Phenotypic and functional attributes of lentivirus-modified CD19-specific Human CD8+ central memory T cells manufactured at clinical scale

Journal of Immunotherapy

Volumn 35, Issue 9, 2012, Pages 689-701

  Wang, Xiuli ^a   Naranjo, Araceli ^a   Brown, Christine E ^a   Bautista, Cherrilyn ^a   Wong, Chinglam W ^a   Chang, Wen Chung ^a   Aguilar, Brenda ^a   Ostberg, Julie R ^a   Riddell, Stanley R ^b,c   Forman, Stephen J ^a   Jensen, Michael C ^a,b,d  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

cell product manufacturing; chimeric antigen receptor; T cell immunotherapy

Indexed keywords

CD19 ANTIGEN; CD8 ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 2; LENTIVIRUS VECTOR;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL GROWTH; CELL POPULATION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; ENGRAFTMENT; EX VIVO STUDY; HUMAN; HUMAN CELL; LYMPHOCYTE; LYMPHOMA; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD19; ANTIGENS, CD27; ANTIGENS, CD28; ANTIGENS, CD3; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CRYOPRESERVATION; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; GENETIC VECTORS; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOMAGNETIC SEPARATION; IMMUNOPHENOTYPING; L-SELECTIN; LENTIVIRUS; LYMPHOCYTE ACTIVATION; LYMPHOMA; MICE; MICE, INBRED NOD; MICE, SCID; PHENOTYPE; RECEPTORS, ANTIGEN, T-CELL; TRANSDUCTION, GENETIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84868221578     PISSN: 15249557     EISSN: 15374513     Source Type: Journal    
DOI: 10.1097/CJI.0b013e318270dec7     Document Type: Article

References (40)

1. Dalgleish A, Pandha H. Tumor antigens as surrogate markers and targets for therapy and vaccines. Adv Cancer Res. 2007;96:175-190.
2. Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol. 2006;90:51-81.
3. Dudley ME, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer. 2003;3:666-675.
4. Dudley ME, Wunderlich JR, Yang JC, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol. 2005;23: 2346-2357.
5. Dudley ME, Rosenberg SA. Adoptive cell transfer therapy. Semin Oncol. 2007;34:524-531.
6. Morgan RA, Dudley ME, Rosenberg SA. Adoptive cell therapy: genetic modification to redirect effector cell specificity. Cancer J. 2010;16:336-341.
7. Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol. 2009;21:215-223.
8. 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.
9. Wang X, Berger C, Wong CW, et al. Engraftment of human central memory-derived effector CD8+ T cells in immunodeficient mice. Blood. 2011;117:1888-1898.
10. Cooper LJ, Topp MS, Serrano LM, et al. T-cell clones can be rendered specific for CD19: toward the selective augmentation of the graft-versus-B- lineage leukemia effect. Blood. 2003;101: 1637-1644.
11. Pelloquin F, Lamelin JP, Lenoir GM. Human B lymphocytes immortalization by Epstein-Barr virus in the presence of cyclosporin A. In Vitro Cell Dev Biol. 1986;22:689-694.
12. Gonzalez S, Naranjo A, Serrano LM, et al. Genetic engineering of cytolytic T lymphocytes for adoptive T-cell therapy of neuroblastoma. J Gene Med. 2004;6:704-711.
13. Stastny MJ, Brown CE, Ruel C, et al. Medulloblastomas expressing IL13Ralpha2 are targets for IL13-zetakine+ cytolytic T cells. J Pediatr Hematol Oncol. 2007;29:669-677.
14. Charrier S, Stockholm D, Seye K, et al. A lentiviral vector encoding the human Wiskott-Aldrich syndrome protein corrects immune and cytoskeletal defects in WASP knockout mice. Gene Ther. 2005;12:597-606.
15. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol. 2004;22:745-763.
16. Smalley DM, Ley K. L-selectin: mechanisms and physiological significance of ectodomain cleavage. J Cell Mol Med. 2005;9:255-266.
17. Park JR, Digiusto DL, Slovak M, et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther. 2007;15: 825-833.
18. Jensen MC, Popplewell L, Cooper LJ, et al. Antitransgene rejection responses contribute to attenuated persistence of adoptively transferred CD20/CD19-specific chimeric antigen receptor redirected T cells in humans. Biol Blood Marrow Transplant. 2010;16:1245-1256.
19. 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.
20. 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.
21. Turtle CJ, Swanson HM, Fujii N, et al. A distinct subset of self-renewing human memory CD8(+) T cells survives cytotoxic chemotherapy. Immunity. 2009;31:834-844.
22. 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 (1997). 2005;28:258-267.
23. Savoldo B, Huls MH, Liu Z, et al. Autologous Epstein-Barr virus (EBV)-specific cytotoxic T cells for the treatment of persistent active EBV infection. Blood. 2002;100:4059-4066.
24. 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.
25. Gattinoni L, Lugli E, Ji Y, et al. A human memory T cell subset with stem cell-like properties. Nat Med. 2011;17: 1290-1297.
26. Klebanoff CA, Gattinoni L, Palmer DC, et al. Determinants of successful CD8+ T cell adoptive immunotherapy for large established tumors in mice. Clin Cancer Res. 2011;17:5343-5352.
27. 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.
28. 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.
29. Gattinoni L, Klebanoff CA, Palmer DC, et al. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest. 2005;115:1616-1626.
30. Kaech SM,Wherry EJ. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity. 2007;27:393-405.
31. Gattinoni L, Finkelstein SE, Klebanoff CA, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med. 2005;202:907-912.
32. Dudley ME, Yang JC, Sherry R, et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol. 2008;26:5233-5239.
33. Berger C, Flowers ME, Warren EH, et al. Analysis of transgene-specific immune responses that limit the in vivo persistence of adoptively transferred HSV-TK-modified donor T cells after allogeneic hematopoietic cell transplantation. Blood. 2006;107:2294-2302.
34. Griffioen M, van Egmond EH, Kester MG, et al. Retroviral transfer of human CD20 as a suicide gene for adoptive T-cell therapy. Haematologica. 2009;94:1316-1320.
35. Serafini M, Manganini M, Borleri G, et al. Characterization of CD20-transduced T lymphocytes as an alternative suicide gene therapy approach for the treatment of graft-versus-host disease. Hum Gene Ther. 2004;15:63-76.
36. van Meerten T, Claessen MJ, Hagenbeek A, et al. The CD20/alphaCD20 'suicide' system: novel vectors with improved safety and expression profiles and efficient elimination of CD20-transgenic T cells. Gene Ther. 2006;13:789-797.
37. Vogler I, Newrzela S, Hartmann S, et al. An improved bicistronic CD20/tCD34 vector for efficient purification and in vivo depletion of gene-modified T cells for adoptive immunotherapy. Mol Ther. 2010;18:1330-1338.
38. Tey SK, Dotti G, Rooney CM, et al. Inducible caspase 9 suicide gene to improve the safety of allodepleted T cells after haploidentical stem cell transplantation. Biol Blood Marrow Transplant. 2007;13:913-924.
39. Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med. 2011;365:1673-1683.
40. Wang X, Chang WC, Wong CW, et al. A transgene-encoded cell surface polypeptide for selection, in vivo tracking, and ablation of engineered cells. Blood. 2011;118:1255-1263.