Multiplex genome-edited T-cell manufacturing platform for "off-the-shelf" adoptive T-cell immunotherapies

Cancer Research

Volumn 75, Issue 18, 2015, Pages 3853-3864

  Philip, Laurent Poirot Brian ^a   Schiffer Mannioui, Cécile ^b   Le Clerre, Diane ^a   Chion Sotinel, Isabelle ^a   Derniame, Sophie ^a   Potrel, Pierrick ^a   Bas, Cécile ^a   Lemaire, Laetitia ^a   Galetto, Roman ^a   Lebuhotel, Céline ^a   Eyquem, Justin ^a,d   Cheung, Gordon Weng Kit ^b   Duclert, Aymeric ^a   Gouble, Agnès ^a   Arnould, Sylvain ^a   Peggs, Karl ^b   Pule, Martin ^b   Scharenberg, Andrew M ^c   Smith, Julianne ^a  

^a Arvid Wallgrens Backe 20   (France)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF WASHINGTON   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEMTUZUMAB; CD19 ANTIGEN; CD52 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; MESSENGER RNA; NUCLEASE; T LYMPHOCYTE RECEPTOR; GLYCOPROTEIN; HYBRID PROTEIN; LEUKOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; TUMOR ANTIGEN;

ADOPTIVE IMMUNOTHERAPY; ANIMAL EXPERIMENT; ARTICLE; AUTOTRANSPLANTATION; CANCER IMMUNOTHERAPY; CELL ENGINEERING; CONTROLLED STUDY; ELECTROPORATION; ENGRAFTMENT; GENETIC ENGINEERING; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN CELL; MOUSE; MULTIPLEX GENOME EDITING; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; ANIMAL; CYTOTOXICITY; DEFICIENCY; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE INACTIVATION; GENETIC TRANSFECTION; GENETICS; GRAFT VS HOST DISEASE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOMA; MOLECULAR GENETICS; MUTANT MOUSE STRAIN; NUCLEOTIDE SEQUENCE; TRANSPLANTATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD; ANTIGENS, CD19; ANTIGENS, NEOPLASM; BASE SEQUENCE; CYTOTOXICITY, IMMUNOLOGIC; DRUG RESISTANCE; GENE KNOCKOUT TECHNIQUES; GLYCOPROTEINS; GRAFT VS HOST DISEASE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTE ACTIVATION; LYMPHOMA; MICE; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; T-LYMPHOCYTES; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942903938     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3321     Document Type: Article

References (45)

1. Porter DL, Kalos M, Zheng Z, Levine B, June C. Chimeric antigen receptor therapy for B-cell malignancies. J Cancer 2011;2:331-2.
2. Riddell SR, Jensen MC, June CH. Chimeric antigen receptor-modified T cells: clinical translation in stem cell transplantation and beyond. Biol Blood Marrow Transplant 2013;19:S2-5.
3. Kochenderfer JN, Feldman SA, Zhao Y, Xu H, Black MA, Morgan RA, et al. Construction and preclinical evaluation of an anti-CD19 chimeric antigen receptor. J Immunother 2009;32:689-702.
4. Sadelain M. T-cell engineering for cancer immunotherapy. Cancer J 2009;15:451-5.
5. Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol 2009;21:215-23.
6. Sadelain M, Riviere I, Brentjens R. Targeting tumours with genetically enhanced T lymphocytes. Nat Rev Cancer 2003;3:35-45.
7. Berger C, Turtle CJ, Jensen MC, Riddell SR. Adoptive transfer of virus-specific and tumor-specificT cell immunity. Curr Opin Immunol 2009;21:224-32.
8. Cooper LJN, Kalos M, Di Giusto D, Brown C, Forman SJ, Raubitschek A, et al. T-cell genetic modification for re-directed tumor recognition. Cancer Chemother Biol Response Modif 2005;22:293-324.
9. June CH. Adoptive T cell therapy for cancer in the clinic. J Clin Invest 2007;117:1466-76.
10. Brenner MK, Heslop HE. Adoptive T cell therapy of cancer. Curr Opin Immunol 2010;22:251-7.
11. Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, et al. Virus-specificT cells engineered to coexpresstumor-specificreceptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 2008;14:1264-70.
12. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 2013;5:177ra38.
13. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 2011;3:95ra73.
14. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 2013;368:1509-18.
15. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011;365:725-33.
16. Kowolik CM, Topp MS, Gonzalez S, Pfeiffer T, Olivares S, Gonzalez N, etal. CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells. Cancer Res 2006;66:10995-1004.
17. Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, et al. Chimeric antigen receptorT cells for sustained remissions in leukemia. N Engl J Med 2014;371:1507-17.
18. Lee DW, Kochenderfer JN, Stetler-Stevenson M, Cui YK, Delbrook C, Feldman SA, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet 2014;385:517-28.
19. Imai C, Mihara K, Andreansky M, Nicholson IC, Pui CH, Geiger TL, et al. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004;18:676-84.
20. Kugler M, Stein C, Schwenkert M, Saul D, Vockentanz L, Huber T, et al. Stabilization and humanization of a single-chain Fv antibody fragment specific for human lymphocyte antigen CD19 by designed point mutations and CDR-grafting onto a human framework. Protein Eng Des Sel 2009;22:135-47.
21. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 2011;39:e82.
22. Doyle EL, Booher NJ, Standage DS, Voytas DF, Brendel VP, Vandyk JK, et al. TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res 2012;40:W117-122.
23. Bogdanove AJ, Voytas DF. TAL effectors: customizable proteins for DNA targeting. Science 2011;333:1843-6.
24. Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, Joung JK. FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 2012;30:460-5.
25. Joung JK, Sander JD. TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 2013;14:49-55.
26. Mussolino C, Morbitzer R, Lutge F, Dannemann N, Lahaye T, Cathomen T. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 2011;39:9283-93.
27. Hudecek M, Schmitt TM, Baskar S, Lupo-Stanghellini MT, Nishida T, Yamamoto TN, et al. The B-cell tumor-associated antigen ROR1 can be targeted with T cells modified to express a ROR1-specific chimeric antigen receptor. Blood 2010;116:4532-41.
28. Juillerat A, Dubois G, Valton J, Thomas S, Stella S, Marechal A, et al. Comprehensive analysis of the specificity of transcription activator-like effector nucleases. Nucleic Acids Res 2014;42:5390-402.
29. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, Roederer M, etal. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 2003;281:65-78.
30. Sander JD, Ramirez CL, Linder SJ, Pattanayak V, Shoresh N, Ku M, et al. In silico abstraction of zinc finger nuclease cleavage profiles reveals an expanded landscape of off-target sites. Nucleic Acids Res 2013;41:e181.
31. Pattanayak V, Lin S, Guilinger JP, Ma E, Doudna JA, Liu DR. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat Biotechnol 2013;31:839-43.
32. Cradick TJ, Fine EJ, Antico CJ, Bao G. CRISPR/Cas9 systems targeting β-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 2013;41:9584-92.
33. Ran FA, Hsu PD, Lin C-Y, Gootenberg JS, Konermann S, Trevino AE, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 2013;154:1380-9.
34. Torikai H, Reik A, Liu P-Q, Zhou Y, Zhang L, Maiti S, et al. 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 2012;119:5697-705.
35. Torikai H, Reik A, Soldner F, Warren EH, Yuen C, Zhou Y, et al. Toward eliminating HLA class I expression to generate universal cells from allogeneic donors. Blood 2013;122:1341-9.
36. Provasi E, Genovese P, Lombardo A, Magnani Z, Liu P-Q, Reik A, et al. Editing T cell specificity towards leukemia by zinc finger nucleases and lentiviral gene transfer. Nat Med 2012;18:807-15.
37. Delgado J, Pillai S, Benjamin R, Caballero D, Martino R, Nathwani A, et al. The effect of in vivo Tcell depletion with alemtuzumab on reduced-intensity allogeneic hematopoietic cell transplantation for chronic lymphocytic leukemia. Biol Blood Marrow Transplant 2008;14:1288-97.
38. Simpson D. T-cell depleting antibodies: new hope for inductionof allograft tolerance in bone marrow transplantation? BioDrugs 2003;17:147-54.
39. Bunjes D. T cell depletion of allogeneic stem cell grafts with anti-CD 52 monoclonal antibodies: the Ulm experience from 1983-1999. Transfus Sci 2000;23:151-62.
40. Morris EC, Rebello P, Thomson KJ, Peggs KS, Kyriakou C, Goldstone AH, et al. Pharmacokinetics of alemtuzumab used for in vivo and in vitro T-cell depletion in allogeneic transplantations: relevance for early adoptive immunotherapy and infectious complications. Blood 2003;102:404-6.
41. Wadhwa PD, Morrison VA. Infectious complications of chronic lympho-cytic leukemia. Semin Oncol 2006;33:240-9.
42. Kochenderfer JN, Dudley ME, Kassim SH, Somerville RPT, Carpenter RO, Stetler-Stevenson M, et al. 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 2015;33:540-9.
43. Hacke K, Szakmary A, Cuddihy AR, Rozengurt N, Lemp NA, Aubrecht J, et al. Combined preconditioning and in vivo chemoselection with 6-thioguanine alone achieves highly efficient reconstitution of normal hematopoiesis with HPRT-deficient bone marrow. Exp Hematol 2012;40:3-13.e3.
44. Nirschl CJ, Drake CG. Molecular pathways: coexpression of immune checkpoint molecules: signaling pathways and implications for cancer immunotherapy. Clin Cancer Res 2013;19:4917-24.
45. Kyi C, Postow MA. Checkpoint blocking antibodies in cancer immuno-therapy. FEBS Lett 2014;588:368-76.