Off-the-shelf virus-specific T cells to treat BK virus, human herpesvirus 6, cytomegalovirus, Epstein-Barr virus, and adenovirus infections after allogeneic hematopoietic stem-cell transplantation

Journal of Clinical Oncology

Volumn 35, Issue 31, 2017, Pages 3547-3557

  Tzannou, Ifigeneia ^a   Papadopoulou, Anastasia ^a   Naik, Swati ^a   Leung, Kathryn ^a   Martinez, Caridad A ^a   Ramos, Carlos A ^a   Carrum, George ^a   Sasa, Ghadir ^a   Lulla, Premal ^a   Watanabe, Ayumi ^a   Kuvalekar, Manik ^a   Gee, Adrian P ^a   Wu, Meng Fen ^b   Liu, Hao ^b   Grilley, Bambi J ^a   Krance, Robert A ^a   Gottschalk, Stephen ^a   Brenner, Malcolm K ^a   Rooney, Cliona M ^a   Heslop, Helen E ^a   Leen, Ann M ^a   Omer, Bilal ^a   more..

^a HOUSTON METHODIST HOSPITAL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; BUDESONIDE; CD3 ANTIGEN; CD45RA ANTIGEN; CD56 ANTIGEN; CHEMOKINE RECEPTOR CCR7; CIDOFOVIR; CORTICOSTEROID; CREATININE; CYCLOSPORIN; FOSCARNET; GANCICLOVIR; L SELECTIN; NARCOTIC ANALGESIC AGENT; PREDNISONE; RAPAMYCIN; STEROID; TACROLIMUS; TOPICAL AGENT; TRIAMCINOLONE;

ABDOMINAL CRAMP; ACUTE GRAFT VERSUS HOST DISEASE; ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOID LEUKEMIA; ADENOVIRIDAE; ADENOVIRUS INFECTION; ADOPTIVE TRANSFER; ADULT; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANTIVIRAL RESISTANCE; ANTIVIRAL THERAPY; ARTICLE; BACTERIAL INFECTION; BK VIRUS; BK VIRUS INFECTION; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHRONIC GRAFT VERSUS HOST DISEASE; CLINICAL ARTICLE; CLINICAL EFFECTIVENESS; CLINICAL OUTCOME; COLITIS; CORTICOSTEROID THERAPY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DRUG DOSE REDUCTION; DRUG MEGADOSE; EFFECTOR CELL; ENTERITIS; EPITOPE MAPPING; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; FEASIBILITY STUDY; FEMALE; FEVER; GASTROINTESTINAL DISEASE; GRAFT INFECTION; GRAFT VERSUS HOST REACTION; HEMATURIA; HEMORRHAGIC CYSTITIS; HERPES SIMPLEX ENCEPHALITIS; HERPES VIRUS INFECTION; HUMAN; HUMAN HERPESVIRUS 6; HYDRONEPHROSIS; IMMUNOSUPPRESSIVE TREATMENT; INFECTION RATE; KIDNEY DYSFUNCTION; LYMPHOCYTE FUNCTION; LYMPHOMA; MALE; MEMORY T LYMPHOCYTE; MULTIPLE MYELOMA; MYELODYSPLASTIC SYNDROME; NEPHRITIS; PATIENT SAFETY; PHASE 2 CLINICAL TRIAL; POSTTRANSPLANT LYMPHOPROLIFERATIVE DISEASE; PRIORITY JOURNAL; RETREATMENT; SKIN DISEASE; STEROID THERAPY; T LYMPHOCYTE; TOPICAL TREATMENT; TREATMENT RESPONSE; URINARY TRACT INFECTION; VIRAL UPPER RESPIRATORY TRACT INFECTION; VIRUS LOAD; VIRUS PNEUMONIA; VIRUS SPECIFIC T LYMPHOCYTE; ADOPTIVE IMMUNOTHERAPY; ALLOTRANSPLANTATION; CLINICAL TRIAL; DNA VIRUS; DNA VIRUS INFECTIONS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN ADENOVIRUS C; IMMUNOLOGY; PROCEDURES; TRANSPLANTATION; TREATMENT OUTCOME; VIROLOGY;

ADENOVIRUSES, HUMAN; ADULT; BK VIRUS; DNA VIRUS INFECTIONS; DNA VIRUSES; FEMALE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HERPESVIRUS 4, HUMAN; HERPESVIRUS 6, HUMAN; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MALE; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS; TREATMENT OUTCOME;

EID: 85032449683     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2017.73.0655     Document Type: Article

References (43)

1. Locatelli F, Crotta A, Ruggeri A, et al: Analysis of risk factors influencing outcomes after cord blood transplantation in children with juvenile myelomonocytic leukemia: A EUROCORD, EBMT, EWOG-MDS, CIBMTR study. Blood 122:2135-2141, 2013
2. Gratwohl A, Brand R, Frassoni F, et al: Cause of death after allogeneic hematopoietic stem cell transplantation (HSCT) in early leukaemias: An EBMT analysis of lethal infectious complications and changes over calendar time. Bone Marrow Transplant 36:757-769, 2005
3. Styczynski J, Einsele H, Gil L, et al: Outcome of treatment of Epstein-Barr virus-related posttransplant lymphoproliferative disorder in hematopoietic stem cell recipients: A comprehensive review of reported cases. Transpl Infect Dis 11:383-392, 2009
4. Gilis L, Morisset S, Billaud G, et al: High burden of BK virus-associated hemorrhagic cystitis in patients undergoing allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant 49: 664-670, 2014
5. Jain NA, Lu K, Ito S, et al: The clinical and financial burden of pre-emptive management of cytomegalovirus disease after allogeneic stem cell transplantation: Implications for preventative treatment approaches. Cytotherapy 16:927-933, 2014
6. Broers AE, van Der Holt R, van Esser JW, et al: 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, 2000
7. Tzannou I, Leen AM: Preventing stem cell transplantation-associated viral infections using T-cell therapy. Immunotherapy 7:793-810, 2015
8. Heslop HE, Slobod KS, Pule MA, et al: Longterm outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 115:925-935, 2010
9. Feucht J, Opherk K, Lang P, et al: Adoptive T-cell therapy with hexon-specific Th1 cells as a treatment of refractory adenovirus infection after HSCT. Blood 125:1986-1994, 2015
10. Einsele H, Roosnek E, Rufer N, et al: Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 99:3916-3922, 2002
11. Leen AM,Myers GD, Sili U, et al: Monoculturederived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. NatMed 12:1160-1166, 2006
12. Gerdemann U, Katari UL, Papadopoulou A, et al: Safety and clinical efficacy of rapidly-generated trivirus-directed T cells as treatment for adenovirus, EBV, and CMV infections after allogeneic hematopoietic stem cell transplant. Mol Ther 21:2113-2121, 2013
13. Papadopoulou A, Gerdemann U, Katari UL, et al: Activity of broad-spectrum T cells as treatment for AdV, EBV, CMV, BKV, and HHV-6 infections after HSCT. Sci Transl Med 6:242ra83, 2014
14. Peggs KS, Thomson K, Samuel E, et al: Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stemcell transplantation.Clin Infect Dis 52:49-57, 2011
15. Icheva V, Kayser S, Wolff D, 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. J Clin Oncol 31:39-48, 2013
16. Tzannou I, Leen AM: Accelerating immune reconstitution after hematopoietic stem cell transplantation. Clin Transl Immunology 3:e11, 2014
17. Peggs KS, Verfuerth S, Pizzey A, et al: Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 362:1375-1377, 2003
18. Blyth E, Clancy L, Simms R, et al: Donor-derived CMV-specific T cells reduce the requirement for CMVdirected pharmacotherapy after allogeneic stem cell transplantation. Blood 121:3745-3758, 2013
19. Feuchtinger T, Richard C, Joachim S, et al: 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, 2008
20. Doubrovina E, Oflaz-Sozmen B, Prockop SE, et al: Adoptive immunotherapy with unselected or EBV-specific T cells for biopsy-proven EBV+ lymphomas after allogeneic hematopoietic cell transplantation. Blood 119:2644-2656, 2012
21. Vickers MA, Wilkie GM, Robinson N, et al: Establishment and operation of a GoodManufacturing Practice-compliant allogeneic Epstein-Barr virus (EBV)-specific cytotoxic cell bank for the treatment of EBVassociated lymphoproliferative disease. Br J Haematol 167:402-410, 2014
22. Leen AM, Bollard CM, Mendizabal AM, et al: Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stemcell transplantation. Blood 121:5113-5123, 2013
23. Qasim W, Derniame S, Gilmour K, et al: Thirdparty virus-specific T cells eradicate adenoviraemia but trigger bystander graft-versus-host disease. Br J Haematol 154:150-153, 2011
24. Ljungman P, de la Camara R, Cordonnier C, et al: Management of CMV, HHV-6, HHV-7 and Kaposi-sarcoma herpesvirus (HHV-8) infections in patients with hematological malignancies and after SCT. Bone Marrow Transplant 42:227-240, 2008
25. Bedi A, Miller CB, Hanson JL, et al: Association of BK virus with failure of prophylaxis against hemorrhagic cystitis following bone marrow transplantation. J Clin Oncol 13:1103-1109, 1995
26. Gerdemann U, Keukens L, Keirnan JM, et al: Immunotherapeutic strategies to prevent and treat human herpesvirus 6 reactivation after allogeneic stem cell transplantation. Blood 121: 207-218, 2013
27. Halawi M, Khan N, Blake N: Identification of novel CD8+ T cell epitopes in human herpesvirus 6B U11 and U90. Immun Inflamm Dis 3:118-131, 2015
28. Iampietro M, Morissette G, Gravel A, et al: Human herpesvirus 6B immediate-early I protein contains functional HLA-A-02, HLA-A-03, and HLAB-07 class I restricted CD8(+) T-cell epitopes. Eur J Immunol 44:3573-3584, 2014
29. Leen AM, Christin A, Khalil M, et al: Identification of hexon-specific CD4 and CD8 T-cell epitopes for vaccine and immunotherapy. J Virol 82:546-554, 2008
30. Leen AM, Sili U, Vanin EF, et al: Conserved CTL epitopes on the adenovirus hexon protein expand subgroup cross-reactive and subgroup-specific CD8+ T cells. Blood 104:2432-2440, 2004
31. Sukdolak C, Tischer S, Dieks D, et al: CMV-, EBV-and ADV-specific T cell immunity: Screening and monitoring of potential third-party donors to improve post-transplantation outcome. Biol Blood Marrow Transplant 19:1480-1492, 2013
32. Hislop AD, Taylor GS, Sauce D, et al: Cellular responses to viral infection in humans: Lessons from Epstein-Barr virus. Annu Rev Immunol 25:587-617, 2007
33. Kondo E, Akatsuka Y, Kuzushima K, et al: Identification of novel CTL epitopes of CMV-pp65 presented by a variety of HLA alleles. Blood 103: 630-638, 2004
34. Li Pira G, Bottone L, Ivaldi F, et al: Generation of cytomegalovirus (CMV)-specific CD4 T-cell lines devoid of alloreactivity, by use of a mixture of CMVphosphoprotein 65 peptides for reconstitution of the T helper repertoire. J Infect Dis 191:215-226, 2005
35. Paston SJ, Dodi IA, Madrigal JA: Progress made towards the development of a CMV peptide vaccine. Hum Immunol 65:544-549, 2004
36. Wiesner M, Zentz C, Hammer MH, et al: Selection of CMV-specific CD8+ and CD4+ T cells by mini-EBV-transformed B cell lines. Eur J Immunol 35: 2110-2121, 2005
37. Clark DA, Nacheva EP, Leong HN, et al: Transmission of integrated human herpesvirus 6 through stem cell transplantation: Implications for laboratory diagnosis. J Infect Dis 193:912-916, 2006
38. Silva Lde P, Patah PA, Saliba RM, et al: Hemorrhagic cystitis after allogeneic hematopoietic stem-cell transplants is the complex result of BK virus infection, preparative regimen intensity and donor type. Haematologica 95:1183-1190, 2010
39. Azzi A, Cesaro S, Laszlo D, et al: Human polyomavirus BK (BKV) load and haemorrhagic cystitis in bone marrow transplantation patients. J Clin Virol 14:79-86, 1999
40. Cesaro S, Hirsch HH, Faraci M, et al: Cidofovir for BK virus-associated hemorrhagic cystitis: A retrospective study. Clin Infect Dis 49:233-240, 2009
41. Giraud G, Priftakis P, Bogdanovic G, et al: BKviruria and haemorrhagic cystitis are more frequent in allogeneic haematopoietic stem cell transplant patients receiving full conditioning and unrelated-HLAmismatched grafts. Bone Marrow Transplant 41: 737-742, 2008
42. Lee YJ, Zheng J, Kolitsopoulos Y, et al: Relationship of BK polyoma virus (BKV) in the urine with hemorrhagic cystitis and renal function in recipients of T cell-depleted peripheral blood and cord blood stem cell transplantations. Biol Blood Marrow Transplant 20:1204-1210, 2014
43. Leung AY, Suen CK, Lie AK, et al: Quantification of polyoma BK viruria in hemorrhagic cystitis complicating bone marrow transplantation. Blood 98: 1971-1978, 2001