The role of dendritic cells in CNS autoimmunity

Journal of Molecular Medicine

Volumn 88, Issue 6, 2010, Pages 535-544

  Zozulya, Alla L ^a   Clarkson, Benjamin D ^b   Ortler, Sonja ^c   Fabry, Zsuzsanna ^b   Wiendl, Heinz ^c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

B7 H1; CNS; Co inhibitory molecules; Dendritic cells; Experimental autoimmune encephalomyelitis; Multiple sclerosis; PD L1; T cell immune responses

Indexed keywords

BETA INTERFERON; CD135 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR7; COLECALCIFEROL; CYCLOSPORIN A; DEXAMETHASONE; ESTRADIOL; GLUCOCORTICOID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 12; INTERLEUKIN 16; INTERLEUKIN 18; LESTAURTINIB; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PATTERN RECOGNITION RECEPTOR; PREDNISOLONE; RANTES; RAPAMYCIN; SECONDARY LYMPHOID TISSUE CHEMOKINE; TACROLIMUS; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ALLERGIC ENCEPHALOMYELITIS; ANTIGEN RECOGNITION; AUTOIMMUNITY; CELL MATURATION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; MICROENVIRONMENT; MULTIPLE SCLEROSIS; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, CD; AUTOIMMUNITY; CENTRAL NERVOUS SYSTEM; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; IMMUNITY, INNATE; MULTIPLE SCLEROSIS; T-LYMPHOCYTES;

EID: 77954562817     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-010-0607-4     Document Type: Review

References (88)

1. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392:245
2. Shortman K, Liu YJ (2002) Mouse and human dendritic cell subtypes. Nat Rev Immunol 2:151
3. Kadowaki N, Antonenko S, Lau JY, Liu YJ (2000) Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J Exp Med 192:219
4. Steinman RM (1991) The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9:271
5. Matzinger P (2007) Friendly and dangerous signals: is the tissue in control? Nat Immunol 8:11
6. Inaba K, Witmer-Pack M, Inaba M, Hathcock KS, Sakuta H, Azuma M, Yagita H, Okumura K, Linsley PS, Ikehara S, Muramatsu S, Hodes RJ, Steinman RM (1994) The tissue distribution of the B7-2 costimulator in mice: abundant expression on dendritic cells in situ and during maturation in vitro. J Exp Med 180:1849
7. Schuler G, Steinman RM (1985) Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med 161:526
8. Langenkamp A, Messi M, Lanzavecchia A, Sallusto F (2000) Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat Immunol 1:311
9. Menges M, Rossner S, Voigtlander C, Schindler H, Kukutsch NA, Bogdan C, Erb K, Schuler G, Lutz MB (2002) Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity. J Exp Med 195:15
10. Villadangos JA, Heath WR (2005) Life cycle, migration and antigen presenting functions of spleen and lymph node dendritic cells: limitations of the Langerhans cells paradigm. Semin Immunol 17:262
11. Kapsenberg ML (2003) Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol 3:984
12. Reis e Sousa C (2006) Dendritic cells in a mature age. Nat Rev Immunol 6:476
13. Galea I, Bechmann I, Perry VH (2007) What is immune privilege (not)? Trends Immunol 28:12
14. Owens T, Bechmann I, Engelhardt B (2008) Perivascular spaces and the two steps to neuroinflammation. J Neuropathol Exp Neurol 67:1113
15. Matyszak MK, Perry VH (1996) The potential role of dendritic cells in immune-mediated inflammatory diseases in the central nervous system. Neuroscience 74:599
16. McMenamin PG (1999) Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges, and choroid plexus of the rat brain as demonstrated in wholemount preparations. J Comp Neurol 405:553
17. Serot JM, Bene MC, Foliguet B, Faure GC (2000) Monocytederived IL-10-secreting dendritic cells in choroid plexus epithelium. J Neuroimmunol 105:115
18. Pashenkov M, Huang YM, Kostulas V, Haglund M, Soderstrom M, Link H (2001) Two subsets of dendritic cells are present in human cerebrospinal fluid. Brain 124:480
19. Bailey SL, Schreiner B, McMahon EJ, Miller SD (2007) CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4+ T (H)-17 cells in relapsing EAE. Nat Immunol 8:172
20. Lande R, Gafa V, Serafini B, Giacomini E, Visconti A, Remoli ME, Severa M, Parmentier M, Ristori G, Salvetti M, Aloisi F, Coccia EM (2008) Plasmacytoid dendritic cells in multiple sclerosis: intracerebral recruitment and impaired maturation in response to interferon-beta. J Neuropathol Exp Neurol 67:388
21. Bailey SL, Carpentier PA, McMahon EJ, Begolka WS, Miller SD (2006) Innate and adaptive immune responses of the central nervous system. Crit Rev Immunol 26:149
22. Fabry Z, Schreiber HA, Harris MG, Sandor M (2008) Sensing the microenvironment of the central nervous system: immune cells in the central nervous system and their pharmacological manipulation. Curr Opin Pharmacol 8:496
23. Suter T, Biollaz G, Gatto D, Bernasconi L, Herren T, Reith W, Fontana A (2003) The brain as an immune privileged site: dendritic cells of the central nervous system inhibit T cell activation. Eur J Immunol 33:2998
24. Fischer HG, Reichmann G (2001) Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J Immunol 166:2717
25. Santambrogio L, Belyanskaya SL, Fischer FR, Cipriani B, Brosnan CF, Ricciardi-Castagnoli P, Stern LJ, Strominger JL, Riese R (2001) Developmental plasticity of CNS microglia. Proc Natl Acad Sci USA 98:6295
26. Willenborg DO, Staykova MA (2003) Cytokines in the pathogenesis and therapy of autoimmune encephalomyelitis and multiple sclerosis. Adv Exp Med Biol 520:96
27. Maraskovsky E, Brasel K, Teepe M, Roux ER, Lyman SD, Shortman K, McKenna HJ (1996) Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligandtreated mice: multiple dendritic cell subpopulations identified. J Exp Med 184:1953
28. Curtin JF, King GD, Barcia C, Liu C, Hubert FX, Guillonneau C, Josien R, Anegon I, Lowenstein PR, Castro MG (2006) Fms-like tyrosine kinase 3 ligand recruits plasmacytoid dendritic cells to the brain. J Immunol 176:3566
29. Zozulya AL, Reinke E, Baiu DC, Karman J, Sandor M, Fabry Z (2007) Dendritic cell transmigration through brain microvessel endothelium is regulated by MIP-1alpha chemokine and matrix metalloproteinases. J Immunol 178:520
30. Alt C, Laschinger M, Engelhardt B (2002) Functional expression of the lymphoid chemokines CCL19 (ELC) and CCL 21 (SLC) at the blood-brain barrier suggests their involvement in G-proteindependent lymphocyte recruitment into the central nervous system during experimental autoimmune encephalomyelitis. Eur J Immunol 32:2133
31. Randolph GJ, Beaulieu S, Lebecque S, Steinman RM, Muller WA (1998) Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282:480
32. Bai B, Song W, Ji Y, Liu X, Tian L, Wang C, Chen D, Zhang X, Zhang M (2009) Microglia and microglia-like cell differentiated from DC inhibit CD4 T cell proliferation. PLoS ONE 4: e7869
33. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD (2000) Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR) 2. J Exp Med 192:1075
34. Pashenkov M, Teleshova N, Kouwenhoven M, Kostulas V, Huang YM, Soderstrom M, Link H (2002) Elevated expression of CCR5 by myeloid (CD11c+) blood dendritic cells in multiple sclerosis and acute optic neuritis. Clin Exp Immunol 127:519
35. Trebst C, Sorensen TL, Kivisakk P, Cathcart MK, Hesselgesser J, Horuk R, Sellebjerg F, Lassmann H, Ransohoff RM (2001) CCR1+/CCR5+ mononuclear phagocytes accumulate in the central nervous system of patients with multiple sclerosis. Am J Pathol 159:1701
36. Sellebjerg F, Madsen HO, Jensen CV, Jensen J, Garred P (2000) CCR5 delta32, matrix metalloproteinase-9 and disease activity in multiple sclerosis. J Neuroimmunol 102:98
37. Kivisakk P, Mahad DJ, Callahan MK, Sikora K, Trebst C, Tucky B, Wujek J, Ravid R, Staugaitis SM, Lassmann H, Ransohoff RM (2004) Expression of CCR7 in multiple sclerosis: implications for CNS immunity. Ann Neurol 55:627
38. de Vos AF, van Meurs M, Brok HP, Boven LA, Hintzen RQ, van der Valk P, Ravid R, Rensing S, Boon L, t Hart BA, Laman JD (2002) Transfer of central nervous system autoantigens and presentation in secondary lymphoid organs. J Immunol 169:5415
39. Karman J, Ling C, Sandor M, Fabry Z (2004) Initiation of immune responses in brain is promoted by local dendritic cells. J Immunol 173:2353
40. Greter M, Heppner FL, Lemos MP, Odermatt BM, Goebels N, Laufer T, Noelle RJ, Becher B (2005) Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat Med 11:328
41. McMahon EJ, Bailey SL, Castenada CV, Waldner H, Miller SD (2005) Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 11:335
42. Serafini B, Rosicarelli B, Magliozzi R, Stigliano E, Capello E, Mancardi GL, Aloisi F (2006) Dendritic cells in multiple sclerosis lesions: maturation stage, myelin uptake, and interaction with proliferating T cells. J Neuropathol Exp Neurol 65:124
43. Zozulya AL, Ortler S, Lee J, Weidenfeller C, Sandor M, Wiendl H, Fabry Z (2009) Intracerebral dendritic cells critically modulate encephalitogenic versus regulatory immune responses in the CNS. J Neurosci 29:140
44. Bailey-Bucktrout SL, Caulkins SC, Goings G, Fischer JA, Dzionek A, Miller SD (2008) Cutting edge: central nervous system plasmacytoid dendritic cells regulate the severity of relapsing experimental autoimmune encephalomyelitis. J Immunol 180:6457
45. Korn T, Reddy J, Gao W, Bettelli E, Awasthi A, Petersen TR, Backstrom BT, Sobel RA, Wucherpfennig KW, Strom TB, Oukka M, Kuchroo VK (2007) Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat Med 13:423
46. O'Connor RA, Malpass KH, Anderton SM (2007) The inflamed central nervous system drives the activation and rapid proliferation of Foxp3+ regulatory T cells. J Immunol 179:958
47. Hirata S, Matsuyoshi H, Fukuma D, Kurisaki A, Uemura Y, Nishimura Y, Senju S (2007) Involvement of regulatory T cells in the experimental autoimmune encephalomyelitis-preventive effect of dendritic cells expressing myelin oligodendrocyte glycoprotein plus TRAIL. J Immunol 178:918
48. Hubert P, Jacobs N, Caberg JH, Boniver J, Delvenne P (2007) The cross-talk between dendritic and regulatory T cells: good or evil. J Leukoc Biol 82:781-794
49. Dong H, Zhu G, Tamada K, Chen L (1999) B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 5:1365
50. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC, Horton HF, Fouser L, Carter L, Ling V, Bowman MR, Carreno BM, Collins M, Wood CR, Honjo T (2000) Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 192:1027
51. Sharpe AH, Freeman GJ (2002) The B7-CD28 superfamily. Nat Rev Immunol 2:116
52. Nishimura H, Honjo T (2001) PD-1: an inhibitory immunoreceptor involved in peripheral tolerance. Trends Immunol 22:265
53. Nishimura H, Minato N, Nakano T, Honjo T (1998) Immunological studies on PD-1 deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int Immunol 10:1563
54. Carter LL, Leach MW, Azoitei ML, Cui J, Pelker JW, Jussif J, Benoit S, Ireland G, Luxenberg D, Askew GR, Milarski KL, Groves C, Brown T, Carito BA, Percival K, Carreno BM, Collins M, Marusic S (2007) PD-1/PD-L1, but not PD-1/PD-L2, interactions regulate the severity of experimental autoimmune encephalomyelitis. J Neuroimmunol 182:124
55. Cheng X, Zhao Z, Ventura E, Gran B, Shindler KS, Rostami A (2007) The PD-1/PD-L pathway is up-regulated during IL-12-induced suppression of EAE mediated by IFN-gamma. J Neuroimmunol 185:75
56. Liang SC, Latchman YE, Buhlmann JE, Tomczak MF, Horwitz BH, Freeman GJ, Sharpe AH (2003) Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur J Immunol 33:2706
57. Salama AD, Chitnis T, Imitola J, Ansari MJ, Akiba H, Tushima F, Azuma M, Yagita H, Sayegh MH, Khoury SJ (2003) Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis. J Exp Med 198:71
58. Zhu B, Guleria I, Khosroshahi A, Chitnis T, Imitola J, Azuma M, Yagita H, Sayegh MH, Khoury SJ (2006) Differential role of programmed death-ligand 1 [corrected] and programmed deathligand 2 [corrected] in regulating the susceptibility and chronic progression of experimental autoimmune encephalomyelitis. J Immunol 176:3480
59. Ortler S, Leder C, Mittelbronn M, Zozulya AL, Knolle PA, Chen L, Kroner A, Wiendl H (2008) B7-H1 restricts neuroantigenspecific T cell responses and confines inflammatory CNS damage: implications for the lesion pathogenesis of multiple sclerosis. Eur J Immunol 38:1734
60. Zozulya AL, Ortler S, Fabry Z, Sandor M, Wiendl H (2009) The level of B7 homologue 1 expression on brain DC is decisive for CD8 Treg cell recruitment into the CNS during EAE. Eur J Immunol 39:1536
61. Wang S, Bajorath J, Flies DB, Dong H, Honjo T, Chen L (2003) Molecular modeling and functional mapping of B7-H1 and B7-DC uncouple costimulatory function from PD-1 interaction. J Exp Med 197:1083
62. Waisman A, Yogev N (2009) B7-H1 and CD8+ Treg: the enigmatic role of B7-H1 in peripheral tolerance. Eur J Immunol 39:1448
63. Huang YM, Xiao BG, Ozenci V, Kouwenhoven M, Teleshova N, Fredrikson S, Link H (1999) Multiple sclerosis is associated with high levels of circulating dendritic cells secreting pro-inflammatory cytokines. J Neuroimmunol 99:82
64. Navarro J, Aristimuno C, Sanchez-Ramon S, Vigil D, Martinez-Gines ML, Fernandez-Cruz E, de Andres C (2006) Circulating dendritic cells subsets and regulatory T-cells at multiple sclerosis relapse: differential short-term changes on corticosteroids therapy. J Neuroimmunol 176:153
65. Stasiolek M, Bayas A, Kruse N, Wieczarkowiecz A, Toyka KV, Gold R, Selmaj K (2006) Impaired maturation and altered regulatory function of plasmacytoid dendritic cells in multiple sclerosis. Brain 129:1293
66. Lopez C, Comabella M, Al-zayat H, Tintore M, Montalban X (2006) Altered maturation of circulating dendritic cells in primary progressive MS patients. J Neuroimmunol 175:183
67. Schreiner B, Mitsdoerffer M, Kieseier BC, Chen L, Hartung HP, Weller M, Wiendl H (2004) Interferon-beta enhances monocyte and dendritic cell expression of B7-H1 (PD-L1), a strong inhibitor of autologous T-cell activation: relevance for the immune modulatory effect in multiple sclerosis. J Neuroimmunol 155:172
68. Berghella AM, Totaro R, Pellegrini P, Contasta I, Russo T, Carolei A, Adorno D (2005) Immunological study of IFNbeta-1a-treated and untreated multiple sclerosis patients: clarifying IFNbeta mechanisms and establishing specific dendritic cell immunotherapy. Neuroimmunomodulation 12:29
69. Pellegrini P, Totaro R, Contasta I, Berghella AM, Carolei A, Adorno D (2005) CD30 antigen and multiple sclerosis: CD30, an important costimulatory molecule and marker of a regulatory subpopulation of dendritic cells, is involved in the maintenance of the physiological balance between TH1/TH2 immune responses and tolerance. The role of IFN-beta-1a in the treatment of multiple sclerosis. Neuroimmunomodulation 12:220
70. Morelli AE, Thomson AW (2007) Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7:610
71. Palucka K, Ueno H, Fay J, Banchereau J (2009) Harnessing dendritic cells to generate cancer vaccines. Ann N Y Acad Sci 1174:88
72. Skarica M, Wang T, McCadden E, Kardian D, Calabresi PA, Small D, Whartenby KA (2009) Signal transduction inhibition of APCs diminishes th17 and Th1 responses in experimental autoimmune encephalomyelitis. J Immunol 182:4192
73. Blanchfield JL, Mannie MD (2010) A GMCSF-neuroantigen fusion protein is a potent tolerogen in experimental autoimmune encephalomyelitis (EAE) that is associated with efficient targeting of neuroantigen to APC. J. Leukoc. Biol. 87:509-521
74. Laouar Y, Town T, Jeng D, Tran E, Wan Y, Kuchroo VK, Flavell RA (2008) TGF-beta signaling in dendritic cells is a prerequisite for the control of autoimmune encephalomyelitis. Proc Natl Acad Sci USA 105:10865
75. Hasserjian RP, Chen S, Perkins SL, de Leval L, Kinney MC, Barry TS, Said J, Lim MS, Finn WG, Medeiros LJ, Harris NL, O'Malley DP (2009) Immunomodulator agent-related lymphoproliferative disorders. Mod Pathol 22:1532
76. Kajiwara T, Tomita Y, Okano S, Iwai T, Yasunami Y, Yoshikai Y, Nomoto K, Yasui H, Tominaga R (2007) Effects of cyclosporin A on the activation of natural killer T cells induced by alpha-galactosylceramide. Transplantation 83:184
77. Penna G, Amuchastegui S, Giarratana N, Daniel KC, Vulcano M, Sozzani S, Adorini L (2007) 1, 25-Dihydroxyvitamin D3 selectively modulates tolerogenic properties in myeloid but not plasmacytoid dendritic cells. J Immunol 178:145
78. Steinbrink K, Wolfl M, Jonuleit H, Knop J, Enk AH (1997) Induction of tolerance by IL-10-treated dendritic cells. J Immunol 159:4772
79. Kuwana M, Kaburaki J, Wright TM, Kawakami Y, Ikeda Y (2001) Induction of antigen-specific human CD4 (+) T cell anergy by peripheral blood DC2 precursors. Eur J Immunol 31:2547
80. Fallarino F, Asselin-Paturel C, Vacca C, Bianchi R, Gizzi S, Fioretti MC, Trinchieri G, Grohmann U, Puccetti P (2004) Murine plasmacytoid dendritic cells initiate the immunosuppressive pathway of tryptophan catabolism in response to CD200 receptor engagement. J Immunol 173:3748
81. Gilliet M, Liu YJ (2002) Human plasmacytoid-derived dendritic cells and the induction of T-regulatory cells. Hum Immunol 63:1149
82. Gilliet M, Liu YJ (2002) Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J Exp Med 195:695
83. Moseman EA, Liang X, Dawson AJ, Panoskaltsis-Mortari A, Krieg AM, Liu YJ, Blazar BR, Chen W (2004) Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4+CD25+ regulatory T cells. J Immunol 173:4433
84. Kadowaki N (2007) Dendritic cells-a conductor of T cell differentiation. Allergol Int 56:193
85. Ito T, Yang M, Wang YH, Lande R, Gregorio J, Perng OA, Qin XF, Liu YJ, Gilliet M (2007) Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 204:105
86. Kawamura K, Kadowaki N, Kitawaki T, Uchiyama T (2006) Virus-stimulated plasmacytoid dendritic cells induce CD4+ cytotoxic regulatory T cells. Blood 107:1031
87. Miller SD, McMahon EJ, Schreiner B, Bailey SL (2007) Antigen presentation in the CNS by myeloid dendritic cells drives progression of relapsing experimental autoimmune encephalomyelitis. Ann N Y Acad Sci 1103:179
88. Schnurr M, Toy T, Shin A, Wagner M, Cebon J, Maraskovsky E (2005) Extracellular nucleotide signaling by P2 receptors inhibits IL-12 and enhances IL-23 expression in human dendritic cells: a novel role for the cAMP pathway. Blood 105:1582