Peptide vaccines for hematological malignancies: A missed promise?

International Journal of Hematology

Volumn 99, Issue 2, 2014, Pages 107-116

  Bocchia, Monica ^a   Defina, Marzia ^a   Aprile, Lara ^a   Sicuranza, Anna ^a  

^a UNIVERSITY OF SIENA   (Italy)

Author keywords

Antigens; Hematological malignancies; Immunotherapy; Leukemia; Peptide vaccines

Indexed keywords

ANIMALS; CANCER VACCINES; HEMATOLOGIC NEOPLASMS; HUMANS; IMMUNOTHERAPY; NEOPLASM RECURRENCE, LOCAL; RECURRENCE; VACCINES, SUBUNIT;

EID: 84894414879     PISSN: 09255710     EISSN: 18653774     Source Type: Journal    
DOI: 10.1007/s12185-013-1497-3     Document Type: Article

References (77)

1. Horowitz MM, Gale RP, Sondel PM, Goldman JM, Kersey J, Kolb HJ, et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood. 1990;75:555-62.
2. Collins RH Jr, Shpilberg O, Drobyski WR, Porter DL, Giralt S, Champlin R, et al. Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation. J Clin Oncol. 1997;15:433-44.
3. Tricot G, Vesole DH, Jagannath S, Hilton J, Munshi N, Barlogie B. Graft-versus-myeloma effect: proof of principle. Blood. 1996;87:1196-8.
4. Pardoll DM. Cancer vaccines. Nat Med. 1998;4:525-31.
5. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van der Eynde B, et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 1991;254:1643-7.
6. Novellino L, Castelli C, Parmiani G. A listing of human tumor antigens recognized by T cells: March 2004 update. Cancer Immunol Immunother. 2005;54:187-207.
7. Traversari C, van der Bruggen P, Luescher IF, Lurquin C, Chomez P, Van Pel A, et al. A nonapeptide encoded by human gene MAGE-1 is recognized on HLA-A1 by cytolytic T lymphocytes directed against tumor antigen MZ2-E. J Exp Med. 1992;176:1453-7.
8. van Baren N, Brasseur F, Godelaine D, Hames G, Ferrant A, Lehmann F, et al. Genes encoding tumor-specific antigens are expressed in human myeloma cells. Blood. 1999;94:1156-64.
9. Greiner J, Ringhoffer M, Simikopinko O, Szmaragowska A, Huebsch S, Maurer U, et al. Simultaneous expression of different immunogenic antigens in acute myeloid leukemia. Exp Hematol. 2000;28:1413-22.
10. Molldrem J, Dermime S, Parker K, Jiang YZ, Mavroudis D, Hensel N, et al. Targeted T-cell therapy for human leukemia: cytotoxic T lymphocytes specific for a peptide derived from proteinase 3 preferentially lyse human myeloid leukemia cells. Blood. 1996;88:2450-7.
11. Bergmann L, Maurer U, Weidmann E. Wilms tumor gene expression in acute myeloid leukemias. Leuk Lymphoma. 1997;25:435-43.
12. Takahashi T, Makiguchi Y, Hinoda Y, Kakiuchi H, Nakagawa N, Imai K, et al. Expression of MUC1 on myeloma cells and induction of HLA-unrestricted CTL against MUC1 from a multiple myeloma patient. J Immunol. 1994;153:2102-9.
13. Bocchia M, Wentworth PA, Southwood S, Sidney J, McGraw K, Scheinberg DA, et al. Specific binding of leukemia oncogene fusion protein peptides to HLA class I molecules. Blood. 1995;85:2680-4.
14. Disis ML, Cheever MA. Oncogenic proteins as tumor antigens. Curr Opin Immunol. 1996;8:637-42.
15. Bendandi M. Idiotype vaccines for lymphoma: proof of principles and clinical trial failures. Nat Rev Cancer. 2009;9:675-81.
16. Stevenson G, Elliott TE, Stevenson FK. Idiotypic determinants on the surface immunoglobulin of neoplastic lymphocytes: a therapeutic target. Fed Proc. 1977;36:2268-71.
17. Unanue ER, Cerottini JC. Antigen presentation. FASEB J. 1989;3:2496-502.
18. Kirkwood JM, Strawderman MH, Ernstoff MS, Smith TJ, Borden EC, Blum RH. Interferon alpha-2b adjuvant therapy of high risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J Clin Oncol. 1996;14:7-17.
19. Rosemberg SA, Yang JC, Topalian SL, Schwartzentruber DJ, Weber JS, Parkinson DR, et al. Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high dose bolus interleukin-2. JAMA. 1994;271:907-13.
20. de Visser KE, Cordaro TA, Kessels HW, Tirion FH, Schumacher TN, Kruisbeek AM. Low avidity self-specific T cells display a pronounced expansion defect that can be overcome by altered peptide-ligands. J Immunol. 2001;167:3818-28.
21. Toes RE, Offringa R, Blom RJ, Melief CJ, Kast WM. Peptide vaccination can lead to enhanced tumor growth through specific T-cell tolerance induction. Proc Natl Acad Sci USA. 1996;93:7855-60.
22. Srinivasan M, Domanico SZ, Kaumaya PT, Pierce SK. Peptides of 23 residues or greater are required to stimulate a high affinity class II-restricted T cell response. Eur J Immunol. 1993;23:1011-6.
23. Janssen EM, Droin NM, Lemmens EE, Pinkoski MJ, Bensinger SJ, Ehst BD, et al. CD4 + T cell help helps control CD8 + T-cell memory via TRAIL-mediated activation-induced cell death. Nature. 2010;434:88-93.
24. Nishikawa H, Jager E, Ritter G, Old LJ, Gnjatic S. CD4 + CD25 + regulatory T cells control the induction of antigen-specific CD4 + helper T cell responses in cancer patients. Blood. 2005;106:1008-11.
25. Ichihara F, Kono K, Takahashi A, Kawaida H, Sugai H, Fujii H. Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers. Clin Cancer Res. 2003;9:4404-8.
26. Sasada T, Kimura M, Yoshida Y, Kanai M, Takabayashi A. CD4 + CD25 + regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer. 2003;98:1089-99.
27. Emadi A, Jones RJ, Brodsky RA. Cyclophosphamide and cancer: golden anniversary. Nat Rev Clin Oncol. 2009;6:638-47.
28. Mahnke K, Schonfeld K, Fondel S, Ring S, Karakhanova S, Wiedemeyer K, et al. Depletion of CD4 + CD25 + human regulatory T cells in vivo: kinetics of Treg depletion and alterations in immune functions in vivo and in vitro. Int J Cancer. 2007;120:2723-33.
29. Rech AJ, Vonderheide RH. Clinical use of anti-CD25 antibody daclizumab to enhance immune responses to tumor antigen vaccination by targeting regulatory T cells. Ann NY Acad Sci. 2009;1174:99-106.
30. Fraser CK, Diener KR, Brown MP, Hayball JD. Improving vaccines by incorporating immunological coadjuvants. Exp Rev Vaccines. 2007;6:559-78.
31. Bendandi M, Gocke CD, Kobrin CB, Benko FA, Sternas LA, Pennington R, et al. Complete molecular remissions induced by patient-specific vaccination plus granulocyte-monocyte colony-stimulating factor against lymphoma. Nat Med. 1999;5:1171-7.
32. Kusmartsev S, Gabrilovich DI. Immature myeloid cells and cancer-associated immune suppression. Cancer Immunol Immunother. 2002;51:293-8.
33. Parmiani G, Castelli C, Pilla L, Santinami M, Colombo P, Rivoltini L. Opposite immune functions of GM-CSF administered as vaccine adjuvant in cancer patients. Ann Oncol. 2007;18:226-32.
34. Aggarwal S, van de Loosdrecht AA, Alhan C, Ossenkoppele GJ, Westers TM, Bontkes HJ. Role of immune responses in the pathogenesis of low-risk MDS and high-risk MDS: implications for immunotherapy. Br J Haematol. 2011;153:568-81.
35. Qazilbash MH, Wieder ED, Thall PF, Wang X, Rios RL, Lu S, et al. PR1 peptide vaccine-induced immune response is associated with better event-free survival in patients with myeloid leukemia. [Abstract]. Blood. 2007;110:283.
36. Greiner J, Schmitt A, Giannopoulos K, Rojewski MT, Götz 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.
37. Oka Y, Tsuboi A, Taguchi T, Osaki T, Kyo T, Nakajima H, et al. Induction of WT1 (Wilms' tumor gene)-specific cytotoxic T lymphocytes by WT1 peptide vaccine and the resultant cancer regression. Proc Natl Acad Sci USA. 2004;101:13885-90.
38. Keilholz U, Letsch A, Busse A, Asemissen AM, Bauer S, Blau IW, et al. A clinical and immunologic phase 2 trial of Wilms tumor gene product 1 (WT1) peptide vaccination in patients with AML and MDS. Blood. 2009;113:6541-8.
39. Maslak PG, Dao T, Krug LM, Chanel S, Korontsvit T, Zakhaleva V, et al. Vaccination with synthetic analog peptides derived from WT1 oncoprotein induces T-cell responses in patients with complete remission from acute myeloid leukemia. Blood. 2010;116:171-9.
40. Sugiyama H, Tsuboi A, Oka Y, Kio T, Katayama Y, Olga E, et al. Long-term WT1 peptide vaccination over 7 years for 3 AML patients with molecular relapse. [Abstract]. Blood. 2010;116:3295.
41. Rezvani K, Yong AS, Mielke S, Savani BN, Musse L, Superata J, et al. Leukemia-associated antigen specific T-cell responses following combined PR1 and WT1 peptide vaccination in patients with myeloid malignancies. Blood. 2008;111:236-42.
42. Rezvani K, Yong AS, Mielke S, Jafarpour B, Savani BN, Le RQ, et al. Repeated PR1 and WT1 peptide vaccination in Montanide-adjuvant fails to induce sustained high-avidity, epitope-specific CD8+ T cells in myeloid malignancies. Haematologica. 2011;96:432-40.
43. Sugiyama H. Wilms' tumor gene WT1: its oncogenic function and clinical application. Int J Hematol. 2001;73:177-87.
44. Elisseeva OA, Oka Y, Tsuboi A, Ogata K, Wu F, Kim EH, et al. Humoral immune responses against Wilms tumor gene WT1 product in patients with hematopoietic malignancies. Blood. 2002;99:3272-9.
45. Ochsenreither S, Fusi A, Geikowski A, Stather D, Busse A, Stroux A, et al. Wilms' tumor protein 1 (WT1) peptide vaccination in AML patients: predominant TCR CDR3β sequence associated with remission in one patient is detectable in other vaccinated patients. Cancer Immunol Immunother. 2012;61:313-22.
46. Padua RA, Chomienne C. Use of animal models for the treatment of leukemias: efficacy of DNA vaccination combined with ATRA. Discov Med. 2004;4:41-4.
47. Bocchia M, Ippoliti M, Gozzetti A, Abruzzese E, Calabrese S, Amabile M, et al. CD34+/Ph+cells are still detectable in chronic myeloid leukaemia patients with sustained and prolonged complete cytogenetic remission during treatment with imatinib mesylate. Leukemia. 2007;22:426-8.
48. Bocchia M, Korontsvit T, Xu Q, Mackinnon S, Yang SY, Sette A, et al. Specific human cellular immunity to bcr-abl oncogene derived peptides. Blood. 1996;87:3587-92.
49. Clark RE, Dodi IA, Hill SC, Lill JR, Aubert G, Macintyre AR, et al. Direct evidence that leukemic cells present HLA-associated immunogenic peptides derived from the BCR-ABL b3a2 fusion protein. Blood. 2001;98:2887-93.
50. Pinilla-Ibarz J, Cathcart K, Korontsvit T, Soignet S, Bocchia M, Caggiano J, et al. Vaccination of patients with chronic myelogenous leukemia with bcr-abl oncogene breakpoint fusion peptides generates specific immune responses. Blood. 2000;95:1781-7.
51. Cathcart K, Pinilla-Ibarz J, Korontsvit T, Schwartz J, Zakhaleva V, Papadopoulos EB, et al. A multivalent bcr-abl fusion peptide vaccination trial in patients with chronic myeloid leukemia. Blood. 2004;103:1037-42.
52. Bocchia M, Gentili S, Abruzzese E, Fanelli A, Iuliano F, Tabilio A, et al. Effect of a p210 multipeptide vaccine associated with imatinib or interferon in patients with chronic myeloid leukaemia and persistent residual disease: a multicentre observational trial. Lancet. 2005;365:657-62.
53. Rojas JM, Knight K, Wang L, Clark RE. Clinical evaluation of BCR-ABL peptide immunization in chronic myeloid leukaemia: results of the EPIC study. Leukemia. 2007;21:2287-95.
54. Maslak PG, Dao T, Gomez M, Chanel S, Packin J, Korontsvit T, Zakhaleva V, et al. A pilot vaccination trial of synthetic analog peptides derived from the BCR-ABL breakpoints in CML patients with minimal disease. Leukemia. 2008;22:1613-6.
55. Jain N, Reuben JM, Kantarjian H, Li C, Gao H, Lee BN, Cohen EN, et al. Synthetic tumor-specific breakpoint peptide vaccine in patients with chronic myeloid leukemia and minimal residual disease: a phase 2 trial. Cancer. 2009;115:3924-34.
56. Bocchia M, Defina M, Ippoliti M, Amabile M, Breccia M, Iuliano F, et al. BCR-ABL derived peptide vaccine in chronic myeloid leukemia patients with molecular minimal residual disease during imatinib: interim analysis of a phase 2 multicenter GIMEMA CML working party trial [Abstract]. Blood. 2009;114:648.
57. Deinenger M, O'Brien S, Guilhot F, Goldman JM, Hochhaus A, Hughes TP, et al. International randomized study of Interferon vs STI571 (IRIS) 8-year follow up: sustained survival and low risk for progression on events in patients with newly diagnosed chronic myeloid leukemia in chronic phase (CML-CP) treated with imatinib. [Abstract]. Blood. 2009;114:1126.
58. Brauer KM, Werth D, von Schwarzenberg K, Bringmann A, Kanz L, Grünebach F, et al. BCR-ABL activity is critical for the immunogenicity of chronic myelogenous leukemia cells. Cancer Res. 2007;67:5489-97.
59. Vonka V. Immunotherapy of chronic myeloid leukemia: present state and future prospects. Immunotherapy. 2010;2:227-41.
60. Schetelig J, Kiani A, Schmitz M, Ehninger G, Bornhäuser M. T cell-mediated graft-versus-leukemia reactions after allogeneic stem cell transplantation. Cancer Immunol Immunother. 2005;54:1043-58.
61. Yi Q, Osterborg A, Bergenbrant S, Mellstedt H, Holm G, Lefvert AK. Idiotype-reactive T-cell subsets and tumor load in monoclonal gammopathies. Blood. 1995;86:3043-9.
62. Osterborg A, Yi Q, Henriksson L, Fagerberg J, Bergenbrant S, Jeddi-Tehrani M, et al. Idiotype immunization combined with granulocyte- macrophage colony-stimulating factor in myeloma patients induced type I, major histocompatibility complex-restricted, CD8- and CD4-specific T-cell responses. Blood. 1998;91:2459-66.
63. Rasmussen T, Hansson L, Osterborg A, Johnsen HE, Mellstedt H. Idiotype vaccination in multiple myeloma induced a reduction of circulating clonal tumor B cells. Blood. 2003;11:4607-10.
64. Coscia M, Mariani S, Battaglio S, Di Bello C, Fiore F, Foglietta M, et al. Long-term follow-up of idiotype vaccination in human myeloma as a maintenance therapy after high-dose chemotherapy. Leukemia. 2004;1:139-45.
65. Foglietta M, Neelapu SS, Kwak LW, Jiang Y, Nattamai D, Lee ST, et al. Neoantigen and tumor antigen-specific immunity transferred from immunized donors is detectable early after allogeneic transplantation in myeloma patients. Bone Marrow Transplant. 2013;48:269-77.
66. Szmania S, Tricot G, van Rhee F. NY-ESO-1 immunotherapy for multiple myeloma. Leukemia Lymphoma. 2006;47:2037-48.
67. Kuball J, de Boer K, Wagner E, Wattad M, Antunes E, Weeratna RD, et al. Pitfalls of vaccinations with WT1-, Proteinase3- and MUC1-derived peptides in combination with MontanideISA51 and CpG7909. Cancer Immunol Immunother. 2011;60:161-71.
68. Qian J, Zheng Y, Zheng C, Wang L, Qin H, Hong S, et al. Active vaccination with Dickkopf-1 induces protective and therapeutic antitumor immunity in murine multiple myeloma. Blood. 2012;119:161-9.
69. Biernacki MA, Tai YT, Zhang GL, Alonso A, Zhang W, Prabhala R, et al. Novel myeloma-associated antigens revealed in the context of syngeneic hematopoietic stem cell transplantation. Blood. 2012;119:3142-50.
70. Kang YJ, Zeng W, Song W, Reinhold B, Choi J, Brusic V, et al. Identification of human leucocyte antigen (HLA)-A*0201-restricted cytotoxic T lymphocyte epitopes derived from HLA-DOβ as a novel target for multiple myeloma. Br J Haematol. 2013;163:343-51.
71. Giannopoulos K, Własiuk P, Dmoszyńska A, Roliński J, Schmitt M. Peptide vaccination induces profound changes in the immune system in patients with B-cell chronic lymphocytic leukemia. Folia Histochem Cytobiol. 2011;49:161-7.
72. Dubensky TW Jr, Reed SG. Adjuvants for cancer vaccines. Semin Immunol. 2010;22:155-61.
73. Schuster SJ, Neelapu SS, Gause BL, Janik JE, Muggia FM, Gockerman JP, et al. Vaccination with patient-specific tumor-derived antigen in first remission improves disease-free survival in follicular lymphoma. Clin Oncol. 2011;29:2787-94.
74. Levy R, Robertson MJ, Ganjoo K, Leonard J, Vose J, Denney DJ. Results of a Phase 3 trial evaluating safety and efficacy of specific immunotherapy, recombinant idiotype (Id) conjugated to KLH (Id-KLH) with GM-CSF, compared with non-specific immunotherapy, KLH with GM-CSF, in patients with follicular non-Hodgkin's lymphoma (fNHL). AACR Meeting Abstracts. 2008;LB-204.
75. Freedman A, Neelapu SS, Nichols C, Robertson MJ, Djulbegovic B, Winter JN, et al. Placebo-controlled phase III trial of patient-specific immunotherapy with mitumprotimut-T and granulocyte-macrophage colony-stimulating factor after rituximab in patients with follicular lymphoma. J Clin Oncol. 2009;27:3036-43.
76. Rubio V, Stuge TB, Singh N, Betts MR, Weber JS, Roederer M, et al. Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat Med. 2003;9:1377-82.
77. Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, Hodge JW. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res. 2004;64:4328-37.