A Multidrug-resistant Engineered CAR T Cell for Allogeneic Combination Immunotherapy

Molecular Therapy

Volumn 23, Issue 9, 2015, Pages 1507-1518

  Valton, Julien ^a   Guyot, Valérie ^a   Marechal, Alan ^a   Filhol, Jean Marie ^a   Juillerat, Alexandre ^a   Duclert, Aymeric ^a   Duchateau, Philippe ^a   Poirot, Laurent ^a  

^a Arvid Wallgrens Backe 20   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; CLOFARABINE; CYTARABINE; FLUDARABINE; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA BETA CHAIN; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CD19 ANTIGEN; DEOXYCYTIDINE KINASE; HYBRID PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE TRANSFER; ALLOGENEIC COMBINATION IMMUNOTHERAPY; ALLOIMMUNITY; ARTICLE; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; DCK GENE; GENE; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MULTIDRUG RESISTANCE; T LYMPHOCYTE; TRAC GENE; ADOPTIVE IMMUNOTHERAPY; ADVERSE EFFECTS; ALLOTRANSPLANTATION; BIOLOGICAL THERAPY; CYTOTOXICITY; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION; GENE SILENCING; GENETICS; HUMAN; IC50; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MIXED LYMPHOCYTE CULTURE; MULTIMODALITY CANCER THERAPY; NEOPLASMS; PROCEDURES;

ANTIGENS, CD19; ANTINEOPLASTIC AGENTS; CELL- AND TISSUE-BASED THERAPY; COMBINED MODALITY THERAPY; CYTOTOXICITY, IMMUNOLOGIC; DEOXYCYTIDINE KINASE; DRUG RESISTANCE, MULTIPLE; GENE EXPRESSION; GENE SILENCING; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INHIBITORY CONCENTRATION 50; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 84940718499     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2015.104     Document Type: Article

References (49)

1. Marcus, A and Eshhar, Z (2014). Allogeneic chimeric antigen receptor-modified cells for adoptive cell therapy of cancer. Expert Opin Biol Ther 14: 947-954.
2. Torikai, H, Reik, A, Liu, PQ, Zhou, Y, Zhang, L, Maiti, S et al. (2012). A foundation for universal T-cell based immunotherapy: T cells engineered to express a CD19-specific chimeric-antigen-receptor and eliminate expression of endogenous TCR. Blood 119: 5697-5705.
3. Marcus, A, Waks, T and Eshhar, Z (2011). Redirected tumor-specific allogeneic T cells for universal treatment of cancer. Blood 118: 975-983.
4. Berdien, B, Mock, U, Atanackovic, D and Fehse, B (2014). TALEN-mediated editing of endogenous T-cell receptors facilitates efficient reprogramming of T lymphocytes by lentiviral gene transfer. Gene Ther 21: 539-548.
5. Benichou, G, Yamada, Y, Yun, SH, Lin, C, Fray, M and Tocco, G (2011). Immune recognition and rejection of allogeneic skin grafts. Immunotherapy 3: 757-770.
6. Jordheim, LP, Durantel, D, Zoulim, F and Dumontet, C (2013). Advances in the development of nucleoside and nucleotide analogues for cancer and viral diseases. Nat Rev Drug Discov 12: 447-464.
7. 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.
8. Maude, SL, Frey, N, Shaw, PA, Aplenc, R, Barrett, DM, Bunin, NJ et al. (2014). Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med 371: 1507-1517.
9. Kochenderfer, JN, Dudley, ME, Kassim, SH, Somerville, RP, Carpenter, RO, Stetler-Stevenson, M et al. (2015). Chemotherapy-refractory diffuse large B-cell lymphoma and indolent B-cell malignancies can be effectively treated with autologous T cells expressing an anti-CD19 chimeric antigen receptor. J Clin Oncol 33: 540-549.
10. Grupp, SA, Kalos, M, Barrett, D, Aplenc, R, Porter, DL, Rheingold, SR et al. (2013). Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368: 1509-1518.
11. 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.
12. Galetto, R, Lebuhotel, C, Poirot, L, Gouble, A, Toribio, ML, Smith, J et al. (2014). Pre-TCR? supports CD3-dependent reactivation and expansion of TCR?-deficient primary human T-cells. Mol Ther Methods Clin Dev 1: 14021.
13. Kim, Y, Kweon, J and Kim, JS (2013). TALENs and ZFNs are associated with different mutation signatures. Nat Methods 10: 185.
14. Juillerat, A, Dubois, G, Valton, J, Thomas, S, Stella, S, Maréchal, A et al. (2014). Comprehensive analysis of the specificity of transcription activator-like effector nucleases. Nucleic Acids Res 42: 5390-5402.
15. Guilinger, JP, Pattanayak, V, Reyon, D, Tsai, SQ, Sander, JD, Joung, JK et al. (2014). Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificity. Nat Methods 11: 429-435.
16. Philip, B, Kokalaki, E, Mekkaoui, L, Thomas, S, Straathof, K, Flutter, B et al. (2014). A highly compact epitope-based marker/suicide gene for easier and safer T-cell therapy. Blood 124: 1277-1287.
17. Gandhi, V, Kantarjian, H, Faderl, S, Bonate, P, Du, M, Ayres, M et al. (2003). Pharmacokinetics and pharmacodynamics of plasma clofarabine and cellular clofarabine triphosphate in patients with acute leukemias. Clin Cancer Res 9: 6335-6342.
18. Long-Boyle, JR, Green, KG, Brunstein, CG, Cao, Q, Rogosheske, J, Weisdorf, DJ et al. (2011). High fludarabine exposure and relationship with treatment-related mortality after nonmyeloablative hematopoietic cell transplantation. Bone Marrow Transplant 46: 20-26.
19. Avramis, VI, Champagne, J, Sato, J, Krailo, M, Ettinger, LJ, Poplack, DG et al. (1990). Pharmacology of fludarabine phosphate after a phase I/II trial by a loading bolus and continuous infusion in pediatric patients. Cancer Res 50: 7226-7231.
20. Zhao, Y, Moon, E, Carpenito, C, Paulos, CM, Liu, X, Brennan, AL et al. (2010). Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res 70: 9053-9061.
21. Bagley, RG, Roth, S, Kurtzberg, LS, Rouleau, C, Yao, M, Crawford, J et al. (2009). Bone marrow CFU-GM and human tumor xenograft efficacy of three antitumor nucleoside analogs. Int J Oncol 34: 1329-1340.
22. Waud, WR, Schmid, SM, Montgomery, JA and Secrist, JA 3rd (2000). Preclinical antitumor activity of 2-chloro-9-(2-deoxy-2-fluoro-beta-D-arabinofuranosyl)adenine (Cl-F-ara-A). Nucleosides Nucleotides Nucleic Acids 19: 447-460.
23. Takahashi, T, Kanazawa, J, Akinaga, S, Tamaoki, T and Okabe, M (1999). Antitumor activity of 2-chloro-9-(2-deoxy-2-fluoro-beta-D-arabinofuranosyl) adenine, a novel deoxyadenosine analog, against human colon tumor xenografts by oral administration. Cancer Chemother Pharmacol 43: 233-240.
24. Valdez, BC, Murray, D, Nieto, Y, Li, Y, Wang, G, Champlin, RE et al. (2012). Synergistic cytotoxicity of the DNA alkylating agent busulfan, nucleoside analogs and suberoylanilide hydroxamic acid in lymphoma cell lines. Leuk Lymphoma 53: 973-981.
25. Valton, J, Cabaniols, JP, Galetto, R, Delacote, F, Duhamel, M, Paris, S et al. (2014). Efficient strategies for TALEN-mediated genome editing in mammalian cell lines. Methods 69: 151-170.
26. Piganeau, M, Ghezraoui, H, De Cian, A, Guittat, L, Tomishima, M, Perrouault, L et al. (2013). Cancer translocations in human cells induced by zinc finger and TALE nucleases. Genome Res 23: 1182-1193.
27. Ghezraoui, H, Piganeau, M, Renouf, B, Renaud, JB, Sallmyr, A, Ruis, B et al. (2014). Chromosomal translocations in human cells are generated by canonical nonhomologous end-joining. Mol Cell 55: 829-842.
28. Reichard, P (1988). Interactions between deoxyribonucleotide and DNA synthesis. Annu Rev Biochem 57: 349-374.
29. Wallen, H, Thompson, JA, Reilly, JZ, Rodmyre, RM, Cao, J and Yee, C (2009). Fludarabine modulates immune response and extends in vivo survival of adoptively transferred CD8 T cells in patients with metastatic melanoma. PLoS One 4: e4749.
30. Gattinoni, L, Finkelstein, SE, Klebanoff, CA, Antony, PA, Palmer, DC, Spiess, PJ et al. (2005). Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 202: 907-912.
31. Choudhary, R, Baturin, D, Fosmire, S, Freed, B and Porter, CC (2013). Knockdown of HPRT for selection of genetically modified human hematopoietic progenitor cells. PLoS One 8: e59594.
32. Gori, JL, Tian, X, Swanson, D, Gunther, R, Shultz, LD, McIvor, RS et al. (2010). In vivo selection of human embryonic stem cell-derived cells expressing methotrexateresistant dihydrofolate reductase. Gene Ther 17: 238-249.
33. Porter, CC and DeGregori, J (2008). Interfering RNA-mediated purine analog resistance for in vitro and in vivo cell selection. Blood 112: 4466-4474.
34. Dudley, ME, Wunderlich, JR, Robbins, PF, Yang, JC, Hwu, P, Schwartzentruber, DJ et al. (2002). Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854.
35. Dudley, ME, Wunderlich, JR, Yang, JC, Sherry, RM, Topalian, SL, Restifo, NP 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.
36. Nars, MS and Kaneno, R (2013). Immunomodulatory effects of low dose chemotherapy and perspectives of its combination with immunotherapy. Int J Cancer 132: 2471-2478.
37. Takebe, N, Zhao, SC, Adhikari, D, Mineishi, S, Sadelain, M, Hilton, J et al. (2001). Generation of dual resistance to 4-hydroperoxycyclophosphamide and methotrexate by retroviral transfer of the human aldehyde dehydrogenase class 1 gene and a mutated dihydrofolate reductase gene. Mol Ther 3: 88-96.
38. Dasgupta, A, Shields, JE and Spencer, HT (2012). Treatment of a solid tumor using engineered drug-resistant immunocompetent cells and cytotoxic chemotherapy. Hum Gene Ther 23: 711-721.
39. Jonnalagadda, M, Brown, CE, Chang, WC, Ostberg, JR, Forman, SJ and Jensen, MC (2013). Engineering human T cells for resistance to methotrexate and mycophenolate mofetil as an in vivo cell selection strategy. PLoS One 8: e65519.
40. Huye, LE, Nakazawa, Y, Patel, MP, Yvon, E, Sun, J, Savoldo, B et al. (2011). Combining mTor inhibitors with rapamycin-resistant T cells: A two-pronged approach to tumor elimination. Mol Ther 19: 2239-2248.
41. Beyer, M, Kochanek, M, Darabi, K, Popov, A, Jensen, M, Endl, E et al. (2005). Reduced frequencies and suppressive function of CD4+CD25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine. Blood 106: 2018-2025.
42. Gabrilovich, DI, Ostrand-Rosenberg, S and Bronte, V (2012). Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 12: 253-268.
43. Davila, ML, Riviere, I, Wang, X, Bartido, S, Park, J, Curran, K et al. (2014). Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med 6: 224ra25.
44. Kalos, M, Levine, BL, Porter, DL, Katz, S, Grupp, SA, Bagg, A et al. (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.
45. Colovos, C, Villena-Vargas, J and Adusumilli, PS (2012). Safety and stability of retrovirally transduced chimeric antigen receptor T cells. Immunotherapy 4: 899-902.
46. Scholler, J, Brady, TL, Binder-Scholl, G, Hwang, WT, Plesa, G, Hege, KM et al. (2012). Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells. Sci Transl Med 4: 132ra53.
47. Di Stasi, A, Tey, SK, Dotti, G, Fujita, Y, Kennedy-Nasser, A, Martinez, C et al. (2011). Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med 365: 1673-1683.
48. Williams, KM, Hakim, FT and Gress, RE (2007). T cell immune reconstitution following lymphodepletion. Semin Immunol 19: 318-330.
49. Daboussi, F, Leduc, S, Maréchal, A, Dubois, G, Guyot, V, Perez-Michaut, C et al. (2014). Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nat Commun 5: 3831.