2011 ESCI Award for Excellence in Basic/Translational Research: Innate regulation of adaptive immunity by dendritic cells

European Journal of Clinical Investigation

Volumn 41, Issue 8, 2011, Pages 907-916

  Reis e Sousa, Caetano ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

C type lectin receptors; Dendritic cells; Fungi; Innate immunity; Necrosis; RIG I like receptors; Toll like receptors; Viruses

Indexed keywords

DECTIN 1; LECTIN RECEPTOR; PROTEIN KINASE SYK; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9;

ADAPTIVE IMMUNITY; ARTICLE; CELL ACTIVATION; CELL DEATH; DENDRITIC CELL; FUNGUS; HUMAN; INFLUENZA VIRUS; INNATE IMMUNITY; NONHUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL;

ADAPTIVE IMMUNITY; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; LECTINS, C-TYPE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 79960081126     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/j.1365-2362.2011.02541.x     Document Type: Article

References (90)

1. Steinman RM, Nussenzweig MC. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc Natl Acad Sci USA 2002;99:351-8.
2. Reis e Sousa C. Dendritic cells in a mature age. Nat Rev Immunol 2006;6:476-83.
3. Janeway CA Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 1989;54:1-13.
4. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007;449:819-26.
5. Medzhitov R, Janeway CA Jr. Decoding the patterns of self and nonself by the innate immune system. Science 2002;296:298-300.
6. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol 1994;12:991-1045.
7. Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005;436:1186-90.
8. Reis e Sousa C. Activation of dendritic cells: translating innate into adaptive immunity. Curr Opin Immunol 2004;16:21-5.
9. Jacobs BL, Langland JO. When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 1996;219:339-49.
10. Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M, Taira K et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 2005;175:2851-8.
11. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004;5:730-7.
12. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, Flavell RA et al. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci USA 2006;103:8459-64.
13. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006;441:101-5.
14. Garcia-Sastre A. Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 2001;279:375-84.
15. Diebold S, Montoya M, Unger H, Alexopoulou L, Roy P, Haswell L et al. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 2003;424:324-8.
16. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 2006;80:5059-64.
17. Pichlmair A, Schulz O, Tan C, Näslund T, Liljeström P, Weber F et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006;314:997-1001.
18. Mibayashi M, Martínez-Sobrido L, Loo Y, Cárdenas W, Gale M, García-Sastre A. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 2007;81:514-24.
19. Gack MU, Albrecht RA, Urano T, Inn K-S, Huang I-C, Carnero E et al. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 2009;5:439-49.
20. Kim DH, Longo M, Han Y, Lundberg P, Cantin E, Rossi JJ. Interferon induction by siRNAs and ssRNAs synthesized by phage polymerase. Nat Biotechnol 2004;22:321-5.
21. Hornung V, Ellegast J, Kim S, Brzózka K, Jung A, Kato H et al. 5'-Triphosphate RNA is the ligand for RIG-I. Science 2006;314:994-7.
22. Cui S, Eisenächer K, Kirchhofer A, Brzózka K, Lammens A, Lammens K et al. The C-terminal regulatory domain is the RNA 5'-triphosphate sensor of RIG-I. Mol Cell 2008;29:169-79.
23. Takahasi K, Yoneyama M, Nishihori T, Hirai R, Kumeta H, Narita R et al. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol Cell 2008;29:428-40.
24. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell. New York: Garland Publishing Inc; 2002.
25. Ramakrishnan V. Ribosome structure and the mechanism of translation. Cell 2002;108:557-72.
26. Wild K, Weichenrieder O, Strub K, Sinning I, Cusack S. Towards the structure of the mammalian signal recognition particle. Curr Opin Struct Biol 2002;12:72-81.
27. Rehwinkel J, Reis e Sousa C. RIGorous detection: exposing virus through RNA sensing. Science 2010;327:284-6.
28. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A, Bier K et al. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 2010;140:397-408.
29. Baum A, Sachidanandam R, García-Sastre A. Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proc Natl Acad Sci USA 2010;107:16303-8.
30. HI polarization. Nat Immunol 2000;1:305-10.
31. Nakano H, Yanagita M, Gunn MD. Cd11c(+)b220(+)gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med 2001;194:1171-8.
32. Bruno L, Seidl T, Lanzavecchia A. Mouse pre-immunocytes as non-proliferating multipotent precursors of macrophages, interferon-producing cells, CD8alpha(+) and CD8alpha(-) dendritic cells. Eur J Immunol 2001;31:3403-12.
33. O'Keeffe M, Hochrein H, Vremec D, Caminschi I, Miller JL, Anders EM et al. Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J Exp Med 2002;196:1307-19.
34. Fonteneau JF, Gilliet M, Larsson M, Dasilva I, Munz C, Liu YJ et al. Activation of influenza virus-specific CD4+ and CD8+ T cells: a new role for plasmacytoid dendritic cells in adaptive immunity. Blood 2003;101:3520-6.
35. Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 2003;19:225-34.
36. Diebold S, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004;303:1529-31.
37. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, Akira S et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004;303:1526-9.
38. Lund J, Alexopoulou L, Sato A, Karow M, Adams N, Gale N et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci USA 2004;101:5598-603.
39. Lund J, Sato A, Akira S, Medzhitov R, Iwasaki A. Toll-like receptor 9-mediated recognition of herpes simplex virus-2 by plasmacytoid dendritic cells. J Exp Med 2003;198:1-9.
40. Krug A, Luker GD, Barchet W, Leib DA, Akira S, Colonna M. Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 2003;103:1433-7.
41. Pichlmair A, Reis e Sousa C. Innate recognition of viruses. Immunity 2007;27:370-83.
42. Wang J, Asher D, Chan M, Kurt-Jones E, Finberg R. Cutting Edge: antibody-mediated TLR7-dependent recognition of viral RNA. J Immunol 2007;178:3363-7.
43. Diebold S, Massacrier C, Akira S, Paturel C, Morel Y, Reis e Sousa C. Nucleic acid agonists for Toll-like receptor 7 are defined by the presence of uridine ribonucleotides. Eur J Immunol 2006;36:3256-67.
44. Barton GM, Kagan JC, Medzhitov R. Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat Immunol 2006;7:49-56.
45. Villadangos J, Schnorrer P. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat Rev Immunol 2007;7:543-55.
46. Shortman K, Heath WR. The CD8(+) dendritic cell subset. Immunol Rev 2010;234:18-31.
47. + DC correlates with unresponsiveness to imidazoquinolines. Eur J Immunol 2003;33:827-33.
48. + dendritic cells is attributable to their ability to internalise dead cells. Immunology 2002;107:183-9.
49. Iyoda T, Shimoyama S, Liu K, Omatsu Y, Akiyama Y, Maeda Y et al. The CD8(+) dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med 2002;195:1289-302.
50. Schulz O, Diebold S, Chen M, Näslund T, Nolte M, Alexopoulou L et al. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005;433:887-92.
51. McBride S, Hoebe K, Georgel P, Janssen E. Cell-associated double-stranded RNA enhances antitumor activity through the production of type I IFN. J Immunol 2006;177:6122-8.
52. Edwards A, Manickasingham S, Spörri R, Diebold S, Schulz O, Sher A 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 2002;169:3652-60.
53. Rogers N, Slack E, Edwards A, Nolte M, Schulz O, Schweighoffer E et al. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 2005;22:507-17.
54. Robinson MJ, Osorio F, Rosas M, Freitas RP, Schweighoffer E, Gross O et al. Dectin-2 is a Syk-coupled pattern recognition receptor crucial for Th17 responses to fungal infection. J Exp Med 2009;206:2037-51.
55. Robinson M, Sancho D, Slack E, LeibundGut-Landmann S, Reis e Sousa C. Myeloid C-type lectins in innate immunity. Nat Immunol 2006;7:1258-65.
56. Underhill D, Rossnagle E, Lowell C, Simmons R. Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 2005;106:2543-50.
57. Suzuki-Inoue K, Fuller G, García A, Eble J, Pöhlmann S, Inoue O et al. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood 2006;107:542-9.
58. Yoshitomi H, Sakaguchi N, Kobayashi K, Brown GD, Tagami T, Sakihama T et al. A role for fungal {beta}-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med 2005;201:949-60.
59. LeibundGut-Landmann S, Groß O, Robinson M, Osorio F, Slack E, Tsoni S et al. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol 2007;8:630-8.
60. Groß O, Gewies A, Finger K, Schäfer M, Sparwasser T, Peschel C et al. Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 2006;442:651-6.
61. Sato K, Yang X, Yudate T, Chung J, Wu J, Luby-Phelps K et al. Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor gamma chain to induce innate immune responses. J Biol Chem 2006;281:38854-66.
62. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A et al. Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 2010;32:681-91.
63. Yamasaki S, Ishikawa E, Sakuma M, Hara H, Ogata K, Saito T. Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat Immunol 2008;9:1179-88.
64. Bugarcic A, Hitchens K, Beckhouse AG, Wells CA, Ashman RB, Blanchard H. Human and mouse macrophage-inducible C-type lectin (Mincle) bind Candida albicans. Glycobiology 2008;18:679-85.
65. Wells CA, Salvage-Jones JA, Li X, Hitchens K, Butcher S, Murray RZ et al. The macrophage-inducible C-Type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J Immunol 2008;180:7404.
66. Yamasaki S, Matsumoto M, Takeuchi O, Matsuzawa T, Ishikawa E, Sakuma M et al. C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc Natl Acad Sci USA 2009;106:1897-902.
67. Ishikawa E, Ishikawa T, Morita YS, Toyonaga K, Yamada H, Takeuchi O et al. Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med 2009;206:2879-88.
68. Zelante T, De Luca A, Bonifazi P, Montagnoli C, Bozza S, Moretti S et al. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur J Immunol 2007;37:2695-706.
69. Huang W, Na L, Fidel PL, Schwarzenberger P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 2004;190:624-31.
70. Conti HR, Shen F, Nayyar N, Stocum E, Sun JN, Lindemann MJ et al. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med 2009;206:299-311.
71. Ho AW, Shen F, Conti HR, Patel N, Childs EE, Peterson AC et al. IL-17RC is required for immune signaling via an extended SEF/IL-17R signaling domain in the cytoplasmic tail. J Immunol 2010;185:1063-70.
72. Kagami S, Rizzo HL, Kurtz SE, Miller LS, Blauvelt A. IL-23 and IL-17A, but not IL-12 and IL-22, are required for optimal skin host defense against Candida albicans. J Immunol 2010;185:5453-62.
73. De Luca A, Zelante T, D'Angelo C, Zagarella S, Fallarino F, Spreca A et al. IL-22 defines a novel immune pathway of antifungal resistance. Mucosal Immunol 2010;3:361-73.
74. Ma CS, Chew GY, Simpson N, Priyadarshi A, Wong M, Grimbacher B et al. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J Exp Med 2008;205:1551-7.
75. Milner JD, Brenchley JM, Laurence A, Freeman AF, Hill BJ, Elias KM et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 2008;452:773-6.
76. de Beaucoudrey L, Puel A, Filipe-Santos O, Cobat A, Ghandil P, Chrabieh M et al. Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells. J Exp Med 2008;205:1543-50.
77. Puel A, Doffinger R, Natividad A, Chrabieh M, Barcenas-Morales G, Picard C et al. Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J Exp Med 2010;207:291-7.
78. Kisand K, Boe Wolff AS, Podkrajsek KT, Tserel L, Link M, Kisand KV et al. Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J Exp Med 2010;207:299-308.
79. Puel A, Cypowyj S, Bustamante J, Wright JF, Liu L, Lim HK et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011;332:65-8.
80. Ferwerda B, Ferwerda G, Plantinga TS, Willment JA, van Spriel AB, Venselaar H et al. Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 2009;361:1760-7.
81. Glocker E-O, Hennigs A, Nabavi M, Schäffer AA, Woellner C, Salzer U et al. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med 2009;361:1727-35.
82. Sancho D, Mourão-Sá D, Joffre OP, Schulz O, Rogers NC, Pennington DJ et al. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J Clin Invest 2008;118:2098-110.
83. Sancho D, Joffre O, Keller A, Rogers NC, Martinez D, Hernanz-Falcón P et al. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 2009;458:899-903.
84. Caminschi I, Lahoud MH, Shortman K. Enhancing immune responses by targeting antigen to DC. Eur J Immunol 2009;39:931-8.
85. Joffre O, Sancho D, Zelenay S, Keller AM, Reis e Sousa C. Efficient and versatile manipulation of the peripheral CD4+ T cell compartment by antigen targeting to DNGR-1/CLEC9A. Eur J Immunol 2010;40:1255-65.
86. Robbins SH, Walzer T, Dembele D, Thibault C, Defays A, Bessou G et al. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol 2008;9:R17.
87. Poulin LF, Salio M, Griessinger E, Anjos-Afonso F, Craciun L, Chen J-L et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med 2010;207:1261-71.
88. Jongbloed SL, Kassianos AJ, McDonald KJ, Clark GJ, Ju X, Angel CE et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010;207:1247-60.
89. Crozat K, Guiton R, Contreras V, Feuillet V, Dutertre C-A, Ventre E et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J Exp Med 2010;207:1283-92.
90. Bachem A, Güttler S, Hartung E, Ebstein F, Schaefer M, Tannert A et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J Exp Med 2010;207:1273-81.