Both CD4 and CD8 T cells mediate equally effective in vivo tumor treatment when engineered with a highly avid TCR targeting tyrosinase

Journal of Immunology

Volumn 184, Issue 11, 2010, Pages 5988-5998

  Frankel, Timothy L ^a   Burns, William R ^a   Peng, Peter D ^a   Yu, Zhiya ^a   Chinnasamy, Dhanalakshmi ^a   Wargo, Jennifer A ^a   Zheng, Zhili ^a   Restifo, Nicholas P ^a   Rosenberg, Steven A ^a   Morgan, Richard A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; GLYCOPROTEIN GP 100; HLA A2 ANTIGEN; MELANOMA ANTIGEN; MONOPHENOL MONOOXYGENASE; PEPTIDE; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TETRAMER; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ARTICLE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL TRANSFER; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISULFIDE BOND; GENE TRANSFER; IN VITRO STUDY; IN VIVO STUDY; MELANOMA B16; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; SPLEEN CELL; TRANSGENIC MOUSE; TUMOR REGRESSION; ANIMAL; CELL SEPARATION; EXPERIMENTAL MELANOMA; FLOW CYTOMETRY; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; IMMUNOLOGY; METHODOLOGY; RETROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR ASSOCIATED LEUKOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, NEOPLASM; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; FLOW CYTOMETRY; GENE THERAPY; GENETIC VECTORS; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; MICE; MICE, TRANSGENIC; MONOPHENOL MONOOXYGENASE; RECEPTORS, ANTIGEN, T-CELL; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSDUCTION, GENETIC;

EID: 77953457564     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000189     Document Type: Article

References (50)

1. 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.
2. Dudley, M. E., J. C. Yang, R. Sherry, M. S. Hughes, R. Royal, U. Kammula, P. F. Robbins, J. Huang, D. E. Citrin, S. F. Leitman, et al. 2008. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 26: 5233-5239.
3. Rosenberg, S. A., and M. E. Dudley. 2004. Cancer regression in patients with metastatic melanoma after the transfer of autologous antitumor lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 101(Suppl 2): 14639-14645.
4. Rosenberg, S. A., N. P. Restifo, J. C. Yang, R. A. Morgan, and M. E. Dudley. 2008. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat. Rev. Cancer 8: 299-308.
5. 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.
6. 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.
7. Jorritsma, A., R. Gomez-Eerland, M. Dokter, W. van de Kasteele, Y. M. Zoet, I. I. Doxiadis, N. Rufer, P. Romero, R. A. Morgan, T. N. Schumacher, and J. B. Haanen. 2007. Selecting highly affine and well-expressed TCRs for gene therapy of melanoma. Blood 110: 3564-3572.
8. Johnson, L. A., B. Heemskerk, D. J. Powell, Jr., C. J. Cohen, R. A. Morgan, M. E. Dudley, P. F. Robbins, and S. A. Rosenberg. 2006. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J. Immunol. 177: 6548-6559.
9. Cohen, C. J., Y. F. Li, M. El-Gamil, P. F. Robbins, S. A. Rosenberg, and R. A. Morgan. 2007. Enhanced antitumor activity of T cells engineered to express T-cell receptors with a second disulfide bond. Cancer Res. 67: 3898-3903.
10. Cohen, C. J., Y. Zhao, Z. Zheng, S. A. Rosenberg, and R. A. Morgan. 2006. 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. 66: 8878-8886.
11. Kuball, J., M. L. Dossett, M. Wolfl, W. Y. Ho, R. H. Voss, C. Fowler, and P. D. Greenberg. 2007. Facilitating matched pairing and expression of TCR chains introduced into human T cells. Blood 109: 2331-2338.
12. Cormier, J. N., A. Abati, P. Fetsch, Y. M. Hijazi, S. A. Rosenberg, F. M. Marincola, and S. L. Topalian. 1998. Comparative analysis of the in vivo expression of tyrosinase, MART-1/Melan-A, and gp100 in metastatic melanoma lesions: implications for immunotherapy. J. Immunother. 21: 27-31.
13. de Vries, T. J., A. Fourkour, T. Wobbes, G. Verkroost, D. J. Ruiter, and G. N. van Muijen. 1997. Heterogeneous expression of immunotherapy candidate proteins gp100, MART-1, and tyrosinase in human melanoma cell lines and in human melanocytic lesions. Cancer Res. 57: 3223-3229.
14. de Vries, T. J., M. Smeets, R. de Graaf, K. Hou-Jensen, E. B. Bröcker, N. Renard, A. M. Eggermont, G. N. van Muijen, and D. J. Ruiter. 2001. Expression of gp100, MART-1, tyrosinase, and S100 in paraffin-embedded primary melanomas and locoregional, lymph node, and visceral metastases: implications for diagnosis and immunotherapy. A study conducted by the EORTC Melanoma Cooperative Group. J. Pathol. 193: 13-20.
15. Chen, Y. T., E. Stockert, S. Tsang, K. A. Coplan, and L. J. Old. 1995. Immunophenotyping of melanomas for tyrosinase: implications for vaccine development. Proc. Natl. Acad. Sci. U.S.A. 92: 8125-8129.
16. Cormier, J. N., Y. M. Hijazi, A. Abati, P. Fetsch, M. Bettinotti, S. M. Steinberg, S. A. Rosenberg, and F. M. Marincola. 1998. Heterogeneous expression of melanoma-associated antigens and HLA-A2 in metastatic melanoma in vivo. Int. J. Cancer 75: 517-524.
17. Brichard, V. G., J. Herman, A. Van Pel, C. Wildmann, B. Gaugler, T. Wölfel, T. Boon, and B. Lethé. 1996. A tyrosinase nonapeptide presented by HLA-B44 is recognized on a human melanoma by autologous cytolytic T lymphocytes. Eur. J. Immunol. 26: 224-230.
18. Kang, X., Y. Kawakami, M. el-Gamil, R. Wang, K. Sakaguchi, J. R. Yannelli, E. Appella, S. A. Rosenberg, and P. F. Robbins. 1995. Identification of a tyrosinase epitope recognized by HLA-A24-restricted, tumor-infiltrating lymphocytes. J. Immunol. 155: 1343-1348.
19. Kittlesen, D. J., L. W. Thompson, P. H. Gulden, J. C. Skipper, T. A. Colella, J. Shabanowitz, D. F. Hunt, V. H. Engelhard, C. L. Slingluff, Jr., and J. A. Shabanowitz. 1998. Human melanoma patients recognize an HLA-A1-restricted CTL epitope from tyrosinase containing two cysteine residues: implications for tumor vaccine development. [Published erratum appears in 1999 J. Immunol. 162: 3106.] J. Immunol. 160: 2099-2106.
20. Morel, S., A. Ooms, A. Van Pel, T. Wölfel, V. G. Brichard, P. van der Bruggen, B. J. Van den Eynde, and G. Degiovanni. 1999. A tyrosinase peptide presented by HLA-B35 is recognized on a human melanoma by autologous cytotoxic T lymphocytes. Int. J. Cancer 83: 755-759.
21. Wölfel, T., A. Van Pel, V. Brichard, J. Schneider, B. Seliger, K. H. Meyer zum Büschenfelde, and T. Boon. 1994. Two tyrosinase nonapeptides recognized on HLA-A2 melanomas by autologous cytolytic T lymphocytes. Eur. J. Immunol. 24: 759-764.
22. Kawakami, Y., P. F. Robbins, and S. A. Rosenberg. 1996. Human melanoma antigens recognized by T lymphocytes. Keio J. Med. 45: 100-108.
23. Skipper, J. C., R. C. Hendrickson, P. H. Gulden, V. Brichard, A. Van Pel, Y. Chen, J. Shabanowitz, T. Wolfel, C. L. Slingluff, Jr., T. Boon, et al. 1996. An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins. J. Exp. Med. 183: 527-534.
24. Tjandrawan, T., D. M. Martin, M. J. Maeurer, C. Castelli, M. T. Lotze, and W. J. Storkus. 1998. Autologous human dendriphages pulsed with synthetic or natural tumor peptides elicit tumor-specific CTLs in vitro. J. Immunother. 21: 149-157.
25. Lau, R., F. Wang, G. Jeffery, V. Marty, J. Kuniyoshi, E. Bade, M. E. Ryback, and J. Weber. 2001. Phase I trial of intravenous peptide-pulsed dendritic cells in patients with metastatic melanoma. J. Immunother. 24: 66-78. (Pubitemid 32103309)
26. Nishimura, M. I., D. Avichezer, M. C. Custer, C. S. Lee, C. Chen, M. R. Parkhurst, R. A. Diamond, P. F. Robbins, D. J. Schwartzentruber, and S. A. Rosenberg. 1999. MHC class I-restricted recognition of a melanoma antigen by a human CD4+ tumor infiltrating lymphocyte. Cancer Res. 59: 6230-6238.
27. Roszkowski, J. J., G. E. Lyons, W. M. Kast, C. Yee, K. Van Besien, and M. I. Nishimura. 2005. Simultaneous generation of CD8+ and CD4+ melanoma- reactive T cells by retroviral-mediated transfer of a single T-cell receptor. Cancer Res. 65: 1570-1576.
28. Salter, R. D., D. N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics 21: 235-246. (Pubitemid 15117182)
29. Kawakami, Y., S. Eliyahu, K. Sakaguchi, P. F. Robbins, L. Rivoltini, J. R. Yannelli, E. Appella, and S. A. Rosenberg. 1994. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes. J. Exp. Med. 180: 347-352.
30. Hughes, M. S., Y. Y. Yu, M. E. Dudley, Z. Zheng, P. F. Robbins, Y. Li, J. Wunderlich, R. G. Hawley, M. Moayeri, S. A. Rosenberg, and R. A. Morgan. 2005. Transfer of a TCR gene derived from a patient with a marked antitumor response conveys highly active T-cell effector functions. Hum. Gene Ther. 16: 457-472.
31. Topalian, S. L., D. Solomon, and S. A. Rosenberg. 1989. Tumor-specific cytolysis by lymphocytes infiltrating human melanomas. J. Immunol. 142: 3714-3725.
32. Vitiello, A., D. Marchesini, J. Furze, L. A. Sherman, and R. W. Chesnut. 1991. Analysis of the HLA-restricted influenza-specific cytotoxic T lymphocyte response in transgenic mice carrying a chimeric human-mouse class I major histocompatibility complex. J. Exp. Med. 173: 1007-1015.
33. Irvine, K. R., M. R. Parkhurst, E. P. Shulman, J. P. Tupesis, M. Custer, C. E. Touloukian, P. F. Robbins, A. G. Yafal, P. Greenhalgh, R. P. Sutmuller, et al. 1999. Recombinant virus vaccination against "self" antigens using anchor- fixed immunogens. Cancer Res. 59: 2536-2540.
34. Zhao, Y., Z. Zheng, C. J. Cohen, L. Gattinoni, D. C. Palmer, N. P. Restifo, S. A. Rosenberg, and R. A. Morgan. 2006. High-efficiency transfection of primary human and mouse T lymphocytes using RNA electroporation. Mol. Ther. 13: 151-159.
35. Wargo, J. A., P. F. Robbins, Y. Li, Y. Zhao, M. El-Gamil, D. Caragacianu, Z. Zheng, J. A. Hong, S. Downey, D. S. Schrump, et al. 2009. Recognition of NY-ESO-1+ tumor cells by engineered lymphocytes is enhanced by improved vector design and epigenetic modulation of tumor antigen expression. Cancer Immunol. Immunother. 58: 383-394.
36. Heckman, K. L., and L. R. Pease. 2007. Gene splicing and mutagenesis by PCRdriven overlap extension. Nat. Protoc. 2: 924-932.
37. Yang, S., C. J. Cohen, P. D. Peng, Y. Zhao, L. Cassard, Z. Yu, Z. Zheng, S. Jones, N. P. Restifo, S. A. Rosenberg, and R. A. Morgan. 2008. Development of optimal bicistronic lentiviral vectors facilitates high-level TCR gene expression and robust tumor cell recognition. Gene Ther. 15: 1411-1423.
38. Morita, S., T. Kojima, and T. Kitamura. 2000. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7: 1063-1066. (Pubitemid 30398356)
39. Boulter, J. M., M. Glick, P. T. Todorov, E. Baston, M. Sami, P. Rizkallah, and B. K. Jakobsen. 2003. Stable, soluble T-cell receptor molecules for crystallization and therapeutics. Protein Eng. 16: 707-711.
40. Romeo, M. J., J. Wunderlich, L. Ngo, S. A. Rosenberg, S. M. Steinberg, and D. M. Berman. 2006. Measuring tissue-based biomarkers by immunochromatography coupled with reverse-phase lysate microarray. Clin. Cancer Res. 12: 2463-2467.
41. Hunder, N. N., H. Wallen, J. Cao, D. W. Hendricks, J. Z. Reilly, R. Rodmyre, A. Jungbluth, S. Gnjatic, J. A. Thompson, and C. Yee. 2008. Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N. Engl. J. Med. 358: 2698-2703.
42. Khong, H. T., and S. A. Rosenberg. 2002. Pre-existing immunity to tyrosinase-related protein (TRP)-2, a new TRP-2 isoform, and the NY-ESO-1 melanoma antigen in a patient with a dramatic response to immunotherapy. J. Immunol. 168: 951-956.
43. Robbins, P. F., M. el-Gamil, Y. Kawakami, E. Stevens, J. R. Yannelli, and S. A. Rosenberg. 1994. Recognition of tyrosinase by tumor-infiltrating lymphocytes from a patient responding to immunotherapy. Cancer Res. 54: 3124-3126.
44. Marincola, F. M., L. Rivoltini, M. L. Salgaller, M. Player, and S. A. Rosenberg. 1996. Differential anti-MART-1/MelanA CTL activity in peripheral blood of HLA-A2 melanoma patients in comparison to healthy donors: evidence of in vivo priming by tumor cells. J. Immunother. Emphasis Tumor Immunol. 19: 266-277.
45. Antony, P. A., C. A. Piccirillo, A. Akpinarli, S. E. Finkelstein, P. J. Speiss, D. R. Surman, D. C. Palmer, C. C. Chan, C. A. Klebanoff, W. W. Overwijk, et al. 2005. CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J. Immunol. 174: 2591-2601.
46. Xie, Y., A. Akpinarli, C. Maris, E. L. Hipkiss, M. Lane, E. K. Kwon, P. Muranski, N. P. Restifo, and P. A. Antony. 2010. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J. Exp. Med. 207: 651-667.
47. Quezada, S. A., T. R. Simpson, K. S. Peggs, T. Merghoub, J. Vider, X. Fan, R. Blasberg, H. Yagita, P. Muranski, P. A. Antony, et al. 2010. Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J. Exp. Med. 207: 637-650.
48. Colella, T. A., T. N. Bullock, L. B. Russell, D. W. Mullins, W. W. Overwijk, C. J. Luckey, R. A. Pierce, N. P. Restifo, and V. H. Engelhard. 2000. Selftolerance to the murine homologue of a tyrosinase-derived melanoma antigen: implications for tumor immunotherapy. J. Exp. Med. 191: 1221-1232.
49. Corthay, A., D. K. Skovseth, K. U. Lundin, E. Røsjø, H. Omholt, P. O. Hofgaard, G. Haraldsen, and B. Bogen. 2005. Primary antitumor immune response mediated by CD4+ T cells. Immunity 22: 371-383. (Pubitemid 40387478)
50. Perez-Diez, A., N. T. Joncker, K. Choi, W. F. Chan, C. C. Anderson, O. Lantz, and P. Matzinger. 2007. CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood 109: 5346-5354. (Pubitemid 46890556)