Dendritic cells as therapeutic vaccines against cancer

Mouse studies have shown that the immune system can reject tumours, and the identification of tumour antigens that can be recognized by human T cells has facilitated the development of immunotherapy protocols. Vaccines against cancer aim to induce tumour-specific effector T cells that can reduce the tumour mass, as well as tumour-specific memory T cells that can control tumour relapse. Owing to their capacity to regulate T-cell immunity, dendritic cells are increasingly used as adjuvants for vaccination, and the immunogenicity of antigens delivered by dendritic cells has now been shown in patients with cancer. A better understanding of how dendritic cells regulate immune responses will allow us to better exploit these cells to induce effective antitumour immunity.

[1]  C. Figdor,et al.  Dendritic cell immunotherapy: mapping the way , 2004, Nature Medicine.

[2]  S. Miltenyi,et al.  BDCA-2, BDCA-3, and BDCA-4: Three Markers for Distinct Subsets of Dendritic Cells in Human Peripheral Blood , 2000, The Journal of Immunology.

[3]  S. Dzik The nature of the principal type 1 interferon-producing cells in human blood , 2000 .

[4]  Susan M. Kaech,et al.  Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol. , 2002 .

[5]  Michel C. Nussenzweig,et al.  Efficient Targeting of Protein Antigen to the Dendritic Cell Receptor DEC-205 in the Steady State Leads to Antigen Presentation on Major Histocompatibility Complex Class I Products and Peripheral CD8+ T Cell Tolerance , 2002, The Journal of experimental medicine.

[6]  Christoph Schaniel,et al.  Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation , 1998, European journal of immunology.

[7]  Laurence Zitvogel,et al.  Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell derived exosomes , 1998, Nature Medicine.

[8]  Bali Pulendran,et al.  Lipopolysaccharides from Distinct Pathogens Induce Different Classes of Immune Responses In Vivo1 , 2001, The Journal of Immunology.

[9]  E. Margoliash,et al.  T-lymphocyte response to cytochrome c. I. Demonstration of a T-cell heteroclitic proliferative response and identification of a topographic antigenic determinant on pigeon cytochrome c whose immune recognition requires two complementing major histocompatibility complex-linked immune response genes , 1979, The Journal of experimental medicine.

[10]  B. Fox,et al.  Anti‐tumor T cell response and protective immunity in mice that received sublethal irradiation and immune reconstitution , 2003, European journal of immunology.

[11]  M. Jefford,et al.  Rational approaches to human cancer immunotherapy , 2003, Journal of leukocyte biology.

[12]  J. Banchereau,et al.  Interleukin 15 Skews Monocyte Differentiation into Dendritic Cells with Features of Langerhans Cells , 2001, The Journal of experimental medicine.

[13]  Wolfgang Weninger,et al.  Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells , 2003, Nature.

[14]  S. Rosenberg,et al.  Cancer immunotherapy: moving beyond current vaccines , 2004, Nature Medicine.

[15]  K. Pang,et al.  Type I IFNs enhance the terminal differentiation of dendritic cells. , 1998, Journal of immunology.

[16]  Mitchell Kronenberg,et al.  Toward an understanding of NKT cell biology: progress and paradoxes. , 2005, Annual review of immunology.

[17]  Freddie H. Fu,et al.  Costimulatory molecule-deficient dendritic cell progenitors (MHC class II+, CD80dim, CD86-) prolong cardiac allograft survival in nonimmunosuppressed recipients. , 1996, Transplantation.

[18]  R. Steinman,et al.  Single Injection of CD34+ Progenitor-Derived Dendritic Cell Vaccine Can Lead to Induction of T-Cell Immunity in Patients With Stage IV Melanoma , 2003, Journal of immunotherapy.

[19]  R. Förster,et al.  Prostaglandin E2 is a key factor for CCR7 surface expression and migration of monocyte-derived dendritic cells. , 2002, Blood.

[20]  P. Gibbs,et al.  Two phase I studies of low dose recombinant human IL-12 with Melan-A and influenza peptides in subjects with advanced malignant melanoma. , 2003, Cancer immunity.

[21]  A. Enk,et al.  Vaccination with Mage-3a1 Peptide–Pulsed Mature, Monocyte-Derived Dendritic Cells Expands Specific Cytotoxic T Cells and Induces Regression of Some Metastases in Advanced Stage IV Melanoma , 1999, The Journal of experimental medicine.

[22]  T. Schumacher,et al.  Synergism of Cytotoxic T Lymphocyte–Associated Antigen 4 Blockade and Depletion of Cd25+ Regulatory T Cells in Antitumor Therapy Reveals Alternative Pathways for Suppression of Autoreactive Cytotoxic T Lymphocyte Responses , 2001, The Journal of experimental medicine.

[23]  J. Banchereau,et al.  GM-CSF and TNF-α cooperate in the generation of dendritic Langerhans cells , 1992, Nature.

[24]  R. Zinkernagel On natural and artificial vaccinations. , 2003, Annual review of immunology.

[25]  N. Kadowaki,et al.  The nature of the principal type 1 interferon-producing cells in human blood. , 1999, Science.

[26]  G. Nossal Host immunobiology and vaccine development , 1997, The Lancet.

[27]  C Caux,et al.  CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to granulocyte-macrophage colony-stimulating factor plus tumor necrosis factor alpha: II. Functional analysis. , 1997, Blood.

[28]  J. Sprent,et al.  Stimulation of naive and memory T cells by cytokines , 1999, Immunological reviews.

[29]  J. Davey,et al.  Cytotoxic T cells recognize fragments of the influenza nucleoprotein , 1985, Cell.

[30]  E. J. Foley Antigenic properties of methylcholanthrene-induced tumors in mice of the strain of origin. , 1953, Cancer research.

[31]  T. Blankenstein,et al.  B cells inhibit induction of T cell-dependent tumor immunity , 1998, Nature Medicine.

[32]  P. Kourilsky,et al.  Foxp3 Expressing CD4+CD25high Regulatory T Cells Are Overrepresented in Human Metastatic Melanoma Lymph Nodes and Inhibit the Function of Infiltrating T Cells1 , 2004, The Journal of Immunology.

[33]  Mark M. Davis,et al.  Altered peptide ligand vaccination with Flt3 ligand expanded dendritic cells for tumor immunotherapy , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  P. Ricciardi-Castagnoli,et al.  Fcγ Receptor–mediated Induction of Dendritic Cell Maturation and Major Histocompatibility Complex Class I–restricted Antigen Presentation after Immune Complex Internalization , 1999, The Journal of experimental medicine.

[35]  P. Bruggen,et al.  Tumor antigens recognized by T lymphocytes. , 1994, Annual review of immunology.

[36]  J. Mayordomo,et al.  Peptide-pulsed dendritic cells induce antigen-specific CTL-mediated protective tumor immunity , 1996, The Journal of experimental medicine.

[37]  S. Holmes,et al.  Diversity and Recognition Efficiency of T Cell Responses to Cancer , 2004, PLoS medicine.

[38]  D. Jarrossay,et al.  Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon , 1999, Nature Medicine.

[39]  E. Wherry,et al.  Viral Persistence Alters CD8 T-Cell Immunodominance and Tissue Distribution and Results in Distinct Stages of Functional Impairment , 2003, Journal of Virology.

[40]  J. Davoust,et al.  Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. , 2000, Immunity.

[41]  R. Steinman,et al.  Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. , 1999, Immunity.

[42]  J. Banchereau,et al.  CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to GM-CSF+TNF alpha , 1996, The Journal of experimental medicine.

[43]  V. Sondak,et al.  Results of clinical trials with an allogenic melanoma tumor cell lysate vaccine: Melacine. , 2003, Seminars in cancer biology.

[44]  Lukas Hunziker,et al.  Dendritic cell–induced autoimmune heart failure requires cooperation between adaptive and innate immunity , 2003, Nature Medicine.

[45]  Virginia Pascual,et al.  Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. , 2003, Immunity.

[46]  N. Kadowaki,et al.  Reciprocal control of T helper cell and dendritic cell differentiation. , 1999, Science.

[47]  E. Shevach,et al.  Tumor-specific human CD4+ regulatory T cells and their ligands: implications for immunotherapy. , 2004, Immunity.

[48]  Hao Shen,et al.  CD8+ T-cell memory: only the good ones last. , 2004, Current opinion in immunology.

[49]  D. Pardoll,et al.  Cancer immunotherapy: breaking the barriers to harvest the crop , 2004, Nature Medicine.

[50]  Wei Lu,et al.  Therapeutic dendritic-cell vaccine for chronic HIV-1 infection , 2004, Nature Medicine.

[51]  R. Steinman,et al.  The dendritic cell system and its role in immunogenicity. , 1991, Annual review of immunology.

[52]  Edgar G. Engleman,et al.  Dendritic Cells Injected Via Different Routes Induce Immunity in Cancer Patients1 , 2001, The Journal of Immunology.

[53]  E. Gilboa,et al.  Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo , 1996, The Journal of experimental medicine.

[54]  M. Moser,et al.  Antigen-pulsed dendritic cells can efficiently induce an antibody response in vivo , 1992, The Journal of experimental medicine.

[55]  Yong‐jun Liu,et al.  Mouse and human dendritic cell subtypes , 2002, Nature Reviews Immunology.

[56]  S. Swain,et al.  Reciprocal regulation of polarized cytokine production by effector B and T cells , 2000, Nature Immunology.

[57]  R. Maldonado-López,et al.  CD8α+ and CD8α− Subclasses of Dendritic Cells Direct the Development of Distinct T Helper Cells In Vivo , 1999, The Journal of experimental medicine.

[58]  R. Coleman,et al.  Migration of human dendritic cells after injection in patients with metastatic malignancies. , 1999, Cancer research.

[59]  Nina Bhardwaj,et al.  Antigen-Specific Inhibition of Effector T Cell Function in Humans after Injection of Immature Dendritic Cells , 2001, The Journal of experimental medicine.

[60]  C. Reis e Sousa,et al.  Dendritic cells as sensors of infection. , 2001, Immunity.

[61]  T. Luft,et al.  Functionally distinct dendritic cell (DC) populations induced by physiologic stimuli: prostaglandin E(2) regulates the migratory capacity of specific DC subsets. , 2002, Blood.

[62]  D. Morton,et al.  Antigen-based immunotherapy of melanoma: Canvaxin therapeutic polyvalent cancer vaccine. , 2003, Seminars in cancer biology.

[63]  E. Gilboa,et al.  Regression of tumors in mice vaccinated with professional antigen‐presenting cells pulsed with tumor extracts , 1997, International journal of cancer.

[64]  Virginia Pascual,et al.  Induction of Dendritic Cell Differentiation by IFN-α in Systemic Lupus Erythematosus , 2001, Science.

[65]  S. Rosenberg,et al.  Cloning genes encoding MHC class II-restricted antigens: mutated CDC27 as a tumor antigen. , 1999, Science.

[66]  M. Peshwa,et al.  Immunotherapy of hormone-refractory prostate cancer with antigen-loaded dendritic cells. , 2000, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[67]  M. Mescher,et al.  Phase I Trial of Large Multivalent Immunogen Derived from Melanoma Lysates in Patients with Disseminated Melanoma , 2004, Clinical Cancer Research.

[68]  M. Albert,et al.  Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs , 1998, Nature.

[69]  O. Finn,et al.  Cancer vaccines: between the idea and the reality , 2003, Nature Reviews Immunology.

[70]  N. Kadowaki,et al.  Natural Interferon α/β–Producing Cells Link Innate and Adaptive Immunity , 2000, The Journal of experimental medicine.

[71]  R. Steinman,et al.  Immunotherapy: Bewitched, Bothered, and Bewildered No More , 2004, Science.

[72]  A. Palucka,et al.  TNF Skews Monocyte Differentiation from Macrophages to Dendritic Cells 1 , 2003, The Journal of Immunology.

[73]  Antonio Lanzavecchia,et al.  Regulation of T Cell Immunity by Dendritic Cells , 2001, Cell.

[74]  Antonio Lanzavecchia,et al.  Regulation of Dendritic Cell Migration to the Draining Lymph Node , 2003, The Journal of experimental medicine.

[75]  F. Sallusto,et al.  Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha , 1994, The Journal of experimental medicine.

[76]  R. Steinman,et al.  Dendritic cells pulsed with protein antigens in vitro can prime antigen- specific, MHC-restricted T cells in situ [published erratum appears in J Exp Med 1990 Oct 1;172(4):1275] , 1990, The Journal of experimental medicine.

[77]  J. Banchereau,et al.  The monoclonal antibody DCGM4 recognizes Langerin, a protein specific of Langerhans cells, and is rapidly internalized from the cell surface , 1999, European journal of immunology.

[78]  A. Zlotnik,et al.  The biology of chemokines and their receptors. , 2000, Annual review of immunology.

[79]  L. Kemény,et al.  Skin cancers after organ transplantation. , 2003, The New England journal of medicine.

[80]  R. Steinman,et al.  Direct Expansion of Functional CD25+ CD4+ Regulatory T Cells by Antigen-processing Dendritic Cells , 2003, The Journal of experimental medicine.

[81]  G. Coukos,et al.  Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. , 2001, Cancer research.

[82]  S. Imamura,et al.  CD 34 + Hematopoietic Progenitors from Human Cord Blood Differentiate Along Two Independent Dendritic Cell Pathways in Response to GM-CSF + TNFoL , 2003 .

[83]  D. Berd,et al.  Effect of low dose cyclophosphamide on the immune system of cancer patients: depletion of CD4+, 2H4+ suppressor-inducer T-cells. , 1988, Cancer research.

[84]  T. Tüting,et al.  Depletion of CD25(+) CD4(+) T cells and treatment with tyrosinase-related protein 2-transduced dendritic cells enhance the interferon alpha-induced, CD8(+) T-cell-dependent immune defense of B16 melanoma. , 2001, Cancer research.

[85]  V. Engelhard,et al.  Route of Immunization with Peptide-pulsed Dendritic Cells Controls the Distribution of Memory and Effector T Cells in Lymphoid Tissues and Determines the Pattern of Regional Tumor Control , 2003, Journal of Experimental Medicine.

[86]  A. Enk,et al.  Pro‐inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum‐free conditions , 1997, European journal of immunology.

[87]  B. Pulendran,et al.  Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[88]  A. Enk,et al.  A comparison of two types of dendritic cell as adjuvants for the induction of melanoma‐specific T‐cell responses in humans following intranodal injection , 2001, International journal of cancer.

[89]  P. Marrack,et al.  Type I Interferons Keep Activated T Cells Alive , 1999, The Journal of experimental medicine.

[90]  M. Bevan,et al.  Defective CD8 T Cell Memory Following Acute Infection Without CD4 T Cell Help , 2003, Science.

[91]  Hervé Groux,et al.  A CD4+T-cell subset inhibits antigen-specific T-cell responses and prevents colitis , 1997, Nature.

[92]  J. Mulé,et al.  Current developments of immunotherapy in the clinic. , 2004, Current opinion in immunology.

[93]  W. Storkus,et al.  B 7 Cost imulat ion , and T Helper Cell 1-associated Cytokines , 2003 .

[94]  T. Brocker,et al.  The role of dendritic cells in T cell selection and survival , 1999, Journal of leukocyte biology.

[95]  D. Schadendorf,et al.  Phase 2 Trial of Vaccination With Tyrosinase Peptides and Granulocyte-Macrophage Colony-Stimulating Factor in Patients With Metastatic Melanoma , 2000, Journal of immunotherapy.

[96]  A. Aguzzi,et al.  Dangerous Liaisons between a Microbe and the Prion Protein , 2003, The Journal of experimental medicine.

[97]  D. Gabrilovich Mechanisms and functional significance of tumour-induced dendritic-cell defects , 2004, Nature Reviews Immunology.

[98]  J. Mulé,et al.  Tumor lysate-pulsed dendritic cells can elicit an effective antitumor immune response during early lymphoid recovery , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[99]  S. Rosenberg Cancer vaccines based on the identification of genes encoding cancer regression antigens. , 1997, Immunology today.

[100]  Dirk Schadendorf,et al.  Vaccination of melanoma patients with peptide- or tumorlysate-pulsed dendritic cells , 1998, Nature Medicine.

[101]  Edgar G. Engleman,et al.  Vaccination of patients with B–cell lymphoma using autologous antigen–pulsed dendritic cells , 1996, Nature Medicine.

[102]  R. Medzhitov,et al.  Toll-dependent control mechanisms of CD4 T cell activation. , 2004, Immunity.

[103]  A Sette,et al.  Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. , 1996, Journal of immunology.

[104]  A. N. Park,et al.  Interferon‐α and granulocyte‐macrophage colony‐stimulating factor differentiate peripheral blood monocytes into potent antigen‐presenting cells , 1998, Journal of leukocyte biology.

[105]  J. Banchereau,et al.  IL-6 switches the differentiation of monocytes from dendritic cells to macrophages , 2000, Nature Immunology.

[106]  Urs Christen,et al.  CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes , 2003, Nature.

[107]  C Caux,et al.  Immunobiology of dendritic cells. , 2000, Annual review of immunology.

[108]  J. Fay,et al.  Expansion of Melanoma-specific Cytolytic CD8+ T Cell Precursors in Patients with Metastatic Melanoma Vaccinated with CD34+ Progenitor-derived Dendritic Cells , 2004, The Journal of experimental medicine.

[109]  Loise M. Francisco,et al.  Tumor-specific killer cells in paraneoplastic cerebellar degeneration , 1998, Nature Medicine.

[110]  J. Altman,et al.  Viral Immune Evasion Due to Persistence of Activated T Cells Without Effector Function , 1998, The Journal of experimental medicine.

[111]  P. Ricciardi-Castagnoli,et al.  Dendritic cells directly trigger NK cell functions: Cross-talk relevant in innate anti-tumor immune responses in vivo , 1999, Nature Medicine.

[112]  A. Palucka,et al.  Cross-Priming of Naive Cd8 T Cells against Melanoma Antigens Using Dendritic Cells Loaded with Killed Allogeneic Melanoma Cells , 2000, The Journal of experimental medicine.

[113]  E. Gilboa The makings of a tumor rejection antigen. , 1999, Immunity.

[114]  A. Ribas,et al.  Cancer immunotherapy using gene-modified dendritic cells. , 2002, Current gene therapy.

[115]  S. Menzies,et al.  Phase I/II study of treatment with dendritic cell vaccines in patients with disseminated melanoma , 2004, Cancer Immunology, Immunotherapy.

[116]  D. Morton,et al.  Suppressor cell activity in a randomized trial of patients receiving active specific immunotherapy with melanoma cell vaccine and low dosages of cyclophosphamide. , 1990, Cancer research.

[117]  G. Schuler,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 , 2002, The Journal of experimental medicine.

[118]  Kathleen M. Smith,et al.  Human epithelial cells trigger dendritic cell–mediated allergic inflammation by producing TSLP , 2002, Nature Immunology.

[119]  J. Peters,et al.  Signals required for differentiating dendritic cells from human monocytes in vitro. , 1993, Advances in experimental medicine and biology.

[120]  N. Kadowaki,et al.  Subsets of Human Dendritic Cell Precursors Express Different Toll-like Receptors and Respond to Different Microbial Antigens , 2001, The Journal of experimental medicine.

[121]  T. Di Pucchio,et al.  Type I Interferon as a Powerful Adjuvant for Monocyte-Derived Dendritic Cell Development and Activity in Vitro and in Hu-Pbl-Scid Mice , 2000, The Journal of experimental medicine.

[122]  A. Enk,et al.  Induction of Interleukin 10–Producing, Nonproliferating Cd4+ T Cells with Regulatory Properties by Repetitive Stimulation with Allogeneic Immature Human Dendritic Cells , 2000, The Journal of experimental medicine.

[123]  H. Weiner,et al.  Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. , 1994, Science.

[124]  A. Rudensky,et al.  Foxp3 programs the development and function of CD4+CD25+ regulatory T cells , 2003, Nature Immunology.

[125]  R. North,et al.  The murine antitumor immune response and its therapeutic manipulation. , 1984, Advances in immunology.

[126]  A. Palucka,et al.  Dendritic cells loaded with killed breast cancer cells induce differentiation of tumor-specific cytotoxic T lymphocytes , 2004, Breast Cancer Research.

[127]  Foley Ej Antigenic properties of methylcholanthrene-induced tumors in mice of the strain of origin. , 1953 .

[128]  R. Steinman,et al.  Proliferating dendritic cell progenitors in human blood , 1994, The Journal of experimental medicine.

[129]  E. Gilboa,et al.  Immunotherapy of cancer with dendritic-cell-based vaccines , 1998, Cancer Immunology, Immunotherapy.

[130]  J. Kirkwood,et al.  alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. , 2004, Cancer research.

[131]  J. Cormier,et al.  Immunization against epitopes in the human melanoma antigen gp100 following patient immunization with synthetic peptides. , 1996, Cancer research.

[132]  Hao Shen,et al.  Requirement for CD4 T Cell Help in Generating Functional CD8 T Cell Memory , 2003, Science.

[133]  M. Gilliet,et al.  Activation of influenza virus-specific CD4+ and CD8+ T cells: a new role for plasmacytoid dendritic cells in adaptive immunity. , 2003, Blood.

[134]  E. Leventhal,et al.  Aging, immunity, and cancer. , 2000, Cancer control : journal of the Moffitt Cancer Center.

[135]  A. Naji,et al.  Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide , 2001, Nature Immunology.

[136]  Antonio Lanzavecchia,et al.  BDCA-2, a Novel Plasmacytoid Dendritic Cell–specific Type II C-type Lectin, Mediates Antigen Capture and Is a Potent Inhibitor of Interferon α/β Induction , 2001, The Journal of experimental medicine.

[137]  F. Marincola,et al.  T-cell-directed cancer vaccines: mechanisms of immune escape and immune tolerance , 2001, Expert opinion on biological therapy.

[138]  Jay A. Berzofsky,et al.  NKT cell–mediated repression of tumor immunosurveillance by IL-13 and the IL-4R–STAT6 pathway , 2000, Nature Immunology.

[139]  L. Lanier,et al.  Distinct Cytokine Profiles of Neonatal Natural Killer T Cells after Expansion with Subsets of Dendritic Cells , 2001, The Journal of experimental medicine.

[140]  Concepción Marañón,et al.  An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope , 2003, Nature Immunology.

[141]  M. Roncarolo,et al.  Type 1 T regulatory cells , 2001, Immunological reviews.

[142]  D. Neuberg,et al.  Vaccination with irradiated autologous melanoma cells engineered to secrete human granulocyte-macrophage colony-stimulating factor generates potent antitumor immunity in patients with metastatic melanoma. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[143]  E. Jaffee,et al.  Cancer Vaccines , 1997, Current protocols in human genetics.

[144]  R. Schreiber,et al.  Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. , 1994, Immunity.

[145]  Ira Mellman,et al.  Dendritic Cells Specialized and Regulated Antigen Processing Machines , 2001, Cell.

[146]  L. Lefrançois,et al.  Preferential Localization of Effector Memory Cells in Nonlymphoid Tissue , 2001, Science.

[147]  Adelheid Cerwenka,et al.  Natural killer cells, viruses and cancer , 2001, Nature Reviews Immunology.

[148]  R. Steinman,et al.  In Vivo Targeting of Antigens to Maturing Dendritic Cells via the DEC-205 Receptor Improves T Cell Vaccination , 2004, The Journal of experimental medicine.

[149]  R. Steinman,et al.  Immune and clinical responses in patients with metastatic melanoma to CD34(+) progenitor-derived dendritic cell vaccine. , 2001, Cancer research.