T cells redirected to EphA2 for the immunotherapy of glioblastoma

Molecular Therapy

Volumn 21, Issue 3, 2013, Pages 629-637

  Chow, Kevin KH ^a,b   Naik, Swati ^a,b   Kakarla, Sunitha ^a,b   Brawley, Vita S ^a,b   Shaffer, Donald R ^a,b   Yi, Zhongzhen ^a,b   Rainusso, Nino ^a,b   Wu, Meng Fen ^b   Liu, Hao ^b   Kew, Yvonne ^c   Grossman, Robert G ^c   Powell, Suzanne ^c   Lee, Dean ^d   Ahmed, Nabil ^a,b   Gottschalk, Stephen ^a,b,e  

^a TEXAS CHILDREN S HOSPITAL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c HOUSTON METHODIST HOSPITAL   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e CENTER FOR CELL AND GENE THERAPY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; EPHRIN RECEPTOR A2; GAMMA INTERFERON; INTERLEUKIN 2; LYMPHOCYTE ANTIGEN RECEPTOR; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CANCER REGRESSION; CANCER SURVIVAL; CELL ASSAY; CELL PROTECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LYMPHOCYTE FUNCTION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; T LYMPHOCYTE; THERAPY EFFECT;

MUS;

EID: 84875215925     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.210     Document Type: Article

References (41)

1. DeAngelis, LM (2001). Brain tumors. N Engl J Med 344: 114-123.
2. Stupp, R, Mason, WP, van den Bent, MJ, Weller, M, Fisher, B, Taphoorn, MJ et al. (2005). Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352: 987-996.
3. Stupp, R, Hegi, ME, Mason, WP, van den Bent, MJ, Taphoorn, MJ, Janzer, RC et al. (2009). Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10: 459-466.
4. Okada, H, Kalinski, P, Ueda, R, Hoji, A, Kohanbash, G, Donegan, TE et al. (2011). Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J Clin Oncol 29: 330-336.
5. Sampson, JH, Heimberger, AB, Archer, GE, Aldape, KD, Friedman, AH, Friedman, HS et al. (2010). Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. J Clin Oncol 28: 4722-4729.
6. Liau, LM, Prins, RM, Kiertscher, SM, Odesa, SK, Kremen, TJ, Giovannone, AJ et al. (2005). Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin Cancer Res 11: 5515-5525.
7. Eshhar, Z, Waks, T, Gross, G and Schindler, DG (1993). Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci USA 90: 720-724.
8. Pule, MA, Savoldo, B, Myers, GD, Rossig, C, Russell, HV, Dotti, G et al. (2008). Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 14: 1264-1270.
9. Porter, DL, Levine, BL, Kalos, M, Bagg, A and June, CH (2011). Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365: 725-733.
10. Wykosky, J, Gibo, DM, Stanton, C and Debinski, W (2005). EphA2 as a novel molecular marker and target in glioblastoma multiforme. Mol Cancer Res 3: 541-551.
11. Hatano, M, Eguchi, J, Tatsumi, T, Kuwashima, N, Dusak, JE, Kinch, MS et al. (2005). EphA2 as a glioma-associated antigen: a novel target for glioma vaccines. Neoplasia 7: 717-722.
12. Liu, F, Park, PJ, Lai, W, Maher, E, Chakravarti, A, Durso, L et al. (2006). A genome-wide screen reveals functional gene clusters in the cancer genome and identifies EphA2 as a mitogen in glioblastoma. Cancer Res 66: 10815-10823.
13. Wang, LF, Fokas, E, Bieker, M, Rose, F, Rexin, P, Zhu, Y et al. (2008). Increased expression of EphA2 correlates with adverse outcome in primary and recurrent glioblastoma multiforme patients. Oncol Rep 19: 151-156.
14. Zelinski, DP, Zantek, ND, Stewart, JC, Irizarry, AR and Kinch, MS (2001). EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res 61: 2301-2306.
15. Miao, H, Li, DQ, Mukherjee, A, Guo, H, Petty, A, Cutter, J et al. (2009). EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 16: 9-20.
16. Ogawa, K, Pasqualini, R, Lindberg, RA, Kain, R, Freeman, AL and Pasquale, EB (2000). The ephrin-A1 ligand and its receptor, EphA2, are expressed during tumor neovascularization. Oncogene 19: 6043-6052.
17. Cheng, N, Brantley, DM, Liu, H, Lin, Q, Enriquez, M, Gale, N et al. (2002). Blockade of EphA receptor tyrosine kinase activation inhibits vascular endothelial cell growth factor-induced angiogenesis. Mol Cancer Res 1: 2-11.
18. Dobrzanski, P, Hunter, K, Jones-Bolin, S, Chang, H, Robinson, C, Pritchard, S et al. (2004). Antiangiogenic and antitumor efficacy of EphA2 receptor antagonist. Cancer Res 64: 910-919.
19. Brantley-Sieders, DM, Fang, WB, Hwang, Y, Hicks, D and Chen, J (2006). Ephrin- A1 facilitates mammary tumor metastasis through an angiogenesis- dependent mechanism mediated by EphA receptor and vascular endothelial growth factor in mice. Cancer Res 66: 10315-10324.
20. Ahmed, N, Salsman, VS, Kew, Y, Shaffer, D, Powell, S, Zhang, YJ et al. (2010). HER2-specific T cells target primary glioblastoma stem cells and induce regression of autologous experimental tumors. Clin Cancer Res 16: 474-485.
21. Damschroder, MM, Widjaja, L, Gill, PS, Krasnoperov, V, Jiang, W, Dall'Acqua, WF et al. (2007). Framework shuffling of antibodies to reduce immunogenicity and manipulate functional and biophysical properties. Mol Immunol 44: 3049-3060.
22. Coffman, KT, Hu, M, Carles-Kinch, K, Tice, D, Donacki, N, Munyon, K et al. (2003). Differential EphA2 epitope display on normal versus malignant cells. Cancer Res 63: 7907-7912.
23. Murat, A, Migliavacca, E, Gorlia, T, Lambiv, WL, Shay, T, Hamou, MF et al. (2008). Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol 26: 3015-3024.
24. Bao, S, Wu, Q, McLendon, RE, Hao, Y, Shi, Q, Hjelmeland, AB et al. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760.
25. Sampson, JH, Archer, GE, Mitchell, DA, Heimberger, AB and Bigner, DD (2008). Tumor-specific immunotherapy targeting the EGFRvIII mutation in patients with malignant glioma. Semin Immunol 20: 267-275.
26. Debinski, W, Obiri, NI, Powers, SK, Pastan, I and Puri, RK (1995). Human glioma cells overexpress receptors for interleukin 13 and are extremely sensitive to a novel chimeric protein composed of interleukin 13 and pseudomonas exotoxin. Clin Cancer Res 1: 1253-1258.
27. Zhang, JG, Eguchi, J, Kruse, CA, Gomez, GG, Fakhrai, H, Schroter, S et al. (2007). Antigenic profiling of glioma cells to generate allogeneic vaccines or dendritic cellbased therapeutics. Clin Cancer Res 13(2 Pt 1): 566-575.
28. Kuan, CT, Wakiya, K, Dowell, JM, Herndon, JE 2nd, Reardon, DA, Graner, MW et al. (2006). Glycoprotein nonmetastatic melanoma protein B, a potential molecular therapeutic target in patients with glioblastoma multiforme. Clin Cancer Res 12(7 Pt 1): 1970-1982.
29. Kurpad, SN, Zhao, XG, Wikstrand, CJ, Batra, SK, McLendon, RE and Bigner, DD (1995). Tumor antigens in astrocytic gliomas. Glia 15: 244-256.
30. Bullain, SS, Sahin, A, Szentirmai, O, Sanchez, C, Lin, N, Baratta, E et al. (2009). Genetically engineered T cells to target EGFRvIII expressing glioblastoma. J Neurooncol 94: 373-382.
31. Kahlon, KS, Brown, C, Cooper, LJ, Raubitschek, A, Forman, SJ and Jensen, MC (2004). Specific recognition and killing of glioblastoma multiforme by interleukin 13-zetakine redirected cytolytic T cells. Cancer Res 64: 9160-9166.
32. Brown CE, Starr R, Naranjo A, Wright C, Bading J, Ressler J, A et al. (2011). Adoptive transfer of autologous IL13-zetakine+ engineered T cell clones for the treatment of recurrent glioblastoma: lessons from the Clinic. Mol Ther 19 (suppl 1): S136-S137.
33. Morgan, RA, Yang, JC, Kitano, M, Dudley, ME, Laurencot, CM, Rosenberg, SA (2010). Case Report of a Serious Adverse Event Following the Administration of T Cells Transduced With a Chimeric Antigen Receptor Recognizing ERBB2. Mol Ther 18:843-851.
34. Brown, CE, Starr, R, Martinez, C, Aguilar, B, D'Apuzzo, M, Todorov, I et al. (2009). Recognition and killing of brain tumor stem-like initiating cells by CD8+ cytolytic T cells. Cancer Res 69: 8886-8893.
35. Hua, W, Yao, Y, Chu, Y, Zhong, P, Sheng, X, Xiao, B et al. (2011). The CD133+ tumor stem-like cell-associated antigen may elicit highly intense immune responses against human malignant glioma. J Neurooncol 105:149-157.
36. Sun, Y, Kong, W, Falk, A, Hu, J, Zhou, L, Pollard, S et al. (2009). CD133 (Prominin) negative human neural stem cells are clonogenic and tripotent. PLoS ONE 4: e5498.
37. Hammond, SA, Lutterbuese, R, Roff, S, Lutterbuese, P, Schlereth, B, Bruckheimer, E et al. (2007). Selective targeting and potent control of tumor growth using an EphA2/CD3-Bispecific single-chain antibody construct. Cancer Res 67: 3927-3935.
38. Wels, W, Harwerth, IM, Zwickl, M, Hardman, N, Groner, B and Hynes, NE (1992). Construction, bacterial expression and characterization of a bifunctional singlechain antibody-phosphatase fusion protein targeted to the human erbB-2 receptor. Biotechnology (NY) 10: 1128-1132.
39. Vera, J, Savoldo, B, Vigouroux, S, Biagi, E, Pule, M, Rossig, C et al. (2006). T lymphocytes redirected against the kappa light chain of human immunoglobulin efficiently kill mature B lymphocyte-derived malignant cells. Blood 108: 3890-3897.
40. Pulè, MA, Straathof, KC, Dotti, G, Heslop, HE, Rooney, CM and Brenner, MK (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.
41. Gottschalk, S, Edwards, OL, Sili, U, Huls, MH, Goltsova, T, Davis, AR et al. (2003). Generating CTL against the subdominant Epstein-Barr virus LMP1 antigen for the adoptive Immunotherapy of EBV-associated malignancies. Blood 101: 1905-1912.