Idiotypic vaccination for B-cell malignancies as a model for therapeutic cancer vaccines: From prototype protein to second generation vaccines

Haematologica

Volumn 87, Issue 9, 2002, Pages 989-1001

  Ruffini, Pier Adelchi ^a   Neelapu, Sattva S ^a   Kwak, Larry W ^a   Biragyn, Arya ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

B cell malignancies; Chemokines; Idiotype; Vaccine

Indexed keywords

CANCER VACCINE; CHEMOKINE; DNA VACCINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN IDIOTYPE; INTERLEUKIN 2; KEYHOLE LIMPET HEMOCYANIN; MONOCYTE CHEMOTACTIC PROTEIN 3; RECOMBINANT PROTEIN; TUMOR ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; B LYMPHOCYTE; CANCER IMMUNOTHERAPY; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DENDRITIC CELL; DRUG EFFECT; DRUG FORMULATION; DRUG POTENCY; FOLLICULAR LYMPHOMA; HUMAN; IMMUNOGENICITY; MANTLE CELL LYMPHOMA; MEDLINE; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PHASE 3 CLINICAL TRIAL; PROTEIN ENGINEERING; RANDOMIZED CONTROLLED TRIAL; REVIEW; SCISEARCH; TUMOR IMMUNITY; VACCINATION;

ANIMALS; CANCER VACCINES; CLINICAL TRIALS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOGLOBULIN IDIOTYPES; LYMPHOMA, B-CELL; MODELS, IMMUNOLOGICAL;

EID: 0036739731     PISSN: 03906078     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (110)

1. Rosenberg SA. A new era for cancer immunotherapy based on the genes that encode cancer antigens. Immunity 1999; 10:281-7.
2. Melief CJ, Kast WM. T-cell immunotherapy of tumors by adoptive transfer of cytotoxic T lymphocytes and by vaccination with minimal essential epitopes. Immunol Rev 1995; 145:167-77.
3. + T cells in antitumor immunity. Trends Immunol 2001; 22:269-76.
4. Renkvist N, Castelli C, Robbins PF, Parmiani G. A listing of human tumor antigens recognized by T cells. Cancer Immunol Immunother 2001; 50:3-15.
5. Lynch RG, Craff RG, Sirisinha S, Simms ES, Eisen HN. Myeloma proteins as tumor-specific transplantation antigens. Proc Natl Acad Sci USA 1972; 69:1540-4.
6. Syrengelas AD, Chen IT, Levy R. DNA immunization induces protective immunity against B-cell lymphoma. Nat Med 1996; 2:1038-41.
7. King CA, Spellerberg MB, Zhu D, Rice J, Sahota SS, Thompsett AR, et al. DNA vaccines with single-chain Fv fused to fragment C of tetanus toxin induce protective immunity against lymphoma and myeloma. Nat Med 1998; 4:1281-6.
8. Engering AJ, Cella M, Fluitsma D, Brockhaus M, Hoefsmit EC, Lanzavecchia A, et al. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur J Immunol 1997; 27:2417-25.
9. Guyre PM, Graziano RF, Goldstein J, Wallace PK, Morganelli PM, Wardwell K, et al. Increased potency of Fc-receptor-targeted antigens. Cancer Immunol Immunother 1997; 45:146-8.
10. Hawiger D, Inaba K, Dorsett Y, Guo M, Mahnke K, Rivera M, et al. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med 2001; 194:769-79.
11. Biragyn A, Tani K, Grimm MC, Weeks S, Kwak LW. Genetic fusion of chemokines to a self tumor antigen induces protective, T-cell dependent antitumor immunity. Nat Biotechnol 1999; 17:253-8.
12. Biragyn A, Surenhu M, Yang D, Ruffini PA, Haines BA, Klyushnenkova E, et al. Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J Immunol 2001; 167:6644-53.
13. Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML, et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994; 84:1361-92.
14. Levy R, Warnke R, Dorfman RF, Haimovich J. The monoclonality of human B-cell lymphomas. J Exp Med 1977; 145:1014-28.
15. 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.
16. 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.
17. Bendandi M, Gocke CD, Kobrin CB, Benko FA, Sternas LA, Pennington R, et al. Complete molecular remissions induced by patient-specific vaccination plus granulocytemonocyte colony-stimulating factor against lymphoma. Nat Med 1999; 5:1171-7.
18. rd Annual Meeting of the American Association for Cancer Research, San Francisco 2002; Suppl LB-125:78.
19. Zinneman HH, Hall WH. Recurrent pneumonia in multiple myeloma and some observations on immunologic response. Ann Intern Med 1954; 41:1152-70.
20. Ratta M, Fagnoni F, Curti A, Vescovini R, Sansoni P, Oliviero B, et al. Dendritic cells are functionally defective in multiple myeloma: the role of interleukin-6. Blood 2002; 100: 230-7.
21. 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-β1 and interleukin-10. Blood 2001; 98:2992-8.
22. 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.
23. Wen YJ, Barlogie B, Yi Q. Idiotype-specific cytotoxic T lymphocytes in multiple myeloma: evidence for their capacity to lyse autologous primary tumor cells. Blood 2001; 97: 1750-5.
24. Timmerman JM, Vose J, Kunkel SL, et al. A phase II study demonstrating recombinant idiotype vaccine elicits specific anti-idiotype immune responses in aggressive non-Hodgkin's lymphoma. Blood 2001; 98 Suppl 1: 341 [abstract].
25. Kugler A, Stuhler G, Walden P, Zoller G, Zobywalski A, Brossart P, et al. Regression of human metastatic renal cell carcinoma after vaccination with tumor cell-dendritic cell hybrids. Nat Med 2000; 6:332-6.
26. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392:245-52.
27. 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.
28. Hsu FJ, Benike C, Fagnoni F, Liles TM, Czerwinski D, Taidi B, et al. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat Med 1996; 2:52-8.
29. Reichardt VL, Okada CY, Liso A, Benike CJ, Stockerl-Goldstein KE, Engleman E, 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.
30. Liso A, Stockerl-Goldstein KE, Auffermann-Gretzinger S, et al. Idiotype vaccination using dendritic cells after autologous peripheral blood progenitor cell transplantation for multiple myeloma. Biol Blood Marrow Transplant 2000; 6:621-7.
31. Timmerman JM, Levy R. Linkage of foreign carrier protein to a self-tumor antigen enhances the immunogenicity of a pulsed dendritic cell vaccine. J Immunol 2000; 164: 4797-803.
32. Lim SH, Bailey-Wood R. Idiotypic protein-pulsed dendritic cell vaccination in multiple myeloma. Int J Cancer 1999; 83:215-22.
33. Liu YJ. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 2001; 106: 259-62.
34. Kwak LW, Taub DD, Duffey PL, Bensinger WI, Bryant EM, Reynolds CW, et al. Transfer of myeloma idiotype-specific immunity from an actively immunised-marrow donor. Lancet 1995; 345:1016-20.
35. Kwak LW. Tumor vaccination strategies combined with autologous peripheral stem cell transplantation. Ann Oncol 1998; 9 Suppl 1:S41-S46.
36. Offringa R, van der Burg SH, Ossendorp F, Toes RE, Melief CJ. Design and evaluation of antigen-specific vaccination strategies against cancer. Curr Opin Immunol 2000; 12: 576-82.
37. Davis TA, Maloney DG, Czerwinski DK, Liles TM, Levy R. Anti-idiotype antibodies can induce long-term complete remissions in non-Hodgkin's lymphoma without eradicating the malignant clone. Blood 1998; 92:1184-90.
38. Neelapu SS, Baskar S, Kwak LW. Detection of keyhole limpet hemocyanin (KLH)-specific immune responses by intracellular cytokine assay in patients vaccinated with idiotype-KLH vaccine. J Cancer Res Clin Oncol 2001; 127 Suppl 2: R14-R19.
39. Gocke CD, Kopreski MS, Benko FA, Sternas L, Kwak LW. Serum BCL2/IGH DNA in follicular lymphoma patients: a minimal residual disease marker. Leuk Lymphoma 2000; 39:165-72.
40. 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.
41. Kwak LW, Pennington R, Boni L, Ochoa AC, Robb RJ, Popescu MC. Liposomal formulation of a self lymphoma antigen induces potent protective antitumor immunity. J Immunol 1998; 160:3637-41.
42. Kwak LW, Pennington R, Longo DL. Active immunization of murine allogeneic bone marrow transplant donors with B-cell tumor-derived idiotype: a strategy for enhancing the specific antitumor effect of marrow grafts. Blood 1996; 87:3053-60.
43. Krolick KA, Isakson PC, Uhr JW, Vitetta ES. BCL1, a murine model for chronic lymphocytic leukemia: use of the surface immunoglobulin idiotype for the detection and treatment of tumor. Immunol Rev 1979; 48:81-106.
44. Manning LS, BergerJD, O'Donoghue HL, Sheridan GN, Claringbold PG, Turner JH. A model of multiple myeloma: culture of 5T33 murine myeloma cells and evaluation of tumorigenicity in the C57BL/KaLwRij mouse. Br J Cancer 1992; 66:1088-93.
45. Valeriote F, Grates H. MOPC-315 murine plasmacytoma as a model anticancer screen for human multiple myeloma. J Natl Cancer Inst 1986; 76:61-5.
46. Kim KJ, Kanellopoulos LC, Merwin RM, Sachs DH, Asofsky R. Establishment and characterization of BALB/c lymphoma lines with B cell properties. J Immunol 1979; 122:549-54.
47. Bergman Y, Haimovich J. Characterization of a carcinogen-induced murine B lymphocyte cell line of C3H/eB origin. Eur J Immunol 1977; 7:413-7.
48. George AJ, Folkard SG, Hamblin TJ, Stevenson FK. Idiotypic vaccination as a treatment for a B cell lymphoma. J Immunol 1988; 141:2168-74.
49. Campbell MJ, Esserman L, Byars NE, Allison AC, Levy R. Idiotype vaccination against murine B cell lymphoma. Humoral and cellular requirements for the full expression of antitumor immunity. J Immunol 1990; 145:1029-36.
50. Perek Y, Hurwitz E, Burowski D, Haimovich J. Immunotherapy of a murine B cell tumor with antibodies and F(ab′)2 fragments against idiotypic determinants of its cell surface IgM. J Immunol 1983; 131:1600-3.
51. + T-cell mediated immunity against B-cell malignancies. Nat Biotechnol 2001; 19:760-4.
52. Haimovich J, Kukulansky T, Weissman B, Hollander N. Rejection of tumors of the B cell lineage by idiotype-vaccinated mice. Cancer Immunol Immunother 1999; 47:330-6.
53. Heyfets A, Haimovich J, Hollander N. Determination of idiotype-specific T cells in idiotype-vaccinated mice. Immunol Lett 2002; 80:207-13.
54. Snodgrass HR, Fisher AM, Bruyns E, Bogen B. Restricted α/β receptor gene usage of idiotype-specific major histocompatibility complex-restricted T cells: selection for CDR3-related sequences. Eur J Immunol 1992; 22:2169-72.
55. Vitetta ES, Tucker TF, Racila E, Huang YW, Marches R, Lane N, et al. Tumor dormancy and cell signaling. V. Regrowth of the BCL1 tumor after dormancy is established. Blood 1997; 89:4425-36.
56. Huston JS, Mudgett-Hunter M, Tai MS, McCartney J, Warren F, Haber E, et al. Protein engineering of single-chain Fv analogs and fusion proteins. Methods Enzymol 1991; 203:46-88.
57. Worn A, Pluckthun A. Stability engineering of antibody single-chain Fv fragments. J Mol Biol 2001; 305:989-1010.
58. Wolff JA, Malone RW, Williams P, Chong W, Acsadi G, Jani A, et al. Direct gene transfer into mouse muscle in vivo. Science 1990; 247:1465-8.
59. Haynes JR, McCabe DE, Swain WF, Widera G, Fuller JT. Particle-mediated nucleic acid immunization. J Biotechnol 1996; 44:37-42.
60. Klinman DM, Takeshita F, Kamstrup S, Takeshita S, Ishii K, Ichino M, et al. DNA vaccines: capacity to induce auto-immunity and tolerance. Dev Biol (Basel) 2000; 104:45-51.
61. McCluskie MJ, Brazolot Millan CL, Gramzinski RA, Robinson HL, Santoro JC, et al. Route and method of delivery of DNA vaccine influence immune responses in mice and nonhuman primates. Mol Med 1999; 5:287-300.
62. Boyle CM, Robinson HL. Basic mechanisms of DNA-raised antibody responses to intramuscular and gene gun immunizations. DNA Cell Biol 2000; 19:157-65.
63. Klinman DM, Yamshchikov G, Ishigatsubo Y. Contribution of CpG motifs to the immunogenicity of DNA vaccines. J Immunol 1997; 158:3635-9.
64. Krieg AM. CpG oligonucleotides as immune adjuvants. Ernst Schering Res Found Workshop 2000; 30:105-18.
65. Hawkins RE, Winter G, Hamblin TJ, Stevenson FK, Russell SJ. A genetic approach to idiotypic vaccination. J Immunother 1993; 14:273-8.
66. Watanabe A, Raz E, Kohsaka H, Tighe H, Baird SM, Kipps TJ, et al. Induction of antibodies to a κV region by gene immunization. J Immunol 1993; 151:2871-6.
67. Biragyn A, Kwak LW. B-cell malignancies as a model for cancer vaccines: from prototype protein to next generation genetic chemokine fusions. Immunol Rev 1999; 170:115-26.
68. Chen TT, Tao MH, Levy R. Idiotype-cytokine fusion proteins as cancer vaccines. Relative efficacy of IL-2, IL-4, and granulocyte-macrophage colony-stimulating factor. J Immunol 1994; 153:4775-87.
69. Rao KV, Nayak AR. Enhanced immunogenicity of a sequence derived from hepatitis B virus surface antigen in a composite peptide that includes the immunostimulatory region from human interleukin 1. Proc Natl Acad Sci USA 1990; 87:5519-22.
70. Beckers W, Villa L, Gonfloni S, Castagnoli L, Newton SM, Cesareni G, et al. Increasing the immunogenicity of protein antigens through the genetic insertion of VQGEESNDK sequence of human IL-1β into their sequence. J Immunol 1993; 151:1757-64.
71. Hakim I, Levy S, Levy R. A nine-amino acid peptide from IL-1β augments antitumor immune responses induced by protein and DNA vaccines. J Immunol 1996; 157:5503-11.
72. Benvenuti F, Burrone OR, Efremov DG. Anti-idiotypic DNA vaccines for lymphoma immunotherapy require the presence of both variable region genes for tumor protection. Gene Ther 2000; 7:605-11.
73. Medzhitov R, Janeway CJ. Innate immunity. N Engl J Med 2000; 343:338-44.
74. Medzhitov R, Janeway CAJ. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 1997; 9:4-9.
75. Matzinger P. An innate sense of danger. Semin Immunol 1998; 10:399-415.
76. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A, et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999; 5:919-23.
77. Fraser IP, Koziel H, Ezekowitz RA. The serum mannose-binding protein and the macrophage mannose receptor are pattern recognition molecules that link innate and adaptive immunity. Semin Immunol 1998; 10:363-72.
78. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, Ho S, et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999; 284: 1835-7.
79. Kopp EB, Medzhitov R. The Toll-receptor family and control of innate immunity. Curr Opin Immunol 1999; 11:13-8.
80. Colaco CA. Towards a unified theory of immunity: dendritic cells, stress proteins and antigen capture. Cell Mol Biol (Noisy-le-grand) 1998; 44:883-90.
81. Krieg AM, Love-Homan L, Yi AK, Harty JT. CpG DNA induces sustained IL-12 expression in vivo and resistance to Listeria monocytogenes challenge. J Immunol 1998; 161:2428-34.
82. Lanzavecchia A, Sallusto F. The instructive role of dendritic cells on T cell responses: lineages, plasticity and kinetics. Curr Opin Immunol 2001; 13:291-8.
83. Sallusto F, Schaerli P, Loetscher P, Schaniel C, Lenig D, Mackay CR, et al. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol 1998; 28:2760-9.
84. Dieu MC, Vanbervliet B, Vicari A, Bridon JM, Oldham E, Ait-Yahia S, et al. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 1998; 188:373-86.
85. Homey B, Muller A, Zlotnik A. Chemokines: agents for the immunotherapy of cancer? Nat Rev Immunol 2002; 2:17584.
86. Sozzani S, Allavena P, D'Amico G, Luini W, Blanchi G, Kataura M, et al. Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J Immunol 1998; 161:1083-6.
87. Moser B, Loetscher P. Lymphocyte traffic control by chemokines. Nat Immunol 2001; 2:123-8.
88. Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, et al. β-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 1999; 286:525-8.
89. Yamashita T, Saito K. Purification, primary structure, and biological activity of guinea pig neutrophil cationic peptides. Infect Immun 1989; 57:2405-9.
90. Lillard JWJ, Boyaka PN, Chertov O, Oppenheim JJ, McGhee JR. Mechanisms for induction of acquired host immunity by neutrophil peptide defensins. Proc Natl Acad Sci USA 1999; 96:651-6.
91. Luster AD, Leder P. IP-10, a -C-X-C- chemokine, elicits a potent thymus-dependent antitumor response in vivo. J Exp Med 1993; 178:1057-65.
92. Prado GN, Suzuki H, Wilkinson N, Cousins B, Navarro J. Role of the C terminus of the interleukin 8 receptor in signal transduction and internalization. J Biol Chem 1996; 271:19186-90.
93. Solari R, Offord RE, Remy S, Aubry JP, Wells TN, Whitehorn E, et al. Receptor-mediated endocytosis of CC-chemokines. J Biol Chem 1997; 272:9617-20.
94. Bogen B, Weiss S. Processing and presentation of idiotypes to MHC-restricted T cells. Int Rev Immunol 1993; 10:337-55.
95. + T cells in tumor resistance against major histocompatibility complex class II molecule negative plasmacytoma cells. Cell Immunol 1993; 148:177-88.
96. 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.
97. Barrios Y, Cabrera R, Yanez R, Briz M, Plaza A, Fores R, et al. Anti-idiotypic vaccination in the treatment of low-grade B-cell lymphoma. Haematologica 2002; 87:400-7.
98. Hsu FJ, Komarovskaya M, Song L, Doyon AG. A clinical trial of sequential dendritic cell and protein/adjuvant idiotype vaccine in patients with follicular lymphoma. Blood 2001; 98 Suppl 1:466[abstract].
99. 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.
100. Schuetze SM, Smith BE, Bensinger WI, Appelbaum FR, Maloney DG. Myeloma idiotype vaccination post allogenic or autologous transplant can amplify idiotype-specific cellular immunity. Blood 1999; 94 Suppl 1: 122 [abstract].
101. Munshi NC, Desikan RK, Siegal D. Preliminary report of clinical efficacy of patient (pt) specific vaccination using purified idiotype protein in myeloma. Blood 1999; 94 Suppl 1:704[abstract].
102. Kwak LW, Sternas LA, Jagnnath S, Siegal D, Munshi N, Barlogie B. T-cell responses elicited by immunization of multiple myeloma patients with idiotypic protein pluc GM-CSF in remission after autologous transplantation (PSCT). Blood 1997; 90 Suppl 1:579[abstract].
103. 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.
104. Reichardt VL, Milazzo C, Brugger W, Einsele H, Kanz L, Brossart P. Specific immunotherapy of multiple myeloma patients using idiotype pulsed serum-free generated dendritic cells. Blood 2001; 98 Suppl 1:378[abstract].
105. Lacy MQ, Wettstein P, Gertz MA. Dendritic cell-based idiotypic vaccination in post transplant multiple myeloma. Blood 2000; 96 Suppl 1:374[abstract].
106. Yi Q, Desikan R, Barlogie B, Munshi N. Optimizing dendritic cell-based immunotherapy in multiple myeloma. Blood 2001; 98 Suppl 1:374[abstract].
107. 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.
108. MacKenzie M, Peshwa MV, Wun T. Immunotherapy of advanced refractory multiple myeloma with idiotype-pulsed dendritic cells (mylovenge). Blood 2000; 96 Suppl 1:166[abstract].
109. Wen YJ, Ling M, Bailey-Wood R, Lim SH. Idiotypic protein-pulsed adherent peripheral blood mononuclear cell-derived dendritic cells prime immune system in multiple myeloma. Clin Cancer Res 1998; 4:957-62.
110. 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.