Peptide vaccination in the presence of adjuvants in patients after hematopoietic stem cell transplantation with CD4+ T cell reconstitution elicits consistent CD8+ T cell responses

Theranostics

Volumn 7, Issue 6, 2017, Pages 1705-1718

  Schmitt, Michael ^a,b   Schmitt, Anita ^a   Wiesneth, Markus ^c   Hückelhoven, Angela ^a   Wu, Zeguang ^d   Kuball, J ^e   Wang, Lei ^a   Schauwecker, Peter ^c   Hofmann, Susanne ^a,c   Götz, Marlies ^c   Michels, Birgit ^a   Maccari, Birgit ^c   Wuchter, Patrick ^a   Eckstein, Volker ^a   Mertens, Thomas ^d   Schnitzler, Paul ^f   Döhner, Hartmut ^c   Ho, Anthony D ^a,b   Bunjes, Donald W ^c   Dreger, Peter ^a   Schrezenmeier, Hubert ^c   Greiner, Jochen ^c,g   more..

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF ULM   (Germany)

^d UNIVERSITY HOSPITAL ULM   (Germany)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^f UNIVERSITY OF HEIDELBERG   (Germany)

^g Diakonie Hospital Stuttgart   (Germany)

Author keywords

CMV; CMVpp65

Indexed keywords

ASPARAGINYLLEUCYLVALYLPROLYLMETHIIONYLVALYLALANYLTHREONYLVALINE; NEUTRALIZING ANTIBODY; PEPTIDE VACCINE; UNCLASSIFIED DRUG; CYTOMEGALOVIRUS MATRIX PROTEIN 65KDA; CYTOMEGALOVIRUS VACCINE; IMMUNOLOGICAL ADJUVANT; MATRIX PROTEIN; PHOSPHOPROTEIN; VIRUS ANTIBODY;

ADULT; AGED; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANTIBODY TITER; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHRONIC GRAFT VERSUS HOST DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; FEMALE; FLOW CYTOMETRY; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; MALE; NONHUMAN; VACCINATION; VIRAL CLEARANCE; VIRUS REACTIVATION; BLOOD; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; TREATMENT OUTCOME;

ADJUVANTS, IMMUNOLOGIC; ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS INFECTIONS; CYTOMEGALOVIRUS VACCINES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; PHOSPHOPROTEINS; TREATMENT OUTCOME; VIRAL MATRIX PROTEINS;

EID: 85018499720     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.18301     Document Type: Article

References (45)

1. Boeckh M, Murphy WJ, Peggs KS. Reprint of: Recent advances in cytomegalovirus: an update on pharmacologic and cellular therapies. Biol Blood Marrow Transplant. 2015; 21: S19-24.
2. Ljungman P, Brand R, Hoek J, de la Camara R, Cordonnier C, Einsele H, et al. Donor cytomegalovirus status influences the outcome of allogeneic stem cell transplant: a study by the European group for blood and marrow transplantation. Clin Infect Dis. 2014; 59: 473-81.
3. Einsele H, Mielke S, Grigoleit GU. Diagnosis and treatment of cytomegalovirus 2013. Curr Opin Hematol. 2014; 21: 470-5.
4. Bacigalupo A, Bregante S, Tedone E, Isaza A, Van Lint MT, Trespi G, et al. Combined foscarnet-ganciclovir treatment for cytomegalovirus infections after allogeneic hemopoietic stem cell transplantation. Transplantation. 1996; 62: 376-80.
5. Marty FM, Ljungman P, Papanicolaou GA, Winston DJ, Chemaly RF, Strasfeld L, et al. Maribavir prophylaxis for prevention of cytomegalovirus disease in recipients of allogeneic stem-cell transplants: a phase 3, double-blind, placebo-controlled, randomised trial. Lancet Infect Dis. 2011; 11: 284-92.
6. Chemaly RF, Ullmann AJ, Stoelben S, Richard MP, Bornhauser M, Groth C, et al. Letermovir for cytomegalovirus prophylaxis in hematopoietic-cell transplantation. N Engl J Med. 2014; 370: 1781-9.
7. Boeckh M, Murphy WJ, Peggs KS. Recent advances in cytomegalovirus: an update on pharmacologic and cellular therapies. Biol Blood Marrow Transplant. 2015; 21: 24-9.
8. Ljungman P, Boeckh M, Hirsch HH, Josephson F, Lundgren J, Nichols G, et al. Definitions of Cytomegalovirus Infection and Disease in Transplant Patients for Use in Clinical Trials. Clin Infect Dis. 2017; 64: 87-91.
9. Boeckh M, Leisenring W, Riddell SR, Bowden RA, Huang ML, Myerson D, et al. Late cytomegalovirus disease and mortality in recipients of allogeneic hematopoietic stem cell transplants: importance of viral load and T-cell immunity. Blood. 2003; 101: 407-14.
10. Quinnan GV, Jr., Kirmani N, Rook AH, Manischewitz JF, Jackson L, Moreschi G, et al. Cytotoxic t cells in cytomegalovirus infection: HLA-restricted T-lymphocyte and non-T-lymphocyte cytotoxic responses correlate with recovery from cytomegalovirus infection in bone-marrow-transplant recipients. N Engl J Med. 1982; 307: 7-13.
11. Reusser P, Riddell SR, Meyers JD, Greenberg PD. Cytotoxic T-lymphocyte response to cytomegalovirus after human allogeneic bone marrow transplantation: pattern of recovery and correlation with cytomegalovirus infection and disease. Blood. 1991; 78: 1373-80.
12. Meyers JD, Flournoy N, Thomas ED. Risk factors for cytomegalovirus infection after human marrow transplantation. J Infect Dis. 1986; 153: 478-88.
13. Wills MR, Okecha G, Weekes MP, Gandhi MK, Sissons PJ, Carmichael AJ. Identification of naive or antigen-experienced human CD8(+) T cells by expression of costimulation and chemokine receptors: analysis of the human cytomegalovirus-specific CD8(+) T cell response. J Immunol. 2002; 168: 5455-64.
14. Hanley PJ, Bollard CM. Controlling cytomegalovirus: helping the immune system take the lead. Viruses. 2014; 6: 2242-58.
15. Riddell SR, Rabin M, Geballe AP, Britt WJ, Greenberg PD. Class I MHC-restricted cytotoxic T lymphocyte recognition of cells infected with human cytomegalovirus does not require endogenous viral gene expression. J Immunol. 1991; 146: 2795-804.
16. Reddehase MJ, Mutter W, Munch K, Buhring HJ, Koszinowski UH. CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity. J Virol. 1987; 61: 3102-8.
17. 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.
18. Papadopoulou A, Gerdemann U, Katari UL, Tzannou I, Liu H, Martinez C, et al. Activity of broad-spectrum T cells as treatment for AdV, EBV, CMV, BKV, and HHV6 infections after HSCT. Sci Transl Med. 2014; 6: 242ra83.
19. Odendahl M, Grigoleit GU, Bonig H, Neuenhahn M, Albrecht J, Anderl F, et al. Clinical-scale isolation of 'minimally manipulated' cytomegalovirus-specific donor lymphocytes for the treatment of refractory cytomegalovirus disease. Cytotherapy. 2014; 16: 1245-56.
20. Schmitt A, Tonn T, Busch DH, Grigoleit GU, 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: 591-9.
21. Grigoleit GU, Kapp M, Hebart H, Fick K, Beck R, Jahn G, et al. Dendritic cell vaccination in allogeneic stem cell recipients: induction of human cytomegalovirus (HCMV)-specific cytotoxic T lymphocyte responses even in patients receiving a transplant from an HCMV-seronegative donor. J Infect Dis. 2007; 196: 699-704.
22. Salguero G, Daenthanasanmak A, Munz C, Raykova A, Guzman CA, Riese P, et al. Dendritic cell-mediated immune humanization of mice: implications for allogeneic and xenogeneic stem cell transplantation. J Immunol. 2014; 192: 4636-47.
23. Nakamura R, Rosa CL, Longmate J, Drake J, Slape C, Zhou Q, et al. Viraemia, immunogenicity, and survival outcomes of cytomegalovirus chimeric epitope vaccine supplemented with PF03512676 (CMVPepVax) in allogeneic haemopoietic stem-cell transplantation: randomised phase 1b trial. Lancet Haematol. 2016; 3: e87-98.
24. Kharfan-Dabaja MA, Boeckh M, Wilck MB, Langston AA, Chu AH, Wloch MK, et al. A novel therapeutic cytomegalovirus DNA vaccine in allogeneic haemopoietic stem-cell transplantation: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Infect Dis. 2012; 12: 290-9.
25. Cardenoso L, Pinsky BA, Lautenschlager I, Aslam S, Cobb B, Vilchez RA, et al. CMV antigenemia and quantitative viral load assessments in hematopoietic stem cell transplant recipients. J Clin Virol. 2013; 56: 108-12.
26. Wu Z, Sinzger C, Reichel JJ, Just M, Mertens T. Natural killer cells can inhibit the transmission of human cytomegalovirus in cell culture by using mechanisms from innate and adaptive immune responses. J Virol. 2015; 89: 2906-17.
27. Schmitt A, Bechter C, Yao J, Goetz M, Maccari B, Schauwecker P, et al. Cytomegalovirus vaccination of leukemia and lymphoma patients after allogeneic stem cell transplantation--validation of a peptide vaccine. J Immunol Methods. 2009; 343: 140-7.
28. Greiner J, Li L, Ringhoffer M, Barth TF, Giannopoulos K, Guillaume P, et al. Identification and characterization of epitopes of the receptor for hyaluronic acid-mediated motility (RHAMM/CD168) recognized by CD8+ T cells of HLA-A2-positive patients with acute myeloid leukemia. Blood. 2005; 106: 938-45.
29. Schmitt M, Schmitt A, Reinhardt P, Thess B, Manfras B, Lindhofer H, et al. Opsonization with a trifunctional bispecific (alphaCD3 x alphaEpCAM) antibody results in efficient lysis in vitro and in vivo of EpCAM positive tumor cells by cytotoxic T lymphocytes. Int J Oncol. 2004; 25: 841-8.
30. Scheper W, van Dorp S, Kersting S, Pietersma F, Lindemans C, Hol S, et al. gammadeltaT cells elicited by CMV reactivation after allo-SCT cross-recognize CMV and leukemia. Leukemia. 2013; 27: 1328-38.
31. Aucouturier J, Dupuis L, Deville S, Ascarateil S, Ganne V. Montanide ISA 720 and 51: a new generation of water in oil emulsions as adjuvants for human vaccines. Expert Rev Vaccines. 2002; 1: 111-8.
32. Schmitt M, Schmitt A, Rojewski MT, Chen J, Giannopoulos K, Fei F, et al. RHAMM-R3 peptide vaccination in patients with acute myeloid leukemia, myelodysplastic syndrome, and multiple myeloma elicits immunologic and clinical responses. Blood. 2008; 111: 1357-65.
33. Knight A, Madrigal AJ, Grace S, Sivakumaran J, Kottaridis P, Mackinnon S, et al. The role of Vdelta2-negative gammadelta T cells during cytomegalovirus reactivation in recipients of allogeneic stem cell transplantation. Blood. 2010; 116: 2164-72.
34. Meyers JD, Bowden RA, Counts GW. Infectious complications of marrow transplant: risk factors for infection. Prog Clin Biol Res. 1989; 309: 357-66.
35. Gimenez E, Blanco-Lobo P, Munoz-Cobo B, Solano C, Amat P, Perez-Romero P, et al. Role of cytomegalovirus (CMV)-specific polyfunctional CD8+ T-cells and antibodies neutralizing virus epithelial infection in the control of CMV infection in an allogeneic stem-cell transplantation setting. J Gen Virol. 2015; 96: 2822-31.
36. Bernstein DI, Munoz FM, Callahan ST, Rupp R, Wootton SH, Edwards KM, et al. Safety and efficacy of a cytomegalovirus glycoprotein B (gB) vaccine in adolescent girls: A randomized clinical trial. Vaccine. 2016; 34: 313-9.
37. Pass RF, Zhang C, Evans A, Simpson T, Andrews W, Huang ML, et al. Vaccine prevention of maternal cytomegalovirus infection. N Engl J Med. 2009; 360: 1191-9.
38. Wloch MK, Smith LR, Boutsaboualoy S, Reyes L, Han C, Kehler J, et al. Safety and immunogenicity of a bivalent cytomegalovirus DNA vaccine in healthy adult subjects. J Infect Dis. 2008; 197: 1634-42.
39. Stachel D, Stevens-Ayers T, Boeckh M. In vitro studies of the impact of maribavir on CMV-specific cellular immune responses. J Clin Virol. 2016; 75: 53-9.
40. Parmiani G, Pilla L, Castelli C, Rivoltini L. Vaccination of patients with solid tumours. Ann Oncol. 2003; 14: 817-24.
41. Giannopoulos K, Dmoszynska A, Kowal M, Rolinski J, Gostick E, Price DA, et al. Peptide vaccination elicits leukemia-associated antigen-specific cytotoxic CD8+ T-cell responses in patients with chronic lymphocytic leukemia. Leukemia. 2010; 24: 798-805.
42. Greiner J, Schmitt A, Giannopoulos K, Rojewski MT, Gotz M, Funk I, et al. High-dose RHAMM-R3 peptide vaccination for patients with acute myeloid leukemia, myelodysplastic syndrome and multiple myeloma. Haematologica. 2010; 95: 1191-7.
43. Ravens S, Schultze-Florey C, Raha S, Sandrock I, Drenker M, Oberdorfer L, et al. Human gammadelta T cells are quickly reconstituted after stem-cell transplantation and show adaptive clonal expansion in response to viral infection. Nat Immunol. 2017.
44. Schuessler A, Walker DG, Khanna R. Cytomegalovirus as a novel target for immunotherapy of glioblastoma multiforme. Front Oncol. 2014; 4: 275.
45. Nemunaitis J, Anasetti C, Storb R, Bianco JA, Buckner CD, Onetto N, et al. Phase II trial of recombinant human granulocyte-macrophage colony-stimulating factor in patients undergoing allogeneic bone marrow transplantation from unrelated donors. Blood. 1992; 79: 2572-7.