Elimination of progressive mammary cancer by repeated administrations of chimeric antigen receptor-modified T cells

Molecular Therapy

Volumn 22, Issue 5, 2014, Pages 1029-1038

  Globerson Levin, Anat ^a   Waks, Tova ^a   Eshhar, Zelig ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPITOPE; GAMMA INTERFERON; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; BREAST CANCER; BREAST METASTASIS; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER PREVENTION; CANCER RECURRENCE; CANCER SURVIVAL; CELLULAR DISTRIBUTION; CHIMERIC ANTIBODY BASED RECEPTOR MODIFIED T LYMPHOCYTE; CLINICAL EFFECTIVENESS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ELIMINATION; ERBB 2 GENE; FEMALE; HISTOPATHOLOGY; IMMUNOCYTOTOXICITY; IMMUNOREACTIVITY; LYMPHOCYTE MIGRATION; MALE; MEMORY CELL; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIMARY TUMOR; PROTEIN EXPRESSION; SURVIVAL TIME; T LYMPHOCYTE; TRANSGENIC MOUSE; ADOPTIVE IMMUNOTHERAPY; ANIMAL; BREAST NEOPLASMS; DRUG SCREENING; GENETICS; HUMAN; IMMUNOLOGY; TRANSPLANTATION; TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MICE; RECEPTOR, ERBB-2; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899972495     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.28     Document Type: Article

References (50)

1. 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.
2. Kochenderfer, JN, Dudley, ME, Feldman, SA, Wilson, WH, Spaner, DE, Maric, I et al. (2012. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood 119: 2709-2720.
3. Davila, ML, Brentjens, R, Wang, X, Rivi?e, I and Sadelain, M (2012. How do CARs work?: Early insights from recent clinical studies targeting CD19. Oncoimmunology 1: 1577-1583.
4. Louis, CU, Savoldo, B, Dotti, G, Pule, M, Yvon, E, Myers, GD et al. (2011. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118: 6050-6056.
5. Carter, P, Presta, L, Gorman, CM, Ridgway, JB, Henner, D, Wong, WL et al. (1992. Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc Natl Acad Sci USA 89: 4285-4289.
6. Milani, A, Sangiolo, D, Montemurro, F, Aglietta, M and Valabrega, G (2013. Active immunotherapy in HER2 overexpressing breast cancer: current status and future perspectives. Ann Oncol 24: 1740-1748.
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. Eshhar, Z (1997. Tumor-specific T-bodies: towards clinical application. Cancer Immunol Immunother 45: 131-136.
9. Stancovski, I, Schindler, DG, Waks, T, Yarden, Y, Sela, M and Eshhar, Z (1993. Targeting of T lymphocytes to Neu/HER2-expressing cells using chimeric single chain Fv receptors. J Immunol 151: 6577-6582.
10. Altenschmidt, U, Klundt, E and Groner, B (1997. Adoptive transfer of in vitrotargeted, activated T lymphocytes results in total tumor regression. J Immunol 159: 5509-5515.
11. Moritz, D, Wels, W, Mattern, J and Groner, B (1994. Cytotoxic T lymphocytes with a grafted recognition specificity for ERBB2-expressing tumor cells. Proc Natl Acad Sci USA 91: 4318-4322.
12. Pinthus, JH, Waks, T, Kaufman-Francis, K, Schindler, DG, Harmelin, A, Kanety, H et al. (2003. Immuno-gene therapy of established prostate tumors using chimeric receptor-redirected human lymphocytes. Cancer Res 63: 2470-2476.
13. Maliar, A, Servais, C, Waks, T, Chmielewski, M, Lavy, R, Altevogt, P et al. (2012. Redirected T cells that target pancreatic adenocarcinoma antigens eliminate tumors and metastases in mice. Gastroenterology 143: 1375-84.e1.
14. Engels, B, Rowley, DA and Schreiber, H (2012. Targeting stroma to treat cancers. Semin Cancer Biol 22: 41-49.
15. Kochenderfer, JN, Yu, Z, Frasheri, D, Restifo, NP and Rosenberg, SA (2010. Adoptive transfer of syngeneic T cells transduced with a chimeric antigen receptor that recognizes murine CD19 can eradicate lymphoma and normal B cells. Blood 116: 3875-3886.
16. Chmielewski, M, Hahn, O, Rappl, G, Nowak, M, Schmidt-Wolf, IH, Hombach, AA et al. (2012. T cells that target carcinoembryonic antigen eradicate orthotopic pancreatic carcinomas without inducing autoimmune colitis in mice. Gastroenterology 143: 1095-107.e2.
17. Klebanoff, CA, Gattinoni, L, Palmer, DC, Muranski, P, Ji, Y, Hinrichs, CS et al. (2011. Determinants of successful CD8+ T-cell adoptive immunotherapy for large established tumors in mice. Clin Cancer Res 17: 5343-5352.
18. de Witte, MA, Bendle, GM, van den Boom, MD, Coccoris, M, Schell, TD, Tevethia, SS et al. (2008. TCR gene therapy of spontaneous prostate carcinoma requires in vivo T cell activation. J Immunol 181: 2563-2571.
19. Kohn, DB, Dotti, G, Brentjens, R, Savoldo, B, Jensen, M, Cooper, LJ et al. (2011. CARs on track in the clinic. Mol Ther 19: 432-438.
20. Willimsky, G and Blankenstein, T (2005. Sporadic immunogenic tumours avoid destruction by inducing T-cell tolerance. Nature 437: 141-146.
21. Willimsky, G and Blankenstein, T (2007. The adaptive immune response to sporadic cancer. Immunol Rev 220: 102-112.
22. Blankenstein, T (2005. The role of tumor stroma in the interaction between tumor and immune system. Curr Opin Immunol 17: 180-186.
23. Finkle, D, Quan, ZR, Asghari, V, Kloss, J, Ghaboosi, N, Mai, E et al. (2004. HER2-targeted therapy reduces incidence and progression of midlife mammary tumors in female murine mammary tumor virus huHER2-transgenic mice. Clin Cancer Res 10: 2499-2511.
24. Zhao, Y, Wang, QJ, Yang, S, Kochenderfer, JN, Zheng, Z, Zhong, X et al. (2009. A herceptin-based chimeric antigen receptor with modified signaling domains leads to enhanced survival of transduced T lymphocytes and antitumor activity. J Immunol 183: 5563-5574.
25. Proietti, E, Greco, G, Garrone, B, Baccarini, S, Mauri, C, Venditti, M et al. (1998. Importance of cyclophosphamide-induced bystander effect on T cells for a successful tumor eradication in response to adoptive immunotherapy in mice. J Clin Invest 101: 429-441.
26. Fendly, BM, Winget, M, Hudziak, RM, Lipari, MT, Napier, MA and Ullrich, A (1990. Characterization of murine monoclonal antibodies reactive to either the human epidermal growth factor receptor or HER2/neu gene product. Cancer Res 50: 1550-1558.
27. Nguyen, VH, Zeiser, R, Dasilva, DL, Chang, DS, Beilhack, A, Contag, CH et al. (2007. In vivo dynamics of regulatory T-cell trafficking and survival predict effective strategies to control graft-versus-host disease following allogeneic transplantation. Blood 109: 2649-2656.
28. Lamers, CH, Sleijfer, S, Vulto, AG, Kruit, WH, Kliffen, M, Debets, R et al. (2006. Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J Clin Oncol 24: e20-e22.
29. Morgan, RA, Chinnasamy, N, Abate-Daga, D, Gros, A, Robbins, PF, Zheng, Z et al. (2013. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother 36: 133-151.
30. Lipowska-Bhalla, G, Gilham, DE, Hawkins, RE and Rothwell, DG (2012. Targeted immunotherapy of cancer with CAR T cells: achievements and challenges. Cancer Immunol Immunother 61: 953-962.
31. Xu, XJ, Zhao, HZ and Tang, YM (2013. Efficacy and safety of adoptive immunotherapy using anti-CD19 chimeric antigen receptor transduced T-cells: a systematic review of phase I clinical trials. Leuk Lymphoma 54: 255-260.
32. Wen, FT, Thisted, RA, Rowley, DA and Schreiber, H (2012. A systematic analysis of experimental immunotherapies on tumors differing in size and duration of growth. Oncoimmunology 1: 172-178.
33. Haugsten, EM, Wiedlocha, A, Olsnes, S and Wesche, J (2010. Roles of fibroblast growth factor receptors in carcinogenesis. Mol Cancer Res 8: 1439-1452.
34. Pinthus, JH, Waks, T, Malina, V, Kaufman-Francis, K, Harmelin, A, Aizenberg, I et al. (2004. Adoptive immunotherapy of prostate cancer bone lesions using redirected effector lymphocytes. J Clin Invest 114: 1774-1781.
35. Friedmann-Morvinski, D, Bendavid, A, Waks, T, Schindler, D and Eshhar, Z (2005. Redirected primary T cells harboring a chimeric receptor require costimulation for their antigen-specific activation. Blood 105: 3087-3093.
36. Yip, YL, Smith, G, Koch, J, D?el, S and Ward, RL (2001. Identification of epitope regions recognized by tumor inhibitory and stimulatory anti-ErbB-2 monoclonal antibodies: implications for vaccine design. J Immunol 166: 5271-5278.
37. Ben-Kasus, T, Schechter, B, Lavi, S, Yarden, Y and Sela, M (2009. Persistent elimination of ErbB-2/HER2-overexpressing tumors using combinations of monoclonal antibodies: relevance of receptor endocytosis. Proc Natl Acad Sci USA 106: 3294-3299.
38. Peinert, S, Kershaw, MH and Prince, HM (2009. Chimeric T cells for adoptive immunotherapy of cancer: using what have we learned to plan for the future. Immunotherapy 1: 905-912.
39. Kershaw, MH, Teng, MW, Smyth, MJ and Darcy, PK (2005. Supernatural T cells: genetic modification of T cells for cancer therapy. Nat Rev Immunol 5: 928-940.
40. Berger, C, Jensen, MC, Lansdorp, PM, Gough, M, Elliott, C and Riddell, SR (2008. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest 118: 294-305.
41. Klebanoff, CA, Yu, Z, Hwang, LN, Palmer, DC, Gattinoni, L and Restifo, NP (2009. Programming tumor-reactive effector memory CD8+ T cells in vitro obviates the requirement for in vivo vaccination. Blood 114: 1776-1783.
42. Cruz, CR, Micklethwaite, KP, Savoldo, B, Ramos, CA, Lam, S, Ku, S et al. (2013. Infusion of donor-derived CD19-redirected virus-specific T cells for B-cell malignancies relapsed after allogeneic stem cell transplant: a phase 1 study. Blood 122: 2965-2973.
43. Marcus, A, Waks, T and Eshhar, Z (2011. Redirected tumor-specific allogeneic T cells for universal treatment of cancer. Blood 118: 975-983.
44. Morgan, RA, Yang, JC, Kitano, M, Dudley, ME, Laurencot, CM and 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.
45. Hawkins, RE, Gilham, DE, Debets, R, Eshhar, Z, Taylor, N, Abken, H et al. (2010. Development of adoptive cell therapy for cancer: a clinical perspective. Hum Gene Ther 21: 665-672.
46. Wang, LX, Westwood, JA, Moeller, M, Duong, CP, Wei, WZ, Malaterre, J et al. (2010. Tumor ablation by gene-modified T cells in the absence of autoimmunity. Cancer Res 70: 9591-9598.
47. Klapper, LN, Glathe, S, Vaisman, N, Hynes, NE, Andrews, GC, Sela, M et al. (1999. The ErbB-2/HER2 oncoprotein of human carcinomas may function solely as a shared coreceptor for multiple stroma-derived growth factors. Proc Natl Acad Sci USA 96: 4995-5000.
48. Stancovski, I, Hurwitz, E, Leitner, O, Ullrich, A, Yarden, Y and Sela, M (1991. Mechanistic aspects of the opposing effects of monoclonal antibodies to the ERBB2 receptor on tumor growth. Proc Natl Acad Sci USA 88: 8691-8695.
49. Janik, P, Briand, P and Hartmann, NR (1975. The effect of estrone-progesterone treatment on cell proliferation kinetics of hormone-dependent GR mouse mammary tumors. Cancer Res 35: 3698-3704.
50. Kaufmann, Y, Berke, G and Eshhar, Z (1981. Cytotoxic T lymphocyte hybridomas that mediate specific tumor-cell lysis in vitro. Proc Natl Acad Sci USA 78: 2502-2506