Cord blood T cells retain early differentiation phenotype suitable for immunotherapy after TCR gene transfer to confer EBV specificity

American Journal of Transplantation

Volumn 13, Issue 1, 2013, Pages 45-55

  Frumento, G ^a,b   Zheng, Y ^b   Aubert, G ^c,d   Raeiszadeh, M ^a,b   Lansdorp, P M ^c,d,e,f   Moss, P ^b,g   Lee, S P ^b   Chen, F E ^a,b,g  

^a NHS BLOOD AND TRANSPLANT   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

^d Repeat Diagnostics Inc   (Canada)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^g UNIVERSITY HOSPITALS BIRMINGHAM NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Epstein Barr virus; gene transfer; T cell receptor; T cell therapy; T lymphocytes

Indexed keywords

T LYMPHOCYTE RECEPTOR;

ADOPTIVE TRANSFER; ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; EPSTEIN BARR VIRUS; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MELANOMA; POSTTRANSPLANT LYMPHOPROLIFERATIVE DISEASE; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; UMBILICAL CORD BLOOD;

CELL DIFFERENTIATION; CYTOKINES; FETAL BLOOD; FLOW CYTOMETRY; GENE TRANSFER TECHNIQUES; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84871719817     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2012.04286.x     Document Type: Article

References (56)

1. Manlhiot C, Pollock-Barziv SM, Holmes C, et al.. Past-transplant lymphoproliferative disorder in pediatric heart transplant recipients. J Heart Lung Transplant 2010; 29: 648-657.
2. Haque T, Wilkie GM, Jones MM, et al.. Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: Results of a phase 2 multicenter clinical trial. Blood 2007; 110: 1123-1131.
3. Barker JN, Doubrovina E, Sauter C, et al.. Successful treatment of EBV-associated posttransplantation lymphoma after cord blood transplantation using third-party EBV-specific cytotoxic T lymphocytes. Blood 2010; 116: 5045-5049.
4. Heslop HE, Slobod KS, Pule MA, et al.. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 2010; 115: 925-935.
5. Micklethwaite KP, Savoldo B, Hanley PJ, et al.. Derivation of human T lymphocytes from cord blood and peripheral blood with antiviral and antileukemic specificity from a single culture as protection against infection and relapse after stem cell transplantation. Blood 2010; 115: 2695-2703.
6. Gattinoni L, Powell DJ, Jr., Rosenberg SA, Restifo NP,. Adoptive immunotherapy for cancer: building on success. Nat Rev Immunol 2006; 6: 383-93.
7. Rosenberg SA, Yang JC, Sherry RM, et al.. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011; 17: 4550-4557.
8. Gilboa E,. The makings of a tumor rejection antigen. Immunity 1999; 11: 263-270.
9. Goodyear O, Piper K, Khan N, et al.. CD8+ T cells specific for cancer germline gene antigens are found in many patients with multiple myeloma, and their frequency correlates with disease burden. Blood 2005; 106: 4217-4224.
10. Stauss HJ, Thomas S, Cesco-Gaspere M, et al.. WT1-specific T cell receptor gene therapy: improving TCR function in transduced T cells. Blood Cells Mol Dis 2008; 40: 113-116.
11. Robbins PF, Morgan RA, Feldman SA, et al.. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 2011; 29: 917-924.
12. Morgan RA, Dudley ME, Wunderlich JR, et al.. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006; 314: 126-129.
13. 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: 725-733.
14. Robbins PF, Dudley ME, Wunderlich J, et al.. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J Immunol 2004; 173: 7125-7130.
15. 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.
16. Zhou J, Dudley ME, Rosenberg SA, Robbins PF,. Persistence of multiple tumor-specific T-cell clones is associated with complete tumor regression in a melanoma patient receiving adoptive cell transfer therapy. J Immunother 2005; 28: 53-62.
17. 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.
18. Klebanoff CA, Gattinoni L, Torabi-Parizi P, et al.. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci USA 2005; 102: 9571-9576.
19. Berger C, Jensen MC, Lansdorp PM, Gough M, Elliott C, Riddell SR,. 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.
20. 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.
21. Hinrichs CS, Borman ZA, Gattinoni L, et al.. Human effector CD8+ T cells derived from naive rather than memory subsets possess superior traits for adoptive immunotherapy. Blood 2010; 117: 808-814.
22. Dietz AB, Bulur PA, Emery RL, et al.. A novel source of viable peripheral blood mononuclear cells from leukoreduction system chambers. Transfusion 2006; 46: 2083-2089.
23. Jonuleit H, Kuhn U, Muller G, et al.. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 1997; 27: 3135-3142.
24. Lee SP, Tierney RJ, Thomas WA, Brooks JM, Rickinson AB,. Conserved CTL epitopes within EBV latent membrane protein 2: A potential target for CTL-based tumor therapy. J Immunol 1997; 158: 3325-3334.
25. Engels B, Cam H, Schuler T, et al.. Retroviral vectors for high-level transgene expression in T lymphocytes. Human Gene Therapy 2003; 14: 1155-1168.
26. Kinsella TM, Nolan GP,. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Human Gene Therapy 1996; 7: 1405-1413.
27. Moore A, Donahue CJ, Bauer KD, Mather JP,. Simultaneous measurement of cell cycle and apoptotic cell death. Methods Cell Biol 1998; 57: 265-278.
28. Masucci MG, Zhang QJ, Gavioli R, et al.. Immune escape by Epstein-Barr virus (EBV) carrying Burkitts lymphoma-in vitro reconstitution of sensitivity to EBV-specific cytotoxic T-cells. Int Immunol 1992; 4: 1283-1292.
29. Gavioli R, Kurilla MG, de Campos-Lima PO, et al.. Multiple HLA A11-restricted cytotoxic T-lymphocyte epitopes of different immunogenicities in the Epstein-Barr virus-encoded nuclear antigen 4. J Virol 1993; 67: 1572-1578.
30. Cerottini JC, Brunner, KT,. In vitro assay of target cell lysis by sensitized lymphocytes. In:, Bloom BR, Glade PR, eds. In Vitro Methods in Cell-Mediated Immunity. New York: Academic Press Inc., 1971, p. 369.
31. Baerlocher GM, Vulto I, de Jong G, Lansdorp PM,. Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat Protoc 2006; 1: 2365-2376.
32. Brenchley JM, Karandikar NJ, Betts MR, et al.. Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8 +T cells. Blood 2003; 101: 2711-2720.
33. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR,. Multiple-cytokine-producing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J Virol 2007; 81: 8468-8476.
34. Darrah PA, Patel DT, De Luca PM, et al.. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 2007; 13: 843-850.
35. Wherry EJ, Teichgraber V, Becker TC, et al.. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003; 4: 225-234.
36. Scheinberg P, Melenhorst JJ, Brenchley JM, et al.. The transfer of adaptive immunity to CMV during hematopoietic stem cell transplantation is dependent on the specificity and phenotype of CMV-specific T cells in the donor. Blood 2009; 114: 5071-5080.
37. Johnson LA, Morgan RA, Dudley ME, et al.. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009; 114: 535-546.
38. Kuball J, Schmitz FW, Voss RH, et al.. Cooperation of human tumor-reactive CD4+ and CD8+ T cells after redirection of their specificity by a high-affinity p53A2.1-specific TCR. Immunity 2005; 22: 117-129.
39. Frankel TL, Burns WR, Peng PD, et al.. Both CD4 and CD8 T cells mediate equally effective in vivo tumor treatment when engineered with a highly avid TCR targeting tyrosinase. J Immunol 2010; 184: 5988-5998.
40. Weng NP,. Telomeres and immune competency. Curr Opin Immunol 2012; 24: 470-475.
41. Rufer N, Brummendorf TH, Kolvraa S, et al.. Telomere fluorescence measurements in granulocytes and T lymphocyte subsets point to a high turnover of hematopoietic stem cells and memory T cells in early childhood. J Exp Med 1999; 190: 157-167.
42. Son NH, Murray S, Yanovski J, Hodes RJ, Weng N,. Lineage-specific telomere shortening and unaltered capacity for telomerase expression in human T and B lymphocytes with age. J Immunol 2000; 165: 1191-1196.
43. Aubert G, Baerlocher GM, Vulto I, Poon SS, Lansdorp PM,. Collapse of telomere homeostasis in hematopoietic cells caused by heterozygous mutations in telomerase genes. PLoS Genet 2012; 8: e1002696.
44. Wang JC, Warner JK, Erdmann N, Lansdorp PM, Harrington L, Dick JE,. Dissociation of telomerase activity and telomere length maintenance in primitive human hematopoietic cells. Proc Natl Acad Sci USA 2005; 102: 14398-14403.
45. Aubert G, Lansdorp PM,. Telomeres and aging. Physiol Rev 2008; 88: 557-579.
46. Shore D, Bianchi A,. Telomere length regulation: Coupling DNA end processing to feedback regulation of telomerase. EMBO J 2009; 28: 2309-2322.
47. El Ghalbzouri A, Drenou B, Blancheteau V, et al.. An in vitro model of allogeneic stimulation of cord blood: Induction of Fas independent apoptosis. Hum Immunol 1999; 60: 598-607.
48. Hagihara M, Chargui J, Gansuvd B, et al.. Umbilical cord blood T lymphocytes are induced to apoptosis after being allo-primed in vitro. Bone Marrow Transplant 1999; 24: 1229-1233.
49. Mold JE, Venkatasubrahmanyam S, Burt TD, et al.. Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science 2010; 330: 1695-1699.
50. Schottker B, Feuchtinger T, Schumm M, et al.. Five donors-one recipient: Modeling a mosaic of granulocytes, natural killer and T cells from cord-blood and third-party donors. Nat Clin Pract Oncol 2008; 5: 291-295.
51. Chen IH, Lai YL, Wu CL, et al.. Immune impairment in patients with terminal cancers: influence of cancer treatments and cytomegalovirus infection. Cancer Immunol Immunother 2010; 59: 323-334.
52. Mackall CL, Gress RE,. Thymic aging and T-cell regeneration. Immunol Rev 1997; 160: 91-102.
53. Rocha V, Wagner JE Jr., Sobocinski KA, et al.. Graft-versus-host disease in children who have received a cord-blood or bone marrow transplant from an HLA-identical sibling. Eurocord and International Bone Marrow Transplant Registry Working Committee on Alternative Donor and Stem Cell Sources. N Engl J Med 2000; 342: 1846-1854.
54. MacMillan ML, Weisdorf DJ, Brunstein CG, et al.. Acute graft-versus-host disease after unrelated donor umbilical cord blood transplantation: Analysis of risk factors. Blood 2009; 113: 2410-2415.
55. Taylor DK, Neujahr D, Turka LA,. Heterologous immunity and homeostatic proliferation as barriers to tolerance. Curr Opin Immunol 2004; 16: 558-564.
56. Burrows SR, Khanna R, Burrows JM, Moss DJ,. An alloresponse in humans is dominated by cytotoxic T lymphocytes (CTL) cross-reactive with a single Epstein-Barr virus CTL epitope: Implications for graft-versus-host disease. J Exp Med 1994; 179: 1155-1161.