Generation of CD8+ T cells expressing two additional T-cell receptors (TETARs) for personalised melanoma therapy

Cancer Biology and Therapy

Volumn 16, Issue 9, 2015, Pages 1323-1331

  Höfflin, Sandra ^a,b   Prommersberger, Sabrina ^a,b   Uslu, Ugur ^a   Schuler, Gerold ^a   Schmidt, Christopher W ^c   Lennerz, Volker ^d   Dörrie, Jan ^a   Schaft, Niels ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

Adoptive T cell therapy; anti tumor activity; immune escape; immunotherapy; melanoma; neo antigen; TCR transfer

Indexed keywords

CCT6A PROTEIN; CD8 ANTIGEN; CHAPERONIN; CYTOKINE; GAMMA INTERFERON; GLYCOPROTEIN GP 100; INTERLEUKIN 2; MELANOMA ANTIGEN; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CCT6A PROTEIN, HUMAN; CHAPERONIN CONTAINING TCP1; LYMPHOCYTE ANTIGEN RECEPTOR; MELANOCYTE PROTEIN PMEL 17;

ADOPTIVE IMMUNOTHERAPY; ARTICLE; AUTOIMMUNITY; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOLYSIS; DOWN REGULATION; ELECTROPORATION; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; MELANOMA; MUTATION; PERSONALIZED MEDICINE; PROTEIN EXPRESSION; TRANSIENT TRANSFECTION; IMMUNOLOGY; METABOLISM; SKIN NEOPLASMS; TUMOR CELL LINE;

CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CHAPERONIN CONTAINING TCP-1; GP100 MELANOMA ANTIGEN; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MELANOMA; PRECISION MEDICINE; RECEPTORS, ANTIGEN, T-CELL; SKIN NEOPLASMS;

EID: 84941804801     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.1080/15384047.2015.1070981     Document Type: Article

References (32)

1. S.Xue, R.Gillmore, A.Downs, A.Tsallios, A.Holler, L.Gao, V.Wong, E.Morris, H.J.Stauss. Exploiting T cell receptor genes for cancer immunotherapy. Clin Exp Immunol 2005; 139:167-72; PMID:15654813; http://dx.doi.org/10.1111/j.1365-2249.2005.02715.x.
2. R.L.Bolhuis, R.A.Willemsen, J.W.Gratama. Clinical applications of redirected cytotoxicity. In Sitkovsky MV, Henkart PA, editors. Cytotoxic cells. Philadelphia: Lippincott, Williams & Wilkins; 2000; 423-40.
3. M.E.Dudley, J.R.Wunderlich, P.F.Robbins, J.C.Yang, P.Hwu, D.J.Schwartzentruber, S.L.Topalian, R.Sherry, N.P.Restifo, A.M.Hubicki et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002; 298:850-4; PMID:12242449; http://dx.doi.org/10.1126/science.1076514.
4. N.P.Restifo, M.E.Dudley, S.A.Rosenberg. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012; 12:269-81; PMID:22437939; http://dx.doi.org/10.1038/nri3191.
5. R.E.Hawkins, D.E.Gilham, R.Debets, Z.Eshhar, N.Taylor, H.Abken, T.N.Schumacher, ATTACK Consortium. Development of adoptive cell therapy for cancer: a clinical perspective. Hum Gene Ther 2010; 21:665-72; PMID:20408760; http://dx.doi.org/10.1089/hum.2010.086.
6. T.N.Schumacher. T-cell-receptor gene therapy. Nat Rev Immunol 2002; 2:512-9; PMID:12094225; http://dx.doi.org/10.1038/nri841.
7. N.Schaft, J.Dorrie, I.Muller, V.Beck, S.Baumann, T.Schunder, E.Kampgen, G.Schuler. A new way to generate cytolytic tumor-specific T cells: electroporation of RNA coding for a T cell receptor into T lymphocytes. Cancer Immunol Immunother 2006; 55:1132-41; PMID:16344988; http://dx.doi.org/10.1007/s00262-005-0098-2.
8. Y.Zhao, Z.Zheng, C.J.Cohen, L.Gattinoni, D.C.Palmer, N.P.Restifo, S.A.Rosenberg, R.A.Morgan. High-efficiency transfection of primary human and mouse T lymphocytes using RNA electroporation. Mol Ther 2006; 13:151-9; PMID:16140584; http://dx.doi.org/10.1016/j.ymthe.2005.07.688.
9. C.Krug, M.Wiesinger, H.Abken, B.Schuler-Thurner, G.Schuler, J.Dorrie, N.Schaft. A GMP-compliant protocol to expand and transfect cancer patient T cells with mRNA encoding a tumor-specific chimeric antigen receptor. Cancer Immunol Immunother 2014; 63:999-1008; PMID:24938475; http://dx.doi.org/10.1007/s00262-014-1572-5.
10. G.P.Dunn, A.T.Bruce, H.Ikeda, L.J.Old, R.D.Schreiber. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002; 3:991-8; PMID:12407406; http://dx.doi.org/10.1038/ni1102-991.
11. V.Lennerz, M.Fatho, C.Gentilini, R.A.Frye, A.Lifke, D.Ferel, C.Wolfel, C.Huber, T.Wolfel. The response of autologous T cells to a human melanoma is dominated by mutated neoantigens. Proc Natl Acad Sci U S A 2005; 102:16013-8; PMID:16247014; http://dx.doi.org/10.1073/pnas.0500090102.
12. S.Hadrup, M.Donia, S.P.thor. Effector CD4 and CD8 T cells and their role in the tumor microenvironment. Cancer Microenviron 2013; 6:123-33; PMID:23242673; http://dx.doi.org/10.1007/s12307-012-0127-6.
13. N.P.Restifo, J.R.Wunderlich. Principles of tumor immunity: biology of cellular immune responses. In DeVita VT, Hellman S, Rosenberg SA, editors. Biologic Therapy of Cancer. Philadelphia: Lippincott Co 1996; 3-21.
14. C.Hofmann, S.Hofflin, A.Huckelhoven, S.Bergmann, E.Harrer, G.Schuler, J.Dorrie, N.Schaft, T.Harrer. Human T cells expressing two additional receptors (TETARs) specific for HIV-1 recognize both epitopes. Blood 2011; 118:5174-7; PMID:21926350; http://dx.doi.org/10.1182/blood-2011-04-347005.
15. G.Bialer, M.Horovitz-Fried, S.Ya'acobi, R.A.Morgan, C.J.Cohen. Selected murine residues endow human TCR with enhanced tumor recognition. J Immunol 2010; 184:6232-41; PMID:20427762; http://dx.doi.org/10.4049/jimmunol.0902047.
16. C.J.Cohen, Y.Zhao, Z.Zheng, S.A.Rosenberg, R.A.Morgan. 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; 66:8878-86; PMID:16951205; http://dx.doi.org/10.1158/0008-5472.CAN-06-1450.
17. D.Sommermeyer, W.Uckert. Minimal amino acid exchange in human TCR constant regions fosters improved function of TCR gene-modified T cells. J Immunol 2010; 184:6223-31; PMID:20483785; http://dx.doi.org/10.4049/jimmunol.0902055.
18. N.Tanic, G.Brkic, B.Dimitrijevic, N.Dedovic-Tanic, N.Gefen, D.Benharroch, J.Gopas. Identification of differentially expressed mRNA transcripts in drug-resistant versus parental human melanoma cell lines. Anticancer Res 2006; 26:2137-42; PMID:16827156.
19. I.M.Svane, E.M.Verdegaal. Achievements and challenges of adoptive T cell therapy with tumor-infiltrating or blood-derived lymphocytes for metastatic melanoma: what is needed to achieve standard of care? Cancer Immunol Immunother 2014; 63:1081-91; PMID:25099366; http://dx.doi.org/10.1007/s00262-014-1580-5.
20. C.L.Slingluff, Jr., T.A.Colella, L.Thompson, D.D.Graham, J.C.Skipper, J.Caldwell, L.Brinckerhoff, D.J.Kittlesen, D.H.Deacon, C.Oei et al. Melanomas with concordant loss of multiple melanocytic differentiation proteins: immune escape that may be overcome by targeting unique or undefined antigens. Cancer Immunol Immunother 2000; 48:661-72; PMID:10752474; http://dx.doi.org/10.1007/s002620050015.
21. M.Marchand, V.Brichard, N.van Baren, P.G.Coulie. Biological and clinical developments in melanoma vaccines. Expert Opin Biol Ther 2001; 1:497-510; PMID:11727521; http://dx.doi.org/10.1517/14712598.1.3.497.
22. K.M.Kaluza, J.M.Thompson, T.J.Kottke, H.C.Flynn Gilmer, D.L.Knutson, R.G.Vile. Adoptive T cell therapy promotes the emergence of genomically altered tumor escape variants. Int J Cancer 2012; 131:844-54; PMID:21935923; http://dx.doi.org/10.1002/ijc.26447.
23. J.Landsberg, J.Kohlmeyer, M.Renn, T.Bald, M.Rogava, M.Cron, M.Fatho, V.Lennerz, T.Wolfel, M.Holzel et al. Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 2012; 490:412-6; PMID:23051752; http://dx.doi.org/10.1038/nature11538.
24. K.Liu, S.A.Caldwell, K.M.Greeneltch, D.Yang, S.I.Abrams. CTL adoptive immunotherapy concurrently mediates tumor regression and tumor escape. J Immunol 2006; 176:3374-82; PMID:16517705; http://dx.doi.org/10.4049/jimmunol.176.6.3374.
25. R.Carretero, J.M.Romero, F.Ruiz-Cabello, I.Maleno, F.Rodriguez, F.M.Camacho, L.M.Real, F.Garrido, T.Cabrera. Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy. Immunogenetics 2008; 60:439-47; PMID:18545995; http://dx.doi.org/10.1007/s00251-008-0303-5.
26. D.M.Barrett, N.Singh, D.L.Porter, S.A.Grupp, C.H.June. Chimeric antigen receptor therapy for cancer. Annu Rev Med 2014; 65:333-47; PMID:24274181; http://dx.doi.org/10.1146/annurev-med-060512-150254.
27. D.P.Hart, S.A.Xue, S.Thomas, M.Cesco-Gaspere, A.Tranter, B.Willcox, S.P.Lee, N.Steven, E.C.Morris, H.J.Stauss. Retroviral transfer of a dominant TCR prevents surface expression of a large proportion of the endogenous TCR repertoire in human T cells. Gene Ther 2008; 15:625-31; PMID:18305579; http://dx.doi.org/10.1038/sj.gt.3303078.
28. D.M.Barrett, X.Liu, S.Jiang, C.H.June, S.A.Grupp, Y.Zhao. Regimen-specific effects of RNA-modified chimeric antigen receptor T cells in mice with advanced leukemia. Hum Gene Ther 2013; 24:717-27; PMID:23883116; http://dx.doi.org/10.1089/hum.2013.075.
29. Y.Zhao, E.Moon, C.Carpenito, C.M.Paulos, X.Liu, A.L.Brennan, A.Chew, R.G.Carroll, J.Scholler, B.L.Levine et al. Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res 2010; 70:9053-61; PMID:20926399; http://dx.doi.org/10.1158/0008-5472.CAN-10-2880.
30. G.L.Beatty, A.R.Haas, M.V.Maus, D.A.Torigian, M.C.Soulen, G.Plesa, A.Chew, Y.Zhao, B.L.Levine, S.M.Albelda et al. Mesothelin-specific Chimeric Antigen Receptor mRNA-Engineered T cells Induce Anti-Tumor Activity in Solid Malignancies. Cancer Immunol Res 2014; 2:112-20; PMID:24579088; http://dx.doi.org/10.1158/2326-6066.CIR-13-0170.
31. N.Schaft, J.Dorrie, P.Thumann, V.E.Beck, I.Muller, E.S.Schultz, E.Kampgen, D.Dieckmann, G.Schuler. Generation of an optimized polyvalent monocyte-derived dendritic cell vaccine by transfecting defined RNAs after rather than before maturation. J Immunol 2005; 174:3087-97; PMID:15728524; http://dx.doi.org/10.4049/jimmunol.174.5.3087.
32. A.Bonehill, C.Heirman, S.Tuyaerts, A.Michiels, K.Breckpot, F.Brasseur, Y.Zhang, B.P.Van Der, K.Thielemans. Messenger RNA-electroporated dendritic cells presenting MAGE-A3 simultaneously in HLA class I and class II molecules. J Immunol 2004; 172:6649-57; PMID:15153480; http://dx.doi.org/10.4049/jimmunol.172.11.6649.