Short-Term In-Vitro Expansion Improves Monitoring and Allows Affordable Generation of Virus-Specific T-Cells against Several Viruses for a Broad Clinical Application

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Geyeregger, René ^a   Freimüller, Christine ^a   Stevanovic, Stefan ^c   Stemberger, Julia ^a   Mester, Gabor ^c   Dmytrus, Jasmin ^a   Lion, Thomas ^a,b   Rammensee, Hans Georg ^c   Fischer, Gottfried ^b   Eiz Vesper, Britta ^d   Lawitschka, Anita ^b,e   Matthes, Susanne ^b,e   Fritsch, Gerhard ^a,b  

^a CHILDREN'S CANCER RESEARCH INSTITUTE   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e ST ANNA CHILDREN S HOSPITAL   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

E1A PROTEIN; GAMMA INTERFERON; INTERLEUKIN 15; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ADULT; ALLOIMMUNITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL SPECIFICITY; CHILD; CONTROLLED STUDY; COST EFFECTIVENESS ANALYSIS; CRYOPRESERVATION; CYTOTOXIC T LYMPHOCYTE; FEMALE; FLOW CYTOMETRY; GOOD MANUFACTURING PRACTICE; HLA TYPING; HUMAN; HUMAN ADENOVIRUS; HUMAN ADENOVIRUS INFECTION; HUMAN CELL; IN VITRO STUDY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; T LYMPHOCYTE; VIRAL CLEARANCE; VIRUS DETECTION; VIRUS LOAD; VIRUS SPECIFIC T LYMPHOCYTE;

ADENOVIRIDAE; ADENOVIRIDAE INFECTIONS; ANTIGENS, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; MALE; PHENOTYPE; TRANSPLANTATION, HOMOLOGOUS; VIRUS CULTIVATION; YOUNG ADULT;

BK POLYOMAVIRUS; HUMAN ADENOVIRUS; HUMAN HERPESVIRUS 4;

EID: 84876428945     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059592     Document Type: Article

References (49)

1. Lion T, Baumgartinger R, Watzinger F, Matthes-Martin S, Suda M, 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.
2. Gooley TA, Chien JW, Pergam SA, Hingorani S, Sorror ML, et al. (2010) Reduced mortality after allogeneic hematopoietic-cell transplantation. N Engl J Med 363: 2091-2101.
3. Watcharananan SP, Kiertiburanakul S, Piyatuctsanawong W, Anurathapan U, Sungkanuparph 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.
4. George D, El-Mallawany NK, Jin Z, Geyer M, Della-Latta P, et al. (2012) Adenovirus infection in paediatric allogeneic stem cell transplantation recipients is a major independent factor for significantly increasing the risk of treatment related mortality. Br J Haematol 156: 99-108.
5. Schilham MW, Claas EC, van Zaane W, Heemskerk B, Vossen JM, et al. (2002) High levels of adenovirus DNA in serum correlate with fatal outcome of adenovirus infection in children after allogeneic stem-cell transplantation. Clin Infect Dis 35: 526-532.
6. Symeonidis N, Jakubowski A, Pierre-Louis S, Jaffe D, Pamer E, et al. (2007) Invasive adenoviral infections in T-cell-depleted allogeneic hematopoietic stem cell transplantation: high mortality in the era of cidofovir. Transpl Infect Dis 9: 108-113.
7. Myers GD, Krance RA, Weiss H, Kuehnle I, Demmler G, et al. (2005) Adenovirus infection rates in pediatric recipients of alternate donor allogeneic bone marrow transplants receiving either antithymocyte globulin (ATG) or alemtuzumab (Campath). Bone Marrow Transplant 36: 1001-1008.
8. Lion T, Kosulin K, Landlinger C, Rauch M, Preuner S, et al. (2010) Monitoring of adenovirus load in stool by real-time PCR permits early detection of impending invasive infection in patients after allogeneic stem cell transplantation. Leukemia 24: 706-714.
9. Hoffman JA, Shah AJ, Ross LA, Kapoor N, (2001) Adenoviral infections and a prospective trial of cidofovir in pediatric hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 7: 388-394.
10. Lankester AC, Heemskerk B, Claas EC, Schilham MW, Beersma MF, et al. (2004) Effect of ribavirin on the plasma viral DNA load in patients with disseminating adenovirus infection. Clin Infect Dis 38: 1521-1525.
11. Chakrabarti S, Mautner V, Osman H, Collingham KE, Fegan CD, et al. (2002) Adenovirus infections following allogeneic stem cell transplantation: incidence and outcome in relation to graft manipulation, immunosuppression, and immune recovery. Blood 100: 1619-1627.
12. Feuchtinger T, Lucke J, Hamprecht K, Richard C, Handgretinger R, 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.
13. Heemskerk B, Lankester AC, van Vreeswijk T, Beersma MF, Claas EC, et al. (2005) Immune reconstitution and clearance of human adenovirus viremia in pediatric stem-cell recipients. J Infect Dis 191: 520-530.
14. Zandvliet ML, Falkenburg JH, van Liempt E, Veltrop-Duits LA, Lankester AC, 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.
15. Einsele H, Roosnek E, Rufer N, Sinzger C, Riegler S, et al. (2002) Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 99: 3916-3922.
16. Leen AM, Christin A, Myers GD, Liu H, Cruz CR, et al. (2009) 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 114: 4283-4292.
17. Leen AM, Myers GD, Sili U, Huls MH, Weiss H, 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.
18. Feuchtinger T, Matthes-Martin S, Richard C, Lion T, Fuhrer M, 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.
19. Cobbold M, Khan N, Pourgheysari B, Tauro S, McDonald D, 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.
20. Feuchtinger T, Opherk K, Bethge WA, Topp MS, Schuster FR, et al. (2010) 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 116: 4360-4367.
21. Schmitt A, Tonn T, Busch DH, Grigoleit GU, Einsele H, 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.
22. Uhlin M, Gertow J, Uzunel M, Okas M, Berglund S, et al. (2012) Rapid Salvage Treatment With Virus-Specific T Cells for Therapy-Resistant Disease. Clin Infect Dis.
23. Jones MS 2nd, Harrach B, Ganac RD, Gozum MM, Dela Cruz WP, et al. (2007) New adenovirus species found in a patient presenting with gastroenteritis. J Virol 81: 5978-5984.
24. Leen AM, Sili U, Vanin EF, Jewell AM, Xie W, et al. (2004) Conserved CTL epitopes on the adenovirus hexon protein expand subgroup cross-reactive and subgroup-specific CD8+ T cells. Blood 104: 2432-2440.
25. Zandvliet ML, van Liempt E, Jedema I, Kruithof S, Kester MG, et al. (2011) Simultaneous isolation of CD8(+) and CD4(+) T cells specific for multiple viruses for broad antiviral immune reconstitution after allogeneic stem cell transplantation. J Immunother 34: 307-319.
26. Zandvliet ML, Kester MG, van Liempt E, de Ru AH, van Veelen PA, et al. (2012) Efficiency and Mechanism of Antigen-specific CD8+ T-cell Activation Using Synthetic Long Peptides. J Immunother 35: 142-153.
27. Leen AM, Christin A, Khalil M, Weiss H, Gee AP, et al. (2008) Identification of hexon-specific CD4 and CD8 T-cell epitopes for vaccine and immunotherapy. J Virol 82: 546-554.
28. Schipper RF, van Els CA, D'Amaro J, Oudshoorn M, (1996) Minimal phenotype panels. A method for achieving maximum population coverage with a minimum of HLA antigens. Hum Immunol 51: 95-98.
29. Comoli P, Basso S, Labirio M, Baldanti F, Maccario R, et al. (2008) T cell therapy of Epstein-Barr virus and adenovirus infections after hemopoietic stem cell transplant. Blood Cells Mol Dis 40: 68-70.
30. Sellar RS, Peggs KS, (2012) The role of virus-specific adoptive T-cell therapy in hematopoietic transplantation. Cytotherapy 14: 391-400.
31. Gerdemann U, Keirnan JM, Katari UL, Yanagisawa R, Christin AS, et al. (2012) Rapidly Generated Multivirus-specific Cytotoxic T Lymphocytes for the Prophylaxis and Treatment of Viral Infections. Mol Ther 20: 1622-1632.
32. Garnett CT, Erdman D, Xu W, Gooding LR, (2002) Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes. J Virol 76: 10608-10616.
33. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S, (1999) SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50: 213-219.
34. Dohnal AM, Graffi S, Witt V, Eichstill C, Wagner D, et al. (2009) Comparative evaluation of techniques for the manufacturing of dendritic cell-based cancer vaccines. J Cell Mol Med 13: 125-135.
35. Vellinga J, van den Wollenberg DJ, van der Heijdt S, Rabelink MJ, Hoeben RC, (2005) The coiled-coil domain of the adenovirus type 5 protein IX is dispensable for capsid incorporation and thermostability. J Virol 79: 3206-3210.
36. Ohrmalm L, Lindblom A, Omar H, Norbeck O, Gustafson I, et al. (2011) Evaluation of a surveillance strategy for early detection of adenovirus by PCR of peripheral blood in hematopoietic SCT recipients: incidence and outcome. Bone Marrow Transplant 46: 267-272.
37. Abate D, Cesaro S, Cofano S, Fiscon M, Saldan A, et al. (2012) Diagnostic utility of human cytomegalovirus-specific T-cell response monitoring in predicting viremia in pediatric allogeneic stem-cell transplant patients. Transplantation 93: 536-542.
38. Gratama JW, Boeckh M, Nakamura R, Cornelissen JJ, Brooimans RA, et al. (2010) Immune monitoring with iTAg MHC Tetramers for prediction of recurrent or persistent cytomegalovirus infection or disease in allogeneic hematopoietic stem cell transplant recipients: a prospective multicenter study. Blood 116: 1655-1662.
39. Guerin-El Khourouj V, Dalle JH, Pedron B, Yakouben K, Bensoussan D, et al. (2011) Quantitative and qualitative CD4 T cell immune responses related to adenovirus DNAemia in hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 17: 476-485.
40. Olive M, Eisenlohr L, Flomenberg N, Hsu S, Flomenberg P, (2002) The adenovirus capsid protein hexon contains a highly conserved human CD4+ T-cell epitope. Hum Gene Ther 13: 1167-1178.
41. Serangeli C, Bicanic O, Scheible MH, Wernet D, Lang P, et al. (2010) Ex vivo detection of adenovirus specific CD4+ T-cell responses to HLA-DR-epitopes of the Hexon protein show a contracted specificity of T(HELPER) cells following stem cell transplantation. Virology 397: 277-284.
42. Stemberger C, Huster KM, Koffler M, Anderl F, Schiemann M, et al. (2007) A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity 27: 985-997.
43. Boeckh M, Nichols WG, (2004) The impact of cytomegalovirus serostatus of donor and recipient before hematopoietic stem cell transplantation in the era of antiviral prophylaxis and preemptive therapy. Blood 103: 2003-2008.
44. Comoli P, Basso S, Zecca M, Pagliara D, Baldanti F, et al. (2007) Preemptive therapy of EBV-related lymphoproliferative disease after pediatric haploidentical stem cell transplantation. Am J Transplant 7: 1648-1655.
45. Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, et al. (2005) Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105: 3051-3057.
46. Linn YC, Niam M, Chu S, Choong A, Yong HX, et al. (2012) The anti-tumour activity of allogeneic cytokine-induced killer cells in patients who relapse after allogeneic transplant for haematological malignancies. Bone Marrow Transplant 47: 957-966.
47. Veltrop-Duits LA, Heemskerk B, Sombroek CC, van Vreeswijk T, Gubbels S, et al. (2006) Human CD4+ T cells stimulated by conserved adenovirus 5 hexon peptides recognize cells infected with different species of human adenovirus. Eur J Immunol 36: 2410-2423.
48. Chen BJ, Deoliveira D, Cui X, Le NT, Son J, et al. (2007) Inability of memory T cells to induce graft-versus-host disease is a result of an abortive alloresponse. Blood 109: 3115-3123.
49. Melenhorst JJ, Leen AM, Bollard CM, Quigley MF, Price DA, et al. (2010) Allogeneic virus-specific T cells with HLA alloreactivity do not produce GVHD in human subjects. Blood 116: 4700-4702.