Expansion of T cells targeting multiple antigens of cytomegalovirus, Epstein–Barr virus and adenovirus to provide broad antiviral specificity after stem cell transplantation

References

• Chakrabarti S, Mackinnon S, Chopra R, Kottaridis PD, Peggs K, O'Gorman P, . High incidence of cytomegalovirus infection after nonmyeloablative stem cell transplantation: potential role of Campath-1H in delaying immune reconstitution. Blood. 2002;99:4357–63.
   PubMed Web of Science ®Google Scholar
• Chakrabarti S, Mautner V, Osman H, Collingham KE, Fegan CD, Klapper PE, . Adenovirus infections following allogeneic stem cell transplantation: incidence and outcome in relation to graft manipulation, immunosuppression, and immune recovery. Blood. 2002;100:1619–27.
   PubMed Web of Science ®Google Scholar
• Tomblyn M, Chiller T, Einsele H, Gress R, Sepkowitz K, Storek J, . Guidelines for preventing infectious complications among hematopoietic cell transplantation recipients: a global perspective. Biol Blood Marrow Transplant. 2009;15: 1143–238.
   PubMed Web of Science ®Google Scholar
• Bao L, Dunham K, Stamer M, Mulieri KM, Lucas KG. Expansion of cytomegalovirus pp65 and IE-1 specific cytotoxic T lymphocytes for cytomegalovirus-specific immunotherapy following allogeneic stem cell transplantation. Biol Blood Marrow Transplant. 2008;14:1156–62.
   PubMedGoogle Scholar
• Erice A. Resistance of human cytomegalovirus to antiviral drugs. Clin Microbiol Rev. 1999;12:286–97.
   PubMed Web of Science ®Google Scholar
• Mentzer SJ, Perrine SP, Faller DV. Epstein–Barr virus post-transplant lymphoproliferative disease and virus-specific therapy: pharmacological re-activation of viral target genes with arginine butyrate. Transpl Infect Dis. 2001;3:177–85.
   PubMedGoogle Scholar
• Lindemans CA, Leen AM, Boelens JJ. How I treat adenovirus in haematopoietic stem cell transplantation recipients. Blood. 2010;116:5476–85;
   PubMed Web of Science ®Google Scholar
• Leen AM, Myers GD, Sili U, Huls MH, Weiss H, Leung KS, . Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat Med. 2006;12:1160–6.
   PubMed Web of Science ®Google Scholar
• Riddell SR, Watanabe KS, Goodrich JM, Li CR, Agha ME, Greenberg PD. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science. 1992;257:238–41.
   PubMed Web of Science ®Google Scholar
• O'Reilly RJ, Doubrovina E, Trivedi D, Hasan A, Kollen W, Koehne G. Adoptive transfer of antigen-specific T-cells of donor type for immunotherapy of viral infections following allogeneic hematopoietic cell transplants. Immunol Res. 2007;38:237–50.
   PubMed Web of Science ®Google Scholar
• Laughlin-Taylor E, Pande H, Forman SJ, Tanamachi B, Li CR, Zaia JA, . Identification of the major late human cytomegalovirus matrix protein pp65 as a target antigen for CD8+ virus-specific cytotoxic T lymphocytes. J Med Virol. 1994;43:103–10.
   PubMedGoogle Scholar
• Greenberg PD, Reusser P, Goodrich JM, Riddell SR. 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 NY Acad Sci. 1991;636:184–95.
   PubMed Web of Science ®Google Scholar
• Peggs KS, Verfuerth S, Pizzey A, Khan N, Guiver M, Moss PA, . Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet. 2003;362:1375–7.
   PubMed Web of Science ®Google Scholar
• Bunde T, Kirchner A, Hoffmeister B, Habedank D, Hetzer R, Cherepnev G, . Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J Exp Med. 2005;201:1031–6.
   PubMed Web of Science ®Google Scholar
• Besold K, Frankenberg N, Pepperl-Klindworth S, Kuball J, Theobald M, Hahn G, . Processing and MHC class I presentation of human cytomegalovirus pp65-derived peptides persist despite gpUS2-11-mediated immune evasion. J Gen Virol. 2007;88:1429–39.
   PubMedGoogle Scholar
• Gilbert MJ, Riddell SR, Plachter B, Greenberg PD. Cytomegalovirus selectively blocks antigen processing and presentation of its immediate-early gene product. Nature. 1996;383: 720–2.
   PubMed Web of Science ®Google Scholar
• Zandvliet ML, van Liempt E, Jedema I, Veltrop-Duits LA, Willemze R, Guchelaar HJ, . 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. 2010;12:933–44.
   PubMed Web of Science ®Google Scholar
• Slezak SL, Bettinotti M, Selleri S, Adams S, Marincola FM, Stroncek DF CMV pp65 and IE-1 T cell epitopes recognized by healthy subjects. J Transl Med. 2007;5:17.
   PubMedGoogle Scholar
• Jacobson MA, Sinclair E, Bredt B, Agrillo L, Black D, Epling CL, . Antigen-specific T cell responses induced by Towne cytomegalovirus (CMV) vaccine in CMV-seronegative vaccine recipients. J Clin Virol. 2006;35:332–7.
   PubMed Web of Science ®Google Scholar
• Micklethwaite KP, Savoldo B, Hanley PJ, Leen AM, Demmler-Harrison GJ, Cooper LJ, . 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;115:2695–703.
   PubMed Web of Science ®Google Scholar
• Leen AM, Christin A, Myers GD, Liu H, Cruz CR, Hanley PJ, . Cytotoxic T lymphocyte therapy with donor T cells prevents and treats adenovirus and Epstein-Barr virus infections after haploidentical and matched unrelated stem cell transplantation. Blood. 2009;114:4283–92.
   PubMed Web of Science ®Google Scholar
• Sili U, Huls MH, Davis AR, Gottschalk S, Brenner MK, Heslop HE, . Large-scale expansion of dendritic cell-primed polyclonal human cytotoxic T-lymphocyte lines using lymphoblastoid cell lines for adoptive immunotherapy. J Immunother. 2003;26:241–56.
   PubMed Web of Science ®Google Scholar
• Rooney CM, Smith CA, Ng CY, Loftin S, Li C, Krance RA, . Use of gene-modified virus-specific T lymphocytes to control Epstein–Barr-virus-related lymphoproliferation. Lancet. 1995;345:9–13.
   PubMed Web of Science ®Google Scholar
• Leen A, Ratnayake M, Foster A, Heym K, Ahmed N, Rooney CM, . Contact-activated monocytes: efficient antigen presenting cells for the stimulation of antigen-specific T cells. J Immunother. 2007;30:96–107.
   PubMed Web of Science ®Google Scholar
• Kern F, Faulhaber N, Frommel C, Khatamzas E, Prosch S, Schonemann C, . Analysis of CD8 T cell reactivity to cytomegalovirus using protein-spanning pools of overlapping pentadecapeptides. Eur J Immunol. 2000;30:1676–82.
   PubMed Web of Science ®Google Scholar
• Leen AM, Christin A, Khalil M, Weiss H, Gee AP, Brenner MK, . Identification of hexon-specific CD4 and CD8 T-cell epitopes for vaccine and immunotherapy. J Virol. 2008; 82:546–54.
   PubMed Web of Science ®Google Scholar
• Chang ST, Ghosh D, Kirschner DE, Linderman JJ. Peptide length-based prediction of peptide-MHC class II binding. Bioinformatics. 2006;22:2761–7.
   PubMedGoogle Scholar
• Hanley PJ, Cruz CR, Savoldo B, Leen AM, Stanojevic M, Khalil M, . Functionally active virus-specific T cells that target CMV, adenovirus, and EBV can be expanded from naive T-cell populations in cord blood and will target a range of viral epitopes. Blood. 2009;114:1958–67.
   PubMed Web of Science ®Google Scholar
• Kumar D, Humar A. Cytomegalovirus prophylaxis: how long is enough? Nat Rev Nephrol. 2010;6:13–4.
   PubMedGoogle Scholar
• Salzberger B, Bowden RA, Hackman RC, Davis C, Boeckh M. Neutropenia in allogeneic marrow transplant recipients receiving ganciclovir for prevention of cytomegalovirus disease: risk factors and outcome. Blood. 1997;90:2502–8.
   PubMed Web of Science ®Google Scholar
• Boeckh M, Gooley TA, Myerson D, Cunningham T, Schoch G, Bowden RA. Cytomegalovirus pp65 antigenemia-guided early treatment with ganciclovir versus ganciclovir at engraftment after allogeneic marrow transplantation: a randomized double-blind study. Blood. 1996;88:4063–71.
   PubMed Web of Science ®Google Scholar
• Cobbold M, Khan N, Pourgheysari B, Tauro S, McDonald D, Osman H, . Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J Exp Med. 2005;202:379–86.
   PubMed Web of Science ®Google Scholar
• Gustafsson A, Levitsky V, Zou JZ, Frisan T, Dalianis T, Ljungman P, . Epstein–Barr virus (EBV) load in bone marrow transplant recipients at risk to develop posttransplant lymphoproliferative disease: prophylactic infusion of EBV-specific cytotoxic T cells. Blood. 2000;95:807–14.
   PubMed Web of Science ®Google Scholar
• Micklethwaite KP, Clancy L, Sandher U, Hansen AM, Blyth E, Antonenas V, . Prophylactic infusion of cytomegalovirus-specific cytotoxic T lymphocytes stimulated with Ad5f35pp65 gene-modified dendritic cells after allogeneic hemopoietic stem cell transplantation. Blood. 2008;112:3974–81.
   PubMed Web of Science ®Google Scholar
• Einsele H, Roosnek E, Rufer N, Sinzger C, Riegler S, Loffler J, . Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood. 2002;99:3916–22.
   PubMed Web of Science ®Google Scholar
• Walter EA, Greenberg PD, Gilbert MJ, Finch RJ, Watanabe KS, Thomas ED, . 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. 1995;333:1038–44.
   PubMed Web of Science ®Google Scholar
• Cruz CR, Hanley PJ, Liu H, Torrano V, Lin YF, Arce JA, . Adverse events following infusion of T cells for adoptive immunotherapy: a 10-year experience. Cytotherapy. 2010;12:743–9.
   PubMed Web of Science ®Google Scholar
• Heslop HE, Slobod KS, Pule MA, Hale GA, Rousseau A, Smith CA, . Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood. 2010;115:925–35.
   PubMed Web of Science ®Google Scholar
• Gottschalk S, Ng CY, Perez M, Smith CA, Sample C, Brenner MK, . An Epstein–Barr virus deletion mutant associated with fatal lymphoproliferative disease unresponsive to therapy with virus-specific CTLs. Blood. 2001;97:835–43.
   PubMed Web of Science ®Google Scholar
• Savoldo B, Cubbage ML, Durett AG, Goss J, Huls MH, Liu Z, . Generation of EBV-specific CD4+ cytotoxic T cells from virus naive individuals. J Immunol. 2002;168: 909–18.
   PubMed Web of Science ®Google Scholar
• Waller EC, Day E, Sissons JG, Wills MR. Dynamics of T cell memory in human cytomegalovirus infection. Med Microbiol Immunol. 2008;197:83–96.
   PubMedGoogle Scholar
• Foster AE, Bradstock KF, Sili U, Marangolo M, Rooney CM, Gottlieb DJ. A comparison of gene transfer and antigen-loaded dendritic cells for the generation of CD4+ and CD8+cytomegalovirus-specific T cells in HLA-A2 + and HLA-A2-donors. Biol Blood Marrow Transplant. 2004; 10:761–71.
   PubMedGoogle Scholar
• Matloubian M, Concepcion RJ, Ahmed R. CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. J Virol. 1994;68:8056–63.
   PubMed Web of Science ®Google Scholar