TCRs genetically linked to CD28 and CD3ε Do not mispair with endogenous tcr chains and mediate enhanced T cell persistence and anti-melanoma activity

Journal of Immunology

Volumn 193, Issue 10, 2014, Pages 5315-5326

  Govers, Coen ^a   Sebestyén, Zsolt ^a   Roszik, János ^b   Van Brakel, Mandy ^a   Berrevoets, Cor ^a   Szöor, Árpád ^b   Panoutsopoulou, Konstantina ^a   Broertjes, Marieke ^a   Van, Tan ^a   Vereb, György ^b,c   Szöllosi, János ^a   Debets, Reno ^a  

^a ERASMUS MC CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIBODY; CD3 EPSILON ANTIBODY; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE LCK; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; CD3 ANTIGEN; CD3E PROTEIN, HUMAN; HYBRID PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN BINDING;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ANTIMELANOMA ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BASE MISPAIRING; BINDING AFFINITY; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME PHOSPHORYLATION; GENETIC LINKAGE; HUMAN; HUMAN CELL; IMMUNOCOMPETENCE; IMMUNOSTIMULATION; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SYNAPSE; T LYMPHOCYTE; TRANSGENE; ANIMAL; CANCER TRANSPLANTATION; CHEMISTRY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGICAL SYNAPSE; IMMUNOLOGY; MELANOMA; METABOLISM; MORTALITY; NEOPLASM RECURRENCE, LOCAL; PROTEIN ENGINEERING; SKIN NEOPLASMS; SURVIVAL; TRANSPLANTATION; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTIGENS, CD28; ANTIGENS, CD3; CELL LINE, TUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; IMMUNOLOGICAL SYNAPSES; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MELANOMA; MICE; NEOPLASM RECURRENCE, LOCAL; NEOPLASM TRANSPLANTATION; PROTEIN BINDING; PROTEIN ENGINEERING; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; SURVIVAL ANALYSIS; T-LYMPHOCYTES; TUMOR BURDEN;

EID: 84910122146     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302074     Document Type: Article

References (63)

1. Kunert, A., T. Straetemans, C. Govers, C. Lamers, R. Mathijssen, S. Sleijfer, and R. Debets. 2013. TCR-Engineered T Cells Meet New Challenges to Treat Solid Tumors: Choice of Antigen, T Cell Fitness, and Sensitization of Tumor Milieu. Front. Immunol. 4: 363
2. Rosenberg, S. A. 2012. Raising the bar: the curative potential of human cancer immunotherapy. Sci. Transl. Med. 4: 127ps8
3. Morgan, R. A., M. E. Dudley, J. R. Wunderlich, M. S. Hughes, J. C. Yang, R. M. Sherry, R. E. Royal, S. L. Topalian, U. S. Kammula, N. P. Restifo, et al. 2006. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129
4. Robbins, P. F., R. A. Morgan, S. A. Feldman, J. C. Yang, R. M. Sherry, M. E. Dudley, J. R. Wunderlich, A. V. Nahvi, L. J. Helman, C. L. Mackall, et al. 2011. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J. Clin. Oncol. 29: 917-924
5. Johnson, L. A., R. A. Morgan, M. E. Dudley, L. Cassard, J. C. Yang, M. S. Hughes, U. S. Kammula, R. E. Royal, R. M. Sherry, J. R. Wunderlich, et al. 2009. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114: 535-546
6. Parkhurst, M. R., J. C. Yang, R. C. Langan, M. E. Dudley, D. A. Nathan, S. A. Feldman, J. L. Davis, R. A. Morgan, M. J. Merino, R. M. Sherry, et al. 2011. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol. Ther. 19: 620-626
7. Linette, G. P., E. A. Stadtmauer, M. V. Maus, A. P. Rapoport, B. L. Levine, L. Emery, L. Litzky, A. Bagg, B. M. Carreno, P. J. Cimino, et al. 2013. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 122: 863-871
8. Morgan, R. A., N. Chinnasamy, D. Abate-Daga, A. Gros, P. F. Robbins, Z. Zheng, M. E. Dudley, S. A. Feldman, J. C. Yang, R. M. Sherry, et al. 2013. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J. Immunother. 36: 133-151
9. van Loenen, M. M., R. de Boer, A. L. Amir, R. S. Hagedoorn, G. L. Volbeda, R. Willemze, J. J. van Rood, J. H. Falkenburg, and M. H. Heemskerk. 2010. Mixed T cell receptor dimers harbor potentially harmful neoreactivity. Proc. Natl. Acad. Sci. USA 107: 10972-10977
10. Bendle, G. M., C. Linnemann, A. I. Hooijkaas, L. Bies, M. A. de Witte, A. Jorritsma, A. D. Kaiser, N. Pouw, R. Debets, E. Kieback, et al. 2010. Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat. Med. 16: 565-570, 1p following 570
11. Govers, C., Z. Sebestyén, M. Coccoris, R. A. Willemsen, and R. Debets. 2010. T cell receptor gene therapy: strategies for optimizing transgenic TCR pairing. Trends Mol. Med. 16: 77-87
12. Provasi, E., P. Genovese, A. Lombardo, Z. Magnani, P. Q. Liu, A. Reik, V. Chu, D. E. Paschon, L. Zhang, J. Kuball, et al. 2012. Editing T cell specificity towards leukemia by zinc finger nucleases and lentiviral gene transfer. Nat. Med. 18: 807-815
13. Besser, M. J., R. Shapira-Frommer, A. J. Treves, D. Zippel, O. Itzhaki, L. Hershkovitz, D. Levy, A. Kubi, E. Hovav, N. Chermoshniuk, et al. 2010. Clinical responses in a phase II study using adoptive transfer of short-Term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin. Cancer Res. 16: 2646-2655
14. Dudley, M. E., J. R. Wunderlich, J. C. Yang, R. M. Sherry, S. L. Topalian, N. P. Restifo, R. E. Royal, U. Kammula, D. E. White, S. A. Mavroukakis, et al. 2005. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J. Clin. Oncol. 23: 2346-2357
15. Rosenberg, S. A., J. C. Yang, R. M. Sherry, U. S. Kammula, M. S. Hughes, G. Q. Phan, D. E. Citrin, N. P. Restifo, P. F. Robbins, J. R. Wunderlich, et al. 2011. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 17: 4550-4557
16. Kalos, M., B. L. Levine, D. L. Porter, S. Katz, S. A. Grupp, A. Bagg, and C. H. June. 2011. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 3: 95ra73
17. Couzin-Frankel, J. 2013. Breakthrough of the year 2013. Cancer immunotherapy. Science 342: 1432-1433
18. Kochenderfer, J. N., M. E. Dudley, S. A. Feldman, W. H. Wilson, D. E. Spaner, I. Maric, M. Stetler-Stevenson, G. Q. Phan, M. S. Hughes, R. M. Sherry, et al. 2012. B-cell depletion and remissions of malignancy along with cytokineassociated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptortransduced T cells. Blood 119: 2709-2720
19. Brentjens, R. J., I. Rivière, J. H. Park, M. L. Davila, X. Wang, J. Stefanski, C. Taylor, R. Yeh, S. Bartido, O. Borquez-Ojeda, et al. 2011. Safety and persistence of adoptively transferred autologous CD19-Targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood 118: 4817-4828
20. Butler, M. O., P. Friedlander, M. I. Milstein, M. M. Mooney, G. Metzler, A. P. Murray, M. Tanaka, A. Berezovskaya, O. Imataki, L. Drury, et al. 2011. Establishment of antitumor memory in humans using in vitro-educated CD8+ T cells. Sci. Transl. Med. 3: 80ra34
21. Van de Griend, R. J., B. A. Van Krimpen, S. J. Bol, A. Thompson, and R. L. Bolhuis. 1984. Rapid expansion of human cytotoxic T cell clones: growth promotion by a heat-labile serum component and by various types of feeder cells. J. Immunol. Methods 66: 285-298
22. Sebestyén, Z., E. Schooten, T. Sals, I. Zaldivar, E. San José, B. Alarcón, S. Bobisse, A. Rosato, J. Szöllosi, J. W. Gratama, et al. 2008. Human TCR that incorporate CD3zeta induce highly preferred pairing between TCRalpha and beta chains following gene transfer. J. Immunol. 180: 7736-7746
23. Roszik, J., Z. Sebestyén, C. Govers, Y. Guri, A. Szöor, Z. Pályi-Krekk, G. Vereb, P. Nagy, J. Szö llosi, and R. Debets. 2011. T-cell synapse formation depends on antigen recognition but not CD3 interaction: studies with TCR:ζ, a candidate transgene for TCR gene therapy. Eur. J. Immunol. 41: 1288-1297
24. Govers, C., C. Berrevoets, E. Treffers-Westerlaken, M. Broertjes, and R. Debets. 2012. Magnetic-activated cell sorting of TCR-engineered T cells, using tCD34 as a gene marker, but not peptide-MHC multimers, results in significant numbers of functional CD4(+) and CD8(+) T cells. Human Gene Ther. Meth. 23: 213-224
25. Schaft, N., R. A. Willemsen, J. de Vries, B. Lankiewicz, B. W. Essers, J. W. Gratama, C. G. Figdor, R. L. Bolhuis, R. Debets, and G. J. Adema. 2003. Peptide fine specificity of anti-glycoprotein 100 CTL is preserved following transfer of engineered TCR alpha beta genes into primary human T lymphocytes. J. Immunol. 170: 2186-2194
26. van der Bruggen, P., C. Traversari, P. Chomez, C. Lurquin, E. De Plaen, B. Van den Eynde, A. Knuth, and T. Boon. 1991. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254: 1643-1647
27. Willemsen, R. A., M. E. Weijtens, C. Ronteltap, Z. Eshhar, J. W. Gratama, P. Chames, and R. L. Bolhuis. 2000. Grafting primary human T lymphocytes with cancer-specific chimeric single chain and two chain TCR. Gene Ther. 7: 1369-1377
28. Schaft, N., B. Lankiewicz, J. Drexhage, C. Berrevoets, D. J. Moss, V. Levitsky, M. Bonneville, S. P. Lee, A. J. McMichael, J. W. Gratama, et al. 2006. T cell retargeting to EBV antigens following TCR gene transfer: CD28-containing receptors mediate enhanced antigen-specific IFNgamma production. Int. Immunol. 18: 591-601
29. Kofler, D. M., M. Chmielewski, G. Rappl, A. Hombach, T. Riet, A. Schmidt, A. A. Hombach, C. M. Wendtner, and H. Abken. 2011. CD28 costimulation impairs the efficacy of a redirected T-cell antitumor attack in the presence of regulatory T cells which can be overcome by preventing Lck activation. Mol. Ther. 19: 760-767
30. Lamers, C. H., R. A. Willemsen, P. van Elzakker, B. A. van Krimpen, J. W. Gratama, and R. Debets. 2006. Phoenix-ampho outperforms PG13 as retroviral packaging cells to transduce human T cells with tumor-specific receptors: implications for clinical immunogene therapy of cancer. Cancer Gene Ther. 13: 503-509
31. Govers, C., Z. Sebestyen, C. Berrevoets, H. Venselaar, and R. Debets. 2011. T cell receptor fused to CD3z: transmembrane domain of CD3z prevents TCR mis-pairing, whereas complete CD3z directs functional TCR expression. Open Gene Ther. J. 4: 11-22
32. Roszik, J., J. Szöllosi, and G. Vereb. 2008. AccPbFRET: An ImageJ plugin for semi-automatic, fully corrected analysis of acceptor photobleaching FRET images. BMC Bioinformatics 9: 346
33. Szentesi, G., G. Horváth, I. Bori, G. Vámosi, J. Szöllosi, R. Gáspár, S. Damjanovich, A. Jenei, and L. Mátyus. 2004. Computer program for determining fluorescence resonance energy transfer efficiency from flow cytometric data on a cell-by-cell basis. Comput. Methods Programs Biomed. 75: 201-211
34. Pascolo, S., N. Bervas, J. M. Ure, A. G. Smith, F. A. Lemonnier, and B. Pérarnau. 1997. HLA-A2.1-restricted education and cytolytic activity of CD8 (+) T lymphocytes from beta2 microglobulin (beta2m) HLA-A2.1 monochain transgenic H-2Db beta2m double knockout mice. J. Exp. Med. 185: 2043-2051
35. Pouw, N. M., E. J. Westerlaken, R. A. Willemsen, and R. Debets. 2007. Gene transfer of human TCR in primary murine T cells is improved by pseudo-Typing with amphotropic and ecotropic envelopes. J. Gene Med. 9: 561-570
36. Seynhaeve, A. L., S. Hoving, D. Schipper, C. E. Vermeulen, Ga. de Wiel-Ambagtsheer, S. T. van Tiel, A. M. Eggermont, and T. L. Ten Hagen. 2007. Tumor necrosis factor alpha mediates homogeneous distribution of liposomes in murine melanoma that contributes to a better tumor response. Cancer Res. 67: 9455-9462
37. Wooldridge, L., H. A. van den Berg, M. Glick, E. Gostick, B. Laugel, S. L. Hutchinson, A. Milicic, J. M. Brenchley, D. C. Douek, D. A. Price, and A. K. Sewell. 2005. Interaction between the CD8 coreceptor and major histocompatibility complex class I stabilizes T cell receptor-antigen complexes at the cell surface. J. Biol. Chem. 280: 27491-27501
38. Sussman, J. J., J. S. Bonifacino, J. Lippincott-Schwartz, A. M. Weissman, T. Saito, R. D. Klausner, and J. D. Ashwell. 1988. Failure to synthesize the T cell CD3-zeta chain: structure and function of a partial T cell receptor complex. Cell 52: 85-95
39. Boomer, J. S., and J. M. Green. 2010. An enigmatic tail of CD28 signaling. Cold Spring Harb. Perspect. Biol. 2: A002436
40. Gallo, E. M., K. Canté-Barrett, and G. R. Crabtree. 2006. Lymphocyte calcium signaling from membrane to nucleus. Nat. Immunol. 7: 25-32
41. DeFord-Watts, L. M., J. A. Young, L. A. Pitcher, and N. S. van Oers. 2007. The membrane-proximal portion of CD3 epsilon associates with the serine/threonine kinase GRK2. J. Biol. Chem. 282: 16126-16134
42. Schaft, N., M. Coccoris, J. Drexhage, C. Knoop, I. J. de Vries, G. J. Adema, and R. Debets. 2013. An Altered gp100 Peptide Ligand with Decreased Binding by TCR and CD8a Dissects T Cell Cytotoxicity from Production of Cytokines and Activation of NFAT. Front. Immunol. 4: 270
43. Blanco, R., and B. Alarcón. 2012. TCR Nanoclusters as the Framework for Transmission of Conformational Changes and Cooperativity. Front. Immunol. 3: 115
44. Kuhns, M. S., A. T. Girvin, L. O. Klein, R. Chen, K. D. Jensen, E. W. Newell, J. B. Huppa, B. F. Lillemeier, M. Huse, Y. H. Chien, et al. 2010. Evidence for a functional sidedness to the alphabetaTCR. Proc. Natl. Acad. Sci. USA 107: 5094-5099
45. Kumar, R., M. Ferez, M. Swamy, I. Arechaga, M. T. Rejas, J. M. Valpuesta, W. W. Schamel, B. Alarcon, and H. M. van Santen. 2011. Increased sensitivity of antigen-experienced T cells through the enrichment of oligomeric T cell receptor complexes. Immunity 35: 375-387
46. Fernández-Miguel, G., B. Alarcón, A. Iglesias, H. Bluethmann, M. Alvarez-Mon, E. Sanz, and A. de la Hera. 1999. Multivalent structure of an alphabetaT cell receptor. Proc. Natl. Acad. Sci. USA 96: 1547-1552
47. Schamel, W. W., I. Arechaga, R. M. Risueño, H. M. van Santen, P. Cabezas, C. Risco, J. M. Valpuesta, and B. Alarcón. 2005. Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response. J. Exp. Med. 202: 493-503
48. Ahmed, F., S. Friend, T. C. George, N. Barteneva, and J. Lieberman. 2009. Numbers matter: quantitative and dynamic analysis of the formation of an immunological synapse using imaging flow cytometry. J. Immunol. Methods 347: 79-86
49. Bunnell, S. C., D. I. Hong, J. R. Kardon, T. Yamazaki, C. J. McGlade, V. A. Barr, and L. E. Samelson. 2002. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158: 1263-1275
50. Stefanová, I., B. Hemmer, M. Vergelli, R. Martin, W. E. Biddison, and R. N. Germain. 2003. TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways. Nat. Immunol. 4: 248-254
51. Schneider, H., and C. E. Rudd. 2008. CD28 and Grb-2, relative to Gads or Grap, preferentially co-operate with Vav1 in the activation of NFAT/AP-1 transcription. Biochem. Biophys. Res. Commun. 369: 616-621
52. Lin, J., and A. Weiss. 2001. T cell receptor signalling. J. Cell Sci. 114: 243-244
53. Lazar-Molnar, E., S. C. Almo, and S. G. Nathenson. 2006. The interchain disulfide linkage is not a prerequisite but enhances CD28 costimulatory function. Cell. Immunol. 244: 125-129
54. Charo, J., C. Perez, C. Buschow, A. Jukica, M. Czeh, and T. Blankenstein. 2011. Visualizing the dynamic of adoptively transferred T cells during the rejection of large established tumors. Eur. J. Immunol. 41: 3187-3197
55. David, R., L. Ma, A. Ivetic, A. Takesono, A. J. Ridley, J. G. Chai, V. L. Tybulewicz, and F. M. Marelli-Berg. 2009. T-cell receptor-and CD28-induced Vav1 activity is required for the accumulation of primed T cells into antigenic tissue. Blood 113: 3696-3705
56. Kirchhoff, S., W. W. Müller, M. Li-Weber, and P. H. Krammer. 2000. Upregulation of c-FLIPshort and reduction of activation-induced cell death in CD28-costimulated human T cells. Eur. J. Immunol. 30: 2765-2774
57. Boise, L. H., A. J. Minn, P. J. Noel, C. H. June, M. A. Accavitti, T. Lindsten, and C. B. Thompson. 1995. CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity 3: 87-98
58. Zhao, Y., Q. J. Wang, S. Yang, J. N. Kochenderfer, Z. Zheng, X. Zhong, M. Sadelain, Z. Eshhar, S. A. Rosenberg, and R. A. Morgan. 2009. A herceptinbased chimeric antigen receptor with modified signaling domains leads to enhanced survival of transduced T lymphocytes and antitumor activity. J. Immunol. 183: 5563-5574
59. Tammana, S., X. Huang, M. Wong, M. C. Milone, L. Ma, B. L. Levine, C. H. June, J. E. Wagner, B. R. Blazar, and X. Zhou. 2010. 4-1BB and CD28 signaling plays a synergistic role in redirecting umbilical cord blood T cells against B-cell malignancies. Hum. Gene Ther. 21: 75-86
60. Pule, M. A., K. C. Straathof, G. Dotti, H. E. Heslop, C. M. Rooney, and M. K. Brenner. 2005. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol. Ther. 12: 933-941
61. Milone, M. C., J. D. Fish, C. Carpenito, R. G. Carroll, G. K. Binder, D. Teachey, M. Samanta, M. Lakhal, B. Gloss, G. Danet-Desnoyers, et al. 2009. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 17: 1453-1464
62. Carpenito, C., M. C. Milone, R. Hassan, J. C. Simonet, M. Lakhal, M. M. Suhoski, A. Varela-Rohena, K. M. Haines, D. F. Heitjan, S. M. Albelda, et al. 2009. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc. Natl. Acad. Sci. USA 106: 3360-3365
63. Gilham, D. E., R. Debets, M. Pule, R. E. Hawkins, and H. Abken. 2012. CART cells and solid tumors: tuning T cells to challenge an inveterate foe. Trends Mol. Med. 18: 377-384.