Cellular immunotherapy for patients with reactivation of JC and BK polyomaviruses after transplantation

Cytotherapy

Volumn 16, Issue 10, 2014, Pages 1325-1335

  Mani, Jiju ^a   Jin, Nan ^a,b   Schmitt, Michael ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b SOUTHEAST UNIVERSITY   (China)

Author keywords

BKV; Hemorrhagic cystitis; JCV; PML; Polyomavirus; Streptamer technology; T cells

Indexed keywords

ADOPTIVE IMMUNOTHERAPY; BK VIRUS INFECTION; CD8+ T LYMPHOCYTE; CELL THERAPY; CELLULAR IMMUNITY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; JC VIRUS INFECTION; KIDNEY TRANSPLANTATION; NONHUMAN; PERSONALIZED MEDICINE; POLYOMAVIRUS INFECTION; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; REVIEW; SEQUENCE HOMOLOGY; VIRUS REACTIVATION; ADVERSE EFFECTS; ANIMAL; BK VIRUS; COMPLICATION; IMMUNOCOMPROMIZED PATIENT; IMMUNOLOGY; JC VIRUS; PHYSIOLOGY; POLYOMAVIRUS INFECTIONS; PROCEDURES; TUMOR VIRUS INFECTIONS; VIRUS ACTIVATION;

BK POLYOMAVIRUS; POLYOMAVIRUS;

ANIMALS; BK VIRUS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOCOMPROMISED HOST; IMMUNOTHERAPY, ADOPTIVE; JC VIRUS; KIDNEY TRANSPLANTATION; POLYOMAVIRUS INFECTIONS; TUMOR VIRUS INFECTIONS; VIRUS ACTIVATION;

EID: 84908555722     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2014.04.003     Document Type: Review

References (117)

1. Gratwohl A., Brand R., Frassoni F., Rocha V., Niederwieser D., Reusser P., et al. Cause of death after allogeneic haematopoietic stem cell transplantation (HSCT) in early leukaemias: an EBMT analysis of lethal infectious complications and changes over calendar time. Bone Marrow Transplant 2005, 36:757-769.
2. Smits E.L., Berneman Z.N. Viral infections following allogeneic stem cell transplantation: how to cure the cure?. Leuk Lymphoma 2010, 51:965-966.
3. Padgett B.L., Walker D.L. New human papovaviruses. Prog Med Virol 1976, 22:1-35.
4. Zu Rhein G.M. Association of papova-virions with a human demyelinating disease (progressive multifocal leukoencephalopathy). Prog Med Virol 1969, 11:185-247.
5. Chesters P.M., Heritage J., McCance D.J. Persistence of DNA sequences of BK virus and JC virus in normal human tissues and in diseased tissues. JInfect Dis 1983, 147:676-684.
6. Doerries K. Human polyomaviruses. Principles and Practice of Clinical Virology 2004, Wiley, Chichester, England. 5th ed. A.J. Zuckerman, J.E. Banatvala, J.R. Pattison, P.D. Griffiths, P. Mortimer (Eds.).
7. Berger J.R., Houff S. Progressive multifocal leukoencephalopathy: lessons from AIDS and natalizumab. Neurol Res 2006, 28:299-305.
8. De Luca A., Ammassari A., Pezzotti P., Cinque P., Gasnault J., Berenguer J., et al. Cidofovir in addition to antiretroviral treatment is not effective for AIDS-associated progressive multifocal leukoencephalopathy: a multicohort analysis. AIDS 2008, 22:1759-1767.
9. Berenguer J., Miralles P., Arrizabalaga J., Ribera E., Dronda F., Baraia-Etxaburu J., et al. Clinical course and prognostic factors of progressive multifocal leukoencephalopathy in patients treated with highly active antiretroviral therapy. Clin Infect Dis 2003, 36:1047-1052.
10. Tassie J.M., Gasnault J., Bentata M., Deloumeaux J., Boue F., Billaud E., et al. Survival improvement of AIDS-related progressive multifocal leukoencephalopathy in the era of protease inhibitors: Clinical Epidemiology Group, French Hospital Database on HIV. AIDS 1999, 13:1881-1887.
11. Comoli P., Hirsch H.H., Ginevri F. Cellular immune responses to BK virus. Curr Opin Organ Transplant 2008, 13:569-574.
12. Laskin B.L., Denburg M., Furth S., Diorio D., Goebel J., Davies S.M., et al. BK viremia precedes hemorrhagic cystitis in children undergoing allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2013, 19:1175-1182.
13. Comoli P., Binggeli S., Ginevri F., Hirsch H.H. Polyomavirus-associated nephropathy: update on BK virus-specific immunity. Transpl Infect Dis 2006, 8:86-94.
14. Egli A., Binggeli S., Bodaghi S., Dumoulin A., Funk G.A., Khanna N., et al. Cytomegalovirus and polyomavirus BK posttransplant. Nephrol Dial Transplant 2007, 22(Suppl 8). viii72-82.
15. Wong A.S., Cheng V.C., Yuen K.Y., Kwong Y.L., Leung A.Y. High frequency of polyoma BK virus shedding in the gastrointestinal tract after hematopoietic stem cell transplantation: a prospective and quantitative analysis. Bone Marrow Transplant 2009, 43:43-47.
16. Hirsch H.H., Kardas P., Kranz D., Leboeuf C. The human JC polyomavirus (JCPyV): virological background and clinical implications. APMIS 2013, 121:685-727.
17. Kharfan-Dabaja M.A., Ayala E., Greene J., Rojiani A., Murtagh F.R., Anasetti C. Two cases of progressive multifocal leukoencephalopathy after allogeneic hematopoietic cell transplantation and a review of the literature. Bone Marrow Transplant 2007, 39:101-107.
18. Schmidt-Hieber M., Schwender J., Heinz W.J., Zabelina T., Kuhl J.S., Mousset S., et al. Viral encephalitis after allogeneic stem cell transplantation: a rare complication with distinct characteristics of different causative agents. Haematologica 2011, 96:142-149.
19. Gheuens S., Pierone G., Peeters P., Koralnik I.J. Progressive multifocal leukoencephalopathy in individuals with minimal or occult immunosuppression. JNeurol Neurosurg Psychiatry 2010, 81:247-254.
20. Van Assche G., Van Ranst M., Sciot R., Dubois B., Vermeire S., Noman M., et al. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. NEngl J Med 2005, 353:362-368.
21. Langer-Gould A., Atlas S.W., Green A.J., Bollen A.W., Pelletier D. Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. NEngl J Med 2005, 353:375-381.
22. Carson K.R., Focosi D., Major E.O., Petrini M., Richey E.A., West D.P., et al. Monoclonal antibody-associated progressive multifocal leucoencephalopathy in patients treated with rituximab, natalizumab, and efalizumab: a review from the Research on Adverse Drug Events and Reports (RADAR) Project. Lancet Oncol 2009, 10:816-824.
23. Kleinschmidt-DeMasters B.K., Tyler K.L. Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. NEngl J Med 2005, 353:369-374.
24. Molloy E.S., Calabrese L.H. Therapy: targeted but not trouble-free: efalizumab and PML. Nat Rev Rheumatol 2009, 5:418-419.
25. Hunt D., Giovannoni G. Natalizumab-associated progressive multifocal leucoencephalopathy: a practical approach to risk profiling and monitoring. Pract Neurol 2012, 12:25-35.
26. Berger J.R. Progressive multifocal leukoencephalopathy in acquired immunodeficiency syndrome: explaining the high incidence and disproportionate frequency of the illness relative to other immunosuppressive conditions. JNeurovirol 2003, 9(Suppl 1):38-41.
27. Farber D.L., Yudanin N.A., Restifo N.P. Human memory T cells: generation, compartmentalization and homeostasis. Nat Rev Immunol 2014, 14:24-35.
28. Chen Y., Trofe J., Gordon J., Du Pasquier R.A., Roy-Chaudhury P., Kuroda M.J., et al. Interplay of cellular and humoral immune responses against BK virus in kidney transplant recipients with polyomavirus nephropathy. JVirol 2006, 80:3495-3505.
29. Comoli P., Azzi A., Maccario R., Basso S., Botti G., Basile G., et al. Polyomavirus BK-specific immunity after kidney transplantation. Transplantation 2004, 78:1229-1232.
30. Hariharan S., Cohen E.P., Vasudev B., Orentas R., Viscidi R.P., Kakela J., et al. BK virus-specific antibodies and BKV DNA in renal transplant recipients with BKV nephritis. Am J Transplant 2005, 5:2719-2724.
31. Lukacher A.E., Wilson C.S. Resistance to polyoma virus-induced tumors correlates with CTL recognition of an immunodominant H-2Dk-restricted epitope in the middle T protein. JImmunol 1998, 160:1724-1734.
32. Prosser S.E., Orentas R.J., Jurgens L., Cohen E.P., Hariharan S. Recovery of BK virus large T-antigen-specific cellular immune response correlates with resolution of bk virus nephritis. Transplantation 2008, 85:185-192.
33. Binggeli S., Egli A., Schaub S., Binet I., Mayr M., Steiger J., et al. Polyomavirus BK-specific cellular immune response to VP1 and large T-antigen in kidney transplant recipients. Am J Transplant 2007, 7:1131-1139.
34. Li J., Melenhorst J., Hensel N., Rezvani K., Sconocchia G., Kilical Y., et al. T-cell responses to peptide fragments of the BK virus T antigen: implications for cross-reactivity of immune response to JC virus. JGen Virol 2006, 87:2951-2960.
35. Hammer M.H., Brestrich G., Andree H., Engelmann E., Rosenberger C., Tillmann H., et al. HLA type-independent method to monitor polyoma BK virus-specific CD4 and CD8 T-cell immunity. Am J Transplant 2006, 6:625-631.
36. Randhawa P.S., Popescu I., Macedo C., Zeevi A., Shapiro R., Vats A.N., et al. Detection of CD8+ T cells sensitized to BK virus large T antigen in healthy volunteers and kidney transplant recipients. Hum Immunol 2006, 67:298-302.
37. Ginevri F., Azzi A., Hirsch H.H., Basso S., Fontana I., Cioni M., et al. Prospective monitoring of polyomavirus BK replication and impact of pre-emptive intervention in pediatric kidney recipients. Am J Transplant 2007, 7:2727-2735.
38. Ramaswami B., Popescu I., Macedo C., Metes D., Bueno M., Zeevi A., et al. HLA-A01-, -A03-, and -A024-binding nanomeric epitopes in polyomavirus BK large T antigen. Hum Immunol 2009, 70(9):722-728.
39. Mueller K., Schachtner T., Sattler A., Meier S., Friedrich P., Trydzenskaya H., et al. BK-VP3 as a new target of cellular immunity in BK virus infection. Transplantation 2011, 91:100-107.
40. Trydzenskaya H., Sattler A., Muller K., Schachtner T., Dang-Heine C., Friedrich P., et al. Novel approach for improved assessment of phenotypic and functional characteristics of BKV-specific T-cell immunity. Transplantation 2011, 92:1269-1277.
41. Schachtner T., Muller K., Stein M., Diezemann C., Sefrin A., Babel N., et al. BK virus-specific immunity kinetics: a predictor of recovery from polyomavirus BK-associated nephropathy. Am J Transplant 2011, 11:2443-2452.
42. Lima M.A., Marzocchetti A., Autissier P., Tompkins T., Chen Y., Gordon J., et al. Frequency and phenotype of JC virus-specific CD8+ T lymphocytes in the peripheral blood of patients with progressive multifocal leukoencephalopathy. JVirol 2007, 81:3361-3368.
43. Provenzano M., Bracci L., Wyler S., Hudolin T., Sais G., Gosert R., et al. Characterization of highly frequent epitope-specific CD45RA+/CCR7+/- T lymphocyte responses against p53-binding domains of the human polyomavirus BK large tumor antigen in HLA-A*0201+ BKV-seropositive donors. JTransl Med 2006, 4:47.
44. Krymskaya L., Sharma M.C., Martinez J., Haq W., Huang E.C., Limaye A.P., et al. Cross-reactivity of T lymphocytes recognizing a human cytotoxic T-lymphocyte epitope within BK and JC virus VP1 polypeptides. JVirol 2005, 79:11170-11178.
45. Ramaswami B., Popescu I., Macedo C., Luo C., Shapiro R., Metes D., et al. The polyomavirus BK large T-antigen-derived peptide elicits an HLA-DR promiscuous and polyfunctional CD4+ T-cell response. Clin Vaccine Immunol 2011, 18:815-824.
46. van Aalderen M.C., Remmerswaal E.B., Heutinck K.M., ten Brinke A., Pircher H., van Lier R.A., et al. Phenotypic and functional characterization of circulating polyomavirus BK VP1-specific CD8+ T cells in healthy adults. JVirol 2013, 87(18):10263-10272.
47. Gasnault J., Kahraman M., de Goer de Herve M.G., Durali D., Delfraissy J.F., Taoufik Y., et al. Critical role of JC virus-specific CD4 T-cell responses in preventing progressive multifocal leukoencephalopathy. AIDS 2003, 17(10):1443-1449.
48. Khanna N., Wolbers M., Mueller N.J., Garzoni C., Du Pasquier R.A., Fux C.A., et al. JC virus-specific immune responses in human immunodeficiency virus type 1 patients with progressive multifocal leukoencephalopathy. JVirol 2009, 83:4404-4411.
49. Du Pasquier R.A., Schmitz J.E., Jean-Jacques J., Zheng Y., Gordon J., Khalili K., et al. Detection of JC virus-specific cytotoxic T lymphocytes in healthy individuals. JVirol 2004, 78:10206-10210.
50. Zhou W., Sharma M., Martinez J., Srivastava T., Diamond D.J., Knowles W., et al. Functional characterization of BK virus-specific CD4+ T cells with cytotoxic potential in seropositive adults. Viral Immunol 2007, 20:379-388.
51. Dropulic L.K., Jones R.J. Polyomavirus BK infection in blood and marrow transplant recipients. Bone Marrow Transplant 2008, 41:11-18.
52. Leung A.Y., Chan M.T., Yuen K.Y., Cheng V.C., Chan K.H., Wong C.L., et al. Ciprofloxacin decreased polyoma BK virus load in patients who underwent allogeneic hematopoietic stem cell transplantation. Clin Infect Dis 2005, 40:528-537.
53. Rinaldo C.H., Hirsch H.H. Antivirals for the treatment of polyomavirus BK replication. Expert Rev Anti Infect Ther 2007, 5:105-115.
54. Savona M.R., Newton D., Frame D., Levine J.E., Mineishi S., Kaul D.R. Low-dose cidofovir treatment of BK virus-associated hemorrhagic cystitis in recipients of hematopoietic stem cell transplant. Bone Marrow Transplant 2007, 39:783-787.
55. Bridges B., Donegan S., Badros A. Cidofovir bladder instillation for the treatment of BK hemorrhagic cystitis after allogeneic stem cell transplantation. Am J Hematol 2006, 81:535-537.
56. Vianelli N., Renga M., Azzi A., De Santis R.D., Bandini G., Tosi P., et al. Sequential vidarabine infusion in the treatment of polyoma virus-associated acute haemorrhagic cystitis late after allogeneic bone marrow transplantation. Bone Marrow Transplant 2000, 25:319-320.
57. Seabra C., Perez-Simon J.A., Sierra M., Marcos J.M., Caballero M.D., de la Loma A., et al. Intra-muscular vidarabine therapy for polyomavirus-associated hemorrhagic cystitis following allogeneic hemopoietic stem cell transplantation. Bone Marrow Transplant 2000, 26:1229-1230.
58. Tavazzi E., White M.K., Khalili K. Progressive multifocal leukoencephalopathy: clinical and molecular aspects. Rev Med Virol 2012, 22:18-32.
59. Focosi D., Kast R.E., Maggi F., Ceccherini-Nelli L., Petrini M. Risperidone-induced reduction in JC viruria as a surrogate marker for efficacy against progressive multifocal leukoencephalopathy and hemorrhagic cystitis. JClin Virol 2007, 39:63-64.
60. Cettomai D., McArthur J.C. Mirtazapine use in human immunodeficiency virus-infected patients with progressive multifocal leukoencephalopathy. Arch Neurol 2009, 66:255-258.
61. Vulliemoz S., Lurati-Ruiz F., Borruat F.X., Delavelle J., Koralnik I.J., Kuntzer T., et al. Favourable outcome of progressive multifocal leucoencephalopathy in two patients with dermatomyositis. JNeurol Neurosurg Psychiatry 2006, 77(9):1079-1082.
62. Owczarczyk K., Hilker R., Brunn A., Hallek M., Rubbert A. Progressive multifocal leucoencephalopathy in a patient with sarcoidosis-successful treatment with cidofovir and mirtazapine. Rheumatology 2007, 46:888-890.
63. Verma S., Cikurel K., Koralnik I.J., Morgello S., Cunningham-Rundles C., Weinstein Z.R., et al. Mirtazapine in progressive multifocal leukoencephalopathy associated with polycythemia vera. JInfect Dis 2007, 196:709-711.
64. Kunschner L., Scott T.F. Sustained recovery of progressive multifocal leukoencephalopathy after treatment with IL-2. Neurology 2005, 65:1510.
65. Buckanovich R.J., Liu G., Stricker C., Luger S.M., Stadtmauer E.A., Schuster S.J., et al. Nonmyeloablative allogeneic stem cell transplantation for refractory Hodgkin's lymphoma complicated by interleukin-2 responsive progressive multifocal leukoencephalopathy. Ann Hematol 2002, 81:410-413.
66. Przepiorka D., Jaeckle K.A., Birdwell R.R., Fuller G.N., Kumar A.J., Huh Y.O., et al. Successful treatment of progressive multifocal leukoencephalopathy with low-dose interleukin-2. Bone Marrow Transplant 1997, 20:983-987.
67. Pohlmann C., Hochauf K., Rollig C., Schetelig J., Wunderlich O., Bandt D., et al. Chlorpromazine combined with cidofovir for treatment of a patient suffering from progressive multifocal leukoencephalopathy. Intervirology 2007, 50:412-417.
68. Marra C.M., Rajicic N., Barker D.E., Cohen B.A., Clifford D., Donovan Post M.J., et al. Apilot study of cidofovir for progressive multifocal leukoencephalopathy in AIDS. AIDS 2002, 16:1791-1797.
69. Kraemer C., Evers S., Nolting T., Arendt G., Husstedt I.W. Cidofovir in combination with HAART and survival in AIDS-associated progressive multifocal leukoencephalopathy. JNeurol 2008, 255:526-531.
70. Epker J.L., van Biezen P., van Daele P.L., van Gelder T., Vossen A., van Saase J.L. Progressive multifocal leukoencephalopathy, a review and an extended report of five patients with different immune compromised states. Eur J Intern Med 2009, 20:261-267.
71. Riddell S.R., Watanabe K.S., Goodrich J.M., Li C.R., Agha M.E., Greenberg P.D. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 1992, 257:238-241.
72. Walter E.A., Greenberg P.D., Gilbert M.J., Finch R.J., Watanabe K.S., Thomas E.D., et al. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. NEngl J Med 1995, 333:1038-1044.
73. O'Reilly R.J., Small T.N., Papadopoulos E., Lucas K., Lacerda J., Koulova L. Biology and adoptive cell therapy of Epstein-Barr virus-associated lymphoproliferative disorders in recipients of marrow allografts. Immunol Rev 1997, 157:195-216.
74. Smith C.A., Ng C.Y., Heslop H.E., Holladay M.S., Richardson S., Turner E.V., et al. Production of genetically modified Epstein-Barr virus-specific cytotoxic T cells for adoptive transfer to patients at high risk of EBV-associated lymphoproliferative disease. JHematother 1995, 4:73-79.
75. Heslop H.E., Ng C.Y., Li C., Smith C.A., Loftin S.K., Krance R.A., et al. Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat Med 1996, 2:551-555.
76. Rooney C.M., Smith C.A., Ng C.Y., Loftin S., Li C., Krance R.A., et al. Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 1995, 345:9-13.
77. Perruccio K., Tosti A., Burchielli E., Topini F., Ruggeri L., Carotti A., et al. Transferring functional immune responses to pathogens after haploidentical hematopoietic transplantation. Blood 2005, 106:4397-4406.
78. Einsele H., Roosnek E., Rufer N., Sinzger C., Riegler S., Loffler J., et al. Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 2002, 99:3916-3922.
79. Peggs K.S., Verfuerth S., Pizzey A., Khan N., Guiver M., Moss P.A., et al. Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 2003, 362:1375-1377.
80. Micklethwaite K.P., Clancy L., Sandher U., Hansen A.M., Blyth E., Antonenas V., et al. Prophylactic infusion of cytomegalovirus-specific cytotoxic T lymphocytes stimulated with Ad5f35pp65 gene-modified dendritic cells after allogeneic hemopoietic stem cell transplantation. Blood 2008, 112:3974-3981.
81. Blyth E., Clancy L., Simms R., Ma C.K., Burgess J., Deo S., et al. Donor-derived CMV-specific T cells reduce the requirement for CMV-directed pharmacotherapy after allogeneic stem cell transplantation. Blood 2013, 121:3745-3758.
82. Leen A.M., Myers G.D., Sili U., Huls M.H., Weiss H., Leung K.S., et al. Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat Med 2006, 12:1160-1166.
83. Leen A.M., Christin A., Myers G.D., Liu H., Cruz C.R., Hanley P.J., et al. 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, 114:4283-4292.
84. Park K.D., Marti L., Kurtzberg J., Szabolcs P. In vitro priming and expansion of cytomegalovirus-specific Th1 and Tc1 T cells from naive cord blood lymphocytes. Blood 2006, 108:1770-1773.
85. Savoldo B., Cubbage M.L., Durett A.G., Goss J., Huls M.H., Liu Z., et al. Generation of EBV-specific CD4+ cytotoxic T cells from virus naive individuals. JImmunol 2002, 168:909-918.
86. Safdar A., Decker W.K., Li S., Xing D., Robinson S.N., Yang H., et al. De novo T-lymphocyte responses against baculovirus-derived recombinant influenzavirus hemagglutinin generated by a naive umbilical cord blood model of dendritic cell vaccination. Vaccine 2009, 27:1479-1484.
87. Hanley P.J., Cruz C.R., Savoldo B., Leen A.M., Stanojevic M., Khalil M., et al. 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, 114:1958-1967.
88. Hanley P.J., Lam S., Shpall E.J., Bollard C.M. Expanding cytotoxic T lymphocytes from umbilical cord blood that target cytomegalovirus, Epstein-Barr virus, and adenovirus. JVis Exp 2012, 63:e3627.
89. Vera J.F., Brenner L.J., Gerdemann U., Ngo M.C., Sili U., Liu H., et al. Accelerated production of antigen-specific T cells for preclinical and clinical applications using gas-permeable rapid expansion cultureware (G-Rex). JImmunother 2010, 33:305-315.
90. Feuchtinger T., Matthes-Martin S., Richard C., Lion T., Fuhrer M., Hamprecht K., et al. Safe adoptive transfer of virus-specific T-cell immunity for the treatment of systemic adenovirus infection after allogeneic stem cell transplantation. Br J Haematol 2006, 134:64-76.
91. Feuchtinger T., Opherk K., Bethge W.A., Topp M.S., Schuster F.R., Weissinger E.M., et al. Adoptive transfer of pp65-specific T cells for the treatment of chemorefractory cytomegalovirus disease or reactivation after haploidentical and matched unrelated stem cell transplantation. Blood 2010, 116:4360-4367.
92. Peggs K.S., Thomson K., Samuel E., Dyer G., Armoogum J., Chakraverty R., et al. Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stem cell transplantation. Clin Infect Dis 2011, 52:49-57.
93. Moosmann A., Bigalke I., Tischer J., Schirrmann L., Kasten J., Tippmer S., et al. Effective and long-term control of EBV PTLD after transfer of peptide-selected T cells. Blood 2010, 115:2960-2970.
94. Icheva V., Kayser S., Wolff D., Tuve S., Kyzirakos C., Bethge W., et al. Adoptive transfer of epstein-barr virus (EBV) nuclear antigen 1-specific t cells as treatment for EBV reactivation and lymphoproliferative disorders after allogeneic stem-cell transplantation. JClin Oncol 2013, 31:39-48.
95. Cobbold M., Khan N., Pourgheysari B., Tauro S., McDonald D., Osman H., et al. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. JExp Med 2005, 202:379-386.
96. Uhlin M., Okas M., Gertow J., Uzunel M., Brismar T.B., Mattsson J. Anovel haplo-identical adoptive CTL therapy as a treatment for EBV-associated lymphoma after stem cell transplantation. Cancer Immunol Immunother 2010, 59:473-477.
97. Uhlin M., Gertow J., Uzunel M., Okas M., Berglund S., Watz E., et al. Rapid salvage treatment with virus-specific T cells for therapy-resistant disease. Clin Infect Dis 2012, 55:1064-1073.
98. Schmitt A., Tonn T., Busch D.H., Grigoleit G.U., Einsele H., Odendahl M., et al. 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 2011, 51:591-599.
99. Weissbrich B., Nauerth M., Busch D.H. Adoptive immunotherapy: new assay for the identification of T cells with optimal avidity. Oncoimmunology 2013, 2:e26199.
100. Haque T., Wilkie G.M., Jones M.M., Higgins C.D., Urquhart G., Wingate P., 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.
101. Haque T., Wilkie G.M., Taylor C., Amlot P.L., Murad P., Iley A., et al. Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 2002, 360:436-442.
102. Barker J.N., Doubrovina E., Sauter C., Jaroscak J.J., Perales M.A., Doubrovin M., 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.
103. Leen A.M., Bollard C.M., Mendizabal A.M., Shpall E.J., Szabolcs P., Antin J.H., et al. Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stem cell transplantation. Blood 2013, 121:5113-5123.
104. Balduzzi A., Lucchini G., Hirsch H.H., Basso S., Cioni M., Rovelli A., et al. Polyomavirus JC-targeted T-cell therapy for progressive multiple leukoencephalopathy in a hematopoietic cell transplantation recipient. Bone Marrow Transplant 2011, 46:987-992.
105. Schneidawind D., Schmitt A., Wiesneth M., Mertens T., Bunjes D., Freund M., et al. Polyomavirus BK-specific CD8+ T cell responses in patients after allogeneic stem cell transplant. Leuk Lymphoma 2010, 51:1055-1062.
106. Chen Y., Trofe J., Gordon J., Autissier P., Woodle E.S., Koralnik I.J. BKV and JCV large T antigen-specific CD8+ T cell response in HLA A*0201+ kidney transplant recipients with polyomavirus nephropathy and patients with progressive multifocal leukoencephalopathy. JClin Virol 2008, 42:198-202.
107. Yang W., Beaudoin E.L., Lu L., Du Pasquier R.A., Kuroda M.J., Willemsen R.A., et al. Chimeric immune receptors (CIRs) specific to JC virus for immunotherapy in progressive multifocal leukoencephalopathy (PML). Int Immunol 2007, 19:1083-1093.
108. Mackinnon S., Thomson K., Verfuerth S., Peggs K., Lowdell M. Adoptive cellular therapy for cytomegalovirus infection following allogeneic stem cell transplantation using virus-specific T cells. Blood Cells Mol Dis 2008, 40:63-67.
109. Stemberger C., Huster K.M., Koffler M., Anderl F., Schiemann M., Wagner H., et al. Asingle naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity 2007, 27:985-997.
110. Marzocchetti A., Lima M., Tompkins T., Kavanagh D.G., Gandhi R.T., O'Neill D.W., et al. Efficient in vitro expansion of JC virus-specific CD8(+) T-cell responses by JCV peptide-stimulated dendritic cells from patients with progressive multifocal leukoencephalopathy. Virology 2009, 383:173-177.
111. Du Pasquier R.A., Stein M.C., Lima M.A., Dang X., Jean-Jacques J., Zheng Y., et al. JC virus induces a vigorous CD8+ cytotoxic T cell response in multiple sclerosis patients. JNeuroimmunol 2006, 176:181-186.
112. Du Pasquier R.A., Autissier P., Zheng Y., Jean-Jacques J., Koralnik I.J. Presence of JC virus-specific CTL in the cerebrospinal fluid of PML patients: rationale for immune-based therapeutic strategies. AIDS 2005, 19:2069-2076.
113. Tan C.S., Broge T.A., Seung E., Vrbanac V., Viscidi R., Gordon J., et al. Detection of JC virus-specific immune responses in a novel humanized mouse model. PLoS One 2013, 8:e64313.
114. Sharma M.C., Zhou W., Martinez J., Krymskaya L., Srivastava T., Haq W., et al. Cross-reactive CTL recognizing two HLA-A*02-restricted epitopes within the BK virus and JC virus VP1 polypeptides are frequent in immunocompetent individuals. Virology 2006, 350:128-136.
115. Koralnik I.J. Overview of the cellular immunity against JC virus in progressive multifocal leukoencephalopathy. JNeurovirol 2002, (Suppl 2):59-65.
116. Yang W., Beaudoin E., Du Pasquier R.A., Koralnik I.J., Junghans R.P. Development of anti-JC virus 'designer T cells' for progressive multifocal leukoencephalopathy (PML) immunotherapy. Mol Ther 2006, 13(Suppl 1):S228-S229.
117. Koralnik I.J., Du Pasquier R.A., Kuroda M.J., Schmitz J.E., Dang X., Zheng Y., et al. Association of prolonged survival in HLA-A2+ progressive multifocal leukoencephalopathy patients with a CTL response specific for a commonly recognized JC virus epitope. JImmunol 2002, 168:499-504.