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[Cancer Research 61, 6451-6458, September 1, 2001]
© 2001 American Association for Cancer Research

Immunology

Immune and Clinical Responses in Patients with Metastatic Melanoma to CD34+ Progenitor-derived Dendritic Cell Vaccine1

Jacques Banchereau2,3, A. Karolina Palucka2, Madhav Dhodapkar2, Susan Burkeholder, Nicolas Taquet, Alexandre Rolland, Sybil Taquet, Sebastien Coquery, Knut M. Wittkowski, Nina Bhardwaj, Luis Pineiro, Ralph Steinman and Joseph Fay

Baylor Institute for Immunology Research, Dallas, Texas 75204 [J. B., A. K. P., S. B., N. T., A. R., S. T., S. C., L. P., J. F.]; Laboratory of Cellular Physiology and Immunology, The Rockefeller University, New York, New York 10021-6399 [M. D., N. B., R. S.]; and General Clinical Research Center, The Rockefeller University Hospital, New York, New York 10021-6399 [K. M. W.]

Immunization to multiple defined tumor antigens for specific immune therapy of human cancer has thus far proven difficult. Eighteen HLA A*0201+ patients with metastatic melanoma received injections s.c. of CD34+progenitor-derived autologous dendritic cells (DCs), which included Langerhans cells. DCs were pulsed with peptides derived from four melanoma antigens [(MelAgs) MelanA/MART-1, tyrosinase, MAGE-3, and gp100], as well as influenza matrix peptide (Flu-MP) and keyhole limpet hemocyanin (KLH) as control antigens. Overall immunological effects were assessed by comparing response profiles using marginal likelihood scores. DC injections were well tolerated except for progressive vitiligo in two patients. DCs induced an immune response to control antigens (KLH, Flu-MP) in 16 of 18 patients. An enhanced immune response to one or more MelAgs was seen in these same 16 patients, including 10 patients who responded to >2 MelAgs. The two patients failing to respond to both control and tumor antigens experienced rapid tumor progression. Of 17 patients with evaluable disease, 6 of 7 patients with immunity to two or less MelAgs had progressive disease 10 weeks after study entry, in contrast to tumor progression in only 1 of 10 patients with immunity to >2 MelAgs. Regression of >1 tumor metastases were observed in seven of these patients. The overall immunity to MelAgs after DC vaccination is associated with clinical outcome (P = 0.015).




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Blood, April 1, 2004; 103(7): 2547 - 2553.
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S. Vertuani, A. Sette, J. Sidney, S. Southwood, J. Fikes, E. Keogh, J. A. Lindencrona, G. Ishioka, J. Levitskaya, and R. Kiessling
Improved Immunogenicity of an Immunodominant Epitope of the Her-2/neu Protooncogene by Alterations of MHC Contact Residues
J. Immunol., March 15, 2004; 172(6): 3501 - 3508.
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C. M. Coughlin, B. A. Vance, S. A. Grupp, and R. H. Vonderheide
RNA-transfected CD40-activated B cells induce functional T-cell responses against viral and tumor antigen targets: implications for pediatric immunotherapy
Blood, March 15, 2004; 103(6): 2046 - 2054.
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D. Atanackovic, N. K. Altorki, E. Stockert, B. Williamson, A. A. Jungbluth, E. Ritter, D. Santiago, C. A. Ferrara, M. Matsuo, A. Selvakumar, et al.
Vaccine-Induced CD4+ T Cell Responses to MAGE-3 Protein in Lung Cancer Patients
J. Immunol., March 1, 2004; 172(5): 3289 - 3296.
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M. Kuang, B. G. Peng, M. D. Lu, L. J. Liang, J. F. Huang, Q. He, Y. P. Hua, S. Totsuka, S. Q. Liu, K. W. Leong, et al.
Phase II Randomized Trial of Autologous Formalin-Fixed Tumor Vaccine for Postsurgical Recurrence of Hepatocellular Carcinoma
Clin. Cancer Res., March 1, 2004; 10(5): 1574 - 1579.
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J. Taieb, K. Maruyama, C. Borg, M. Terme, L. Zitvogel, S. Appel, and P. Brossart
Imatinib mesylate impairs Flt3L-mediated dendritic cell expansion and antitumor effects in vivo
Blood, March 1, 2004; 103(5): 1966 - 1967.
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R. H. Vonderheide, S. M. Domchek, J. L. Schultze, D. J. George, K. M. Hoar, D.-Y. Chen, K. F. Stephans, K. Masutomi, M. Loda, Z. Xia, et al.
Vaccination of Cancer Patients Against Telomerase Induces Functional Antitumor CD8+ T Lymphocytes
Clin. Cancer Res., February 1, 2004; 10(3): 828 - 839.
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M. J. Palmowski, L. Lopes, Y. Ikeda, M. Salio, V. Cerundolo, and M. K. Collins
Intravenous Injection of a Lentiviral Vector Encoding NY-ESO-1 Induces an Effective CTL Response
J. Immunol., February 1, 2004; 172(3): 1582 - 1587.
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D. Blaise, J. O. Bay, C. Faucher, M. Michallet, J.-M. Boiron, B. Choufi, J.-Y. Cahn, N. Gratecos, J.-J. Sotto, S. Francois, et al.
Reduced-intensity preparative regimen and allogeneic stem cell transplantation for advanced solid tumors
Blood, January 15, 2004; 103(2): 435 - 441.
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L. A. O'Mara and P. M. Allen
Pulmonary Tumors Inefficiently Prime Tumor-Specific T Cells
J. Immunol., January 1, 2004; 172(1): 310 - 317.
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S. Teitz-Tennenbaum, Q. Li, S. Rynkiewicz, F. Ito, M. A. Davis, C. J. Mcginn, and A. E. Chang
Radiotherapy Potentiates the Therapeutic Efficacy of Intratumoral Dendritic Cell Administration
Cancer Res., December 1, 2003; 63(23): 8466 - 8475.
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R. S. Goldszmid, J. Idoyaga, A. I. Bravo, R. Steinman, J. Mordoh, and R. Wainstok
Dendritic Cells Charged with Apoptotic Tumor Cells Induce Long-Lived Protective CD4+ and CD8+ T Cell Immunity against B16 Melanoma
J. Immunol., December 1, 2003; 171(11): 5940 - 5947.
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I. Bedrosian, R. Mick, S. Xu, H. Nisenbaum, M. Faries, P. Zhang, P. A. Cohen, G. Koski, and B. J. Czerniecki
Intranodal Administration of Peptide-Pulsed Mature Dendritic Cell Vaccines Results in Superior CD8+ T-Cell Function in Melanoma Patients
J. Clin. Oncol., October 15, 2003; 21(20): 3826 - 3835.
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B. de Rijke, H. Fredrix, A. Zoetbrood, F. Scherpen, H. Witteveen, T. de Witte, E. van de Wiel-van Kemenade, and H. Dolstra
Generation of autologous cytotoxic and helper T-cell responses against the B-cell leukemia-associated antigen HB-1: relevance for precursor B-ALL-specific immunotherapy
Blood, October 15, 2003; 102(8): 2885 - 2891.
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N. Haicheur, F. Benchetrit, M. Amessou, C. Leclerc, T. Falguieres, C. Fayolle, E. Bismuth, W. H. Fridman, L. Johannes, and E. Tartour
The B subunit of Shiga toxin coupled to full-size antigenic protein elicits humoral and cell-mediated immune responses associated with a Th1-dominant polarization
Int. Immunol., October 1, 2003; 15(10): 1161 - 1171.
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D. Nagorsen, C. Scheibenbogen, F. M. Marincola, A. Letsch, and U. Keilholz
Natural T Cell Immunity against Cancer
Clin. Cancer Res., October 1, 2003; 9(12): 4296 - 4303.
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M. Girardi, E. Glusac, R. B. Filler, S. J. Roberts, I. Propperova, J. Lewis, R. E. Tigelaar, and A. C. Hayday
The Distinct Contributions of Murine T Cell Receptor (TCR){gamma}{delta}+ and TCR{alpha}{beta}+ T Cells to Different Stages of Chemically Induced Skin Cancer
J. Exp. Med., September 2, 2003; 198(5): 747 - 755.
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R. Soiffer, F. S. Hodi, F. Haluska, K. Jung, S. Gillessen, S. Singer, K. Tanabe, R. Duda, S. Mentzer, M. Jaklitsch, et al.
Vaccination With Irradiated, Autologous Melanoma Cells Engineered to Secrete Granulocyte-Macrophage Colony-Stimulating Factor by Adenoviral-Mediated Gene Transfer Augments Antitumor Immunity in Patients With Metastatic Melanoma
J. Clin. Oncol., September 1, 2003; 21(17): 3343 - 3350.
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I. Lindner, M. A. Kharfan-Dabaja, E. Ayala, D. Kolonias, L. M. Carlson, Y. Beazer-Barclay, U. Scherf, J. H. Hnatyszyn, and K. P. Lee
Induced Dendritic Cell Differentiation of Chronic Myeloid Leukemia Blasts Is Associated with Down-Regulation of BCR-ABL
J. Immunol., August 15, 2003; 171(4): 1780 - 1791.
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E. Orsini, A. Guarini, S. Chiaretti, F. R. Mauro, and R. Foa
The Circulating Dendritic Cell Compartment in Patients with Chronic Lymphocytic Leukemia Is Severely Defective and Unable to Stimulate an Effective T-Cell Response
Cancer Res., August 1, 2003; 63(15): 4497 - 4506.
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A. Camporeale, A. Boni, G. Iezzi, E. Degl'Innocenti, M. Grioni, A. Mondino, and M. Bellone
Critical Impact of the Kinetics of Dendritic Cells Activation on the in Vivo Induction of Tumor-specific T Lymphocytes
Cancer Res., July 1, 2003; 63(13): 3688 - 3694.
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M. Gilliet, M. Kleinhans, E. Lantelme, D. Schadendorf, G. Burg, and F. O. Nestle
Intranodal injection of semimature monocyte-derived dendritic cells induces T helper type 1 responses to protein neoantigen
Blood, July 1, 2003; 102(1): 36 - 42.
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E. Davila, R. Kennedy, and E. Celis
Generation of Antitumor Immunity by Cytotoxic T Lymphocyte Epitope Peptide Vaccination, CpG-oligodeoxynucleotide Adjuvant, and CTLA-4 Blockade
Cancer Res., June 15, 2003; 63(12): 3281 - 3288.
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A. C. Peterson, H. Harlin, and T. F. Gajewski
Immunization With Melan-A Peptide-Pulsed Peripheral Blood Mononuclear Cells Plus Recombinant Human Interleukin-12 Induces Clinical Activity and T-Cell Responses in Advanced Melanoma
J. Clin. Oncol., June 15, 2003; 21(12): 2342 - 2348.
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G. Parmiani, L. Pilla, C. Castelli, and L. Rivoltini
Vaccination of patients with solid tumours
Ann. Onc., June 1, 2003; 14(6): 817 - 824.
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Z. Su, J. Dannull, A. Heiser, D. Yancey, S. Pruitt, J. Madden, D. Coleman, D. Niedzwiecki, E. Gilboa, and J. Vieweg
Immunological and Clinical Responses in Metastatic Renal Cancer Patients Vaccinated with Tumor RNA-transfected Dendritic Cells
Cancer Res., May 1, 2003; 63(9): 2127 - 2133.
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F. S. Hodi, M. C. Mihm, R. J. Soiffer, F. G. Haluska, M. Butler, M. V. Seiden, T. Davis, R. Henry-Spires, S. MacRae, A. Willman, et al.
Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients
PNAS, April 15, 2003; 100(8): 4712 - 4717.
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K. Schlienger, C. S. Chu, E. Y. Woo, P. M. Rivers, A. J. Toll, B. Hudson, M. V. Maus, J. L. Riley, Y. Choi, G. Coukos, et al.
TRANCE- and CD40 Ligand-matured Dendritic Cells Reveal MHC Class I-restricted T Cells Specific for Autologous Tumor in Late-Stage Ovarian Cancer Patients
Clin. Cancer Res., April 1, 2003; 9(4): 1517 - 1527.
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L. H. Butterfield, A. Ribas, V. B. Dissette, S. N. Amarnani, H. T. Vu, D. Oseguera, H.-J. Wang, R. M. Elashoff, W. H. McBride, B. Mukherji, et al.
Determinant Spreading Associated with Clinical Response in Dendritic Cell-based Immunotherapy for Malignant Melanoma
Clin. Cancer Res., March 1, 2003; 9(3): 998 - 1008.
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K. Akiyama, S. Ebihara, A. Yada, K. Matsumura, S. Aiba, T. Nukiwa, and T. Takai
Targeting Apoptotic Tumor Cells to Fc{gamma}R Provides Efficient and Versatile Vaccination Against Tumors by Dendritic Cells
J. Immunol., February 15, 2003; 170(4): 1641 - 1648.
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T. L. Whiteside, Y. Zhao, T. Tsukishiro, E. M. Elder, W. Gooding, and J. Baar
Enzyme-linked Immunospot, Cytokine Flow Cytometry, and Tetramers in the Detection of T-Cell Responses to a Dendritic Cell-based Multipeptide Vaccine in Patients with Melanoma
Clin. Cancer Res., February 1, 2003; 9(2): 641 - 649.
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S. R. Reynolds, A. Zeleniuch-Jacquotte, R. L. Shapiro, D. F. Roses, M. N. Harris, D. Johnston, and J.-C. Bystryn
Vaccine-induced CD8+ T-cell Responses to MAGE-3 Correlate with Clinical Outcome in Patients with Melanoma
Clin. Cancer Res., February 1, 2003; 9(2): 657 - 662.
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G. Consogno, S. Manici, V. Facchinetti, A. Bachi, J. Hammer, B. M. Conti-Fine, C. Rugarli, C. Traversari, and M. P. Protti
Identification of immunodominant regions among promiscuous HLA-DR-restricted CD4+ T-cell epitopes on the tumor antigen MAGE-3
Blood, February 1, 2003; 101(3): 1038 - 1044.
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I. D. Davis, M. Jefford, P. Parente, and J. Cebon
Rational approaches to human cancer immunotherapy
J. Leukoc. Biol., January 1, 2003; 73(1): 3 - 29.
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C. La Rosa, Z. Wang, J. C. Brewer, S. F. Lacey, M. C. Villacres, R. Sharan, R. Krishnan, M. Crooks, S. Markel, R. Maas, et al.
Preclinical development of an adjuvant-free peptide vaccine with activity against CMV pp65 in HLA transgenic mice
Blood, November 15, 2002; 100(10): 3681 - 3689.
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P. Luhrs, W. Schmidt, R. Kutil, M. Buschle, S. N. Wagner, G. Stingl, and A. Schneeberger
Induction of Specific Immune Responses by Polycation-Based Vaccines
J. Immunol., November 1, 2002; 169(9): 5217 - 5226.
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G. Parmiani, C. Castelli, P. Dalerba, R. Mortarini, L. Rivoltini, F. M. Marincola, and A. Anichini
Cancer Immunotherapy With Peptide-Based Vaccines: What Have We Achieved? Where Are We Going?
J Natl Cancer Inst, June 5, 2002; 94(11): 805 - 818.
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B. Schuler-Thurner, E. S. Schultz, T. G. Berger, G. Weinlich, S. Ebner, P. Woerl, A. Bender, B. Feuerstein, P. O. Fritsch, N. Romani, et al.
Rapid Induction of Tumor-specific Type 1 T Helper Cells in Metastatic Melanoma Patients by Vaccination with Mature, Cryopreserved, Peptide-loaded Monocyte-derived Dendritic Cells
J. Exp. Med., May 20, 2002; 195(10): 1279 - 1288.
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M. Schnurr, C. Scholz, S. Rothenfusser, P. Galambos, M. Dauer, J. Robe, S. Endres, and A. Eigler
Apoptotic Pancreatic Tumor Cells Are Superior to Cell Lysates in Promoting Cross-Priming of Cytotoxic T Cells and Activate NK and {gamma}{delta} T Cells
Cancer Res., April 1, 2002; 62(8): 2347 - 2352.
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C. Buteau, S. N. Markovic, and E. Celis
Challenges in the Development of Effective Peptide Vaccines for Cancer
Mayo Clin. Proc., April 1, 2002; 77(4): 339 - 349.
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P. Kufer, A. Zippelius, R. Lutterbuse, I. Mecklenburg, T. Enzmann, A. Montag, D. Weckermann, B. Passlick, N. Prang, P. Reichardt, et al.
Heterogeneous Expression of MAGE-A Genes in Occult Disseminated Tumor Cells: A Novel Multimarker Reverse Transcription-Polymerase Chain Reaction for Diagnosis of Micrometastatic Disease
Cancer Res., January 1, 2002; 62(1): 251 - 261.
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