Microglial activation milieu controls regulatory T cell responses

Journal of Immunology

Volumn 191, Issue 11, 2013, Pages 5594-5602

  Ebner, Friederike ^a   Brandt, Christine ^a   Thiele, Peggy ^a   Richter, Daniel ^a   Schliesser, Ulrike ^a   Siffrin, Volker ^b   Schueler, Jutta ^a   Stubbe, Tobias ^a   Ellinghaus, Agnes ^a   Meisel, Christian ^a   Sawitzki, Birgit ^a   Nitsch, Robert ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSCRIPTION FACTOR FOXP3;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; BRAIN REGION; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; DISEASE COURSE; EFFECTOR CELL; FEMALE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE;

EID: 84888373474     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203331     Document Type: Article

References (47)

1. Engelhardt, B., and R. M. Ransohoff. 2005. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol. 26: 485-495.
2. Weiner, H. L., and D. J. Selkoe. 2002. Inflammation and therapeutic vaccination in CNS diseases. Nature 420: 879-884.
3. Giulian, D., and K. Vaca. 1993. Inflammatory glia mediate delayed neuronal damage after ischemia in the central nervous system. Stroke 24(12, Suppl.): I84-I90.
4. Aloisi, F., F. Ria, and L. Adorini. 2000. Regulation of T-cell responses by CNS antigen-presenting cells: different roles for microglia and astrocytes. Immunol. Today 21: 141-147.
5. Gerritse, K., J. D. Laman, R. J. Noelle, A. Aruffo, J. A. Ledbetter, W. J. Boersma, and E. Claassen. 1996. CD40-CD40 ligand interactions in experimental allergic encephalomyelitis and multiple sclerosis. Proc. Natl. Acad. Sci. USA 93: 2499-2504.
6. Issazadeh, S., V. Navikas, M. Schaub, M. Sayegh, and S. Khoury. 1998. Kinetics of expression of costimulatory molecules and their ligands in murine relapsing experimental autoimmune encephalomyelitis in vivo. J. Immunol. 161: 1104-1112.
7. O'Keefe, G. M., V. T. Nguyen, and E. N. Benveniste. 2002. Regulation and function of class II major histocompatibility complex, CD40, and B7 expression in macrophages and microglia: implications in neurological diseases. J. Neurovirol. 8: 496-512.
8. Thored, P., U. Heldmann, W. Gomes-Leal, R. Gisler, V. Darsalia, J. Taneera, J. M. Nygren, S.-E. W. Jacobsen, C. T. Ekdahl, Z. Kokaia, and O. Lindvall. 2009. Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57: 835-849.
9. Bechmann, I., S. Peter, M. Beyer, U. Gimsa, and R. Nitsch. 2001. Presence of B-7.2 (CD86) and lack of B7-1 (CD80) on myelin-phagocytosing MHC-II positive rat microglia are associated with nondestructive immunity in vivo. FASEB J. 15: 1086-1088.
10. Hailer, N. P., I. Bechmann, S. Heizmann, and R. Nitsch. 1997. Adhesion molecule expression on phagocytic microglial cells following anterograde degeneration of perforant path axons. Hippocampus 7: 341-349.
11. Donnelly, D. J., and P. G. Popovich. 2008. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp. Neurol. 209: 378-388.
12. Jones, T. B., D. M. Basso, A. Sodhi, J. Z. Pan, R. P. Hart, R. C. MacCallum, S. Lee, C. C. Whitacre, and P. G. Popovich. 2002. Pathological CNS autoimmune disease triggered by traumatic spinal cord injury: implications for autoimmune vaccine therapy. J. Neurosci. 22: 2690-2700.
13. Sakaguchi, S., M. Ono, R. Setoguchi, H. Yagi, S. Hori, Z. Fehervari, J. Shimizu, T. Takahashi, and T. Nomura. 2006. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol. Rev. 212: 8-27.
14. Bettini, M., and D. A. Vignali. 2009. Regulatory T cells and inhibitory cytokines in autoimmunity. Curr. Opin. Immunol. 21: 612-618.
15. Taams, L. S., and A. N. Akbar. 2005. Peripheral generation and function of CD4+ CD25+ regulatory T cells. Curr. Top. Microbiol. Immunol. 293: 115-131.
16. Liu, Y., I. Teige, B. Birnir, and S. Issazadeh-Navikas. 2006. Neuron-mediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE. Nat. Med. 12: 518-525.
17. Korn, T., J. Reddy, W. Gao, E. Bettelli, A. Awasthi, T. R. Petersen, B. T. Bäckström, R. A. Sobel, K. W. Wucherpfennig, T. B. Strom, et al. 2007. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 13: 423-431.
18. Kreutzberg, G. W. 1996. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19: 312-318.
19. Bhat, R., and L. Steinman. 2009. Innate and adaptive autoimmunity directed to the central nervous system. Neuron 64: 123-132.
20. Wang, Y., A. Kissenpfennig, M. Mingueneau, S. Richelme, P. Perrin, S. Chevrier, C. Genton, B. Lucas, J. P. DiSanto, H. Acha-Orbea, et al. 2008. Th2 lymphoproliferative disorder of LatY136F mutant mice unfolds independently of TCRMHC engagement and is insensitive to the action of Foxp3+ regulatory T cells. J. Immunol. 180: 1565-1575.
21. Nolte, C., T. Möller, T. Walter, and H. Kettenmann. 1996. Complement 5a controls motility of murine microglial cells in vitro via activation of an inhibitory G-protein and the rearrangement of the actin cytoskeleton. Neuroscience 73: 1091-1107.
22. Baron, U., S. Floess, G. Wieczorek, K. Baumann, A. Grützkau, J. Dong, A. Thiel, T. J. Boeld, P. Hoffmann, M. Edinger, et al. 2007. DNA demethylation in the human FOXP3 locus discriminates regulatory T cells from activated FOXP3+ conventional T cells. Eur. J. Immunol. 37: 2378-2389.
23. Floess, S., J. Freyer, C. Siewert, U. Baron, S. Olek, J. Polansky, K. Schlawe, H.-D. Chang, T. Bopp, E. Schmitt, et al. 2007. Epigenetic control of the Foxp3 locus in regulatory T cells. PLoS Biol. 5: e38.
24. Collawn, J. F., and E. N. Benveniste. 1999. Regulation of MHC class II expression in the central nervous system. Microbes Infect. 1: 893-902.
25. Hackstein, H., and A. W. Thomson. 2004. Dendritic cells: emerging pharmacological targets of immunosuppressive drugs. Nat. Rev. Immunol. 4: 24-34.
26. Giacomini, E., A. Sotolongo, E. Iona, M. Severa, M. E. Remoli, V. Gafa, R. Lande, L. Fattorini, I. Smith, R. Manganelli, and E. M. Coccia. 2006. Infection of human dendritic cells with a Mycobacterium tuberculosis sigE mutant stimulates production of high levels of interleukin-10 but low levels of CXCL10: impact on the T-cell response. Infect. Immun. 74: 3296-3304.
27. Cheeran, M. C.-J., S. Hu, W. S. Sheng, P. K. Peterson, and J. R. Lokensgard. 2003. CXCL10 production from cytomegalovirus-stimulated microglia is regulated by both human and viral interleukin-10. J. Virol. 77: 4502-4515.
28. Huang, C.-J., B. R. Stevens, R. B. Nielsen, P. N. Slovin, X. Fang, D. R. Nelson, and J. W. Skimming. 2002. Interleukin-10 inhibition of nitric oxide biosynthesis involves suppression of CAT-2 transcription. Nitric Oxide 6: 79-84.
29. Stubbe, T., F. Ebner, D. Richter, O. R. Engel, J. Klehmet, G. Royl, A. Meisel, R. Nitsch, C. Meisel, and C. Brandt. 2013. Regulatory T cells accumulate and proliferate in the ischemic hemisphere for up to 30 days after MCAO. J. Cereb. Blood Flow Metab. 33: 37-47.
30. Mutlu, L., C. Brandt, E. Kwidzinski, B. Sawitzki, U. Gimsa, J. Mahlo, O. Aktas, R. Nitsch, M. van Zwam, J. D. Laman, and I. Bechmann. 2007. Tolerogenic effect of fiber tract injury: reduced EAE severity following entorhinal cortex lesion. Exp. Brain Res. 178: 542-553.
31. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
32. Dhodapkar, M. V., R. M. Steinman, J. Krasovsky, C. Munz, and N. Bhardwaj. 2001. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193: 233-238.
33. Korn, T., E. Bettelli, W. Gao, A. Awasthi, A. Jäger, T. B. Strom, M. Oukka, and V. K. Kuchroo. 2007. IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature 448: 484-487.
34. Weber, M. S., T. Prod'homme, S. Youssef, S. E. Dunn, C. D. Rundle, L. Lee, J. C. Patarroyo, O. Stüve, R. A. Sobel, L. Steinman, and S. S. Zamvil. 2007. Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat. Med. 13: 935-943.
35. Kohm, A. P., P. A. Carpentier, H. A. Anger, and S. D. Miller. 2002. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J. Immunol. 169: 4712-4716.
36. Rady, P. L., P. Cadet, T. K. Bui, S. K. Tyring, S. Baron, G. J. Stanton, and T. K. Hughes. 1995. Production of interferon g messenger RNA by cells of nonimmune origin. Cytokine 7: 793-798.
37. De Simone, R., G. Levi, and F. Aloisi. 1998. Interferon g gene expression in rat central nervous system glial cells. Cytokine 10: 418-422.
38. Wei, Y. P., M. Kita, K. Shinmura, X. Q. Yan, R. Fukuyama, S. Fushiki, and J. Imanishi. 2000. Expression of IFN-γ in cerebrovascular endothelial cells from aged mice. J. Interferon Cytokine Res. 20: 403-409.
39. Ponomarev, E. D., L. P. Shriver, and B. N. Dittel. 2006. CD40 expression by microglial cells is required for their completion of a two-step activation process during central nervous system autoimmune inflammation. J. Immunol. 176: 1402-1410.
40. Whiting, D., G. Hsieh, J. J. Yun, A. Banerji, W. Yao, M. C. Fishbein, J. Belperio, R. M. Strieter, B. Bonavida, and A. Ardehali. 2004. Chemokine monokine induced by IFN-g/CXC chemokine ligand 9 stimulates T lymphocyte proliferation and effector cytokine production. J. Immunol. 172: 7417-7424.
41. Mahnke, K., T. Bedke, and A. H. Enk. 2007. Regulatory conversation between antigen presenting cells and regulatory T cells enhance immune suppression. Cell. Immunol. 250: 1-13.
42. Chen, W., W. Jin, N. Hardegen, K. J. Lei, L. Li, N. Marinos, G. McGrady, and S. M. Wahl. 2003. Conversion of peripheral CD4+ CD25- naive T cells to CD4+ CD25+ regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
43. Lindholm, D., E. Castrén, R. Kiefer, F. Zafra, and H. Thoenen. 1992. Transforming growth factor-β1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J. Cell Biol. 117: 395-400.
44. Kiefer, R., M. L. Supler, K. V. Toyka, and W. J. Streit. 1994. In situ detection of transforming growth factor-β mRNA in experimental rat glioma and reactive glial cells. Neurosci. Lett. 166: 161-164.
45. Wan, Y. Y. 2010. Multi-tasking of helper T cells. Immunology 130: 166-171.
46. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
47. Veldhoen, M., and B. Stockinger. 2006. TGFβ1, a "Jack of all trades": the link with pro-inflammatory IL-17-producing T cells. Trends Immunol. 27: 358-361.