Disparate functions of immature and mature human myeloid dendritic cells: Implications for dendritic cell-based vaccines

Journal of Leukocyte Biology

Volumn 74, Issue 1, 2003, Pages 69-80

  Tschoep, Katharina ^a   Manning, Thomas C ^a   Harlin, Helena ^a   George, Christopher ^a   Johnson, Melissa ^a   Gajewski, Thomas F ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Antigen presenting cells; Cancer; CD40; Chemokines; IL 12; Immunotherapy

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; PROSTAGLANDIN E2; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; BETA CHEMOKINE; CC CHEMOKINE RECEPTOR 7; CHEMOKINE RECEPTOR; CYTOKINE; LEUKOCYTE ANTIGEN; SECONDARY LYMPHOID TISSUE CHEMOKINE;

ANTIGEN EXPRESSION; ARTICLE; BONE MARROW CELL; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DOWN REGULATION; FIBROBLAST; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; ADOPTIVE IMMUNOTHERAPY; BIOSYNTHESIS; CELL MOTION; COMPARATIVE STUDY; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECT; IMMUNOPHENOTYPING; METHODOLOGY; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ANTIGENS, CD; CELL CULTURE TECHNIQUES; CELL MOVEMENT; CHEMOKINES, CC; CYTOKINES; DENDRITIC CELLS; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY, ADOPTIVE; MYELOID CELLS; NEOPLASMS; RECEPTORS, CHEMOKINE;

EID: 0041568659     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0702352     Document Type: Article

References (67)

1. Schreurs, M. W., Eggert, A. A., Punt, C. J., Figdor, C. G., Adema, G. J. (2000) Dendritic cell-based vaccines: from mouse models to clinical cancer immunotherapy. Crit. Rev. Oncog. 11, 1-17.
2. Inaba, K., Young, J. W., Steinman, R. M. (1987) Direct activation of CD8+ cytotoxic T lymphocytes by dendritic cells. J. Exp. Med. 166, 182-194.
3. Inaba, K., Metlay, J. P., Crowley, M. T., Steinman, R. M. (1990) Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. J. Exp. Med. 172, 631-640.
4. Ferlazzo, G., Wesa, A., Wei, W. Z., Galy, A. (1999) Dendritic cells generated either from CD34+ progenitor cells or from monocytes differ in their ability to activate antigen-specific CD8+ T cells. J. Immunol. 163, 3597-3604.
5. Larsson, M., Messmer, D., Somersan, S., Fonteneau, J. F., Donahoe, S. M., Lee, M., Dunbar, P. R., Cerundolo, V., Julkunen, I., Nixon, D. F., Bhardwaj, N. (2000) Requirement of mature dendritic cells for efficient activation of influenza A-specific memory CD8+ T cells. J. Immunol. 165, 1182-1190.
6. Young, J. W., Steinman, R. M. (1990) Dendritic cells stimulate primary human cytolytic lymphocyte responses in the absence of CD4+ helper T cells. J. Exp. Med. 171, 1315-1332.
7. Mehta-Damani, A., Markowicz, S., Engleman, E. G. (1994) Generation of antigen-specific CD8+ CTLs from naive precursors. J. Immunol. 153, 996-1003.
8. Colombo, B. M., Lacave, R., Pioche-Durieu, C., Masurier, C., Lemoine, F. M., Guigon, M., Klatzmann, D. (2000) Cellular but not humoral immune responses generated by vaccination with dendritic cells protect mice against leukaemia. Immunology 99, 8-15.
9. Mayordomo, J. I., Zorina, T., Storkus, W. J., Zitvogel, L., Garcia-Prats, M. D., DeLeo, A. B., Lotze, M. T. (1997) Bone marrow-derived dendritic cells serve as potent adjuvants for peptide-based antitumor vaccines. Stem Cells 15, 94-103.
10. Paglia, P., Chiodoni, C., Rodolfo, M., Colombo, M. P. (1996) Murine dendritic cells loaded in vitro with soluble protein prime cytotoxic T lymphocytes against tumor antigen in vivo. J. Exp. Med. 183, 317-322.
11. Dhodapkar, M. V., Krasovsky, J., Steinman, R. M., Bhardwaj, N. (2000) Mature dendritic cells boost functionally superior CD8(+) T-cell in humans without foreign helper epitopes. J. Clin. Invest. 105, R9-R14.
12. Lau, R., Wang, F., Jeffery, G., Marty, V., Kuniyoshi, J., Bade, E., Ryback, M. E., Weber, J. (2001) Phase I trial of intravenous peptide-pulsed dendritic cells in patients with metastatic melanoma. J. Immunother. 24, 66-78.
13. Lodge, P. A., Jones, L. A., Bader, R. A., Murphy, G. P., Salgaller, M. L. (2000) Dendritic cell-based immunotherapy of prostate cancer: immune monitoring of a phase II clinical trial. Cancer Res. 60, 829-833.
14. Nestle, F. O., Alijagic, S., Gilliet, M., Sun, Y., Grabbe, S., Dummer, R., Burg, G., Schadendorf, D. (1998) Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat. Med. 4, 328-332.
15. Schuler-Thurner, B., Dieckmann, D., Keikavoussi, P., Bender, A., Maczek, C., Jonuleit, H., Roder, C., Haendle, I., Leisgang, W., Dunbar, R., Cerundolo, V., von Den Driesch, P., Knop, J., Brocker, E. B., Enk, A., Kampgen, E., Schuler, G. (2000) Mage-3 and influenza-matrix peptide-specific cytotoxic T cells are inducible in terminal stage HLA-A2.1+ melanoma patients by mature monocyte-derived dendritic cells. J. Immunol. 165, 3492-3496.
16. O'Doherty, U., Peng, M., Gezelter, S., Swiggard, W. J., Betjes, M., Bhardwaj, N., Steinman, R. M. (1994) Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology 82, 487-493.
17. Cella, M., Jarrossay, D., Facchetti, F., Alebardi, O., Nakajima, H., Lanzavecchia, A., Colonna, M. (1999) Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 5, 919-923.
18. Zou, W., Borvak, J., Marches, F., Wei, S., Galanaud, P., Emilie, D., Curiel, T. J. (2000) Macrophage-derived dendritic cells have strong Th1-polarizing potential mediated by beta-chemokines rather than IL-12. J. Immunol. 165, 4388-4396.
19. Rissoan, M. C., Soumelis, V., Kadowaki, N., Grouard, G., Briere, F., de Waal Malefyt, R., Liu, Y. J. (1999) Reciprocal control of T helper cell and dendritic cell differentiation. Science 283, 1183-1186.
20. Kawakami, Y., Eliyahu, S., Delgado, C. H., Robbins, P. F., Sakaguchi, K., Appella, E., Yannelli, J. R., Adema, G. J., Miki, T., Rosenberg, S. A. (1994) Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl. Acad. Sci. USA 91, 6458-6462.
21. Zitvogel, L., Couderc, B., Mayordomo, J. I., Robbins, P. D., Lotze, M. T., Storkus, W. J. (1996) IL-12-engineered dendritic cells serve as effective tumor vaccine adjuvants in vivo. Ann. N. Y. Acad. Sci. 795, 284-293.
22. Sallusto, F., Lanzavecchia, A. (1994) 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. J. Exp. Med. 179, 1109-1118.
23. Romani, N., Gruner, S., Brang, D., Kampgen, E., Lenz, A., Trockenbacher, B., Konwalinka, G., Fritsch, P. O., Steinman, R. M., Schuler, G. (1994) Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 180, 83-93.
24. O'Doherty, U., Steinman, R. M., Peng, M., Cameron, P. U., Gezelter, S., Kopeloff, I., Swiggard, W. J., Pope, M., Bhardwaj, N. (1993) Dendritic cells freshly isolated from human blood express CD4 and mature into typical immunostimulatory dendritic cells after culture in monocyte-conditioned medium. J. Exp. Med. 178, 1067-1076.
25. Romani, N., Reider, D., Heuer, M., Ebner, S., Kampgen, E., Eibl, B., Niederwieser, D., Schuler, G. (1996) Generation of mature dendritic cells from human blood. An improved method with special regard to clinical applicability. J. Immunol. Methods 196, 137-151.
26. Kugler, A., Stuhler, G., Walden, P., Zoller, G., Zobywalski, A., Brossart, P., Trefzer, U., Ullrich, S., Muller, C. A., Becker, V., Gross, A. J., Hemmerlein, B., Kanz, L., Muller, G. A., Ringert, R. H. (2000) Regression of human metastatic renal cell carcinoma after vaccination with tumor cell-dendritic cell hybrids. Nat. Med. 6, 332-336.
27. Lim, S. H., Bailey-Wood, R. (1999) Idiotypic protein-pulsed dendritic cell vaccination in multiple myeloma. Int. J. Cancer 83, 215-222.
28. Brossart, P., Wirths, S., Stuhler, G., Reichardt, V. L., Kanz, L., Brugger, W. (2000) Induction of cytotoxic T-lymphocyte responses in vivo after vaccinations with peptide-pulsed dendritic cells. Blood 96, 3102-3108.
29. Schoell, W. M., Mirhashemi, R., Liu, B., Janicek, M. F., Podack, E. R., Penalver, M. A., Averette, H. E. (1999) Generation of tumor-specific cytotoxic T lymphocytes by stimulation with HPV type 16 E7 peptide-pulsed dendritic cells: an approach to immunotherapy of cervical cancer. Gynecol. Oncol. 74, 448-455.
30. Thurner, B., Haendle, I., Roder, C., Dieckmann, D., Keikavoussi, P., Jonuleit, H., Bender, A., Maczek, C., Schreiner, D., von den Driesch, P., Brocker, E. B., Steinman, R. M., Enk, A., Kampgen, E., Schuler, G. (1999) 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. J. Exp. Med. 190, 1669-1678.
31. Panelli, M. C., Wunderlich, J., Jeffries, J., Wang, E., Mixon, A., Rosenberg, S. A., Marincola, F. M. (2000) Phase 1 study in patients with metastatic melanoma of immunization with dendritic cells presenting epitopes derived from the melanoma-associated antigens MART-1 and gp100. J. Immunother. 23, 487-498.
32. Jonuleit, H., Giesecke-Tuettenberg, A., Tuting, T., Thurner-Schuler, B., Stuge, T. B., Paragnik, L., Kandemir, A., Lee, P. P., Schuler, G., Knop, J., Enk, A. H. (2001) A comparison of two types of dendritic cell as adjuvants for the induction of melanoma-specific T-cell responses in humans following intranodal injection. Int. J. Cancer 93, 243-251.
33. Yu, J. S., Wheeler, C. J., Zeltzer, P. M., Ying, H., Finger, D. N., Lee, P. K., Yong, W. H., Incardona, F., Thompson, R. C., Riedinger, M. S., Zhang, W., Prins, R. M., Black, K. L. (2001) Vaccination of malignant glioma patients with peptide-pulsed dendritic cells elicits systemic cytotoxicity and intracranial T-cell infiltration. Cancer Res. 61, 842-847.
34. Morse, M. A., Deng, Y., Coleman, D., Hull, S., Kitrell-Fisher, E., Nair, S., Schlom, J., Ryback, M. E., Lyerly, H. K. (1999) A phase I study of active immunotherapy with carcinoembryonic antigen peptide (CAP-1)-pulsed, autologous human cultured dendritic cells in patients with metastatic malignancies expressing carcinoembryonic antigen. Clin. Cancer Res. 5, 1331-1338.
35. Zitvogel, L., Robbins, P. D., Storkus, W. J., Clarke, M. R., Maeurer, M. J., Campbell, R. L., Davis, C. G., Tahara, H., Schreiber, R. D., Lotze, M. T. (1996) Interleukin-12 and B7.1 co-stimulation cooperate in the induction of effective antitumor immunity and therapy of established tumors. Eur. J. Immunol. 26, 1335-1341.
36. Tsung, K., Meko, J. B., Peplinski, G. R., Tsung, Y. L., Norton, J. A. (1997) IL-12 induces T helper 1-directed antitumor response. J. Immunol. 158, 3359-3365.
37. Cella, M., Scheidegger, D., Palmer-Lehmann, K., Lane, P., Lanzavecchia, A., Alber, G. (1996) Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184, 747-752.
38. Bauer, S., Kirschning, C. J., Hacker, H., Redecke, V., Hausmann, S., Akira, S., Wagner, H., Lipford, G. B. (2001) Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. USA 98, 9237-9242.
39. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745.
40. Takeuchi, O., Hoshino, K., Kawai, T., Sanjo, H., Takada, H., Ogawa, T., Takeda, K., Akira, S. (1999) Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11, 443-451.
41. Sousa, C. R., Hieny, S., Scharton-Kersten, T., Jankovic, D., Charest, H., Germain, R. N., Sher, A. (1997) In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 186, 1819-1829.
42. Forster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner-Muller, I., Wolf, E., Lipp, M. (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99, 23-33.
43. Hirao, M., Onai, N., Hiroishi, K., Watkins, S. C., Matsushima, K., Robbins, P. D., Lotze, M. T., Tahara, H. (2000) CC chemokine receptor-7 on dendritic cells is induced after interaction with apoptotic tumor cells: critical role in migration from the tumor site to draining lymph nodes. Cancer Res. 60, 2209-2217.
44. Jonuleit, H., Kuhn, U., Muller, G., Steinbrink, K., Paragnik, L., Schmitt, E., Knop, J., Enk, A. H. (1997) Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur. J. Immunol. 27, 3135-3142.
45. Mosca, P. J., Hobeika, A. C., Clay, T. M., Nair, S. K., Thomas, E. K., Morse, M. A., Lyerly, H. K. (2000) A subset of human monocyte-derived dendritic cells expresses high levels of interleukin-12 in response to combined CD40 ligand and interferon-gamma treatment. Blood 96, 3499-3504.
46. Lee, P., Wang, F., Kuniyoshi, J., Rubio, V., Stuges, T., Groshen, S., Gee, C., Lau, R., Jeffery, G., Margolin, K., Marty, V., Weber, J. (2001) Effects of interleukin-12 on the immune response to a multipeptide vaccine for resected metastatic melanoma. J. Clin. Oncol. 19, 3836-3847.
47. Gajewski, T. F., Fallarino, F., Ashikari, A., Sherman, M. (2001) Immunization of HLA-A2+ melanoma patients with MAGE-3 or MelanA peptide-pulsed autologous peripheral blood mononuclear cells plus recombinant human interleukin 12. Clin. Cancer Res. 7, 895s-901s.
48. Fallarino, F., Uyttenhove, C., Boon, T., Gajewski, T. F. (1999) Improved efficacy of dendritic cell vaccines and successful immunization with tumor antigen peptide-pulsed peripheral blood mononuclear cells by coadministration of recombinant murine interleukin-12. Int. J. Cancer 80, 324-333.
49. Fallarino, F., Uyttenhove, C., Boon, T., Gajewski, T. F. (1996) Endogenous IL-12 is necessary for rejection of P815 tumor variants in vivo. J. Immunol. 156, 1095-1100.
50. Nanni, P., Nicoletti, G., De Giovanni, C., Landuzzi, L., Di Carlo, E., Cavallo, F., Pupa, S. M., Rossi, I., Colombo, M. P., Ricci, C., Astolfi, A., Musiani, P., Forni, G., Lollini, P. L. (2001) Combined allogeneic tumor cell vaccination and systemic interleukin 12 prevents mammary carcinogenesis in HER-2/neu transgenic mice. J. Exp. Med. 194, 1195-1205.
51. Tatsumi, T., Takehara, T., Kanto, T., Miyagi, T., Kuzushita, N., Sugimoto, Y., Jinushi, M., Kasahara, A., Sasaki, Y., Hori, M., Hayashi, N. (2001) Administration of interleukin-12 enhances the therapeutic efficacy of dendritic cell-based tumor vaccines in mouse hepatocellular carcinoma. Cancer Res. 61, 7563-7567.
52. Dieu-Nosjean, M. C., Vicari, A., Lebecque, S., Caux, C. (1999) Regulation of dendritic cell trafficking: a process that involves the participation of selective chemokines. J. Leukoc. Biol. 66, 252-262.
53. Vieira, P. L., de Jong, E. C., Wierenga, E. A., Kapsenberg, M. L., Kalinski, P. (2000) Development of Th1-inducing capacity in myeloid dendritic cells requires environmental instruction. J. Immunol. 164, 4507-4512.
54. Kadowaki, N., Ho, S., Antonenko, S., de Waal Malefyt, R., Kastelein, R. A., Bazan, F., Liu, Y. J. (2001) Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194, 863-870.
55. Wan, Y., Lu, L., Bramson, J. L., Baral, S., Zhu, Q., Pilon, A., Dayball, K. (2001) Dendritic cell-derived IL-12 is not required for the generation of cytotoxic, IFN-gamma-secreting, CD8(+) CTL in vivo. J. Immunol. 167, 5027-5033.
56. MacDonald, A. S., Pearce, E. J. (2002) Cutting edge: polarized Th cell response induction by transferred antigen-pulsed dendritic cells is dependent on IL-4 or IL-12 production by recipient cells. J. Immunol. 168, 3127-3130.
57. Sallusto, F., Lanzavecchia, A. (2000) Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunol. Rev. 177, 134-140.
58. Kaisho, T., Akira, S. (2001) Dendritic-cell function in Toll-like receptor- and MyD88-knockout mice. Trends Immunol. 22, 78-83.
59. Thoma-Uszynski, S., Kiertscher, S. M., Ochoa, M. T., Bouis, D. A., Norgard, M. V., Miyake, K., Godowski, P. J., Roth, M. D., Modlin, R. L. (2000) Activation of toll-like receptor 2 on human dendritic cells triggers induction of IL-12, but not IL-10. J. Immunol. 165, 3804-3810.
60. Hertz, C., Kiertscher, S., Godowski, P., Bouis, D., Norgard, M., Roth, M., Modlin, R. (2001) Microbial lipopeptides stimulate dendritic cell maturation via Toll-like receptor 2. J. Immunol. 166, 2444-2450.
61. Lauwerys, B. R., Garot, N., Renauld, J. C., Houssiau, F. A. (2000) Cytokine production and killer activity of NK/T-NK cells derived with IL-2, IL-15, or the combination of IL-12 and IL-18. J. Immunol. 165, 1847-1853.
62. Cassatella, M. A., Meda, L., Gasperini, S., D'Andrea, A., Ma, X., Trinchieri, G. (1995) Interleukin-12 production by human polymorphonuclear leukocytes. Eur. J. Immunol. 25, 1-5.
63. Petrofsky, M., Bermudez, L. E. (1999) Neutrophils from Mycobacterium avium-infected mice produce TNF-alpha, IL-12, and IL-1 beta and have a putative role in early host response. Clin. Immunol. 91, 354-358.
64. Ohteki, T., Suzue, K., Maki, C., Ota, T., Koyasu, S. (2001) Critical role of IL-15-IL-15R for antigen-presenting cell functions in the innate immune response. Nat. Immunol. 2, 1138-1143.
65. Jonuleit, H., Schmitt, E., Schuler, G., Knop, J., Enk, A. H. (2000) Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192, 1213-1222.
66. Dhodapkar, M. V., Steinman, R. M., Krasovsky, J., Munz, C., Bhardwaj, N. (2001) Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193, 233-238.
67. Biragyn, A., Surenhu, M., Yang, D., Ruffini, P. A., Haines, B. A., Klyushnenkova, E., Oppenheim, J. J., Kwak, L. W. (2001) Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J. Immunol. 167, 6644-6653.