Adoptive T-cell immunotherapy from third-party donors: Characterization of donors and set up of a T-cell donor registry

Frontiers in Immunology

Volumn 3, Issue JAN, 2012, Pages

  Eiz Vesper, Britta ^a   Maecker Kolhoff, Britta ^a   Blasczyk, Rainer ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Adenovirus; Adoptive immunotherapy; Antiviral T lymphocytes; Cytomegalovirus; Epstein Barr virus; T cell therapy

Indexed keywords

EID: 84874263127     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00410     Document Type: Review

References (105)

1. Amir, A., Shapiro, R., Shulman, L. M., Mor, E., Steinberg, R., Fleishhacker, H., et al. (2011). BK virus infection and its effect on renal function in pediatric liver-transplant recipients: a cross-sectional, longitudinal, prospective study. Transplantation 92, 943-946.
2. Amir, A. L., D'Orsogna, L. J., Roelen, D. L., van Loenen, M. M., Hagedoorn, R. S., de Boer, R., et al. (2010). Allo-HLA reactivity of virus-specific memory T cells is common. Blood 115,3146-3157.
3. Barker, J. N., Doubrovina, E., Sauter, C., Jaroscak, J. J., Perales, M. A., Doubrovin, M., et al. (2010). Successful treatment of EBV-associated posttransplantation lymphoma after cord blood transplantation using third-party EBV-specific cytotoxic T lymphocytes. Blood 116, 5045-5049.
4. Battiwalla, M., Paplham, P., Almyroudis, N. G., McCarthy, A., Abdelhalim, A., Elefante, A., et al. (2007). Leflunomide failure to control recurrent cytomegalovirus infection in the setting of renal failure after allogeneic stem cell transplantation. Transpl. Infect. Dis. 9, 28-32.
5. Berger, C., Jensen, M. C., Lansdorp, P. M., Gough, M., Elliott, C., and Riddell, S. R. (2008). Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 118, 294-305.
6. Berger, C., Turtle, C. J., Jensen, M. C., and Riddell, S. R. (2009). Adoptive transfer of virus-specific and tumor-specific T cell immunity. Curr. Opin. Immunol. 21, 224-232.
7. Boeckh, M., and Ljungman, P. (2009). How we treat cytomegalovirus in hematopoietic cell transplant recipients. Blood 113,5711-5719.
8. Bollard, C. M., Rooney, C. M., and Heslop, H. E. (2012). T-cell therapy in the treatment of post-transplant lymphoproliferative disease. Nat. Rev. Clin. Oncol. 9,510-519.
9. Borchers, S., Luther, S., Lips, U., Hahn, N., Kontsendorn, J., Stadler, M., et al. (2011). Tetramer monitoring to assess risk factors for recurrent cytomegalovirus reactivation and reconstitution of antiviral immunity post allogeneic hematopoietic stem cell transplantation. Transpl. Infect. Dis. 13, 222-236.
10. Brestrich, G., Zwinger, S., Fischer, A., Schmuck, M., Rohmhild, A., Hammer, M. H., et al. (2009). Adoptive T-cell therapy of a lung transplanted patient with severe CMV disease and resistance to antiviral therapy. Am. J. Transplant. 9, 1679-1684.
11. Breuer, S., Rauch, M., Matthes-Martin, S., and Lion, T. (2012). Molecular diagnosis and management of viral infections in hematopoietic stem cell transplant recipients. Mol. Diagn. Ther. 16, 63-77.
12. Broers, A. E., van Der Holt, R., van Esser, J. W., Gratama, J. W., Henzen-Logmans, S., Kuenen-Boumeester, V., et al. (2000). Increased transplant-related morbidity and mortality in CMV-seropositive patients despite highly effective prevention of CMV disease after allogeneic T-cell-depleted stem cell transplantation. Blood 95, 2240-2245.
13. Bruno, B., Gooley, T., Hackman, R. C., Davis, C., Corey, L., and Boeckh, M. (2003). Adenovirus infection in hematopoietic stem cell transplantation: effect of ganciclovir and impact on survival. Biol. Blood Marrow Transplant. 9, 341-352.
14. Carlsson, B., Cheng, W. S., Totterman, T. H., and Essand, M. (2003). Ex vivo stimulation of cytomegalovirus (CMV)-specific T cells using CMV pp65-modified dendritic cells as stimulators. Br. J. Haematol. 121, 428-438.
15. Casalegno-Garduno, R., Schmitt, A., Yao, J., Wang, X., Xu, X., Freund, M., et al. (2010). Multimer technologies for detection and adoptive transfer of antigen-specific T cells. Cancer Immunol. Immunother. 59, 195-202.
16. Chakrabarti, S., Mautner, V., Osman, H., Collingham, K. E., Fegan, C. D., Klapper, P. E., et al. (2002). Adenovirus infections following allogeneic stem cell transplantation: incidence and outcome in relation to graft manipulation, immuno-suppression, and immune recovery. Blood 100, 1619-1627.
17. Choi, S. J., Lee, J. H., Lee, J. H., Kim, S., Lee, Y. S., Seol, M., et al. (2005). Treatment of relapsed acute lym-phoblastic leukemia after allogeneic bone marrow transplantation with chemotherapy followed by G-CSF-primed donor leukocyte infusion: a prospective study. Bone Marrow Transplant. 36, 163-169.
18. Cobbold, M., Khan, N., Pourgheysari, B., Tauro, S., McDonald, D., Osman, H., et al. (2005). Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J. Exp. Med. 202, 379-386.
19. Cohen, J. I. (2000). Epstein-Barr virus infection. N. Engl. J. Med. 343, 481-492.
20. Collins, R. H. Jr., Goldstein, S., Giralt, S., Levine, J., Porter, D., Drobyski, W., et al. (2000). Donor leukocyte infusions in acute lymphocytic leukemia. Bone Marrow Transplant. 26,511-516.
21. Cox, J. H., Ferrari, G., and Janetzki, S. (2006). Measurement of cytokine release at the single cell level using the ELISPOT assay. Methods 38, 274-282.
22. Cwynarski, K., Ainsworth, J., Cobbold, M., Wagner, S., Mahendra, P., Apperley, J., et al. (2001). Direct visualization of cytomegalovirus-specific T-cell reconstitution after allogeneic stem cell transplantation. Blood 97, 1232-1240.
23. D'Orsogna, L. J., Roelen, D. L., Doxiadis, I. I., and Claas, F. H. (2010). Alloreactivity from human viral specific memory T-cells. Transpl. Immunol. 23, 149-155.
24. Doubrovina, E., Oflaz-Sozmen, B., Prockop, S. E., Kernan, N. A., Abramson, S., Teruya-Feldstein, J., et al. (2012). Adoptive immunother-apy with unselected or EBV-specific T cells for biopsy-proven EBV+ lymphomas after allogeneic hematopoietic cell transplantation. Blood 119,2644-2656.
25. Ebner, K., Suda, M., Watzinger, F., and Lion, T. (2005). Molecular detection and quantitative analysis of the entire spectrum of human aden-oviruses by a two-reaction real-time PCR assay. J. Clin. Microbiol. 43, 3049-3053.
26. Einsele, H., Hebart, H., Kauffmann-Schneider, C., Sinzger, C., Jahn, G., Bader, P., et al. (2000). Risk factors for treatment failures in patients receiving PCR-based preemptive therapy for CMV infection. Bone Marrow Transplant. 25, 757-763.
27. Einsele, H., Kapp, M., and Grigoleit, G. U. (2008). CMV-specific T cell therapy. Blood Cells Mol. Dis. 40, 71-75.
28. Elkington, R., Walker, S., Crough, T., Menzies, M., Tellam, J., Bharadwaj, M., et al. (2003). Ex vivo profiling of CD8+-T-cell responses to human cytomegalovirus reveals broad and multispecific reactivities in healthy virus carriers. J. Virol. 77, 5226-5240.
29. Feuchtinger, T., Lucke, J., Hamprecht, K., Richard, C., Handgretinger, R., Schumm, M., et al. (2005). Detection of adenovirus-specific T cells in children with adenovirus infection after allogeneic stem cell transplantation. Br. J. Haematol. 128, 503-509.
30. Feuchtinger, T., Matthes-Martin, S., Richard, C., Lion, T., Fuhrer, M., Hamprecht, K., et al. (2006). Safe adoptive transfer of virus-specific T-cell immunity for the treatment of systemic adenovirus infection after allogeneic stem cell transplantation. Br. J. Haematol. 134, 64-76.
31. Feuchtinger, T., Opherk, K., Bethge, W. A., Topp, M. S., Schuster, F. R., Weissinger, E. M., et al. (2010). Adoptive transfer of pp65-specific T cells for the treatment of chemore-fractory cytomegalovirus disease or reactivation after haploidenti-cal and matched unrelated stem cell transplantation. Blood 116, 4360-4367.
32. Feuchtinger, T., Richard, C., Joachim, S., Scheible, M. H., Schumm, M., Hamprecht, K., et al. (2008). Clinical grade generation of hexon-specific T cells for adoptive T-cell transfer as a treatment of adenovirus infection after allogeneic stem cell transplantation. J. Immunother. 31, 199-206.
33. Fowler, C. J., Dunlap, J., Troyer, D., Stenzel, P., Epner, E., and Maziarz, R. T. (2010). Life-threatening adenovirus infections in the setting of the immunocompromised allogeneic stem cell transplant patients. Adv. Hematol. 2010:601548. doi: 10.1155/2010/601548
34. Franzke, A., Piao, W., Lauber, J., Gatzlaff, P., Konecke, C., Hansen, W., et al. (2003). G-CSF as immune regulator in T cells expressing the G-CSF receptor: implications for transplantation and autoimmune diseases. Blood 102, 734-739.
35. Fuji, S., Kapp, M., Grigoleit, G. U., and Einsele, H. (2011). Adoptive immunotherapy with virus-specific T cells. Best Pract. Res. Clin. Haematol. 24, 413-419.
36. Fujita, Y., Leen, A. M., Sun, J., Nakazawa, Y., Yvon, E., Heslop, H. E., et al. (2008a). Exploiting cytokine secretion to rapidly produce multivirus-specific T cells for adoptive immunotherapy. J. Immunother. 31, 665-674.
37. Fujita, Y., Rooney, C. M., and Heslop, H. E. (2008b). Adoptive cellular immunotherapy for viral diseases. Bone Marrow Transplant. 41, 193-198.
38. Garcia-Vidal, C., Upton, A., Kirby, K. A., and Marr, K. A. (2008). Epidemiology of invasive mold infections in allogeneic stem cell transplant recipients: biological risk factors for infection according to time after transplantation. Clin. Infect. Dis. 47, 1041-1050.
39. Gerdemann, U., Katari, U., Christin, A. S., Cruz, C. R., Tripic, T., Rousseau, A., et al. (2012). Cytotoxic T lymphocytes simultaneously targeting multiple tumor-associated antigens to treat EBV negative lymphoma. Mol. Ther. 19, 2258-2268.
40. Gooley, T. A., Chien, J. W., Pergam, S. A., Hingorani, S., Sorror, M. L., Boeckh, M., et al. (2010). Reduced mortality after allogeneic hematopoietic-cell transplantation. N. Engl. J. Med. 363, 2091-2101.
41. Gottschalk, S., Rooney, C. M., and Heslop, H. E. (2005). Post-transplant lymphoproliferative disorders. Annu. Rev. Med. 56, 29-44.
42. Greenberg, P. D., Reusser, P., Goodrich, J. M., and Riddell, S. R. (1991). Development of a treatment regimen for human cytomegalovirus (CMV) infection in bone marrow transplantation recipients by adoptive transfer of donor-derived CMV-specific T cell clones expanded in vitro. Ann. N.Y. Acad. Sci. 636, 184-195.
43. Guppy, A. E., Rawlings, E., Madrigal, J. A., Amlot, P. L., and Barber, L. D. (2007). A quantitative assay for Epstein-Barr Virus-specific immunity shows interferon-gamma producing CD8+ T cells increase during immunosuppression reduction to treat posttransplant lymphoproliferative disease. Transplantation 84, 1534-1539.
44. Hadrup, S. R., and Schumacher, T. N. (2010). MHC-based detection of antigen-specific CD8+ T cell responses. Cancer Immunol. Immunother. 59, 1425-1433.
45. Haque, T., McAulay, K. A., Kelly, D., and Crawford, D. H. (2010). Allogeneic T-cell therapy for Epstein-Barr virus-positive post-transplant lymphoproliferative disease: long-term follow-up. Transplantation 90, 93-94.
46. Haque, T., Wilkie, G. M., Jones, M. M., Higgins, C. D., Urquhart, G., Wingate, P., et al. (2007). Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood 110, 1123-1131.
47. Haque, T., Wilkie, G. M., Taylor, C., Amlot, P. L., Murad, P., Iley, A., et al. (2002). Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 360, 436-442.
48. Heslop, H. E., Slobod, K. S., Pule, M. A., Hale, G. A., Rousseau, A., Smith, C. A., et al. (2010). Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 115, 925-935.
49. Hoffman, J. A. (2009). Adenovirus infections in solid organ transplant recipients. Curr. Opin. Organ Transplant. 14, 625-633.
50. Houssaint, E., Saulquin, X., Scotet, E., and Bonneville, M. (2001). Immunodominant CD8 T cell response to Epstein-Barr virus. Biomed. Pharmacother. 55, 373-380.
51. Khan, N. (2007). The immunological burden of human cytomegalovirus infection. Arch. Immunol. Ther. Exp. (Warsz) 55, 299-308.
52. Khanna, N., Stuehler, C., Conrad, B., Lurati, S., Krappmann, S., Einsele, H., et al. (2011). Generation of a multipathogen-specific T-cell product for adoptive immunotherapy based on activation-dependent expression of CD154. Blood 118, 1121-1131.
53. Knabel, M., Franz, T. J., Schiemann, M., Wulf, A., Villmow, B., Schmidt, B., et al. (2002). Reversible MHC mul-timer staining for functional isolation of T-cell populations and effective adoptive transfer. Nat. Med. 8, 631-637.
54. Kuehnle, I., Huls, M. H., Liu, Z., Semmelmann, M., Krance, R. A., Brenner, M. K., et al. (2000). CD20 monoclonal antibody (ritux-imab) for therapy of Epstein-Barr virus lymphoma after hemopoietic stem-cell transplantation. Blood 95, 1502-1505.
55. Landgren, O., Gilbert, E. S., Rizzo, J. D., Socie, G., Banks, P. M., Sobocinski, K. A., et al. (2009). Risk factors for lymphoproliferative disorders after allogeneic hematopoi-etic cell transplantation. Blood 113, 4992-5001.
56. Lankester, A. C., Heemskerk, B., Claas, E. C., Schilham, M. W., Beersma, M. F., Bredius, R. G., et al. (2004). Effect of ribavirin on the plasma viral DNA load in patients with disseminating adenovirus infection. Clin. Infect. Dis. 38, 1521-1525.
57. Leen, A. M., Christin, A., Khalil, M., Weiss, H., Gee, A. P., Brenner, M. K., et al. (2008). Identification of hexon-specific CD4 and CD8 T-cell epitopes for vaccine and immunotherapy. J. Virol. 82, 546-554.
58. Leen, A. M., Myers, G. D., Sili, U., Huls, M. H., Weiss, H., Leung, K. S., et al. (2006). Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat. Med. 12, 1160-1166.
59. Lilleri, D., Fornara, C., Chiesa, A., Caldera, D., Alessandrino, E. P., and Gerna, G. (2008). Human cytomegalovirus-specific CD4+ and CD8+ T-cell reconstitution in adult allogeneic hematopoietic stem cell transplant recipients and immune control of viral infection. Haematologica 93, 248-256.
60. Lilleri, D., Gerna, G., Zelini, P., Chiesa, A., Rognoni, V., Mastronuzzi, A., et al. (2012). Monitoring of human cytomegalovirus and virus-specific T-cell response in young patients receiving allogeneic hematopoietic stem cell transplantation. PLoS ONE 7:e41648. doi: 10.1371/journal.pone.0041648
61. Lindemans, C. A., Leen, A. M., and Boelens, J. J. (2010). How I treat adenovirus in hematopoietic stem cell transplant recipients. Blood 116, 5476-5485.
62. Lion, T., Baumgartinger, R., Watzinger, E, Matthes-Martin, S., Suda, M., Preuner, S., et al. (2003). Molecular monitoring of adenovirus in peripheral blood after allogeneic bone marrow transplantation permits early diagnosis of disseminated disease. Blood 102, 1114-1120.
63. Ljungman, P., Bregni, M., Brune, M., Cornelissen, J., de Witte, T., Dini, G., et al. (2010). Allogeneic and autologous transplantation for haematological diseases, solid tumours and immune disorders: current practice in Europe 2009. Bone Marrow Transplant. 45, 219-234.
64. Lozza, L., Lilleri, D., Percivalle, E., Fornara, C., Comolli, G., Revello, M. G., et al. (2005). Simultaneous quantification of human cytomegalovirus (HCMV)-specific CD4+ and CD8+ T cells by a novel method using monocyte-derived HCMV-infected immature dendritic cells. Eur. J. Immunol. 35, 1795-1804.
65. Mackinnon, S., Thomson, K., Verfuerth, S., Peggs, K., and Lowdell, M. (2008). Adoptive cellular therapy for cytomegalovirus infection following allogeneic stem cell transplantation using virus-specific T cells. Blood Cells Mol. Dis. 40, 63-67.
66. Marr, K. A., Carter, R. A., Crippa, F., Wald, A., and Corey, L. (2002). Epidemiology and outcome of mould infections in hematopoietic stem cell transplant recipients. Clin. Infect. Dis. 34,909-917.
67. Meij, P., van Esser, J. W., Niesters, H. G., van Baarle, D., Miedema, F., Blake, N., et al. (2003). Impaired recovery of Epstein-Barr virus (EBV) -specific CD8+ T lymphocytes after partially T-depleted allogeneic stem cell transplantation may identify patients at very high risk for progressive EBV reactivation and lymphoproliferative disease. Blood 101,4290-4297.
68. Moosmann, A., Bigalke, I., Tischer, J., Schirrmann, L., Kasten, J., Tippmer, S., et al. (2010). Effective and long-term control of EBV PTLD after transfer of peptide-selected T cells. Blood 115,2960-2970.
69. Mori, T., Okamoto, S., Matsuoka, S., Yajima, T., Wakui, M., Watanabe, R., et al. (2000). Risk-adapted pre-emptive therapy for cytomegalovirus disease in patients undergoing allogeneic bone marrow transplantation. Bone Marrow Transplant. 25, 765-769.
70. Oelke, M., Maus, M. V., Didiano, D., June, C. H., Mackensen, A., and Schneck, J. P. (2003). Ex vivo induction and expansion of antigen-specific cytotoxic T cells by HLA-Ig-coated artificial antigen-presenting cells. Nat. Med. 9, 619-624.
71. Olagne, J., Caillard, S., Gaub, M. P., Chenard, M. P., and Moulin, B. (2011). Post-transplant lymphoproliferative disorders: determination of donor/recipient origin in a large cohort of kidney recipients. Am. J. Transplant. 11, 1260-1269.
72. Paine, A., Oelke, M., Blasczyk, R., and Eiz-Vesper, B. (2007). Expansion of human cytomegalovirus-specific T lymphocytes from unfraction-ated peripheral blood mononu-clear cells with artificial antigen-presenting cells. Transfusion 47, 2143-2152.
73. Paine, A., Oelke, M., Tischer, S., Heuft, H. G., Blasczyk, R., and Eiz-Vesper, B. (2010). Soluble recombinant CMVpp65 spanning multiple HLA alleles for reconstitution of antiviral CD4+ and CD8+ T-cell responses after allogeneic stem cell transplantation. J. Immunother. 33, 60-72.
74. Pappas, P. G., Alexander, B. D., Andes, D. R., Hadley, S., Kauffman, C. A., Freifeld, A., et al. (2010). Invasive fungal infections among organ transplant recipients: results of the Transplant-Associated Infection Surveillance Network (TRANSNET). Clin. Infect. Dis. 50, 1101-1111.
75. Peggs, K. S., Thomson, K., Samuel, E., Dyer, G., Armoogum, J., Chakraverty, R., et al. (2011). Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stem cell transplantation. Clin. Infect. Dis. 52, 49-57.
76. Peggs, K., Verfuerth, S., and Mackinnon, S. (2001). Induction of cytomegalovirus (CMV)-specific T-cell responses using dendritic cells pulsed with CMV antigen: a novel culture system free of live CMV virions. Blood 97, 994-1000.
77. Pidala, J., Tomblyn, M., Nishihori, T., Ayala, E., Field, T., Fernandez, H., et al. (2011). ATG prevents severe acute graft-versus-host disease in mismatched unrelated donor hematopoietic cell transplantation. Biol. Blood Marrow Transplant. 17, 1237-1244.
78. Qasim, W., Derniame, S., Gilmour, K., Chiesa, R., Weber, M., Adams, S., et al. (2011). Third-party virus-specific T cells eradicate adenovi-raemia but trigger bystander graft-versus-host disease. Br. J. Haematol. 154, 150-153.
79. Rauser, G., Einsele, H., Sinzger, C., Wernet, D., Kuntz, G., Assenmacher, M., et al. (2004). Rapid generation of combined CMV-specific CD4+ and CD8+ T-cell lines for adoptive transfer into recipients of allo-geneic stem cell transplants. Blood 103,3565-3572.
80. Rentenaar, R. J., Gamadia, L. E., van DerHoek, N., van Diepen, F. N., Boom, R., Weel, J. F., et al. (2000). Development of virus-specific CD4(+) T cells during primary cytomegalovirus infection. J. Clin. Invest. 105, 541-548.
81. Riddell, S. R., Reusser, P., and Greenberg, P. D. (1991). Cytotoxic T cells specific for cytomegalovirus: a potential therapy for immuno-compromised patients. Rev. Infect. Dis. 13(Suppl. 11), S966-S973.
82. Runde, V., Ross, S., Trenschel, R., Lagemann, E., Basu, O., Renzing-Kohler, K., et al. (2001). Adenoviral infection after allogeneic stem cell transplantation (SCT): report on 130 patients from a single SCT unit involved in a prospective multi center surveillance study. Bone Marrow Transplant. 28, 51-57.
83. Sallusto, F., Geginat, J., and Lanzavecchia, A. (2004). Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22,745-763.
84. Schmitt, A., Tonn, T., Busch, D. H., Grigoleit, G. U., Einsele, H., Odendahl, M., et al. (2011). Adoptive transfer and selective reconstitution of streptamer-selected cytomegalovirus-specific CD8+ T cells leads to virus clearance in patients after allogeneic peripheral blood stem cell transplantation. Transfusion 51, 591-599.
85. Schottker, B., Feuchtinger, T., Schumm, M., Klinker, E., Handgretinger, R., Einsele, H., et al. (2008). 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. 5,291-295.
86. Shen, Q., Feng, W., Long, M. S., Duan, X., Jaijakul, S., Arias, C. A., et al. (2011). Multicentric hepatic EBV-associated smooth muscle tumors in an AIDS patient: a case report, investigation of mTOR activation and review of the literature. Int. J. Clin. Exp. Pathol. 4, 421-429.
87. Solache, A., Morgan, C. L., Dodi, A. I., Morte, C., Scott, I., Baboonian, C., et al. (1999). Identification of three HLA-A*0201-restricted cytotoxic T cell epitopes in the cytomegalovirus protein pp65 that are conserved between eight strains of the virus.J. Immunol. 163, 5512-5518.
88. Sun, Q., Pollok, K. E., Burton, R. L., Dai, L. J., Britt, W., Emanuel, D. J., et al. (1999). Simultaneous ex vivo expansion of cytomegalovirus and Epstein-Barr virus-specific cytotoxic T lymphocytes using B-lymphoblastoid cell lines expressing cytomegalovirus pp65. Blood 94, 3242-3250.
89. Sylwester, A. W., Mitchell, B. L., Edgar, J. B., Taormina, C., Pelte, C., Ruchti, E, et al. (2005). Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 202, 673-685.
90. Thorley-Lawson, D. A., and Allday, M. J. (2008). The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat. Rev. Microbiol. 6, 913-924.
91. Tischer, S., Kaireit, T., Figueiredo, C., Hiller, O., Maecker-Kolhoff, B., Geyeregger, R., et al. (2012). Establishment of the reversible peptide-major histocompatibility complex (pMHC) class I Histamer technology: tool for visualization and selection of functionally active antigen-specific CD8+ T lymphocytes. Int. Immunol. 24, 561-572.
92. Toh, H. C., Sun, L., Soe, Y., Wu, Y., Phoon, Y. P., Chia, W. K., et al. (2009). G-CSF induces a potentially tolerant gene and immunopheno-type profile in T cells in vivo. Clin. Immunol. 132, 83-92.
93. Trappe, R., Oertel, S., Leblond, V., Mollee, P., Sender, M., Reinke, P., et al. (2012). Sequential treatment with rituximab followed by CHOP chemotherapy in adult B-cell post-transplant lymphoproliferative disorder (PTLD): the prospective international multicentre phase 2 PTLD-1 trial. Lancet Oncol. 13, 196-206.
94. Ugarte-Torres, A., Hoegh-Petersen, M., Liu, Y., Zhou, F., Williamson, T. S., Quinlan, D., et al. (2011). Donor serostatus has an impact on cytomegalovirus-specific immunity, cytomegaloviral disease incidence, and survival in seropositive hematopoietic cell transplant recipients. Biol. Blood Marrow Transplant. 17, 574-585.
95. Uhlin, M., Okas, M., Gertow, J., Uzunel, M., Brismar, T. B., and Mattsson, J. (2010). A novel haplo-identical adoptive CTL therapy as a treatment for EBV-associated lymphoma after stem cell transplantation. Cancer Immunol. Immunother. 59,473-477.
96. van Esser, J. W., Niesters, H. G., van der Holt, B., Meijer, E., Osterhaus, A. D., Gratama, J. W., et al. (2002). Prevention of Epstein-Barr virus-lymphoproliferative disease by molecular monitoring and preemptive rituximab in high-risk patients after allogeneic stem cell transplantation. Blood 99, 4364-4369.
97. Walls, T., Shankar, A. G., and Shingadia, D. (2003). Adenovirus: an increasingly important pathogen in pae-diatric bone marrow transplant patients. Lancet Infect. Dis. 3, 79-86.
98. Walter, E. A., Greenberg, P. D., Gilbert, M. J., Finch, R. J., Watanabe, K. S., Thomas, E. D., et al. (1995). Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N. Engl. J. Med. 333, 1038-1044.
99. Watcharananan, S. P., Kiertiburanakul, S., Piyatuctsanawong, W., Anurathapan, U., Sungkanuparph, S., Pakakasama, S., et al. (2010). Cytomegalovirus, adenovirus, and polyomavirus co-infection among pediatric recipients of allogeneic stem cell transplantation: characteristics and outcome. Pediatr. Transplant. 14,675-681.
100. Wilkie, G. M., Taylor, C., Jones, M. M., Burns, D. M., Turner, M., Kilpatrick, D., et al. (2004). Establishment and characterization of a bank of cytotoxic T lymphocytes for immunotherapy of epstein-barr virus-associated diseases. J. Immunother. 27, 309-316.
101. Wills, M. R., Carmichael, A. J., Mynard, K., Jin, X., Weekes, M. P., Plachter, B., et al. (1996). The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65, frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J. Virol. 70, 7569-7579.
102. Yao, J., Bechter, C., Wiesneth, M., Harter, G., Gotz, M., Germeroth, L., et al. (2008). Multimer staining of cytomegalovirus phosphoprotein 65-specific T cells for diagnosis and therapeutic purposes: a comparative study. Clin. Infect. Dis. 46, e96-e105.
103. Zandvliet, M. L., Falkenburg, J. H., van Liempt, E., Veltrop-Duits, L. A., Lankester, A. C., Kalpoe, J. S., et al. (2010). Combined CD8+ and CD4+ adenovirus hexon-specific T cells associated with viral clearance after stem cell transplantation as treatment for adenovirus infection. Haematologica 95, 1943-1951.
104. Zandvliet, M. L., van Liempt, E., Jedema, I., Veltrop-Duits, L. A., Willemze, R., Guchelaar, H. J., et al. (2011). Co-ordinated isolation of CD8(+) and CD4(+) T cells recognizing a broad repertoire of cytomegalovirus pp65 and IE1 epitopes for highly specific adoptive immunotherapy. Cytotherapy 12, 933-944.
105. Zhou, W., Longmate, J., Lacey, S. F., Palmer, J. M., Gallez-Hawkins, G., Thao, L., et al. (2009). Impact of donor CMV status on viral infection and reconstitution of multifunction CMV-specific T cells in CMV-positive transplant recipients. Blood 113, 6465-6476.