Sleeping beauty system to redirect T-cell specificity for human applications

Journal of Immunotherapy

Volumn 36, Issue 2, 2013, Pages 112-123

  Maiti, Sourindra N ^a   Huls, Helen ^a   Singh, Harjeet ^a   Dawson, Margaret ^a   Figliola, Matthew ^a   Olivares, Simon ^a   Rao, Pullavathi ^c   Zhao, Yi Jue ^c   Multani, Asha ^b   Yang, Ge ^a   Zhang, Ling ^a   Crossland, Denise ^a   Ang, Sonny ^a   Torikai, Hiroki ^a   Rabinovich, Brian ^a   Lee, Dean A ^a   Kebriaei, Partow ^a   Hackett, Perry ^e   Champlin, Richard E ^a   Cooper, Laurence J N ^a,d  

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

^b Cytogenetics Core Facility   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY OF TEXAS   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

aAPC; CD19; chimeric antigen receptor; digital mRNA profiling; Sleeping Beauty transposon and transposase; T cell adoptive immunotherapy

Indexed keywords

CD19 ANTIGEN; CD3 ANTIGEN; T LYMPHOCYTE RECEPTOR; TRANSPOSASE;

ANTIGEN PRESENTING CELL; ARTICLE; CD3+ T LYMPHOCYTE; CELL SPECIFICITY; CELL SURVIVAL; CONTROLLED STUDY; EFFECTOR CELL; ELECTROPORATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SLEEPING BEAUTY TRANSPOSON/TRANSPOSASE DNA PLASMID SYSTEM; T LYMPHOCYTE; TELOMERE; TRANSPOSON;

ANIMALS; ANTIGENS, CD19; ANTIGENS, CD3; CELL LINE, TUMOR; CELLS, CULTURED; ELECTROPORATION; GENE TRANSFER TECHNIQUES; GLIOBLASTOMA; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MICE; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES; TRANSPOSASES;

EID: 84873987094     PISSN: 15249557     EISSN: 15374513     Source Type: Journal    
DOI: 10.1097/CJI.0b013e3182811ce9     Document Type: Article

References (41)

1. Jena B, Dotti G, Cooper LJ. Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor. Blood. 2010;116:1035-1044.
2. Morgan RA, Dudley ME, Rosenberg SA. Adoptive cell therapy: genetic modification to redirect effector cell specificity. Cancer J. 2010;16:336-341.
3. Brenner MK, Heslop HE. Adoptive T cell therapy of cancer. Curr Opin Immunol. 2010;22:251-257.
4. Westwood JA, Kershaw MH. Genetic redirection of T cells for cancer therapy. J Leukoc Biol. 2010;87:791-803.
5. Pule MA, Straathof KC, Dotti G, et al. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol Ther. 2005;12: 933-941.
6. Berry LJ, Moeller M, Darcy PK. Adoptive immunotherapy for cancer: the next generation of gene-engineered immune cells. Tissue Antigen. 2009;74:277-289.
7. Park TS, Rosenberg SA, Morgan RA. Treating cancer with genetically engineered T cells. Trends Biotechnol. 2011;29: 550-557.
8. Kochenderfer JN, Wilson WH, Janik JE, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood. 2010;116:4099-4102.
9. Pule MA, Savoldo B, Myers GD, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med. 2008;14:1264-1270.
10. Porter DL, Levine BL, Kalos M, et al. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365:725-733.
11. Kalos M, Levine BL, Porter DL, 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.
12. Brentjens RJ, Riviere I, Park JH, et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood. 2011;118:4817-4828.
13. Till BG, Jensen MC, Wang J, et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood. 2008;112:2261-2271.
14. Bell JB, Podetz-Pedersen KM, Aronovich EL, et al. Preferential delivery of the Sleeping Beauty transposon system to livers of mice by hydrodynamic injection. Nat Protoc. 2007;2:3153-3165.
15. Belur LR, McIvor RS, Wilber A. Liver-directed gene therapy using the sleeping beauty transposon system. Methods Mol Biol. 2008;434:267-276.
16. Wilber A, Linehan JL, Tian X, et al. Efficient and stable transgene expression in human embryonic stem cells using transposon-mediated gene transfer. Stem Cells. 2007;25: 2919-2927.
17. Mates L, Chuah MK, Belay E, et al. Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat Genet. 2009;41: 753-761.
18. Singh H, Manuri PR, Olivares S, et al. Redirecting specificity of T-cell populations for CD19 using the Sleeping Beauty system. Cancer Res. 2008;68:2961-2971.
19. Davies JK, Singh H, Huls H, et al. Combining CD19 redirection and alloanergization to generate tumor-specific human T cells for allogeneic cell therapy of B-cell malignancies. Cancer Res. 2010;70:3915-3924.
20. Williams DA. Sleeping beauty vector system moves toward human trials in the United States. Mol Ther. 2008;16: 1515-1516.
21. Jin Z, Maiti S, Huls H, et al. The hyperactive Sleeping Beauty transposase SB100X improves the genetic modification of T cells to express a chimeric antigen receptor. Gene Ther. 2011;18:849-856.
22. Kebriaei P, Huls H, Jena B, et al. Infusing CD19-directed T cells to augment disease control in patients undergoing autologous hematopoietic stem-cell transplantation for advanced B-lymphoid malignancies. Hum Gene Ther. 2011;23:444-450.
23. Manuri PV, Wilson MH, Maiti SN, et al. piggyBac transposon/transposase system to generate CD19-specific T cells for the treatment of B-lineage malignancies. Hum Gene Ther. 2009;21:427-437.
24. O'Connor CM, Sheppard S, Hartline CA, et al. Adoptive T-cell therapy improves treatment of canine non-Hodgkin lymphoma post chemotherapy. Sci Rep. 2012;2:249.
25. Serrano LM, Pfeiffer T, Olivares S, et al. Differentiation of naive cord-blood T cells into CD19-specific cytolytic effectors for posttransplantation adoptive immunotherapy. Blood. 2006;107:2643-2652.
26. Multani AS, Ozen M, Narayan S, et al. Caspase-dependent apoptosis induced by telomere cleavage and TRF2 loss. Neoplasia. 2000;2:339-345.
27. Singh H, Figliola MJ, Dawson MJ, et al. Reprogramming CD19-specific T cells with IL-21 signaling can improve adoptive immunotherapy of B-lineage malignancies. Cancer Res. 2011;71:3516-3527.
28. Zhang M, Maiti S, Bernatchez C, et al. A new approach to simultaneously quantify both TCR a-and b-chain diversity after adoptive immunotherapy. Clin Cancer Res. 2012;18: 4733-4742.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-408.
30. Kolacsek O, Krizsik V, Schamberger A, et al. Reliable transgene-independent method for determining Sleeping Beauty transposon copy numbers. Mob DNA. 2011;2:5.
31. Peng PD, Cohen CJ, Yang S, et al. Efficient nonviral Sleeping Beauty transposon-based TCR gene transfer to peripheral blood lymphocytes confers antigen-specific antitumor reactivity. Gene Ther. 2009;16:1042-1049.
32. Huang X, Haley K, Wong M, et al. Unexpectedly high copy number of random integration but low frequency of persistent expression of the Sleeping Beauty transposase after trans delivery in primary human T cells. Hum Gene Ther. 2010;21:1577-1590.
33. Tran KQ, Zhou J, Durflinger KH, et al. Minimally cultured tumor-infiltrating lymphocytes display optimal characteristics for adoptive cell therapy. J Immunother. 2008;31: 742-751.
34. Plunkett FJ, Soares MV, Annels N, et al. The flow cytometric analysis of telomere length in antigen-specific CD8+ T cells during acute Epstein-Barr virus infection. Blood. 2001;97: 700-707.
35. Zhou J, Shen X, Huang J, et al. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol. 2005;175:7046-7052.
36. Shen X, Zhou J, Hathcock KS, et al. Persistence of tumor infiltrating lymphocytes in adoptive immunotherapy correlates with telomere length. J Immunother. 2007;30:123-129.
37. Alter BP, Baerlocher GM, Savage SA, et al. Very short telomere length by flow fluorescence in situ hybridization identifies patients with dyskeratosis congenita. Blood. 2007;110:1439-1447.
38. Huang J, Khong HT, Dudley ME, et al. Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J Immunother. 2005;28:258-267.
39. June CH, Blazar BR, Riley JL. Engineering lymphocyte subsets: tools, trials and tribulations. Nat Rev Immunol. 2009;9: 704-716.
40. Berger C, Jensen MC, Lansdorp PM, et al. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest. 2008;118:294-305.
41. Hinrichs CS, Borman ZA, Cassard L, et al. Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci USA. 2009;106:17469-17474.