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Neuroscience and Behavioral Physiology

, Volume 48, Issue 6, pp 668–675 | Cite as

Dendritic Cells in Multiple Sclerosis

  • M. V. Mel’nikov
  • M. V. Pashchenkov
  • A. N. Boiko
Article
  • 17 Downloads

This review presents data on the main functions of dendritic cells (DC) and their structure and stages of development. The role of DC in maintaining immunological tolerance is discussed, as it their role in the development of autoimmune diseases. The involvement of DC in the immunopathogenesis of multiple sclerosis (MS) is considered, along with their therapeutic potential in these cases.

Keywords

dendritic cells multiple sclerosis 

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References

  1. 1.
    J. Furuzawa-Carballeda, M. I. Vargas-Rojas, and A. R. Cabral, “Autoimmune inflammation from the Th17 perspective,” Autoimmun. Rev., 6, No. 3, 169–175 (2007).PubMedCrossRefGoogle Scholar
  2. 2.
    S. Simpson, Jr., N. Stewart, I. van der Mei, et al., “Stimulated PBMC-produced IFN-γ and TNF-α are associated with altered relapse risk in multiple sclerosis: results from a prospective cohort study,” J. Neurol. Neurosurg. Psychiatry, 86, No. 2, 200–207 (2015).PubMedCrossRefGoogle Scholar
  3. 3.
    R. Dobson, S. Ramagopalan, A. Davis, and G. Giovannoni, “Cerebrospinal fluid oligoclonal bands in multiple sclerosis and clinically isolated syndromes: a meta-analysis of prevalence, prognosis and effect of latitude,” J. Neurol. Neurosurg. Psychiatry, 84, 909–914 (2013).PubMedCrossRefGoogle Scholar
  4. 4.
    S. L. Hauser, “The Charcot Lecture: beating MS: a story of B cells, with twists and turns,” Mult. Scler., 21, No. 1, 8–21 (2015).PubMedCrossRefGoogle Scholar
  5. 5.
    A. I. Martynov, B. V. Pinegin, and M. V. Pashchenkov, Innate Immunity as a System for Protecting the Human Body from the Effects of Anthropogenic Factors, Moscow (2014).Google Scholar
  6. 6.
    B. N. Dittel, I. Visintin, R. M. Merchant, and C. A. Janeway, “Presentation of the self antigen myelin basic protein by dendritic cells leads to experimental autoimmune encephalomyelitis,” J. Immunol., 163, No. 1, 32–39 (1999).PubMedGoogle Scholar
  7. 7.
    S. Henri, D. Vremec, A. Kamath, et al., “The dendritic cell populations of mouse lymph nodes,” J. Immunol., 167, No. 2, 741–748 (2001).PubMedCrossRefGoogle Scholar
  8. 8.
    R. Kushwah and J. Hu, “Complexity of dendritic cell subsets and their function in the host immune system,” Immunology, 133, No. 4, 409–419 (2011), doi:  https://doi.org/10.1111/j.1365-2567.2011.03457.x.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    S. Yona and S. Jung, “Monocytes: subsets, origins, fates and functions,” Curr. Opin. Hematol., 17, No. 1, 53–59 (2010), doi:  https://doi.org/10.1097/MOH.0b013e3283324f80.PubMedCrossRefGoogle Scholar
  10. 10.
    S. Yona and S. Jung, “Monocytes: subsets, origins, fates and functions,” Curr. Opin. Hematol., 17, No. 1, 53–59 (2010), doi:  https://doi.org/10.1097/MOH.0b013e3283324f80.PubMedCrossRefGoogle Scholar
  11. 11.
    C. Ardavin, L. Wu, C. L. Li, and K. Shortman, “Thymic dendritic cells and T cells develop simultaneously in the thymus from a common precursor population,” Nature, 362, No. 6422, 761–763 (1993).PubMedCrossRefGoogle Scholar
  12. 12.
    N. Kohrgruber, N. Halanek, M. Groger, et al., “Survival, maturation, and function of CD11c- and CD11c+ peripheral blood dendritic cells are differentially regulated by cytokines,” J. Immunol., 163, No. 6, 3250–3259 (1999).PubMedGoogle Scholar
  13. 13.
    F. P. Siegal, N. Kadowaki, M. Shodell, et al., “The nature of the principal type 1 interferonproducing cells in human blood,” Science, 284, No. 5421, 1835–1837 (1999).PubMedCrossRefGoogle Scholar
  14. 14.
    M. Cella, F. Facchetti, A. Lanzavecchia, and M. Colonna, “Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization,” Nat. Immunol., 1, No. 4, 305–310 (2000).PubMedCrossRefGoogle Scholar
  15. 15.
    G. Grouard, M. C. Rissoan, L. Filgueira, et al., “The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand,” J. Exp. Med., 185, No. 6, 1101–1111 (1997).PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    A. Krug, A. Towarowski, S. Britsch, 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, No. 10, 3026–3037 (2001).PubMedCrossRefGoogle Scholar
  17. 17.
    M. V. Pashchenkov and B. V. Pinegin, “The basic properties of dendritic cells,” Immunologiya, 30, 7–16 (2001).Google Scholar
  18. 18.
    H. Jonuleit, E. Schmitt, G. Schuler, et al., “Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells,” J. Exp. Med., 192, No. 9, 1213–1222 (2000).PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    F. Sallusto, P. Schaerli, P. Loetscher, et al., “Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation,” Eur. J. Immunol., 28, No. 9, 2760–2769 (1998).PubMedCrossRefGoogle Scholar
  20. 20.
    J. Banchereau, F. Briere, C. Caux, et al., “Immunobiology of dendritic cells,” Annu. Rev. Immunol., 18, 767–811 (2000).PubMedCrossRefGoogle Scholar
  21. 21.
    A. Langenkamp, M. Messi, A. Lanzavecchia, and F. Sallusto, “Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells,” Nat. Immunol., 1, No. 4, 311–316 (2000).PubMedCrossRefGoogle Scholar
  22. 22.
    H. Tanaka, C. E. Demeure, M. Rubio, et al., “Human monocyte-derived dendritic cells induce naive T cell differentiation into T helper cell type 2 (Th2) or Th1/Th2 effectors. Role of stimulator/responder ratio,” J. Exp. Med., 192, No. 3, 405–412 (2000).PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    V. Lombardi, L. Van Overtvelt, S. Horiot, and P. Moingeon, “Human dendritic cells stimulated via TLR7 and/or TLR8 induce the sequential production of Il-10, IFN-gamma, and IL-17A by naive CD4+ T cells,” J. Immunol., 182, No. 6, 3372–3379 (2009).PubMedCrossRefGoogle Scholar
  24. 24.
    E. A. Moseman, X. Liang, A. J. Dawson, et al., “Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4+CD25+ regulatory T cells,” J. Immunol., 173, No. 7, 4433–4442 (2004).PubMedCrossRefGoogle Scholar
  25. 25.
    A. J. Beelen, Z. Zelinkova, E. W. Taanman-Kueter, et al., “Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells,” Immunity, 27, No. 4, 660–669 (2007).PubMedCrossRefGoogle Scholar
  26. 26.
    F. Aloisi, F. Ria, S. Columba-Cabezas, et al., “Relative efficiency of microglia, astrocytes, dendritic cells and B cells in naive CD4+ T cell priming and Th1/Th2 cell restimulation,” Eur. J. Immunol., 29, No. 9, 2705–2714 (1999).PubMedCrossRefGoogle Scholar
  27. 27.
    R. M. Steinman and M. C. Nussenzweig, “Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance,” Proc. Natl. Acad. Sci. USA, 99, No. 1, 351–358 (2002).PubMedCrossRefGoogle Scholar
  28. 28.
    N. Watanabe, Y. H. Wang, H. K. Lee, et al., “Hassall’s corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory T cells in human thymus,” Nature, 436, No. 7054, 1181–1185 (2005).PubMedCrossRefGoogle Scholar
  29. 29.
    F. Lussi, F. Zipp, and E. Witsch, “Dendritic cells as therapeutic targets in neuroinflammation,” Cell. Mol. Life Sci., 73, No. 13, 2425–2450 (2016).CrossRefGoogle Scholar
  30. 30.
    L. S. Walker and A. K. Abbas, “The enemy within: keeping self-reactive T cells at bay in the periphery,” Nat. Rev. Immunol., 2, No. 1, 11–19 (2002).PubMedCrossRefGoogle Scholar
  31. 31.
    M. L. Albert, S. F. Pearce, L. M. Francisco, et al., “Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes,” J. Exp. Med., 188, No. 7, 1359–1368 (1998).PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    M. Nouri-Shirazi, J. Banchereau, D. Bell, et al., “Dendritic cells capture killed tumor cells and present their antigens to elicit tumor-specific immune responses,” J. Immunol., 165, No. 7, 3797–3803 (2000).PubMedCrossRefGoogle Scholar
  33. 33.
    L. Bonifaz, D. Bonnyay, K. Mahnke, et al., “Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance,” J. Exp. Med., 196, No. 12, 1627–1638 (2002).PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    K. Inaba, S. Turley, F. Yamaide, et al., “Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells,” J. Exp. Med., 188, No. 11, 2163–2173 (1998).PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    A. Awasthi, Y. Carrier, J. P. Peron, et al., “A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells,” Nat. Immunol., 8, No. 12, 1380–1389 (2007).PubMedCrossRefGoogle Scholar
  36. 36.
    H. C. Probst, K. McCoy, T. Okazaki, et al., “Resting dendritic cells induce peripheral CD8+ T cell tolerance through PD-1 and CTLA 4,” Nat. Immunol., 6, No. 3, 280–286 (2005).PubMedCrossRefGoogle Scholar
  37. 37.
    D. Hawiger, R. F. Masilamani, E. Bettelli, et al., “Immunological unresponsiveness characterized by increased expression of CD5 on peripheral T cells induced by dendritic cells in vivo,” Immunity, 20, No. 6, 695–705 (2004).PubMedCrossRefGoogle Scholar
  38. 38.
    C. Ohnmacht, A. Pullner, S. B. King, et al., “Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity,” J. Exp. Med., 206, No. 3, 549–559 (2009), doi:  https://doi.org/10.1084/jem.20082394.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    N. Yogev, F. Frommer, D. Lukas, et al., “Dendritic cells ameliorate autoimmunity in the CNS by controlling the homeostasis of PD-1 receptor(+) regulatory T cells,” Immunity, 37, No. 2, 264–275 (2012).PubMedCrossRefGoogle Scholar
  40. 40.
    B. Ludewig, T. Junt, H. Hengartner, and R. M. Zinkernagel, “Dendritic cells in autoimmune diseases,” Curr. Opin. Immunol., 13, No. 6, 657–662 (2001).PubMedCrossRefGoogle Scholar
  41. 41.
    H. Drakesmith, B. Chain, and P. Beverley, “How can dendritic cells cause autoimmune disease?” Immunol. Today, 21, No. 5, 214–212 (2000).PubMedCrossRefGoogle Scholar
  42. 42.
    H. Watanabe, M. Inaba, Y. Adachi, et al., “Experimental autoimmune thyroiditis induced by thyroglobulin-pulsed dendritic cells,” Autoimmunity, 31, No. 4, 273–282 (1999).PubMedCrossRefGoogle Scholar
  43. 43.
    P. J. Kabel, H. A. Voorbij, M. De Haan, et al., “Intrathyroidal dendritic cells,” J. Clin. Endocrinol. Metab., 66, No. 1, 199–207 (1988).PubMedCrossRefGoogle Scholar
  44. 44.
    F. O. Nestle, L. A. Turka, and B. J. Nickoloff, “Characterization of dermal dendritic cells in psoriasis. Autostimulation of T lymphocytes and induction of Th1 type cytokines,” J. Clin. Invest., 94, No. 1, 202–209 (1994).PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    C. A. Seldenrijk, H. A. Drexhage, S. G. Meuwissen, et al., “Dendritic cells and scavenger macrophages in chronic inflammatory bowel disease,” Gut, 30, No. 4, 484–491 (1989).PubMedCrossRefGoogle Scholar
  46. 46.
    R. Thomas, L. S. Davis, and P. E. Lipsky, “Rheumatoid synovium is enriched in mature antigen-presenting dendritic cells,” J. Immunol., 152, No. 5, 2613–2623 (1994).PubMedGoogle Scholar
  47. 47.
    F. M. Moret, C. E. Hack, K. M. van der Wurff-Jacobs, et al., “Intra-articular CD1c-expressing myeloid dendritic cells from rheumatoid arthritis patients express a unique set of T cell-attracting chemokines and spontaneously induce Th1, Th17 and Th2 cell activity,” Arthritis Res. Ther., 15, No. 5, 155 (2013).CrossRefGoogle Scholar
  48. 48.
    D. Saadeh, M. Kurban, and O. Abbas, “Update on the role of plasmacytoid dendritic cells in inflammatory/autoimmune skin diseases,” Exp. Dermatol., 25, No. 6, 415–421 (2016).PubMedCrossRefGoogle Scholar
  49. 49.
    I. Bechmann, I. Galea, and V. H. Perry, “What is the blood-brain barrier (not)?” Trends Immunol., 28, No. 1, 5–11 (2007).PubMedCrossRefGoogle Scholar
  50. 50.
    I. Galea, I. Bechmann, and V. H. Perry, “What is immune privilege (not)?” Trends Immunol., 28, No. 1, 12–18 (2007).PubMedCrossRefGoogle Scholar
  51. 51.
    M. K. Matyszak, and V. H. Perry, “The potential role of dendritic cells in immune-mediated inflammatory diseases in the central nervous system,” Neuroscience, 74, No. 2, 599–608 (1996).PubMedCrossRefGoogle Scholar
  52. 52.
    A. Hanly and C. K. Petito, “HLA-DR-positive dendritic cells of the normal human choroid plexus: a potential reservoir of HIV in the central nervous system,” Hum. Pathol., 29, No. 1, 88–93 (1998).PubMedCrossRefGoogle Scholar
  53. 53.
    P. G. McMenamin, “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, No. 4, 553–562 (1999).PubMedCrossRefGoogle Scholar
  54. 54.
    J. M. Serot, M. C. Bene, B. Foliguet, and G. C. Faure, “Monocyte-derived IL-10-secreting dendritic cells in choroid plexus epithelium,” J. Neuroimmunol., 105, No. 2, 115–119 (2000).PubMedCrossRefGoogle Scholar
  55. 55.
    P. G. McMenamin, R. J. Wealthall, M. Deverall, et al., “Macrophages and dendritic cells in the rat meninges and choroid plexus: three-dimensional localisation by environmental scanning electron microscopy and confocal microscopy,” Cell Tissue Res., 313, No. 3, 259–269 (2003).PubMedCrossRefGoogle Scholar
  56. 56.
    C. Prodinger, J. Bunse, M. Kruger, et al., “CD11c-expressing cells reside in the juxtavascular parenchyma and extend processes into the glia limitans of the mouse nervous system,” Acta Neuropathol., 121, No. 4, 445–458 (2011).PubMedCrossRefGoogle Scholar
  57. 57.
    M. Pashenkov, Y. M. Huang, V. Kostulas, et al., “Two subsets of dendritic cells are present in human cerebrospinal fluid,” Brain, 124, No. 3, 480–492 (2001).PubMedCrossRefGoogle Scholar
  58. 58.
    A. Louveau, I. Smirnov, T. J. Keyes, et al., “Structural and functional features of central nervous system lymphatic vessels,” Nature, 523, No. 7560, 337–341 (2015).PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    M. W. Bradbury, H. F. Cserr, and R. J. Westrop, “Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit,” Am. J. Physiol., 240, No. 4, 329–336 (1981).Google Scholar
  60. 60.
    C. J. Harling-Berg, T. J. Park, and P. M. Knopf, “Role of the cervical lymphatics in the Th2-type hierarchy of CNS immune regulation,” J. Neuroimmunol., 101, No. 2, 111–127 (1999).PubMedCrossRefGoogle Scholar
  61. 61.
    B. M. Segal, “Th17 cells in autoimmune demyelinating disease,” Semin. Immunopathol., 32, No. 1, 71–77 (2010).PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    C. L. Langrish, Y. Chen, W. M. Blumenschein, et al., “IL-23 drives a pathogenic T cell population that induces autoimmune inflammation,” J. Exp. Med., 201, No. 2, 233–240 (2005).PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    C. E. Sutton, S. J. Lalor, C. M. Sweeney, et al., “Interleukin-1 and IL-23 induce innate IL-17 production from gamma/delta T cells, amplifying Th17 responses and autoimmunity,” Immunity, 31, No. 2, 331–341 (2009).PubMedCrossRefGoogle Scholar
  64. 64.
    M. El-Behi, B. Ciric, H. Dai, et al., “The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF,” Nat. Immunol., 12, No. 6, 568–575 (2011), doi:  https://doi.org/10.1038/ni.2031.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    S. Aggarwal, N. Ghilardi, M. H. Xie, et al., “Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17,” J. Biol. Chem., 278, No. 3, 1910–1914 (2003).PubMedCrossRefGoogle Scholar
  66. 66.
    D. J. Cua, J. Sherlock, Y. Chen, et al., “Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain,” Nature, 421, No. 6924, 744–748 (2003).PubMedCrossRefGoogle Scholar
  67. 67.
    P. Thakker, M. W. Leach, W. Kuang, et al., “IL-23 is critical in the induction but not in the effector phase of experimental autoimmune encephalomyelitis,” J. Immunol., 178, No. 4, 2589–2598 (2007).PubMedCrossRefGoogle Scholar
  68. 68.
    B. Gran, G. X. Zhang, and A. Rostami, “Role of the IL-12/IL-23 system in the regulation of T-cell responses in central nervous system inflammatory demyelination,” Crit. Rev. Immunol., 24, No. 2, 111–128 (2004).PubMedCrossRefGoogle Scholar
  69. 69.
    Y. Li, N. Chu, A. Hu, et al., “Increased IL-23p19 expression in multiple sclerosis lesions and its induction in microglia,” Brain, 130, No. 2, 490–501 (2007).PubMedCrossRefGoogle Scholar
  70. 70.
    A. Vaknin-Dembinsky, K. Balashov, and H. L. Weiner, “IL-23 is increased in dendritic cells in multiple sclerosis and down-regulation of IL-23 by antisense oligos increases dendritic cell IL-10 production,” J. Immunol., 176, No. 12, 7768–7774 (2006); Erratum in: J. Immunol., 177, No. 3, 2025 (2006).Google Scholar
  71. 71.
    L. Codarri, G. Gyulveszi, V. Tosevski, et al., “RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation,” Nat. Immunol., 12, No. 6, 560–567 (2011), doi:  https://doi.org/10.1038/ni.2027.PubMedCrossRefGoogle Scholar
  72. 72.
    S. Markowicz and E. G. Engleman, “Granulocyte-macrophage colony-stimulating factor promotes differentiation and survival of human peripheralblood dendritic cells in vitro,” J. Clin. Invest., 85, No. 3, 955–961 (1990).PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    E. D. Ponomarev, L. P. Shriver, K. Maresz, et al., “GM-CSF production by autoreactive T cells is required for the activation of microglial cells and the onset of experimental autoimmune encephalomyelitis,” J. Immunol., 178, No. 1, 39–48 (2007).PubMedCrossRefGoogle Scholar
  74. 74.
    S. S. Diebold, “Determination of T-cell fate by dendritic cells,” Immunol. Cell Biol., 86, No. 5, 389–397 (2008).PubMedCrossRefGoogle Scholar
  75. 75.
    S. L. Bailey, B. Schreiner, E. J. McMahon, and S. D. Miller, “CNS myeloid DCs presenting endogenous myelin peptides ‘preferentially’ polarize CD4+ T(H)-17 cells in relapsing EAE,” Nat. Immunol., 8, No. 2, 172–180 (2007).PubMedCrossRefGoogle Scholar
  76. 76.
    S. D. Miller, E. J. McMahon, B. Schreiner, and S. L. Bailey, “Antigen presentation in the CNS by myeloid dendritic cells drives progression of relapsing experimental autoimmune encephalomyelitis,” Ann. N. Y. Acad. Sci., 1103, 179–191 (2007).PubMedCrossRefGoogle Scholar
  77. 77.
    S. L. Bailey-Bucktrout, S. C. Caulkins, G. Goings, et al., “Cutting edge: central nervous system plasmacytoid dendritic cells regulate the severity of relapsing experimental autoimmune encephalomyelitis,” J. Immunol., 180, No. 10, 6457–6461 (2008).PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    S. Hirata, H. Matsuyoshi, D. Fukuma, et al., “Involvement of regulatory T cells in the experimental autoimmune encephalomyelitis-preventive effect of dendritic cells expressing myelin oligodendrocyte glycoprotein plus TRAIL,” J. Immunol., 178, No. 2, 918–925 (2007).PubMedCrossRefGoogle Scholar
  79. 79.
    M. J. McGeachy, L. A. Stephens, and S. M. Anderton, “Natural recovery and protection from autoimmune encephalomyelitis: contribution of CD4+CD25+ regulatory cells within the central nervous system,” J. Immunol., 175, No. 5, 3025–3032 (2005).PubMedCrossRefGoogle Scholar
  80. 80.
    M. Greter, F. L. Heppner, M. P. Lemos, et al., “Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis,” Nat. Med., 11, No. 3, 328–334 (2005).PubMedCrossRefGoogle Scholar
  81. 81.
    M. Ioannou, T. Alissafi , L. Boon, et al., “In vivo ablation of plasmacytoid dendritic cells inhibits autoimmunity through expansion of myeloid-derived suppressor cells,” J. Immunol., 190, No. 6, 2631–2640 (2013), doi:  https://doi.org/10.4049/jimmunol.1201897.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    B. Serafini, B. Rosicarelli, R. Magliozzi, et al., “Dendritic cells in multiple sclerosis lesions: maturation stage, myelin uptake, and interaction with proliferating T cells,” J. Neuropathol. Exp. Neurol., 65, No. 2, 124–141 (2006).PubMedCrossRefGoogle Scholar
  83. 83.
    A. L. Longhini, F. von Glehn, C. O. Brandao, et al., “Plasmacytoid dendritic cells are increased in cerebrospinal fluid of untreated patients during multiple sclerosis relapse,” J. Neuroinflammation, 8, No. 1, 2 (2011).PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    A. Karni, M. Abraham, A. Monsonego, et al., “Innate immunity in multiple sclerosis: myeloid dendritic cells in secondary progressive multiple sclerosis are activated and drive a proinflammatory immune response,” J. Immunol., 177, No. 6, 4196–4202 (2006).PubMedCrossRefGoogle Scholar
  85. 85.
    C. Lopez, M. Comabella, H. Al-zayat, et al., “Altered maturation of circulating dendritic cells in primary progressive MS patients,” J. Neuroimmunol., 175, No. 1–2, 183–191 (2006).PubMedCrossRefGoogle Scholar
  86. 86.
    M. Stasiolek, A. Bayas, N. Kruse, et al., “Impaired maturation and altered regulatory function of plasmacytoid dendritic cells in multiple sclerosis,” Brain, 129,. No. 5, 1293–1305 (2006).PubMedCrossRefGoogle Scholar
  87. 87.
    N. Schwab, A. L. Zozulya, B. C. Kieseier, et al., “An imbalance of two functionally and phenotypically different subsets of plasmacytoid dendritic cellscharacterizes the dysfunctional immune regulation in multiple sclerosis,” J. Immunol., 184, No. 9, 5368–5374 (2010).PubMedCrossRefGoogle Scholar
  88. 88.
    A. Vaknin-Dembinsky, G. Murugaiyan, D. A. Hafler, et al., “Increased IL-23 secretion and altered chemokine production by dendritic cells upon CD46 activation in patients with multiple sclerosis,” J. Neuroimmunol., 195, No. 1–2, 140–145 (2008).PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    H. Link, Y. M. Huang, T. Masterman, and B. G. Xiao, “Vaccination with autologous dendritic cells: from experimental autoimmune encephalomyelitis to multiple sclerosis,” J. Neuroimmunol., 114, No. 1–2, 1–7 (2001).PubMedCrossRefGoogle Scholar
  90. 90.
    K. Mahnke, Y. Qian, J. Knop, and A. H. Enk, “Dendritic cells, engineered to secrete a T-cell receptor mimic peptide, induce antigen-specific immunosuppression in vivo,” Nat. Biotechnol., 21, No. 8, 903–908 (2003).PubMedCrossRefGoogle Scholar
  91. 91.
    B. G. Xiao, X. C. Wu, J. S. Yang, et al., “Therapeutic potential of IFN-gamma-modified dendritic cells in acute and chronic experimental allergic encephalomyelitis,” Int. Immunol., 16, No. 1, 13–22 (2004).PubMedCrossRefGoogle Scholar
  92. 92.
    M. V. Pashchenkov, B. V. Pinegin, Kh. Link, and A. N. Boiko, “Dendritic cells and their role in inflammation in the central nervous system,” in: Multiple Sclerosis and Other Demyelinating Diseases, E. I. Gusev, I. A. Zavalishin, and A. N. Boiko (eds.), Miklosh, Moscow (2004).Google Scholar
  93. 93.
    T. Nagai, O. Devergne, G. A. van Seventer, and J. M. van Seventer, “Interferon-beta mediates opposing effects on interferon-gamma-dependent Interleukin 12 p70 secretion by human monocyte-derived dendritic cells,” Scand. J. Immunol., 65, No. 2, 107–117 (2007).PubMedCrossRefGoogle Scholar
  94. 94.
    X. Zhang, J. Jin, Y. Tang, et al., “IFNbeta1a inhibits the secretion of Th17 polarizing cytokines in human dendritic cells via TLR7 up-regulation,” J. Immunol., 182, No. 6, 3928–3936 (2009).PubMedCrossRefGoogle Scholar
  95. 95.
    B. Schreiner, M. Mitsdoerffer, B. C. Kieseier, et al., “Interferon-beta enhances monocyte and dendritic cell expression of B7-H1 (PD-L1), a strong inhibitor ofautologous T-cell activation: relevance for the immune modulatory effect in multiple sclerosis,” J. Neuroimmunol., 155, No. 1–2, 172–182 (2004).PubMedCrossRefGoogle Scholar
  96. 96.
    R. Lande, V. Gafa, B. Serafini, et al., “Plasmacytoid dendritic cells in multiple sclerosis: intracerebral recruitment and impaired maturation in response to interferon-beta,” J. Neuropathol. Exp. Neurol., 67, No. 5, 388–401 (2008).PubMedCrossRefGoogle Scholar
  97. 97.
    P. L. Vieira, H. C. Heystek, J. Wormmeester, et al., “Glatiramer acetate (copolymer-1, copaxone) promotes Th2 cell development and increased IL-10 production through modulation of dendritic cells,” J. Immunol., 170, No. 9, 4483–4488 (2003).PubMedCrossRefGoogle Scholar
  98. 98.
    S. Begum-Haque, M. Christy, Y. Wang, et al., “Glatiramer acetate biases dendritic cells towards an anti-inflammatory phenotype by modulating OPN, IL-17, and RORγt responses and by increasing IL-10 production in experimental allergic encephalomyelitis,” J. Neuroimmunol., 254, No. 1–2, 117–124 (2013).PubMedCrossRefGoogle Scholar
  99. 99.
    P. Ludewig, M. Gallizioli, X. Urra, et al., “Dendritic cells in brain diseases,” Biochim. Biophys. Acta, 1862, No. 3, 352–367 (2016).PubMedCrossRefGoogle Scholar
  100. 100.
    H. Müller, S. Hofer, N. Kaneider, et al., “The immuomodulator FTY720 interferes with effector functions of human monocyte-derived dendritic cells,” Eur. J. Immunol., 35, No. 2, 533–545 (2005).PubMedCrossRefGoogle Scholar
  101. 101.
    F. Luessi, S. Kraus, B. Trinschek, et al., “FTY720 (fingolimod) treatment tips the balance towards less immunogenic antigen-presenting cells in patients with multiple sclerosis,” Mult. Scler., 21, No. 14, 1811–1822 (2015).PubMedCrossRefGoogle Scholar
  102. 102.
    C. Andrés, R. Teijeiro, B. Alonso, et al., “Long-term decrease in VLA-4 expression and functional impairment of dendritic cells during natalizumabtherapy in patients with multiple sclerosis,” PLoS One, 7, No. 4, 34103 (2012), doi:  https://doi.org/10.1371/journal.pone.0034103.CrossRefGoogle Scholar
  103. 103.
    H. Peng, M. Guerau-de-Arellano, V. B. Mehta, et al., “Dimethyl fumarate inhibits dendritic cell maturation via nuclear factor ϰB(NF-ϰB) and extracellular signal-regulated kinase 1 and 2 (ERK1/2) and mitogen stress-activated kinase 1 (MSK1) signaling,” J. Biol. Chem., 287, No. 33, 28017–28026 (2012), doi:  https://doi.org/10.1074/jbc.M112.383380.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    K. Ghoreschi, J. Bruck, C. Kellerer, et al., “Fumarates improve psoriasis and multiple sclerosis by inducing type II dendritic cells,” J. Exp. Med., 208, No. 11, 2291–2303 (2011), doi:  https://doi.org/10.1084/jem.20100977.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    V. Jolivel, F. Luessi, J. Masri, et al., “Modulation of dendritic cell properties by laquinimod as a mechanism for modulating multiple sclerosis,” Brain, 136, No. 4, 1048–1066 (2013), doi:  https://doi.org/10.1093/brain/awt023.PubMedCrossRefGoogle Scholar
  106. 106.
    G. F. Xu, L. S. Zhang, L. J. Li, et al., “The immune effects of rituximab on dendritic cells derived from patients with primary immune-thrombocytopenia,” Zhonghua Xue Ye Xue Za Zhi, 33, No. 3, 207–210 (2012).PubMedGoogle Scholar
  107. 107.
    K. Mnasria, C. Lagaraine, F. Velge-Roussel, et al., “Anti-CD25 antibodies affect cytokine synthesis pattern of human dendritic cells and decrease their ability to prime allogeneic CD4+ T cells,” J. Leukoc. Biol., 84, No. 2, 460–467 (2008), doi:  https://doi.org/10.1189/jlb.1007712.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • M. V. Mel’nikov
    • 1
  • M. V. Pashchenkov
    • 2
  • A. N. Boiko
    • 1
    • 3
  1. 1.Department of Neurology, Neurosurgery, and Medical GeneticsPirogov Russian National Research Medical UniversityMoscowRussia
  2. 2.Clinical Immunology Laboratory, State Scientific Center Institute of ImmunologyRussian Federal Medical Biological AgencyMoscowRussia
  3. 3.Interregional Multiple Sclerosis Center at City Clinical Hospital No. 24MoscowRussia

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