, L., Bhore, R., Hodi, F. S. and Larkin, J. (2017) Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N. Engl. J. Med. 377, 1345-1356.   DOI
27 Sahin, U., Derhovanessian, E., Miller, M., Kloke, B. P., Simon, P., Lower, M., Bukur, V., Tadmor, A. D., Luxemburger, U., Schrors, B., Omokoko, T., Vormehr, M., Albrecht, C., Paruzynski, A., Kuhn, A. N., Buck, J., Heesch, S., Schreeb, K. H., Muller, F., Ortseifer, I., Vogler, I., Godehardt, E., Attig, S., Rae, R., Breitkreuz, A., Tolliver, C., Suchan, M., Martic, G., Hohberger, A., Sorn, P., Diekmann, J., Ciesla, J., Waksmann, O., Bruck, A. K., Witt, M., Zillgen, M., Rothermel, A., Kasemann, B., Langer, D., Bolte, S., Diken, M., Kreiter, S., Nemecek, R., Gebhardt, C., Grabbe, S., Holler, C., Utikal, J., Huber, C., Loquai, C. and Tureci, O. (2017) Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature 547, 222-226.   DOI
28 Schlothauer, T., Herter, S., Koller, C. F., Grau-Richards, S., Steinhart, V., Spick, C., Kubbies, M., Klein, C., Umana, P. and Mossner, E. (2016) Novel human IgG1 and IgG4 Fc-engineered antibodies with completely abolished immune effector functions. Protein Eng. Des. Sel. 29, 457-466.   DOI
29 Ishiguro, T., Sano, Y., Komatsu, S. I., Kamata-Sakurai, M., Kaneko, A., Kinoshita, Y., Shiraiwa, H., Azuma, Y., Tsunenari, T., Kayukawa, Y., Sonobe, Y., Ono, N., Sakata, K., Fujii, T., Miyazaki, Y., Noguchi, M., Endo, M., Harada, A., Frings, W., Fujii, E., Nanba, E., Narita, A., Sakamoto, A., Wakabayashi, T., Konishi, H., Segawa, H., Igawa, T., Tsushima, T., Mutoh, H., Nishito, Y., Takahashi, M., Stewart, L., ElGabry, E., Kawabe, Y., Ishigai, M., Chiba, S., Aoki, M., Hattori, K. and Nezu, J. (2017) An anti-glypican 3/CD3 bispecific T cell-redirecting antibody for treatment of solid tumors. Sci. Transl. Med. 9, eaal4291.   DOI
30 Chen, R., Zinzani, P. L., Lee, H. J., Armand, P., Johnson, N. A., Brice, P., Radford, J., Ribrag, V., Molin, D., Vassilakopoulos, T. P., Tomita, A., von Tresckow, B., Shipp, M. A., Lin, J., Kim, E., Nahar, A., Balakumaran, A. and Moskowitz, C. H. (2019) Pembrolizumab in relapsed or refractory Hodgkin lymphoma: 2-year follow-up of KEYNOTE-087. Blood 134, 1144-1153.
31 Porter, D. L., Levine, B. L., Kalos, M., Bagg, A. and June, C. H. (2011b) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365, 725-733.   DOI
32 Ramachandran, I., Lowther, D. E., Dryer-Minnerly, R., Wang, R., Fayngerts, S., Nunez, D., Betts, G., Bath, N., Tipping, A. J., Melchiori, L., Navenot, J. M., Glod, J., Mackall, C. L., D'Angelo, S. P., Araujo, D. M., Chow, W. A., Demetri, G. D., Druta, M., Van Tine, B. A., Grupp, S. A., Abdul Razak, A. R., Wilky, B., Iyengar, M., Trivedi, T., Winkle, E. V., Chagin, K., Amado, R., Binder, G. K. and Basu, S. (2019) Systemic and local immunity following adoptive transfer of NY-ESO-1 SPEAR T cells in synovial sarcoma. J. Immunother. Cancer 7, 276.   DOI
33 Green, E. W., Bunse, L., Bozza, M., Sanghvi, K. and Platten, M. (2019) TCR validation toward gene therapy for cancer. Methods Enzymol. 629, 419-441.   DOI
34 Grosso, J. F. and Jure-Kunkel, M. N. (2013) CTLA-4 blockade in tumor models: an overview of preclinical and translational research. Cancer Immun. 13, 5.
35 Hargadon, K. M., Johnson, C. E. and Williams, C. J. (2018) Immune checkpoint blockade therapy for cancer: an overview of FDA-approved immune checkpoint inhibitors. Int. Immunopharmacol. 62, 29-39.   DOI
36 Grupp, S. A., Kalos, M., Barrett, D., Aplenc, R., Porter, D. L., Rheingold, S. R., Teachey, D. T., Chew, A., Hauck, B., Wright, J. F., Milone, M. C., Levine, B. L. and June, C. H. (2013) Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N. Engl. J. Med. 368, 1509-1518.   DOI
37 Hummel, H. D., Kufer, P., Grullich, C., Seggewiss-Bernhardt, R., Deschler-Baier, B., Chatterjee, M., Goebeler, M. E., Miller, K., de Santis, M., Loidl, W., Dittrich, C., Buck, A., Lapa, C., Thurner, A., Wittemer-Rump, S., Koca, G., Boix, O., Docke, W. D., Finnern, R., Kusi, H., Ajavon-Hartmann, A., Stienen, S., Sayehli, C. M., Polat, B. and Bargou, R. C. (2021) Pasotuxizumab, a BiTE(®) immune therapy for castration-resistant prostate cancer: phase I, dose-escalation study findings. Immunotherapy 13, 125-141.   DOI
38 Reck, M., Rodriguez-Abreu, D., Robinson, A. G., Hui, R., Csoszi, T., Fulop, A., Gottfried, M., Peled, N., Tafreshi, A., Cuffe, S., O'Brien, M., Rao, S., Hotta, K., Leiby, M. A., Lubiniecki, G. M., Shentu, Y., Rangwala, R. and Brahmer, J. R.; KEYNOTE-024 Investigators (2016) Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N. Engl. J. Med. 375, 1823-1833.   DOI
39 Wing, K., Onishi, Y., Prieto-Martin, P., Yamaguchi, T., Miyara, M., Fehervari, Z., Nomura, T. and Sakaguchi, S. (2008) CTLA-4 control over Foxp3+ regulatory T cell function. Science 322, 271-275.   DOI
40 Halliday, G. M., Patel, A., Hunt, M. J., Tefany, F. J. and Barnetson, R. S. (1995) Spontaneous regression of human melanoma/nonmelanoma skin cancer: association with infiltrating CD4+ T cells. World J. Surg. 19, 352-358.   DOI
41 Hilal, T. and Prasad, V. (2018) Eliminating MRD - FDA approval of blinatumomab for B-ALL in complete remission. Nat. Rev. Clin. Oncol. 15, 727-728.   DOI
42 Imai, C., Mihara, K., Andreansky, M., Nicholson, I. C., Pui, C. H., Geiger, T. L. and Campana, D. (2004) Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 18, 676-684.   DOI
43 Karapetyan, A. R., Chaipan, C., Winkelbach, K., Wimberger, S., Jeong, J. S., Joshi, B., Stein, R. B., Underwood, D., Castle, J. C., van Dijk, M. and Seibert, V. (2019) TCR fingerprinting and off-target peptide identification. Front. Immunol. 10, 2501.   DOI
44 Schultz-Thater, E., Piscuoglio, S., Iezzi, G., Le Magnen, C., Zajac, P., Carafa, V., Terracciano, L., Tornillo, L. and Spagnoli, G. C. (2011) MAGE-A10 is a nuclear protein frequently expressed in high percentages of tumor cells in lung, skin and urothelial malignancies. Int. J. Cancer 129, 1137-1148.   DOI
45 Bendell, J. C., Fong, L., Stein, M. N., Beer, T. M., Ross, A., Gao, X., Weitzman, A., Austin, R., Ganti, V., Law, C., Lemon, B., Wesche, H. and De Bono, J. S. (2020) First-in-human phase I study of HPN424, a tri-specific half-life extended PSMA-targeting T-cell engager in patients with metastatic castration-resistant prostate cancer (mCRPC). J. Clin. Oncol. 38, 5552.   DOI
46 Brocker, T. (2000) Chimeric Fv-zeta or Fv-epsilon receptors are not sufficient to induce activation or cytokine production in peripheral T cells. Blood 96, 1999-2001.   DOI
47 Stein, A. S., Schiller, G., Benjamin, R., Jia, C., Zhang, A., Zhu, M., Zimmerman, Z. and Topp, M. S. (2019) Neurologic adverse events in patients with relapsed/refractory acute lymphoblastic leukemia treated with blinatumomab: management and mitigating factors. Ann. Hematol. 98, 159-167.   DOI
48 Song, S., Han, M., Zhang, H., Wang, Y. and Jiang, H. (2013) Full screening and accurate subtyping of HLA-A*02 alleles through group-specific amplification and mono-allelic sequencing. Cell. Mol. Immunol. 10, 490-496.   DOI
49 Tan, M. P., Gerry, A. B., Brewer, J. E., Melchiori, L., Bridgeman, J. S., Bennett, A. D., Pumphrey, N. J., Jakobsen, B. K., Price, D. A., Ladell, K. and Sewell, A. K. (2015) T cell receptor binding affinity governs the functional profile of cancer-specific CD8+ T cells. Clin. Exp. Immunol. 180, 255-270.   DOI
50 Wu, J., Fu, J., Zhang, M. and Liu, D. (2015) Blinatumomab: a bispecific T cell engager (BiTE) antibody against CD19/CD3 for refractory acute lymphoid leukemia. J. Hematol. Oncol. 8, 104.   DOI
51 Zacharakis, N., Chinnasamy, H., Black, M., Xu, H., Lu, Y. C., Zheng, Z., Pasetto, A., Langhan, M., Shelton, T., Prickett, T., Gartner, J., Jia, L., Trebska-McGowan, K., Somerville, R. P., Robbins, P. F., Rosenberg, S. A., Goff, S. L. and Feldman, S. A. (2018) Immune recognition of somatic mutations leading to complete durable regression in metastatic breast cancer. Nat. Med. 24, 724-730.   DOI
52 Zehn, D., Lee, S. Y. and Bevan, M. J. (2009) Complete but curtailed T-cell response to very low-affinity antigen. Nature 458, 211-214.   DOI
53 Zhang, Y., Du, X., Liu, M., Tang, F., Zhang, P., Ai, C., Fields, J. K., Sundberg, E. J., Latinovic, O. S., Devenport, M., Zheng, P. and Liu, Y. (2019) Hijacking antibody-induced CTLA-4 lysosomal degradation for safer and more effective cancer immunotherapy. Cell Res. 29, 609-627.   DOI
54 D'Ippolito, E., Schober, K., Nauerth, M. and Busch, D. H. (2019) T cell engineering for adoptive T cell therapy: safety and receptor avidity. Cancer Immunol. Immunother. 68, 1701-1712.   DOI
55 Motzer, R. J., Tannir, N. M., McDermott, D. F., Aren Frontera, O., Melichar, B., Choueiri, T. K., Plimack, E. R., Barthelemy, P., Porta, C., George, S., Powles, T., Donskov, F., Neiman, V., Kollmannsberger, C. K., Salman, P., Gurney, H., Hawkins, R., Ravaud, A., Grimm, M. O., Bracarda, S., Barrios, C. H., Tomita, Y., Castellano, D., Rini, B. I., Chen, A. C., Mekan, S., McHenry, M. B., Wind-Rotolo, M., Doan, J., Sharma, P., Hammers, H. J. and Escudier, B.; CheckMate 214 Investigators (2018) Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. N. Engl. J. Med. 378, 1277-1290.   DOI
56 Klinger, M., Zugmaier, G., Nagele, V., Goebeler, M. E., Brandl, C., Stelljes, M., Lassmann, H., von Stackelberg, A., Bargou, R. C. and Kufer, P. (2020) Adhesion of T cells to endothelial cells facilitates blinatumomab-associated neurologic adverse events. Cancer Res. 80, 91-101.   DOI
57 Loffler, A., Kufer, P., Lutterbuse, R., Zettl, F., Daniel, P. T., Schwenkenbecher, J. M., Riethmuller, G., Dorken, B. and Bargou, R. C. (2000) A recombinant bispecific single-chain antibody, CD19 x CD3, induces rapid and high lymphoma-directed cytotoxicity by unstimulated T lymphocytes. Blood 95, 2098-2103.   DOI
58 Zhao, J., Zhao, J. and Perlman, S. (2012) Differential effects of IL-12 on Tregs and non-Treg T cells: roles of IFN-gamma, IL-2 and IL-2R. PLoS ONE 7, e46241.   DOI
59 Topp, M. S., Duell, J., Zugmaier, G., Attal, M., Moreau, P., Langer, C., Kronke, J., Facon, T., Salnikov, A. V., Lesley, R., Beutner, K., Kalabus, J., Rasmussen, E., Riemann, K., Minella, A. C., Munzert, G. and Einsele, H. (2020) Anti-B-cell maturation antigen BiTE molecule AMG 420 induces responses in multiple myeloma. J. Clin. Oncol. 38, 775-783.   DOI
60 D'Angelo, S. P., Melchiori, L., Merchant, M. S., Bernstein, D., Glod, J., Kaplan, R., Grupp, S., Tap, W. D., Chagin, K., Binder, G. K., Basu, S., Lowther, D. E., Wang, R., Bath, N., Tipping, A., Betts, G., Ramachandran, I., Navenot, J. M., Zhang, H., Wells, D. K., Van Winkle, E., Kari, G., Trivedi, T., Holdich, T., Pandite, L., Amado, R. and Mackall, C. L. (2018) Antitumor activity associated with prolonged persistence of adoptively transferred NY-ESO-1 (c259) T cells in synovial sarcoma. Cancer Discov. 8, 944-957.   DOI
61 Garrido, F., Aptsiauri, N., Doorduijn, E. M., Garcia Lora, A. M. and van Hall, T. (2016) The urgent need to recover MHC class I in cancers for effective immunotherapy. Curr. Opin. Immunol. 39, 44-51.   DOI
62 Gong, J., Chehrazi-Raffle, A., Reddi, S. and Salgia, R. (2018) Development of PD-1 and PD-L1 inhibitors as a form of cancer immunotherapy: a comprehensive review of registration trials and future considerations. J. Immunother. Cancer 6, 8.
63 Mhawech-Fauceglia, P., Zhang, S., Terracciano, L., Sauter, G., Chadhuri, A., Herrmann, F. R. and Penetrante, R. (2007) Prostate-specific membrane antigen (PSMA) protein expression in normal and neoplastic tissues and its sensitivity and specificity in prostate adenocarcinoma: an immunohistochemical study using mutipletumour tissue microarray technique. Histopathology 50, 472-483.   DOI
64 Schadendorf, D., Hodi, F. S., Robert, C., Weber, J. S., Margolin, K., Hamid, O., Patt, D., Chen, T. T., Berman, D. M. and Wolchok, J. D. (2015) Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma. J. Clin. Oncol. 33, 1889-1894.   DOI
65 Fecci, P. E., Ochiai, H., Mitchell, D. A., Grossi, P. M., Sweeney, A. E., Archer, G. E., Cummings, T., Allison, J. P., Bigner, D. D. and Sampson, J. H. (2007) Systemic CTLA-4 blockade ameliorates glioma-induced changes to the CD4+ T cell compartment without affecting regulatory T-cell function. Clin. Cancer Res. 13, 2158-2167.   DOI
66 Ferris, R. L., Blumenschein, G., Fayette, J., Guigay, J., Colevas, A. D., Licitra, L., Harrington, K., Kasper, S., Vokes, E. E., Even, C., Worden, F., Saba, N. F., Iglesias Docampo, L. C., Haddad, R., Rordorf, T., Kiyota, N., Tahara, M., Monga, M., Lynch, M., Geese, W. J., Kopit, J., Shaw, J. W. and Gillison, M. L. (2016) Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N. Engl. J. Med. 375, 1856-1867.   DOI
67 Gilboa, E. (1999) The makings of a tumor rejection antigen. Immunity 11, 263-270.   DOI
68 Cohen, E. E. W., Soulieres, D., Le Tourneau, C., Dinis, J., Licitra, L., Ahn, M. J., Soria, A., Machiels, J. P., Mach, N., Mehra, R., Burtness, B., Zhang, P., Cheng, J., Swaby, R. F. and Harrington, K. J.; KEYNOTE-040 investigators (2019) Pembrolizumab versus methotrexate, docetaxel, or cetuximab for recurrent or metastatic head-and-neck squamous cell carcinoma (KEYNOTE-040): a randomised, open-label, phase 3 study. Lancet 393, 156-167.   DOI
69 Hodi, F. S., Mihm, M. C., Soiffer, R. J., Haluska, F. G., Butler, M., Seiden, M. V., Davis, T., Henry-Spires, R., MacRae, S., Willman, A., Padera, R., Jaklitsch, M. T., Shankar, S., Chen, T. C., Korman, A., Allison, J. P. and Dranoff, G. (2003) Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc. Natl. Acad. Sci. U.S.A. 100, 4712-4717.   DOI
70 Hodi, F. S., O'Day, S. J., McDermott, D. F., Weber, R. W., Sosman, J. A., Haanen, J. B., Gonzalez, R., Robert, C., Schadendorf, D., Hassel, J. C., Akerley, W., van den Eertwegh, A. J., Lutzky, J., Lorigan, P., Vaubel, J. M., Linette, G. P., Hogg, D., Ottensmeier, C. H., Lebbe, C., Peschel, C., Quirt, I., Clark, J. I., Wolchok, J. D., Weber, J. S., Tian, J., Yellin, M. J., Nichol, G. M., Hoos, A. and Urba, W. J. (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363, 711-723.   DOI
71 Miyoshi, Y., Ando, A., Egawa, C., Taguchi, T., Tamaki, Y., Tamaki, H., Sugiyama, H. and Noguchi, S. (2002) High expression of Wilms' tumor suppressor gene predicts poor prognosis in breast cancer patients. Clin. Cancer Res. 8, 1167-1171.
72 Mullard, A. (2021) FDA approves first BCMA-targeted CAR-T cell therapy. Nat. Rev. Drug Discov. 20, 332.
73 Nair-Gupta, P., Diem, M., Reeves, D., Wang, W., Schulingkamp, R., Sproesser, K., Mattson, B., Heidrich, B., Mendonca, M., Joseph, J., Sendecki, J., Foulk, B., Chu, G., Fink, D., Jiao, Q., Wu, S. J., Packman, K., Elsayed, Y., Attar, R. and Gaudet, F. (2020) A novel C2 domain binding CD33xCD3 bispecific antibody with potent T-cell redirection activity against acute myeloid leukemia. Blood Adv. 4, 906-919.   DOI
74 Neelapu, S. S., Tummala, S., Kebriaei, P., Wierda, W., Locke, F. L., Lin, Y., Jain, N., Daver, N., Gulbis, A. M., Adkins, S., Rezvani, K., Hwu, P. and Shpall, E. J. (2018) Toxicity management after chimeric antigen receptor T cell therapy: one size does not fit 'ALL'. Nat. Rev. Clin. Oncol. 15, 218.   DOI
75 Bubenik, J. (2003) Tumour MHC class I downregulation and immunotherapy (review). Oncol. Rep. 10, 2005-2008.
76 Carpenter, R. O., Evbuomwan, M. O., Pittaluga, S., Rose, J. J., Raffeld, M., Yang, S., Gress, R. E., Hakim, F. T. and Kochenderfer, J. N. (2013) B-cell maturation antigen is a promising target for adoptive T-cell therapy of multiple myeloma. Clin. Cancer Res. 19, 2048-2060.   DOI
77 Lu, Y., Parker, L., Lu, T., Zheng, Z., Yao, X., Robbins, P. F., van der Bruggen, P., Klebanoff, C. A., Hinrichs, C. S., Goff, S., Sherry, R., Kammula, U., Yang, J. C. and Rosenberg, S. A. (2015) A Phase I study of an HLA-DPB1*0401-restricted T cell receptor targeting MAGE-A3 for patients with metastatic cancers. J. Immunother. Cancer 3, P158.   DOI
78 Brentjens, R. J., Davila, M. L., Riviere, I., Park, J., Wang, X., Cowell, L. G., Bartido, S., Stefanski, J., Taylor, C., Olszewska, M., Borquez-Ojeda, O., Qu, J., Wasielewska, T., He, Q., Bernal, Y., Rijo, I. V., Hedvat, C., Kobos, R., Curran, K., Steinherz, P., Jurcic, J., Rosenblat, T., Maslak, P., Frattini, M. and Sadelain, M. (2013) CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 5, 177ra38.   DOI
79 Brudno, J. N. and Kochenderfer, J. N. (2016) Toxicities of chimeric antigen receptor T cells: recognition and management. Blood 127, 3321-3330.   DOI
80 Campbell, C. E., Kuriyan, N. P., Rackley, R. R., Caulfield, M. J., Tubbs, R., Finke, J. and Williams, B. R. (1998) Constitutive expression of the Wilms tumor suppressor gene (WT1) in renal cell carcinoma. Int. J. Cancer 78, 182-188.   DOI
81 Lynn, R. C., Weber, E. W., Sotillo, E., Gennert, D., Xu, P., Good, Z., Anbunathan, H., Lattin, J., Jones, R., Tieu, V., Nagaraja, S., Granja, J., de Bourcy, C. F. A., Majzner, R., Satpathy, A. T., Quake, S. R., Monje, M., Chang, H. Y. and Mackall, C. L. (2019) c-Jun overexpression in CAR T cells induces exhaustion resistance. Nature 576, 293-300.   DOI
82 Mangsbo, S. M., Sandin, L. C., Anger, K., Korman, A. J., Loskog, A. and Totterman, T. H. (2010) Enhanced tumor eradication by combining CTLA-4 or PD-1 blockade with CpG therapy. J. Immunother. 33, 225-235.   DOI
83 Correnti, C. E., Laszlo, G. S., de van der Schueren, W. J, Godwin, C. D., Bandaranayake, A., Busch, M. A., Gudgeon, C. J., Bates, O. M., Olson, J. M., Mehlin, C. and Walter, R. B. (2018) Simultaneous multiple interaction T-cell engaging (SMITE) bispecific antibodies overcome bispecific T-cell engager (BiTE) resistance via CD28 costimulation. Leukemia 32, 1239-1243.   DOI
84 Carreno, B. M. and Collins, M. (2002) The B7 family of ligands and its receptors: new pathways for costimulation and inhibition of immune responses. Annu. Rev. Immunol. 20, 29-53.   DOI
85 Chen, D. S. and Mellman, I. (2013) Oncology meets immunology: the cancer-immunity cycle. Immunity 39, 1-10.   DOI
86 Chow, M. T., Moller, A. and Smyth, M. J. (2012) Inflammation and immune surveillance in cancer. Semin. Cancer Biol. 22, 23-32.   DOI
87 Daver, N., Alotaibi, A. S., Bucklein, V. and Subklewe, M. (2021) T-cell-based immunotherapy of acute myeloid leukemia: current concepts and future developments. Leukemia 35, 1843-1863.   DOI
88 Decker, W. K. and Safdar, A. (2009) Bioimmunoadjuvants for the treatment of neoplastic and infectious disease: Coley's legacy revisited. Cytokine Growth Factor Rev. 20, 271-281.   DOI
89 Viardot, A., Goebeler, M. E., Hess, G., Neumann, S., Pfreundschuh, M., Adrian, N., Zettl, F., Libicher, M., Sayehli, C., Stieglmaier, J., Zhang, A., Nagorsen, D. and Bargou, R. C. (2016) Phase 2 study of the bispecific T-cell engager (BiTE) antibody blinatumomab in relapsed/refractory diffuse large B-cell lymphoma. Blood 127, 1410-1416.   DOI
90 Wilkie, S., Burbridge, S. E., Chiapero-Stanke, L., Pereira, A. C., Cleary, S., van der Stegen, S. J., Spicer, J. F., Davies, D. M. and Maher, J. (2010) Selective expansion of chimeric antigen receptor-targeted T-cells with potent effector function using interleukin-4. J. Biol. Chem. 285, 25538-25544.   DOI
91 Kumar, V., Chaudhary, N., Garg, M., Floudas, C. S., Soni, P. and Chandra, A. B. (2017) Current diagnosis and management of immune related adverse events (irAEs) induced by immune checkpoint inhibitor therapy. Front. Pharmacol. 8, 49.   DOI
92 Chandran, S. S. and Klebanoff, C. A. (2019) T cell receptor-based cancer immunotherapy: emerging efficacy and pathways of resistance. Immunol. Rev. 290, 127-147.   DOI
93 Costa, L. J., Wong, S. W., Bermudez, A., de la Rubia, J., Mateos, M., Ocio, E. M., Rodriguez-Otero, P., San-Miguel, J., Li, S., Sarmiento, R., Lardelli, P., Gaudy, A., Boss, I., Kelly, L. M., Burgess, M. R., Hege, K. and Bensinger, W. I. (2019) First clinical study of the B-cell maturation antigen (BCMA) 2+1 T cell engager (TCE) CC-93269 in patients (Pts) with relapsed/refractory multiple myeloma (RRMM): interim results of a phase 1 multicenter trial. Blood 134(Supplement_1), 143.   DOI
94 Herbst, R. S., Baas, P., Kim, D. W., Felip, E., Perez-Gracia, J. L., Han, J. Y., Molina, J., Kim, J. H., Arvis, C. D., Ahn, M. J., Majem, M., Fidler, M. J., de Castro, G., Garrido, M., Lubiniecki, G. M., Shentu, Y., Im, E., Dolled-Filhart, M. and Garon, E. B. (2016) Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet 387, 1540-1550.   DOI
95 Huang, J., Brameshuber, M., Zeng, X., Xie, J., Li, Q. J., Chien, Y. H., Valitutti, S. and Davis, M. M. (2013) A single peptide-major histocompatibility complex ligand triggers digital cytokine secretion in CD4(+) T cells. Immunity 39, 846-857.   DOI
96 Thakur, A., Huang, M. and Lum, L. G. (2018) Bispecific antibody based therapeutics: strengths and challenges. Blood Rev. 32, 339-347.   DOI
97 Harrison, S. J., Minnema, M. C., Lee, H. C., Spencer, A., Kapoor, P., Madduri, D., Larsen, J., Ailawadhi, S., Kaufman, J. L., Raab, M. S., Hari, P., Iida, S., Vij, R., Davies, F. E., Lesley, R., Upreti, V. V., Yang, Z., Sharma, A., Minella, A. and Lentzsch, S. (2020) A phase 1 first in human (FIH) study of AMG 701, an anti-B-cell maturation antigen (BCMA) half-life extended (HLE) BiTE® (bispecific T-cell engager) molecule, in relapsed/refractory (RR) multiple myeloma (MM). Blood 136, 28-29.
98 Hirano, F., Kaneko, K., Tamura, H., Dong, H., Wang, S., Ichikawa, M., Rietz, C., Flies, D. B., Lau, J. S., Zhu, G., Tamada, K. and Chen, L. (2005) Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res. 65, 1089-1096.   DOI
99 Hoffmann, M. M. and Slansky, J. E. (2020) T-cell receptor affinity in the age of cancer immunotherapy. Mol. Carcinog. 59, 862-870.   DOI
100 Kontermann, R. E. and Brinkmann, U. (2015) Bispecific antibodies. Drug Discov. Today 20, 838-847.   DOI
101 Yang, Y. F., Zou, J. P., Mu, J., Wijesuriya, R., Ono, S., Walunas, T., Bluestone, J., Fujiwara, H. and Hamaoka, T. (1997) Enhanced induction of antitumor T-cell responses by cytotoxic T lymphocyte-associated molecule-4 blockade: the effect is manifested only at the restricted tumor-bearing stages. Cancer Res. 57, 4036-4041.
102 Wang, T. T. and Ravetch, J. V. (2019) Functional diversification of IgGs through Fc glycosylation. J. Clin. Invest. 129, 3492-3498.   DOI
103 Lorenczewski, G., Friedrich, M., Kischel, R., Dahlhoff, C., Anlahr, J., Balazs, M., Rock, D., Boyle, M. C., Goldstein, R., Coxon, A. and Chapman-Arvedson, T. (2017) Generation of a half-life extended anti-CD19 BiTE® antibody construct compatible with once-weekly dosing for treatment of CD19-positive malignancies. Blood 130, 2815.
104 Malik-Chaudhry, H. K., Prabhakar, K., Ugamraj, H. S., Boudreau, A. A., Buelow, B., Dang, K., Davison, L. M., Harris, K. E., Jorgensen, B., Ogana, H., Pham, D., Schellenberger, U., Van Schooten, W., Buelow, R., Iyer, S., Trinklein, N. D. and Rangaswamy, U. S. (2021) TNB-486 induces potent tumor cell cytotoxicity coupled with low cytokine release in preclinical models of B-NHL. mAbs 13, 1890411.   DOI
105 Shimabukuro-Vornhagen, A., Godel, P., Subklewe, M., Stemmler, H. J., Schlosser, H. A., Schlaak, M., Kochanek, M., Boll, B. and von Bergwelt-Baildon, M. S. (2018) Cytokine release syndrome. J. Immunother. Cancer 6, 56.   DOI
106 Strome, S. E., Dong, H., Tamura, H., Voss, S. G., Flies, D. B., Tamada, K., Salomao, D., Cheville, J., Hirano, F., Lin, W., Kasperbauer, J. L., Ballman, K. V. and Chen, L. (2003) B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res. 63, 6501-6505.
107 Sugita, Y., Wada, H., Fujita, S., Nakata, T., Sato, S., Noguchi, Y., Jungbluth, A. A., Yamaguchi, M., Chen, Y. T., Stockert, E., Gnjatic, S., Williamson, B., Scanlan, M. J., Ono, T., Sakita, I., Yasui, M., Miyoshi, Y., Tamaki, Y., Matsuura, N., Noguchi, S., Old, L. J., Nakayama, E. and Monden, M. (2004) NY-ESO-1 expression and immunogenicity in malignant and benign breast tumors. Cancer Res. 64, 2199-2204.   DOI
108 Turley, S. J., Cremasco, V. and Astarita, J. L. (2015) Immunological hallmarks of stromal cells in the tumour microenvironment. Nat. Rev. Immunol. 15, 669-682.   DOI