Th1 polarization of CD4+ T cells by toll-like receptor 3-activated human microglia

Journal of Neuropathology and Experimental Neurology

Volumn 66, Issue 9, 2007, Pages 848-859

  Jack, Carolyn S ^a   Arbour, Nathalie ^b   Blain, Manon ^a   Meier, Ute Christiane ^c   Prat, Alexandre ^b   Antel, Jack P ^a  

^a MCGILL UNIVERSITY   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

CNS; Cytokines; Innate immunity; Interferon ; Multiple sclerosis

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12P40; INTERLEUKIN 23; INTERLEUKIN 6; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4;

ARTICLE; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LYMPHOCYTE PROLIFERATION; MICROGLIA; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TH1 CELL;

ANTIGENS, CD40; ANTIGENS, CD80; ANTIGENS, CD86; BRAIN; CD4-POSITIVE T-LYMPHOCYTES; CELL POLARITY; COCULTURE TECHNIQUES; CYTOKINES; HISTOCOMPATIBILITY ANTIGENS; HUMANS; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROGLIA; SIGNAL TRANSDUCTION; TH1 CELLS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4;

EID: 34548447524     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/nen.0b013e3181492a7     Document Type: Article

References (69)

1. Mack CL, Vanderlugt-Castaneda CL, Neville KL, et al. Microglia are activated to become competent antigen presenting and effector cells in the inflammatory environment of the Theiler's virus model of multiple sclerosis. J Neuroimmunol 2003;144:68-79
2. Santambrogio L, Belyanskaya SL, Fischer FR, et al. Developmental plasticity of CNS microglia. Proc Natl Acad Sci USA 2001;98:6295-300
3. Williams K, Bar-Or A, Ulvestad E, et al. Biology of adult human microglia in culture: Comparisons with peripheral blood monocytes and astrocytes. J Neuropathol Exp Neurol 1992;51:538-49
4. Katz-Levy Y, Neville KL, Padilla J, et al. Temporal development of autoreactive Th1 responses and endogenous presentation of self-myelin epitopes by central nervous system-resident APCs in Theiler's virus-infected mice. J Immunol 2000;165:5304-14
5. Kawakami N, Lassmann S, Li Z, et al. The activation status of neuroantigen-specific T cells in the target organ determines the clinical outcome of autoimmune encephalomyelitis. J Exp Med 2004;199:185-97
6. McMahon EJ, Bailey SL, Castenada CV, et al. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 2005;11:335-39
7. Tuohy VK, Yu M, Yin L, et al. Spontaneous regression of primary autoreactivity during chronic progression of experimental autoimmune encephalomyelitis and multiple sclerosis. J Exp Med 1999;189:1033-42
8. Jack C, Ruffini F, Bar-Or A, et al. Microglia and multiple sclerosis. J Neurosci Res 2005;81:363-73
9. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005;308:1314-18
10. Giulian D, Baker TJ. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 1986;6:2163-78
11. Jack CS, Arbour N, Manusow J, et al. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 2005;175:4320-30
12. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 2004;173:3916-24
13. Bsibsi M, Ravid R, Gveric D, et al. Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 2002;61:1013-21
14. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004;5:987-95
15. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006;124:783-801
16. Honda K, Taniguchi T. IRFs: Master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 2006;6:644-58
17. Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005;23:683-747
18. H-17 cells in relapsing EAE. Nat Immunol 2007;8:172-80
19. Yong VW, Antel JP. Culture of glial cells from human brain biopsies. In: Fedoroff S, Richardson E, eds. Protocols for Neural Cell Culture. Totowa, NJ: Humana Press, Inc., 1992:81-96
20. Pouly S, Becher B, Blain M, et al. Expression of a homologue of rat NG2 on human microglia. Glia 1999;27:259-68
21. Williams K Jr, Ulvestad E, Cragg L, et al. Induction of primary T cell responses by human glial cells. J Neurosci Res 1993;36:382-90
22. D'Souza S, Alinauskas K, McCrea E, et al. Differential susceptibility of human CNS-derived cell populations to TNF-dependent and independent immune-mediated injury. J Neurosci 1995;15:7293-7300
23. +dendritic cells generated in two different culture systems: Immunophenotypic and functional comparison. Scand J Immunol 2003;57:324-32
24. Napolitani G, Rinaldi A, Bertoni F, et al. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 2005;6:769-76
25. Seguin R, Moditi Z, Rotondo R, et al. Human brain endothelial cells supply support for monocyte immunoregulatory functions. J Neuroimmunol 2003;135:96-106
26. Kaisho T, Akira S. Dendritic-cell function in Toll-like receptor- and MyD88-knockout mice. Trends Immunol 2001;22:78-83
27. Hoebe K, Du X, Georgel P, et al. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003;424:743-48
28. + T cell-mediated suppression by dendritic cells. Science 2003;299:1033-36
29. Schnare M, Barton GM, Holt AC, et al. Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2001;2:947-50
30. Leadbetter EA, Rifkin IR, Hohlbaum AM, et al. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002;416:603-7
31. Lau CM, Broughton C, Tabor AS, et al. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J Exp Med 2005;202:1171-77
32. Lang KS, Recher M, Junt T, et al. Toll-like receptor engagement converts T-cell autoreactivity into overt autoimmune disease. Nat Med 2005;11:138-45
33. Prinz M, Garbe F, Schmidt H, et al. Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis. J Clin Invest 2006;116:456-64
34. Ulvestad E, Williams K, Bo L, et al. HLA class II molecules (HLA-DR,-DP,-DQ) on cells in the human CNS studied in situ and in vitro. Immunology 1994;82:535-41
35. Ulvestad E, Williams K, Bjerkvig R, et al. Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigen-presenting cells. J Leukoc Biol 1994;56:732-40
36. Williams K, Ulvestad E, Antel J. Immune regulatory and effector properties of human adult microglia studies in vitro and in situ. Adv Neuroimmunol 1994;4:273-81
37. Williams K, Ulvestad E, Antel JP. B7/BB-1 antigen expression on adult human microglia studied in vitro and in situ. Eur J Immunol 1994;24:3031-37
38. Pecora ND, Gehring AJ, Canaday DH, et al. Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function. J Immunol 2006;177:422-29
39. Hemmi H, Kaisho T, Takeuchi O, et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002;3:196-200
40. Hemmi H, Takeuchi O, Kawai T, et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000;408:740-45
41. Alexopoulou L, Holt AC, Medzhitov R, et al. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 2001;413:732-38
42. Hayashi F, Smith KD, Ozinsky A, et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001;410:1099-103
43. Yamamoto M, Sato S, Hemmi H, et al. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 2002;420:324-29
44. Lancaster GI, Khan Q, Drysdale P, et al. The physiological regulation of toll-like receptor expression and function in humans. J Physiol 2005;563:945-55
45. Cua DJ, Sherlock J, Chen Y, et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003;421:744-48
46. Bettelli E, Kuchroo VK. IL-12- and IL-23-induced T helper cell subsets: Birds of the same feather flock together. J Exp Med 2005;201:169-71
47. Gautier G, Humbert M, Deauvieau F, et al. A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J Exp Med 2005;201:1435-46
48. Li Y, Chu N, Hu A, et al. Increased IL-23p19 expression in multiple sclerosis lesions and its induction in microglia. Brain 2007;130:490-501
49. Hoebe K, Beutler B. LPS, dsRNA and the interferon bridge to adaptive immune responses: Trif, Tram, and other TIR adaptor proteins. J Endotoxin Res 2004;10:130-36
50. Montoya M, Schiavoni G, Mattei F, et al. Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 2002;99:3263071
51. Brassard DL, Grace MJ, Bordens RW. Interferon-α as an immunotherapeutic protein. J Leukoc Biol 2002;71:565-81
52. Lohoff M, Mak TW. Roles of interferon-regulatory factors in T-helper-cell differentiation. Nat Rev Immunol 2005;5:125-35
53. Janssens S, Beyaert R. Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol Cell 2003;11:293-302
54. Moynagh PN. TLR signalling and activation of IRFs: Revisiting old friends from the NF-κB pathway. Trends Immunol 2005;26:469-76
55. Renn CN, Sanchez DJ, Ochoa MT, et al. TLR activation of Langerhans cell-like dendritic cells triggers an antiviral immune response. J Immunol 2006;177:298-305
56. Hertzog PJ, O'Neill LA, Hamilton JA. The interferon in TLR signaling: More than just antiviral. Trends Immunol 2003;24:534-39
57. Doyle SE, O'Connell R, Vaidya SA, et al. Toll-like receptor 3 mediates a more potent antiviral response than Toll-like receptor 4. J Immunol 2003;170:3565-71
58. Gill N, Deacon PM, Lichty B, et al. Induction of innate immunity against herpes simplex virus type 2 infection via local delivery of Toll-like receptor ligands correlates with β interferon production. J Virol 2006;80:9943-50
59. Lang KS, Georgiev P, Recher M, et al. Immunoprivileged status of the liver is controlled by Toll-like receptor 3 signaling. J Clin Invest 2006;116:2456-63
60. Bekeredjian-Ding I, Roth SI, Gilles S, et al. T cell-independent, TLR-induced IL-12p70 production in primary human monocytes. J Immunol 2006;176:7438-46
61. Becher B, Prat A, Antel JP. Brain-immune connection: Immunore-gulatory properties of CNS-resident cells. Glia 2000;29:293-304
62. Budd RC. Activation-induced cell death. Curr Opin Immunol 2001;13:356-62
63. Green DR, Droin N, Pinkoski M. Activation-induced cell death in T cells. Immunol Rev 2003;193:70-81
64. Carson MJ, Sutcliffe JG, Campbell IL. Microglia stimulate naive T-cell differentiation without stimulating T-cell proliferation. J Neurosci Res 1999;55:127-34
65. Langrish CL, McKenzie BS, Wilson NJ, et al. IL-12 and IL-23: Master regulators of innate and adaptive immunity. Immunol Rev 2004;202:96-105
66. Schulz O, Diebold SS, Chen M, et al. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005;433:887-92
67. Owens T. Toll-like receptors on astrocytes: Patterning for immunity. J Neuroimmunol 2005;159:1-2
68. Akira S, Hemmi H. Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 2003;85:85-95
69. Van Noort JM, Bsibsi M, van Duijvenvoorden E, et al. TLR3 on astrocytes mediates neuroprotective responses and can be activated by an endogenous protein agonist (Abstract). J Neuroimmunol 2006;178(Suppl 1):29