Dendritic-cell control of pathogen-driven T-cell polarization

Nature Reviews Immunology

Volumn 3, Issue 12, 2003, Pages 984-993

  Kapsenberg, Martien L ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CD11 ANTIGEN; CD40 ANTIGEN; CHEMOKINE; CYTOKINE; HEAT SHOCK PROTEIN; HLA DR ANTIGEN; ICOSANOID; IMIQUIMOD; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 1 RECEPTOR; PATTERN RECOGNITION RECEPTOR; RECEPTOR; RESIQUIMOD; T LYMPHOCYTE RECEPTOR; THROMBOPLASTIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIGEN SPECIFICITY; CELL ACTIVATION; CELL KINETICS; CELL MATURATION; CELL SUBPOPULATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITIC CELL; EFFECTOR CELL; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INFECTION; MICROORGANISM; NONHUMAN; PHENOTYPE; PLASMODIUM FALCIPARUM; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; REVIEW; SCHISTOSOMA MANSONI; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH1 CELL; TH2 CELL; TISSUE CHARACTERIZATION;

EID: 0348135024     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri1246     Document Type: Review

References (120)

1. Bluestone, J. A. & Abbas, A. K. Natural versus adaptive regulatory T cells. Nature Rev. Immunol. 3, 253-257 (2003). An attractive proposal to distinguish thymus-derived natural and adapative regulatory T cells.
2. Banchereau, J. & Steinman, R. M. Dendritic cells and the control of immunity. Nature 392, 245-252 (1998).
3. Geissmann, F. et al. Accumulation of immature Langerhans cells in human lymph nodes draining chronically inflamed skin. J. Exp. Med. 196, 417-430 (2002).
4. Grouard, G. et al. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J. Exp. Med. 185, 1101-1101 (1997).
5. Kalinski, P., Hilkens, C. M., Wieranga, E. A. & Kapsenberg, M. L. T-cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol. Today 20, 561-567 (1999).
6. Kadowaki, N., Antonenko, S., Lau, J. Y. & Liu, Y. J. Natural interferon α/β-producing cells link innate and adaptive immunity. J. Exp. Med. 192, 219-226 (2000).
7. H2 cells in vivo. J. Immunol. 167, 4345-4350 (2001).
8. van der Kleij, D. et al. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates Toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277, 48122-48129 (2002). An in vitro study on the immune-evading capacity of Schistosoma mansoni by the identification of a lipid compound that primes through the ligation of a Toll-like receptor (TLR) for dendritic cells (DCs) that induce regulatory T cells.
9. Edwards, A. D. et al. Microbial recognition via Toll-like receptor-dependent and-independent pathways determines the cytokine response of murine dendritic cell subsets to CD40 triggering. J. Immunol. 169, 3652-3660 (2002).
10. Cunningham, A. J. & Lafferty, K. J. A simple, conservative explanation of the H-2 restriction of interactions between lymphocytes. Scand. J. Immunol. 6, 1-6 (1977).
11. Trinchieri, G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nature Rev. Immunol. 3, 133-146 (2003).
12. H2 cytokine production. J. Immunol. 161, 5138-5142 (1998).
13. + T cells into high IL-4-producing effectors. Blood 92, 3338-3345 (1998).
14. + T cells. J. Exp. Med. 184, 19-29 (1996).
15. + T cell alloantigen-specific hyporesponsiveness by IL-10 and TGF-β. Immunol. 163, 3684-3691 (1999).
16. Reis e Sousa, C., Edwards, A. D., Manickasingham, S. P. & Schulz, O. Conditioning of dendritic cells by pathogen-derived stimuli. Immunobiology 204, 595-597 (2001).
17. H1 phenotype. Blood 90, 1920-1926 (1997).
18. Snijders, A., Kalinski, P., Hilkens, C. M. & Kapsenberg, M. L. High-level IL-12 production by human dendritic cells requires two signals. Int. Immunol 10, 1593-1598 (1998)
19. Grewal, I. S. & Flavell, R. A. CD40 and CD154 in cell-mediated immunity. Annu Rev. Immunol. 16, 111-135 (1998).
20. Schulz, O. et al. CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity 13, 453-462 (2000).
21. Krug, A. et al. Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur J. Immunol. 31, 3026-3037 (2001).
22. O'Sullivan, B. J. & Thomas, R. CD40 ligation conditions dendritic cell antigen-presenting function through sustained activation of NF-κB. J. Immunol. 168, 5491-5498 (2002).
23. Janeway, C. A., Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol 54, 1-13 (1989).
24. Janeway, C. A., Jr & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216 (2002).
25. Akira, S., Takeda, K. & Kaisho, T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nature Immunol. 2, 675-680 (2001).
26. Schnare, M. et al. Toll-like receptors control activation of adaptive immune responses. Nature Immunol. 2, 947-950 (2001).
27. Beg, A. A. Endogenous ligands of Toll-like receptors: implications for regulating inflammatory and immune responses. Trends Immunol. 23, 509-512 (2002).
28. Matzinger, P. An innate sense of danger. Semin. Immunol. 10, 399-415 (1998).
29. H2 and nonpolarized T cells. Nature Immunol. 1, 311-316 (2000).
30. Brightbill, H. D. et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285, 732-736 (1999).
31. Takeuchi, O. et al. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J. Immunol. 169, 10-14 (2002).
32. Takeuchi, O. et al. Cutting edge: preferentially the R-stereoisomer of the mycoplasmal lipopeptide macrophage-activating lipopeptide-2 activates immune cells through a toll-like receptor 2- and MyD88-dependent signaling pathway. J. Immunol. 164, 554-557 (2000).
33. Takeuchi, O. et al. Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int. Immunol. 13, 933-940 (2001).
34. Thoma-Uszynski, S., Stenger, S. & Modlin, R. L. CTL-mediated killing of intracellular Mycobacterium tuberculosis is independent of target cell nuclear apoptosis. J. Immunol. 165, 5773-5779 (2000).
35. Re, F. & Strominger, J. L. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells J. Biol. Chem. 276, 37692-37699 (2001).
36. Cooper, A. M. et al. Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J. Immunol. 168, 1322-1327 (2002).
37. Yoshimura, A. et al. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 168, 1-5 (1999).
38. Underhill, D. M. et al. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens Nature 401, 811-815 (1999).
39. Weigt, H., Muhlradt, P. F., Emmendorffer, A., Krug, N. & Braun, A. Synthetic mycoplasma-derived lipopeptide MALP-2 induces maturation and function of dendritic cells. Immunobiology 207, 223-233 (2003).
40. Qi H., Denning, T. L. & Soong, L. Differential induction of interleukin-10 and interleukin-12 in dendritic cells by microbial toll-like receptor activators and skewing of T-cell cytokine profiles. Infect. Immun. 71, 3337-3342 (2003).
41. Gantner, B. N., Simmons, R. M., Canavera, S. J., Akira, S. & Underhill, D. M. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197, 1107-1117 (2003).
42. Cambi, A. et al. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur J. Immunol. 33, 532-8 (2003).
43. Sing, A. et al. Yersinia V-antigen exploits toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196, 1017-1024 (2002).
44. Alexopoulou, L., Holt, A. C., Medzhitov, R. & Flavell, R. A. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413, 732-738 (2001).
45. Cella, M. et al. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J. Exp. Med. 189, 821-829 (1999).
46. H cell polarizing signals. Immunol. 168, 1704-1709 (2002).
47. H1 development. J. Immunol. 168, 1710-1716 (2002).
48. Boonstra, A. et al. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential Toll-like receptor ligation. J. Exp. Med. 197, 101-109 (2003).
49. Eisenbarth, S. C. et al. Lipopolysaccharide-enhanced, Toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J. Exp. Med. 196, 1645-1651 (2002).
50. Pulendran, B. et al. Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J. Immunol. 167, 5067-5076 (2001).
51. Ogawa, T. et al. Cell activation by Porphyromonas gingivalis lipid A molecule through Toll-like receptor 4- and myeloid differentiation factor 88-dependent signaling pathway Int Immunol. 14, 1325-1332 (2002).
52. + DC correlates with unresponsiveness to imidazoquinolines. Eur. J. Immunol. 33, 827-833 (2003).
53. Ito, T. et al. Interferon-α and interleukin-12 are induced differentially by Toll-like receptor 7 ligands in human blood dendritic cell subsets. J. Exp. Med. 195, 1507-1512 (2002).
54. Hemmi, H. et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nature Immunol. 3, 196-200 (2002).
55. Lee, J. et al. Molecular basis for the immunostimulatory activity of guanine nucleoside analogs: activation of Toll-like receptor 7. Proc. Natl Acad. Sci. USA 100, 6646-6651 (2003).
56. Kadowaki, N. et al. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194, 863-869 (2001).
57. Hemmi, H. et al. A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745 (2000).
58. Oshiumi, H., Matsumoto, M., Funami, K., Akazawa, T. & Seya, T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-β induction. Nature Immunol. 4, 161-167 (2003).
59. Yamamoto, M. et al. Cutting edge: a novel Toll/L-1 receptor domain-containing adapter that preferentially activates the IFN-β promoter in the Toll-like receptor signaling. J. Immunol. 169, 6668-6672 (2002).
60. Horng, T., Barton, G. M., Flavell, R A. & Medzhitov, R. The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 420, 329-333 (2002).
61. H2 cytokines. J. Allergy Clin. Immunol. 107, 772-780 (2001).
62. H2 cells.
63. H2 responses by a parasitic helminth, Schistosoma mansoni. J. Exp. Med. 173, 159-166 (1991).
64. H2 response development. J. Immunol. 167, 1982-1988 (2001).
65. H-type response. J. Immunol. 167, 442-450 (2001).
66. H2 cell differentiation. Int. Immunol. 14, 695-700 (2002).
67. Sakaguchi, S., Sakaguchi, N., Asano, M. Itoh, M. & Toda, M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155, 1151-1164 (1995).
68. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389, 737-742 (1997).
69. + regulatory T cells control Leishmania major persistence and immunity. Nature 420, 502-507 (2002).
70. + regulatory T cells are essential components of the memory-protective immunity to Candida albicans. J. Immunol. 169, 6298-6308 (2002).
71. Urban, B. C. & Roberts, D. J. Malaria, monocytes, macrophages and myeloid dendritic cells: sticking of infected erythrocytes switches off host cells. Curr. Opin. Immunol. 14, 458-465 (2002).
72. Tailleux, L. et al. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 197, 121-127 (2003).
73. Geijtenbeek, T. B. et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17 (2003). This study, together with reference 72, shows that mycobacteria might evade immunity by binding to DC-SIGN resulting in negative signalling, including the inhibition of DC maturation.
74. Dolganiuc, A. et al. Hepatitis C virus core and nonstructural protein 3 proteins induce pro- and anti-inflammatory cytokines and inhibit dendritic cell differentiation. J. Immunol. 170, 5615-5624 (2003).
75. Salio, M., Cella, M., Suter, M. & Lanzavecchia, A. Inhibition of dendritic cell maturation by herpes simplex virus. Eur. J. Immunol. 29, 3245-3253 (1999).
76. Moutaftsi, M., Mehl, A. M., Borysiewicz, L. K. & Tabi, Z. Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells. Blood 99, 2913-2921 (2002).
77. McGuirk, P., McCann, C. & Mills, K. H. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J. Exp. Med. 195, 221-231 (2002). A mouse model study showing that Bordetella pertussis evades immunity through the virulence factor filamentous haemagglutinin that primes for DCs that induce regulatory T cells. In vitro work is confirmed by data indicating that haemagglutinin-deficient bacteria are more rapidly eradicated.
78. Sacks, D. & Sher, A. Evasion of innate immunity by parasitic protozoa. Nature Immunol. 3, 1041-1047 (2002).
79. Palucka, K. & Banchereau, J. How dendritic cells and microbes interact to elicit or subvert protective immune responses. Curr. Opin. Immunol. 14, 420-431 (2002).
80. Engering, A., Geijtenbeek, T. B. & van Kooyk, Y. Immune escape through C-type lectins on dendritic cells. Trends Immunol. 23, 480-485 (2002).
81. Doyle, S. et al. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17, 251-263 (2002).
82. H1 cells during viral infection. J. Immunol. 160, 3956-3964 (1998).
83. Jouanguy, E. et al. IL-12 and IFN-γ in host defense against mycobacteria and salmonella in mice and men. Curr. Opin. Immunol. 11, 346-351 (1999).
84. Dupuis, S. et al. Impaired response to interferon-α/β and lethal viral disease in human STAT1 deficiency. Nature Genet. 33, 388-391 (2003).
85. Shinkai, K., Mohrs, M. & Locksley, R. M. Helper T cells regulate type-2 innate immunity in vivo. Nature 420, 825-829 (2002).
86. Ohta, K., Wiggert, B., Yamagami, S., Taylor, A. W. & Streilein, J. W. Analysis of immunomodulatory activities of aqueous humor from eyes of mice with experimental autoimmune uveitis. J. Immunol. 164, 1185-1192 (2000).
87. + dendritic cells. Nature Immunol. 1, 83-87 (2000).
88. H1-inducing capacity in myeloid dendritic cells requires environmental instruction. J. Immunol. 164, 4507-4512 (2000).
89. H1 responses by inducing a type-1 polarized phenotype in dendritic cells. Role of keratinocyte-derived TNF-α type IIFNs and IL-18. J. Invest. Dermatol. 120, 990-997 (2003).
90. H2 cell-promoting effector dendritic cells. J. Immunol. 167, 3682-3686 (2001).
91. + dendritic cells: the levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. J. Immunol. 161, 2804-2809 (1998).
92. Soumelis, V. et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nature Immunol. 3, 673-680 (2002).
93. Braun, M. C., Lahey, E. & Kelsall, B. L. Selective suppression of IL-12 production by chemoattractants. J. Immunol. 164, 3009-3017 (2000).
94. Steinbrink, K., Wolfl, M., Jonuleit, H., Knop, J. & Enk, A. H. Induction of tolerance by IL-10-treated dendritic cells. J. Immunol. 159, 4772-4780 (1997).
95. Sato, K., Yamashita, N., Baba, M. & Matsuyama, T. Regulatory dendritic cells protect mice from murine acute graft-versus-host disease and leukemia relapse. Immunity 18, 387-379 (2003).
96. H2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J. Clin. Invest. 106, 551-559 (2000).
97. Alpan, O., Rudomen, G. & Matzinger, P. The role of dendritic cells, B cells, and M cells in gut-oriented immune responses. J. Immunol. 166, 4843-4852 (2001).
98. -, and double-negative Peyer's patch dendritic cells. J. Immunol. 166, 4884-4890 (2001).
99. Akbari, O., DeKruyff, R. H. & Umetsu, D. T. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nature Immunol. 2, 725-731 (2001).
100. - subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189, 587-592 (1999).
101. Pulendran, B. et al. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl Acad. Sci. USA 96, 1036-1041 (1999).
102. Rissoan, M. C. et al. Reciprocal control of T helper cell and dendritic cell differentiation. Science 283, 1183-1186 (1999).
103. Manickasingham, S. P., Edwards, A. D., Schulz, O. & Reis e Sousa, C. The ability of murine dendritic cell subsets to direct T helper cell differentiation is dependent on microbial signals. Eur. J. Immunol. 33, 101-107 (2003).
104. Legge, K. L. et al. On the role of dendritic cells in peripheral T cell tolerance and modulation of autoimmunity. J. Exp. Med. 196, 217-227 (2002).
105. hl DCs with a fixed ability to induce regulatory T cells. Although they are present in homeostatic conditions, they are upregulated in interleukin-10-transgenic mice, indicating that their appearance is regulated by environmental factors.
106. + DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology 108, 481-492 (2003).
107. + T helper cell phenotype development in a T cell receptor-αβ-transgenic model. J. Exp. Med. 182, 1579-1584 (1995).
108. + T cells. J. Exp. Med. 182, 1591-1596 (1995).
109. + T cells by antigenic peptides altered for TCR binding. J. Immunol. 158, 4237-4244 (1997).
110. Dietz, A. B., Bulur, P. A., Knutson, G. J., Matasic, R. & Vuk-Pavlovic, S. Maturation of human monocyte-derived dendritic cells studied by microarray hybridization. Biochem. Biophys. Res. Commun. 275, 731-738 (2000).
111. Huang, Q. et al. The plasticity of dendritic cell responses to pathogens and their components. Science 294, 870-875 (2001). A study on the analysis of RNA-expression profiles in DCs that are affected by different groups of pathogens and their components. This study, similar to references 111 and 112, sets the tune for the identification of the pattern of the adaptive immune response to a given pathogen at the level of DCs.
112. Granucci, F., Vizzardelli, C., Virzi, E., Rescigno, M. & Ricciardi-Castagnoli, P. Transcriptional reprogramming of dendritic cells by differentiation stimuli. Eur. J. Immunol. 31, 2539-2546 (2001).
113. Schlaak, J. F. et al. Cell-type and donor-specific transcriptional responses to interferon-α. Use of customized gene arrays. J. Biol. Chem. 277, 49428-49437 (2002).
114. Vremec, D., Pooley, J., Hochrein, H., Wu, L. & Shortman, K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164, 2978-2986 (2000).
115. Asselin-Paturel, C. et al. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nature Immunol. 2, 1144-1150 (2001).
116. Henri, S. et al. The dendritic cell populations of mouse lymph nodes. J. Immunol. 167, 741-748 (2001).
117. MacDonald, K. P. et al. Characterization of human blood dendritic cell subsets. Blood 100, 4512-4520 (2002).
118. Sallusto, F. & Lanzavecchia, A. 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-α. J. Exp. Med. 179, 1109-1118 (1994).
119. Jarrossay, D., Napolitani, G., Colonna, M., Sallusto, F. & Lanzavecchia, A. Specialization and complementarity in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells. Eur. J. Immunol. 31, 3388-3393 (2001).
120. Luft, T. et al. IFN-α enhances CD40 ligand-mediated activation of immature monocyte-derived dendritic cells. Int Immunol. 14, 367-380 (2002).