Idiotype vaccines for human B-cell malignancies

Current Pharmaceutical Design

Volumn 16, Issue 3, 2010, Pages 300-307

  Inoges, S ^a,b   Lopez Diaz De Cerio, A ^a   Soria, E ^a   Villanueva, H ^a   Pastor, F ^a   Bendandi, M ^a,b,c  

^a UNIVERSITY OF NAVARRA   (Spain)

^b Instituto de Investigación Sanitaria de Navarra   (Spain)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Clinical benefit; Clinical efficacy; Clinical trials; Idiotype; Lymphoma; Myeloma; Vaccine

Indexed keywords

CANCER VACCINE; CYCLOPHOSPHAMIDE; DENDRITIC CELL VACCINE; DOXORUBICIN; EPITOPE; GLUTARALDEHYDE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IDIOTYPE VACCINE; IMMUNOGLOBULIN IDIOTYPE; INTERFERON; INTERLEUKIN 2; KEYHOLE LIMPET HEMOCYANIN; MALEIMIDE; PREDNISOLONE; RITUXIMAB; UNCLASSIFIED DRUG; VINCRISTINE;

ANTIBODY RESPONSE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CANCER IMMUNIZATION; FOLLICULAR LYMPHOMA; HUMAN; IMMUNOGENICITY; IMMUNOMODULATION; MANTLE CELL LYMPHOMA; MULTIPLE MYELOMA; NONHODGKIN LYMPHOMA; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; VACCINE PRODUCTION;

CANCER VACCINES; CLINICAL TRIALS AS TOPIC; EPITOPES; HUMANS; IMMUNOGLOBULIN IDIOTYPES; LYMPHOMA, NON-HODGKIN; MULTIPLE MYELOMA;

EID: 77949478946     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161210790170111     Document Type: Review

References (104)

1. Bendandi M. Role of anti-idiotype vaccines in the modern treatment of human follicular lymphoma. Expert Rev Anticancer Ther 2001; 1: 65-72.
2. McCarty H, Ottensmeier CH, Hamblin TJ, Stevenson FK. Anti-idiotype vaccines. Br J Haematol 2003; 123: 770-81.
3. Bendandi M. The role of idiotype vaccines in the treatment of human B-cell malignancies. Expert Rev Vaccines 2004; 3: 163-70.
4. Baskar S, Kobrin CB, Kwak LW. Autologous lymphoma vaccines induce human T cell responses against multiple, unique epitopes. J Clin Invest 2004; 113: 1498-510.
5. Raffeld M, Neckers L, Longo DL, Cossman J. Spontaneous alteration of idiotype in a monoclonal B-cell lymphoma. Escape from detection by anti-idiotype. N Engl J Med 1985; 312: 1653-8.
6. Meeker T, Lowder J, Cleary ML, Stewart S, Warnke R, Sklar J, et al. Emergence of idiotype variants during treatment of B-cell lymphoma with anti-idiotype antibodies. N Engl J Med 1985; 312: 1658-65.
7. Kobrin CB, Bendandi M, Kwak LW. Novel secondary Ig VH gene rearrangement and in-frame Ig heavy chain complementarity-determining region III insertion/deletion variants in de novo follicular lymphoma. J Immunol 2001; 166: 2235-43.
8. Bendandi M. Idiotype vaccines for lymphoma: proof-of-principles and clinical trial failures. Nat Rev Cancer 2009; 9: 675-81.
9. Lopez-de Cerio A, Inoges S. Future of idiotypic vaccination for Bcell lymphoma. Expert Rev Vaccines 2009; 8: 43-50.
10. Houet L, Veelken H. Active immunotherapy of multiple myeloma. Eur J Cancer 2006; 42: 1653-60.
11. Bertinetti C, Simon F, Zirlik K, Heining-Mikesch K, Pfeifer D, Osterroth F, et al. Cloning of idiotype immunoglobulin genes in B cell lymphomas by anchored PCR and production of individual recombinant idiotype vaccines in Escherichia coli. Eur J Haematol 2006; 77: 395-402.
12. Kanter G, Yang J, Voloshin A, Levy S, Swartz JR, Levy R. Cellfree production of scFv fusion proteins: an efficient approach for personalized lymphoma vaccines. Blood 2007; 109: 3393-9.
13. McCormick AA, Reddy S, Reinl SJ, Cameron TI, Czerwinkski DK, Vojdani F, et al. Plant-produced idiotype vaccines for the treatment of non-Hodgkin's lymphoma: safety and immunogenicity in a phase I clinical study. Proc Natl Acad Sci USA 2008; 105: 10131-6.
14. McCarthy H, Ottensmeier CH, Hamblin TJ, Stevenson FK. Anti-idiotype vaccines. Br J Haematol 2003; 123: 770-81.
15. Sahota SS, Townsend M, Stevenson FK. Identification and assembly of V genes as idiotype-specific DNA fusion vaccines in multiple myeloma. Methods Mol Med 2005; 113: 105-19.
16. Timmerman JM, Czerwinski DK, Davis TA, Hsu FJ, Benike C, Hao ZM, et al. Idiotype-pulsed dendritic cell vaccination for B-cell lymphoma: clinical and immune responses in 35 patients. Blood 2002; 99: 1517-26.
17. Curti A, Tosi P, Comoli P, Terragna C, Ferri E, Cellini C et al. Phase I/II clinical trial of sequential subcutaneous and intravenous delivery of dendritic cell vaccination for refractory multiple myeloma using patient-specific tumour idiotype protein or idiotype (VDJ)-derived class I-restricted peptides. Br J Haematol 2007; 139: 415-24.
18. Neelapu SS, Baskar S, Gause BL, Kobrin CB, Watson TM, Frye AR, et al. Human autologous tumor-specific T-cell responses induced by liposomal delivery of a lymphoma antigen. Clin Cancer Res 2004; 10: 8309-17.
19. Kwak LW, Neelapu SS, Bishop MR. Adoptive immunotherapy with antigen-specific T cells in myeloma: a model of tumor-specific donor lymphocyte infusion. Semin Oncol 2004; 31: 37-46.
20. Bendandi M, Rodríguez-Calvillo M, Inogés S, López-Díaz de Cerio A, Pérez-Simón JA, Rodríguez-Caballero A, et al. Combined vaccination with idiotype-pulsed allogeneic dendritic cells and soluble protein idiotype for multiple myeloma patients relapsing after reduced-intensity conditioning allogeneic stem cell transplantation. Leuk Lymphoma 2006; 47: 29-37.
21. Carroll WL, Thielemans K, Dilley J, Levy R. Mouse x human heterohybridomas as fusion partners with human B cell tumors. J Immunol Methods 1986; 89: 61-72.
22. Rodríguez-Calvillo M, Inogés S, López-Díaz de Cerio A, Zabalegui N, Villanueva H, Bendandi M. Variations in "rescuability" of immunoglobulin molecules from different forms of human lymphoma: implications for anti-idiotype vaccine development. Crit Rev Oncol Hematol 2004; 52: 1-7.
23. Park HJ, Neelapu SS. Developing idiotype vaccines for lymphoma: from preclinical studies to phase III clinical trials. Br J Haematol 2008; 142: 179-91.
24. Inogés S, Rodríguez-Calvillo M, López-Díaz de Cerio A, Zabalegui N, Pérez-Calvo J, Panizo C, et al. Feasibility of idiotype vaccination in relapsed B-cell malignancies.Haematologica 2003; 88: 1438-40.
25. Houot R, Levy R. Vaccines for lymphomas: idiotype vaccines and beyond. Blood Rev 2009; 23: 137-42.
26. McCormick AA, Reddy S, Reinl SJ, Cameron TI, Czerwinkski DK, Vojdani F, et al. Plant-produced idiotype vaccines for the treatment of non-Hodgkin's lymphoma: safety and immunogenicity in a phase I clinical study.Proc Natl Acad Sci USA 2008; 105: 10131-6.
27. Kanter G, Yang J, Voloshin A, Levy S, Swartz JR, Levy R. Cellfree production of scFv fusion proteins: an efficient approach for personalized lymphoma vaccines. Blood 2007; 109: 3393-9.
28. Bertinetti C, Zirlik K, Heining-Mikesch K, Ihorst G, Dierbach H, Waller CF, et al. Phase I trial of a novel intradermal idiotype vaccine in patients with advanced B-cell lymphoma: specific immune responses despite profound immunosuppression. Cancer Res 2006; 66: 4496-502.
29. Rice J, Ottensmeier CH, Stevenson FK. DNA vaccines: precision tools for activating effective immunity against cancer. Nat Rev Cancer 2008; 8: 108-20.
30. Cull G, Durrant L, Stainer C, Haynes A, Russell N. Generation of anti-idiotype immune responses following vaccination with idiotype-protein pulsed dendritic cells in myeloma. Br J Haematol 1999; 107: 648-55.
31. Titzer S, Christensen O, Manzke O, Tesch H, Wolf J, Emmerich B, et al. Vaccination of multiple myeloma patients with idiotype-pulsed dendritic cells: immunological and clinical aspects. Br J Haematol 2000; 108: 805-16.
32. Yi Q, Desikan R, Barlogie B, Munshi N. Optimizing dendritic cellbased immunotherapy in multiple myeloma. Br J Haematol 2002; 117: 297-305.
33. Barrow L, Brown RD, Murray A, Sze DM, Pope B, Gibson J, et al. CMRF44+ dendritic cells from peripheral blood stem cell harvests of patients with myeloma as potential cellular vectors for idiotype vaccination. Leuk Lymphoma 2003; 44: 2117-22.
34. Curti A, Isidori A, Ferri E, Terragna C, Neyroz P, Cellini C, et al. Generation of dendritic cells from positively selected CD14+ monocytes for anti-tumor immunotherapy. Leuk Lymphoma 2004; 45: 1419-28.
35. Szmania S, Yi Q, Cottler-Fox M, Rosen NA, Freeman J, Kordsmeier BJ, et al. Clinical-grade myeloma Ag pre-loaded DC vaccines retain potency after cryopreservation. Cytotherapy 2005; 7: 374-84.
36. Guardino AE, Rajapaksa R, Ong KH, Sheehan K, Levy R. Production of myeloid dendritic cells (DC) pulsed with tumor-specific idiotype protein for vaccination of patients with multiple myeloma. Cytotherapy 2006; 8: 277-89.
37. Brown RD, Pope B, Murray A, Esdale W, Sze DM, Gibson J, et al. Dendritic cells from patients with myeloma are numerically normal but functionally defective as they fail to up-regulate CD80 (B7-1) expression after huCD40LT stimulation because of inhibition by transforming growth factor-beta1 and interleukin-10. Blood 2001; 98: 2992-8.
38. Brimnes MK, Svane IM, Johnsen HE. Impaired functionality and phenotypic profile of dendritic cells from patients with multiple myeloma. Clin Exp Immunol 2006; 144: 76-84.
39. Cesco-Gaspere M, Benvenuti F, Burrone OR. BCL1 lymphoma protection induced by idiotype DNA vaccination is entirely dependent on anti-idiotypic antibodies. Cancer Immunol Immunother 2005; 54: 351-8.
40. Cohen S, Haimovich J, Hollander N. B-cell lymphoma and myeloma protection induced by idiotype vaccination with dendritic cells is mediated entirely by T cells in mice. J Immunother 2005; 28: 461-6.
41. Neelapu SS, Baskar S, Gause BL, Kobrin CB, Watson TM, Frye AR, et al. Human autologous tumor-specific T-cell responses induced by liposomal delivery of a lymphoma antigen. Clin Cancer Res 2004; 10: 8309-17.
42. Kwak LW, Taub DD, Duffey PL, Bensinger WI, Bryant EM, Reynolds CW, et al. Transfer of myeloma idiotype-specific immunity from an actively mmunizat marrow donor. Lancet 1995; 345: 1016-20.
43. Cabrera R, Díaz-Espada F, Barrios Y, Briz M, Forés R, Barbolla L, et al. Infusion of lymphocytes obtained from a donor mmunizat with the paraprotein idiotype as a treatment in a relapsed myeloma. Bone Marrow Transplant 2000; 25: 1105-8.
44. Kwak LW, Young HA, Pennington RW, Weeks SD. Vaccination with syngeneic, lymphoma-derived immunoglobulin idiotype combined with granulocyte/macrophage colony-stimulating factor primes mice for a protective T-cell response. Proc Natl Acad Sci USA 1996; 93: 10972-7.
45. Kwak LW, Campbell MJ, Czerwinski DK, Hart S, Miller RA, Levy R. Induction of immune responses in patients with B-cell lymphoma against the surface-immunoglobulin idiotype expressed by their tumors. N Engl J Med 1992; 327: 1209-15.
46. Nelson EL, Li X, Hsu FJ, Kwak LW, Levy R, Clayberger C, et al. Tumor-specific, cytotoxic T-lymphocyte response after idiotype vaccination for B-cell, non-Hodgkin's lymphoma. Blood 1996; 88: 580-9.
47. Hsu FJ, Caspar CB, Czerwinski D, Kwak LW, Liles TM, Syrengelas A, et al. Tumor-specific idiotype vaccines in the treatment of patients with B-cell lymphoma-long-term results of a clinical trial. Blood 1997; 89: 3129-35.
48. Davis TA, Hsu FJ, Caspar CB, van Beckhoven A, Czerwinsk DK, Liles TM, et al. Idiotype vaccination following ABMT can stimulate specific anti-idiotype immune responses in patients with B-cell lymphoma. Biol Blood Marrow Transplant 2001; 7: 517-22.
49. Neelapu SS, Kwak LW, Kobrin CB, Reynolds CW, Janik JE, Dunleavy K, et al. Vaccine-induced tumor-specific immunity despite severe B-cell depletion in mantle cell lymphoma. Nat Med 2005; 11: 986-91.
50. Timmerman JM, Vose JM, Czerwinski DK, Weng WK, Ingolia D, Mayo M, et al. Tumor-specific recombinant idiotype immunization after chemotherapy as initial treatment for follicular non-Hodgkin lymphoma. Leuk Lymphoma 2009; 50: 37-46.
51. McCormick AA, Reddy S, Reinl SJ, Cameron TI, Czerwinkski DK, Vojdani F, et al. Plant-produced idiotype vaccines for the treatment of non-Hodgkin's lymphoma: safety and immunogenicity in a phase I clinical study. Proc Natl Acad Sci USA 2008; 105: 10131-6.
52. Timmerman JM, Singh G, Hermanson G, Hobart P, Czerwinski DK, Taidi B, et al. Immunogenicity of a plasmid DNA vaccine encoding chimeric idiotype in patients with B-cell lymphoma. Cancer Res 2002; 62: 5845-52.
53. Neelapu SS, Baskar S, Gause BL, Kobrin CB, Watson TM, Frye AR, et al. Human autologous tumor-specific T-cell responses induced by liposomal delivery of a lymphoma antigen. Clin Cancer Res 2004; 10: 8309-17.
54. Bendandi M. Anti-idiotype vaccines for human follicular lymphoma. Leukemia 2000; 14: 1333-9.
55. Lopez de Cerio A, Zabalegui N, Rodríguez-Calvillo M, Inogés S, Bendandi M. Anti-idiotype antibodies in cancer treatment. Oncogene 2007; 26: 3594-602.
56. Weng WK, Czerwinski D, Timmerman J, Hsu FJ, Levy R. Clinical outcome of lymphoma patients after idiotype vaccination is correlated with humoral immune response and immunoglobulin G Fc receptor genotype. J Clin Oncol 2004; 22: 4717-24.
57. Weng WK, Czerwinski D, Levy R. Humoral immune response and immunoglobulin G Fc receptor genotype are associated with better clinical outcome following idiotype vaccination in follicular lymphoma patients regardless of their response to induction chemotherapy. Blood 2007; 109: 951-3.
58. Inoges S, Lopez-Diaz de Cerio A, Zabalegui N, Soria E, Villanueva H, Panizo C, et al. Prolonged idiotypic vaccination against follicular lymphoma. Leuk Lymphoma 2009; 50: 47-53.
59. Bergenbrant S, Yi Q, Osterborg A, Björkholm M, Osby E, Mellstedt H, et al. Modulation of anti-idiotypic immune response by immunization with the autologous M-component protein in multiple myeloma patients. Br J Haematol 1996; 92: 840-6.
60. Massaia M, Borrione P, Battaglio S, Mariani S, Beggiato E, Napoli P, et al. Idiotype vaccination in human myeloma: generation of tumor-specific immune responses after high-dose chemotherapy. Blood 1999; 94: 673-83.
61. Li Y, Bendandi M, Deng Y, Dunbar C, Munshi N, Jagannath S, et al. Tumor-specific recognition of human myeloma cells by idiotype-induced CD8(+) T cells. Blood 2000; 96: 2828-33.
62. Reichardt VL, Okada CY, Liso A, Benike CJ, Stockerl-Goldstein KE, Engleman EG, et al. Idiotype vaccination using dendritic cells after autologous peripheral blood stem cell transplantation for multiple myeloma-a feasibility study. Blood 1999; 93: 2411-9.
63. Titzer S, Christensen O, Manzke O, Tesch H, Wolf J, Emmerich B, et al. Vaccination of multiple myeloma patients with idiotype-pulsed dendritic cells: immunological and clinical aspects. Br J Haematol 2000; 108: 805-16.
64. Reichardt VL, Milazzo C, Brugger W, Einsele H, Kanz L, Brossart P. Idiotype vaccination of multiple myeloma patients using monocyte-derived dendritic cells. Haematologica 2003; 88: 1139-49.
65. Curti A, Tosi P, Comoli P, Terragna C, Ferri E, Cellini C, et al. Phase I/II clinical trial of sequential subcutaneous and intravenous delivery of dendritic cell vaccination for refractory multiple myeloma using patient-specific tumour idiotype protein or idiotype (VDJ)-derived class I-restricted peptides. Br J Haematol 2007; 139: 415-24.
66. 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; 18: 139-45.
67. Hansson L, Abdalla AO, Moshfegh A, Choudhury A, Rabbani H, Nilsson B, et al. Long-term idiotype vaccination combined with interleukin-12 (IL-12), or IL-12 and granulocyte macrophage colony-stimulating factor, in early-stage multiple myeloma patients. Clin Cancer Res 2007; 13: 1503-10.
68. Abdalla AO, Hansson L, Eriksson I, Näsman-Glaser B, Mellstedt H, Osterborg A. Long-term effects of idiotype vaccination on the specific T-cell response in peripheral blood and bone marrow of multiple myeloma patients. Eur J Haematol 2007; 79: 371-81.
69. 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.
70. Barrios Y, Cabrera R, Yáñez R, Briz M, Plaza A, Forés R, et al. Anti-idiotypic vaccination in the treatment of low-grade B-cell lymphoma. Haematologica 2002; 87: 400-7.
71. Yáñez R, Barrios Y, Ruiz E, Cabrera R, Díaz-Espada F. Anti-idiotypic Immunotherapy in follicular lymphoma patients: results of a long follow-up study. J Immunother 2008; 31: 310-2.
72. Timmerman JM, Czerwinski DK, Davis TA, Hsu FJ, Benike C, Hao ZM, et al. Idiotype-pulsed dendritic cell vaccination for B-cell lymphoma: clinical and immune responses in 35 patients. Blood 2002; 99: 1517-26.
73. Redfern CH, Guthrie TH, Bessudo A, Densmore JJ, Holman PR, Janakiraman N, et al. Phase II trial of idiotype vaccination in previously treated patients with indolent non-Hodgkin's lymphoma resulting in durable clinical responses. J Clin Oncol 2006; 24: 3107-12.
74. Gattiker HH, Wiltshaw E, Galton DA. Spontaneous regression in non-Hodgkin's lymphoma. Cancer 1980; 45: 2627-32.
75. Longo DL. Idiotype vaccination in follicular lymphoma: knocking on the doorway to cure. J Natl Cancer Inst 2006; 98: 1263-5.
76. 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; 101: 4607-10.
77. Abdalla AO, Kokhaei P, Hansson L, Mellstedt H, Osterborg A. Idiotype vaccination in patients with myeloma reduced circulating myeloma cells (CMC). Ann Oncol 2008; 19: 1172-9.
78. Inogès S, Rodrìguez-Calvillo M, Zabalegui N, Lòpez-Dìaz de Cerio A, Villanueva H, Soria E, et al. Clinical benefit associated with idiotypic vaccination in patients with follicular lymphoma. J Natl Cancer Inst 2006; 98: 1292-301.
79. Bendandi M. Aiming at a curative strategy for follicular lymphoma. CA Cancer J Clin 2008; 58: 305-17.
80. Foglietta M, Neelapu SS, Kwak LW. Therapeutic vaccines for lymphoma: from bench to bedside. USA: ASCO Educational Book: 2009; pp. 495-500.
81. Bendandi M. Clinical benefit of idiotype vaccines: too many trials for a clever demonstration? Rev Recent Clin Trials 2006; 1: 67-74.
82. Levy R, Robertson MJ, Ganjoo K, Leonard JP, Vose J, Denney D. 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 to non-specific immunotherapy, KLH with GM-CSF, in patients with follicular non-Hodgkin's lymphoma (fNHL), Proceedings of the 99th Annual Meeting of the American Association for Cancer Research 2008 April 12-16, San Diego, CA. Philadelphia, PA, AACR, 2008. Abstract LB-204 (2008).
83. 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(18): 3036-43.
84. Schuster SJ, Neelapu SS, Gause BL, Muggia FM, Gockerman JP, Sotomayor EM, et al. Idiotype vaccine therapy (BiovaxID) in follicular lymphoma in first complete remission: Phase III clinical trial results. J Clin Oncol 2009; 27: 18s (suppl; abstract 2).
85. Ai WZ, Tibshirani R, Taidi B, Czerwinski D, Levy R. Anti-idiotype antibody response after vaccination correlates with better overall survival in follicular lymphoma. Blood 2009; 113(23): 5743-6.
86. Zhu D, McCarthy H, Ottensmeier CH, Johnson P, Hamblin TJ, Stevenson FK.. Acquisition of potential N-glycosylation sites in the immunoglobulin variable region by somatic mutation is a distinctive feature of follicular lymphoma. Blood 2002; 99: 2562-8.
87. Zabalegui N, de Cerio AL, Inogés S, Rodríguez-Calvillo M, Pérez-Calvo J, Hernández M, et al. Acquired potential N-glycosylation sites within the tumor-specific heavy chains of B-cell malignancies. Haematologica 2004; 89: 541-6.
88. Radcliffe CM, Arnold JN, Suter DM, Wormald MR, Harvey DJ, Royle L, et al. Human follicular lymphoma cells contain oligomannose glycans in the antigen-binding site of the B-cell receptor. J Biol Chem 2007; 282: 7405-15.
89. Betting DJ, Mu XY, Kafi K, McDonnel D, Rosas F, Gold DP, et al. Enhanced immune stimulation by a therapeutic lymphoma tumor antigen vaccine produced in insect cells involves mannose receptor targeting to antigen presenting cells. Vaccine 2009; 27: 250-9.
90. Betting DJ, Kafi K, Abdollahi-Fard A, Hurvitz SA. Timmerman J.M. Sulfhydril-based tumor antigen-carrier protein conjugates stimulate superior antitumor immunity against B-cell lymphomas. J Immunol 2008; 181: 4131-40.
91. Kafi K, Betting DJ, Yamada RE, Bacica M, Steward KK, Timmerman JM. Maleimide conjugation markedly enhances the immunogenicity of both human and murine idiotype-KLH vaccines. Mol Immunol 2009; 46: 448-56.
92. Timmerman JM. Carrier protein conjugate vaccines: the "missing link" to improve antibody and CTL responses? Hum Vaccin 2009; 5(3): 181-3.
93. Biragyn A, Tani K, Grimm MC, Weeks S, Kwak LW. Genetic fusion of chemokines to a self tumor antigen induces protective, Tcell dependent antitumor immunity. Nat Biotechnol 1999; 17: 253-8.
94. Biragyn A, Ruffini PA, Coscia M, Harvey LK, Neelapu SS, Baskar S, et al. Chemokine receptor-mediated delivery directs self-tumor antigen efficiently into the class II processing pathway in vitro and induces protective immunity in vivo. Blood 2004; 104: 1961-9.
95. Fredriksen AB, Bogen B. Chemokine-idiotype fusion DNA vaccines are potentiated by bivalency and xenogeneic sequences. Blood 2007; 110: 1797-805.
96. Weiner GJ, Liu HM, Wooldridge JE, Dahle CE, Krieg AM. Immunostimulatory oligodeoxynucleotides containing the CpG motif are effective as immune adjuvants in tumor antigen immunization. Proc Natl Acad Sci USA 1997; 94: 10833-7.
97. Liu HM, Newbrough SE, Bhatia SK, Dahle CE, Krieg AM, Weiner GJ. Immunostimulatory CpG oligodeoxynucleotides enhance the immune response to vaccine strategies involving granulocyte-macrophage colony-stimulating factor. Blood 1998; 92: 3730-6.
98. Neelapu SS, Gause BL, Harvey L, Lee ST, Frye AR, Horton J, et al. A novel proteoliposomal vaccine induces antitumor immunity against follicular lymphoma. Blood 2007; 109: 5160-3.
99. Popescu MC, Robb RJ, Batenjany MM, Boni LT, Neville ME, Pennington RW, et al. A novel proteoliposomal vaccine elicits potent antitumor immunity in mice. Blood 2007; 109: 5407-10.
100. Moshitzky S, Kukulansky T, Haimovich J, Hollander N. Growth inhibition of myeloma cells by anti-idiotype antibodies in the absence of membrane-bound immunoglobulin. Immunol Cell Biol 2008; 86: 261-7.
101. Benaroya-Milshtein N, Apter A, Yaniv I, Kukulansky T, Raz N, Haberman Y, et al. Environmental enrichment augments the efficacy of idiotype vaccination for B-cell lymphoma. J Immunother 2007; 30: 517-22.
102. Adachi Y, Yoshio-Hoshino N, Nishimoto N. The blockade of IL-6 signaling in rational drug design. Curr Pharm Des 2008; 14(12): 1217-24.
103. Louis CU, Brenner MK. Cellular immunotherapy for neuroblastoma: a review of current vaccine and adoptive T cell therapeutics. Curr Pharm Des 2009; 15(4): 424-9.
104. Macor P, Secco E, Zorzet S, Tripodo C, Celeghini C, Tedesco F. An update on the xenograft and mouse models suitable for investigating new therapeutic compounds for the treatment of B-cell malignancies. Curr Pharm Des 2008; 14(21): 2023-39.