A human ErbB2-specific T-cell receptor confers potent antitumor effector functions in genetically engineered primary cytotoxic lymphocytes

Human Gene Therapy

Volumn 25, Issue 8, 2014, Pages 730-739

  Lanitis, Evripidis ^a   Smith, Jenessa B ^a   Dangaj, Denarda ^a   Flingai, Seleeke ^a   Poussin, Mathilde ^a   Xu, Shuwen ^b   Czerniecki, Brian J ^b   Li, Yong F ^c   Robbins, Paul F ^c   Powell, Daniel J ^a,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GAMMA INTERFERON; MELAN A; RETROVIRUS VECTOR; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR 7; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TAPASIN; TETRAMER; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; UNCLASSIFIED DRUG; ERBB2 PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD; BREAST CANCER CELL LINE; CANCER GENE THERAPY; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; COCULTURE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MELANOMA CELL; MOLECULAR CLONING; MONOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; T LYMPHOCYTE ACTIVATION; TARGET CELL; TUMOR CELL LINE; TUMOR GROWTH; TUMOR VOLUME; TUMOR XENOGRAFT; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ANIMAL; BREAST NEOPLASMS; CANCER TRANSPLANTATION; FEMALE; GENETIC ENGINEERING; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE;

ANIMALS; ANTIGEN PRESENTATION; BREAST NEOPLASMS; CELL LINE, TUMOR; DENDRITIC CELLS; FEMALE; GENETIC ENGINEERING; HUMANS; IMMUNOTHERAPY; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; RECEPTOR, ERBB-2; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES, CYTOTOXIC; TUMOR BURDEN;

EID: 84906253986     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2014.006     Document Type: Article

References (44)

1. Ahmadi, M., King, J.W., Xue, S.A., et al. (2011). CD3 limits the efficacy of TCR gene therapy in vivo. Blood 118, 3528-3537.
2. Anderson, B.W., Peoples, G.E., Murray, J.L., et al. (2000). Peptide priming of cytolytic activity to HER-2 epitope 369- 377 in healthy individuals. Clin. Cancer Res. 6, 4192-4200.
3. Bartsch, R., Wenzel, C., Zielinski, C.C., and Steger, G.G. (2007). HER-2-positive breast cancer: hope beyond trastuzumab. BioDrugs 21, 69-77.
4. Bookman, M.A., Darcy, K.M., Clarke-Pearson, D., et al. (2003). Evaluation of monoclonal humanized anti-HER2 antibody, trastuzumab, in patients with recurrent or refractory ovarian or primary peritoneal carcinoma with overexpression of HER2: a phase II trial of the Gynecologic Oncology Group. J. Clin. Oncol. 21, 283-290.
5. Brossart, P., Stuhler, G., Flad, T., et al. (1998). Her-2/neuderived peptides are tumor-associated antigens expressed by human renal cell and colon carcinoma lines and are recognized by in vitro induced specific cytotoxic T lymphocytes. Cancer Res. 58, 732-736.
6. Brossart, P., Wirths, S., Stuhler, G., et al. (2000). Induction of cytotoxic T-lymphocyte responses in vivo after vaccinations with peptide-pulsed dendritic cells. Blood 96, 3102-3108.
7. Cohen, C.J., Zheng, Z., Bray, R., et al. (2005). Recognition of fresh human tumor by human peripheral blood lymphocytes transduced with a bicistronic retroviral vector encoding a murine anti-p53 TCR. J. Immunol. 175, 5799-5808.
8. Cohen, C.J., Zhao, Y., Zheng, Z., et al. (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.
9. Cohen, C.J., Li, Y.F., El-Gamil, M., et al. (2007). Enhanced antitumor activity of T cells engineered to express T-cell receptors with a second disulfide bond. Cancer Res. 67, 3898-3903.
10. Conrad, H., Gebhard, K., Kronig, H., et al. (2008). CTLs directed against HER2 specifically cross-react with HER3 and HER4. J. Immunol. 180, 8135-8145.
11. Cordaro, T.A., de Visser, K.E., Tirion, F.H., et al. (2002). Can the low-avidity self-specific T cell repertoire be exploited for tumor rejection? J. Immunol. 168, 651-660.
12. Czerniecki, B.J., Koski, G.K., Koldovsky, U., et al. (2007). Targeting HER-2/neu in early breast cancer development using dendritic cells with staged interleukin-12 burst secretion. Cancer Res. 67, 1842-1852.
13. Dangaj, D., Lanitis, E., Zhao, A., et al. (2013). Novel recombinant human B7-H4 antibodies overcome tumoral immune escape to potentiate T cell anti-tumor responses. Cancer Res. 73, 4820-4829.
14. Disis, M.L., Schiffman, K., Guthrie, K., et al. (2004). Effect of dose on immune response in patients vaccinated with an her- 2/neu intracellular domain protein-based vaccine. J. Clin. Oncol. 22, 1916-1925.
15. Engel, R.H., and Kaklamani, V.G. (2007). HER2-positive breast cancer: current and future treatment strategies. Drugs 67, 1329-1341.
16. Engels, B., and Uckert, W. (2007). Redirecting T lymphocyte specificity by T cell receptor gene transfer-a new era for immunotherapy. Mol. Aspects Med. 28, 115-142.
17. Han, L.Y., Fletcher, M.S., Urbauer, D.L., et al. (2008). HLA class I antigen processing machinery component expression and intratumoral T-Cell infiltrate as independent prognostic markers in ovarian carcinoma. Clin. Cancer Res. 14, 3372-3379.
18. Henle, A.M., Erskine, C.L., Benson, L.M., et al. (2013). Enzymatic discovery of a HER-2/neu epitope that generates cross-reactive T cells. J. Immunol. 190, 479-488.
19. Johnson, L.A., Heemskerk, B., Powell, D.J., Jr., et al. (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.
20. Johnson, L.A., Morgan, R.A., Dudley, M.E., 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.
21. Keogh, E., Fikes, J., Southwood, S., et al. (2001). Identification of new epitopes from four different tumor-associated antigens: recognition of naturally processed epitopes correlates with HLA-A*0201-binding affinity. J. Immunol. 167, 787-796.
22. Knutson, K.L., Schiffman, K., Cheever, M.A., and Disis, M.L. (2002). Immunization of cancer patients with a HER-2/neu, HLA-A2 peptide, p369-377, results in short-lived peptidespecific immunity. Clin. Cancer Res. 8, 1014-1018.
23. Koski, G.K., Koldovsky, U., Xu, S., et al. (2012). A novel dendritic cell-based immunization approach for the induction of durable Th1-polarized anti-HER-2/neu responses in women with early breast cancer. J. Immunother. 35, 54-65.
24. Lanitis, E., Dangaj, D., Hagemann, I.S., et al. (2012). Primary human ovarian epithelial cancer cells broadly express HER2 at immunologically- detectable levels. PLoS ONE 7, e49829.
25. Levine, B.L., Bernstein, W.B., Connors, M., et al. (1997). Effects of CD28 costimulation on long-term proliferation of CD4 + T cells in the absence of exogenous feeder cells. J. Immunol. 159, 5921-5930.
26. Liu, G., Ying, H., Zeng, G., et al. (2004). HER-2, gp100, and MAGE-1 are expressed in human glioblastoma and recognized by cytotoxic T cells. Cancer Res. 64, 4980-4986.
27. Marincola, F.M., Shamamian, P., Simonis, T.B., et al. (1994). Locus-specific analysis of human leukocyte antigen class I expression in melanoma cell lines. J. Immunother. Emphasis Tumor Immunol. 16, 13-23.
28. Morgan, R.A., Dudley, M.E., Wunderlich, J.R., et al. (2006). Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314, 126-129.
29. Murray, J.L., Gillogly, M.E., Przepiorka, D., et al. (2002). Toxicity, immunogenicity, and induction of E75-specific tumorlytic CTLs by HER-2 peptide E75 (369-377) combined with granulocyte macrophage colony-stimulating factor in HLA-A2+ patients with metastatic breast and ovarian cancer. Clin. Cancer Res. 8, 3407-3418.
30. Okamoto, S., Mineno, J., Ikeda, H., et al. (2009). Improved expression and reactivity of transduced tumor-specific TCRs in human lymphocytes by specific silencing of endogenous TCR. Cancer Res. 69, 9003-9011.
31. Peoples, G.E., Gurney, J.M., Hueman, M.T., et al. (2005). Clinical trial results of a HER2/neu (E75) vaccine to prevent recurrence in high-risk breast cancer patients. J. Clin. Oncol. 23, 7536-7545.
32. Pietras, R.J., Fendly, B.M., Chazin, V.R., et al. (1994). Antibody to HER-2/neu receptor blocks DNA repair after cisplatin in human breast and ovarian cancer cells. Oncogene 9, 1829-1838.
33. Rivoltini, L., Barracchini, K.C., Viggiano, V., et al. (1995). Quantitative correlation between HLA class I allele expression and recognition of melanoma cells by antigen-specific cytotoxic T lymphocytes. Cancer Res. 55, 3149-3157.
34. Rongcun, Y., Salazar-Onfray, F., Charo, J., et al. (1999). Identification of new HER2/neu-derived peptide epitopes that can elicit specific CTL against autologous and allogeneic carcinomas and melanomas. J. Immunol. 163, 1037-1044.
35. Sadelain, M., Riviere, I., and Brentjens, R. (2003). Targeting tumours with genetically enhanced T lymphocytes. Nat. Rev. Cancer 3, 35-45.
36. Schumacher, T.N. (2002). T-cell-receptor gene therapy. Nat. Rev. Immunol. 2, 512-519.
37. Seliger, B., Rongcun, Y., Atkins, D., et al. (2000). HER-2/neu is expressed in human renal cell carcinoma at heterogeneous levels independently of tumor grading and staging and can be recognized by HLA-A2.1-restricted cytotoxic T lymphocytes. Int. J. Cancer 87, 349-359.
38. Voss, R.H., Willemsen, R.A., Kuball, J., et al. (2008). Molecular design of the Calphabeta interface favors specific pairing of introduced TCRalphabeta in human T cells. J. Immunol. 180, 391-401.
39. Wargo, J.A., Robbins, P.F., Li, Y., 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.
40. Willemsen, R.A., Debets, R., Chames, P., and Bolhuis, R.L. (2003). Genetic engineering of T cell specificity for immunotherapy of cancer. Hum. Immunol. 64, 56-68.
41. Wong, Y.F., Cheung, T.H., Lam, S.K., et al. (1995). Prevalence and significance of HER-2/neu amplification in epithelial ovarian cancer. Gynecol. Obstet. Invest. 40, 209-212.
42. Xu, S., Koski, G.K., Faries, M., et al. (2003). Rapid high efficiency sensitization of CD8 + T cells to tumor antigens by dendritic cells leads to enhanced functional avidity and direct tumor recognition through an IL-12-dependent mechanism. J. Immunol. 171, 2251-2261.
43. Zaks, T.Z., and Rosenberg, S.A. (1998). Immunization with a peptide epitope (p369-377) from HER-2/neu leads to peptide-specific cytotoxic T lymphocytes that fail to recognize HER-2/neu + tumors. Cancer Res. 58, 4902-4908.
44. zum Buschenfelde, C.M., Hermann, C., Schmidt, B., et al. (2002). Antihuman epidermal growth factor receptor 2 (HER2) monoclonal antibody trastuzumab enhances cytolytic activity of class I-restricted HER2-specific T lymphocytes against HER2-overexpressing tumor cells. Cancer Res. 62, 2244-2247.