Plasmacytoid dendritic cells and immunotherapy in multiple sclerosis

Immunotherapy

Volumn 4, Issue 10, 2012, Pages 1053-1061

  Von Glehn, Felipe ^a   Santos, Leonilda M ^a   Balashov, Konstantin E ^b  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

innate immunity; multiple sclerosis; plasmacytoid dendritic cells; Toll like receptors; type I interferon

Indexed keywords

BETA INTERFERON; CD137 ANTIGEN; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; RANTES; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

CD4+ T LYMPHOCYTE; CEREBROSPINAL FLUID; CYTOKINE PRODUCTION; GENE EXPRESSION; HUMAN; IMMUNOTHERAPY; MULTIPLE SCLEROSIS; OLIGODENDROGLIA; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

ANIMALS; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HUMANS; IMMUNOTHERAPY; MULTIPLE SCLEROSIS; PLASMA CELLS; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 9;

EID: 84869156109     PISSN: 1750743X     EISSN: 17507448     Source Type: Journal    
DOI: 10.2217/imt.12.117     Document Type: Review

References (104)

1. Lennert K, Remmele W. [Karyometric research on lymph node cells in man. I. Germinoblasts, lymphoblasts & lymphocytes]. Acta Haematol. 19(2), 99-113 (1958).
2. Facchetti F, de Wolf-Peeters C, Mason D, Pulford K, van den Oord J, Desmet V. Plasmacytoid T cells. Immunohistochemical evidence for their monocyte/macrophage origin. Am. J. Pathol. 133(1), 15-21 (1988).
3. Grouard G, Rissoan M, Filgueira L, Durand I, Banchereau J, Liu Y. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J. Exp. Med. 185(6), 1101-1111 (1997).
4. Siegal FP, Kadowaki N, Shodell M et al. The nature of the principal type 1 interferonproducing cells in human blood. Science 284(5421), 1835-1837 (1999).
5. Cella M, Jarrossay D, Facchetti F et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 5(8), 919-923 (1999).
6. Dzionek A, Fuchs A, Schmidt P et al BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J. Immunol. 165(11), 6037-6046 (2000).
7. Dzionek A, Sohma Y, Nagafune J et al. BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon alpha/beta induction. J. Exp. Med. 194(12), 1823-1834 (2001).
8. Asselin-Paturel C, Boonstra A, Dalod M et al. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2(12), 1144-1150 (2001).
9. 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. 194(8), 1171-1178 (2001).
10. Bjorck P. Isolation and characterization of plasmacytoid dendritic cells from Flt3 ligand and granulocyte-macrophage colonystimulating factor-treated mice. Blood 98(13), 3520-3526 (2001).
11. Blom B, Ho S, Antonenko S, Liu YJ. Generation of interferon alpha-producing predendritic cell (pre-DC)2 from human CD34(+) hematopoietic stem cells. J. Exp. Med. 192(12), 1785-1796 (2000).
12. Gilliet M, Boonstra A, Paturel C et al. The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/ macrophage colony-stimulating factor. J. Exp. Med. 195(7), 953-958 (2002).
13. Soumelis V, Liu YJ. From plasmacytoid to dendritic cell: Morphological and functional switches during plasmacytoid pre-dendritic cell differentiation. Eur. J. Immunol. 36(9), 2286-2292 (2006).
14. Olweus J, Bitmansour A, Warnke R et al. Dendritic cell ontogeny: A human dendritic cell lineage of myeloid origin. Proc. Natl Acad. Sci. USA 94(23), 12551-12556 (1997).
15. Segura E, Valladeau-Guilemond J, Donnadieu MH et al. Characterization of resident and migratory dendritic cells in human lymph nodes. J. Exp. Med. 209, 653-660 (2012).
16. Naik SH, Sathe P, Park HY et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8(11), 1217-1226 (2007).
17. Onai N, Obata-Onai A, Schmid MA, Ohteki T, Jarrossay D, Manz M. Identification of clonogenic common Flt3+M-CSFR+plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8(11), 1207-1216 (2007).
18. Schmid M, Kingston D, Boddupalli S, Manz M. Instructive cytokine signals in dendritic cell lineage commitment. Immunol. Rev. 234(1), 32-44 (2010).
19. Cisse B, Caton M, Lehner M et al. Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 135(1), 37-48 (2008).
20. Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V. Plasmacytoid dendritic cells: Recent progress and open questions. Annu. Rev. Immunol. 29, 163-183 (2011).
21. Shigematsu H, Reizis B, Iwasaki H et al. Plasmacytoid dendritic cells activate lymphoid-specific genetic programs irrespective of their cellular origin. Immunity 21(1), 43-53 (2004).
22. Rissoan MC, Duhen T, Bridon JM et al. Subtractive hybridization reveals the expression of immunoglobulin-like transcript 7, Eph-B1, granzyme B, and 3 novel transcripts in human plasmacytoid dendritic cells. Blood 100(9), 3295-3303 (2002).
23. Cao W, Rosen DB, Ito T et al. Plasmacytoid dendritic cell-specific receptor ILT-7-Fc epsilonRI gamma inhibits Toll-like receptor-induced interferon production. J. Exp. Med. 203(6), 1399-1405 (2006).
24. Swiecki M, Colonna M. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol. Rev. 234(1), 142-162 (2010).
25. Liu YJ. IPC: professional type 1 interferonproducing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23, 275-306 (2005).
26. Kawai T, Sato S, Ishii KJ et al. Interferonalpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 5(10), 1061-1068 (2004).
27. O'Keeffe M, Grumont RJ, Hochrein H et al. Distinct roles for the NF-kappaB1 and c-Rel transcription factors in the differentiation and survival of plasmacytoid and conventional dendritic cells activated by TLR-9 signals. Blood 106(10), 3457-3464 (2005).
28. Lande R, Gregorio J, Facchinetti V et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449(7162), 564-569 (2007).
29. Lund JM, Alexopoulou L, Sato A et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl Acad. Sci. USA 101(15), 5598-5603 (2004).
30. Heil F, Hemmi H, Hochrein H et al. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 303(5663), 1526-1529 (2004).
31. Haas T, Metzger J, Schmitz F et al. The DNA sugar backbone 2 deoxyribose determines Toll-like receptor 9 activation. Immunity 28(3), 315-323 (2008).
32. 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. 198(3), 513-520 (2003).
33. Barchet W, Cella M, Odermatt B, Asselin-Paturel C, Colonna M, Kalinke U. Virus-induced interferon alpha production by a dendritic cell subset in the absence of feedback signaling in vivo. J. Exp. Med. 195(4), 507-516 (2002).
34. Kerkmann M, Rothenfusser S, Hornung V et al. Activation with CpG-A and CpG-B oligonucleotides reveals two distinct regulatory pathways of type I IFN synthesis in human plasmacytoid dendritic cells. J. Immunol. 170(9), 4465-4474 (2003).
35. Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: Sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 8(8), 594-606 (2008).
36. Fuchs A, Cella M, Kondo T, Colonna M. Paradoxic inhibition of human natural interferon-producing cells by the activating receptor NKp44. Blood 106(6), 2076-2082 (2005).
37. Penna G, Vulcano M, Roncari A, Facchetti F, Sozzani S, Adorini L. Cutting edge: differential chemokine production by myeloid and plasmacytoid dendritic cells. J. Immunol. 169(12), 6673-6676 (2002).
38. Sozzani S, Allavena P, D'Amico G et al. Differential regulation of chemokine receptors during dendritic cell maturation: A model for their trafficking properties. J. Immunol. 161, 1083-1086 (1998).
39. Jahnsen FL, Farkas L, Lund-Johansen F, Brandtzaeg P. Involvement of plasmacytoid dendritic cells in human diseases. Hum. Immunol. 63(12), 1201-1205 (2002).
40. Zabel BA, Silverio AM, Butcher EC. Chemokine-like receptor 1 expression and chemerin-directed chemotaxis distinguish plasmacytoid from myeloid dendritic cells in human blood. J. Immunol. 174(1), 244-251 (2005).
41. Schnurr M, Toy T, Shin A et al. Role of adenosine receptors in regulating chemotaxis and cytokine production of plasmacytoid dendritic cells. Blood 103(4), 1391-1397 (2004).
42. Gutzmer R, Kother B, Zwirner J et al. Human plasmacytoid dendritic cells express receptors for anaphylatoxins C3a and C5a and are chemoattracted to C3a and C5a. J. Invest. Dermatol. 126(11), 2422-2429 (2006).
43. Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J. Exp. Med. 189(3), 521-530 (1999).
44. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202(5), 637-650 (2005).
45. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3(2), 133-146 (2003).
46. Mescher MF, Curtsinger JM, Agarwal P et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol. Rev. 211, 81-92 (2006).
47. Biron CA. Interferons alpha and beta as immune regulators - a new look. Immunity 14(6), 661-664 (2001).
48. Rissoan MC, Soumelis V, Kadowaki N et al. Reciprocal control of T helper cell and dendritic cell differentiation. Science 283(5405), 1183-1186 (1999).
49. 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 19(2), 225-234 (2003).
50. Poeck H, Wagner M, Battiany J et al. Plasmacytoid dendritic cells, antigen, and CpG-C license human B cells for plasma cell differentiation and immunoglobulin production in the absence of T-cell help. Blood 103(8), 3058-3064 (2004).
51. Shaw J, Wang YH, Ito T, Arima K, Liu YJ. Plasmacytoid dendritic cells regulate B-cell growth and differentiation via CD70. Blood 115(15), 3051-3057 (2010).
52. Douagi I, Gujer C, Sundling C et al. Human B cell responses to TLR ligands are differentially modulated by myeloid and plasmacytoid dendritic cells. J. Immunol. 182(4), 1991-2001 (2009).
53. Villadangos JA, Young L. Antigenpresentation properties of plasmacytoid dendritic cells. Immunity 29(3), 352-361 (2008).
54. Munn DH, Sharma MD, Mellor AL. Ligation of B7-1/B7-2 by human CD4+ T cells triggers indoleamine 2,3-dioxygenase activity in dendritic cells. J. Immunol. 172(7), 4100-4110 (2004).
55. Thomas SR, Stocker R. Antioxidant activities and redox regulation of interferon-gammainduced tryptophan metabolism in human monocytes and macrophages. Adv. Exp. Med. Biol. 467, 541-552 (1999).
56. Taylor MW, Feng GS. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 5(11), 2516-2522 (1991).
57. Kwidzinski E, Bechmann I. IDO expression in the brain: A double-edged sword. J. Mol. Med. (Berl.) 85(12), 1351-1359 (2007).
58. Manlapat AK, Kahler DJ, Chandler PR, Munn DH, Mellor AL. Cell-autonomous control of interferon type I expression by indoleamine 2,3-dioxygenase in regulatory CD19+ dendritic cells. Eur. J. Immunol. 37(4), 1064-1071 (2007).
59. Hill M, Tanguy-Royer S, Royer P et al. IDO expands human CD4+CD25high regulatory T cells by promoting maturation of LPS-treated dendritic cells. Eur. J. Immunol. 37(11), 3054-3062 (2007).
60. Ito T, Hanabuchi S, Wang YH et al. Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 28(6), 870-880 (2008).
61. Ito T, Yang M, Wang YH et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J. Exp. Med. 204(1), 105-115 (2007).
62. Ronnblom L, Alm GV. A pivotal role for the natural interferon alpha-producing cells (plasmacytoid dendritic cells) in the pathogenesis of lupus. J. Exp. Med. 194(12), F59-F63 (2001).
63. Nestle FO, Conrad C, Tun-Kyi A et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J. Exp. Med. 202(1), 135-143 (2005).
64. Ganguly D, Chamilos G, Lande R et al. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J. Exp. Med. 206(9), 1983-1994 (2009).
65. Bave U, Magnusson M, Eloranta ML, Perers A, Alm GV, Ronnblom L. Fc gamma RIIa is expressed on natural IFN-alpha-producing cells (plasmacytoid dendritic cells) and is required for the IFN-alpha production induced by apoptotic cells combined with lupus IgG. J. Immunol. 171(6), 3296-3302 (2003).
66. Barrat FJ, Meeker T, Gregorio J et al. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 202(8), 1131-1139 (2005).
67. Baechler EC, Batliwalla FM, Karypis G et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl Acad. Sci. USA 100(5), 2610-2615 (2003).
68. Cavanagh LL, Boyce A, Smith L et al. Rheumatoid arthritis synovium contains plasmacytoid dendritic cells. Arthritis Res. Ther. 7(2), R230-R240 (2005).
69. Takakubo Y, Takagi M, Maeda K et al. Distribution of myeloid dendritic cells and plasmacytoid dendritic cells in the synovial tissues of rheumatoid arthritis. J. Rheumatol. 35(10), 1919-1931 (2008).
70. Cao W, Bover L, Cho M et al. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT-7 receptor interaction. J. Exp. Med. 206(7), 1603-1614 (2009).
71. Martinelli E, Cicala C, Van Ryk D et al. HIV-1 gp120 inhibits TLR9-mediated activation and IFN-{alpha} secretion in plasmacytoid dendritic cells. Proc. Natl Acad. Sci. USA 104(9), 3396-3401 (2007).
72. Xu Y, Hu Y, Shi B et al. HBsAg inhibits TLR9-mediated activation and IFN-alpha production in plasmacytoid dendritic cells. Mol. Immunol. 46(13), 2640-2646 (2009).
73. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N. Engl. J. Med. 343(13), 938-952 (2000).
74. Sospedra M, Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 23, 683-747 (2005).
75. Bailey-Bucktrout SL, Caulkins SC, Goings G, Fischer JA, Dzionek A, Miller SD. Cutting edge: Central nervous system plasmacytoid dendritic cells regulate the severity of relapsing experimental autoimmune encephalomyelitis. J. Immunol. 180(10), 6457-6461 (2008).
76. Serada S, Fujimoto M, Mihara M et al. IL-6 blockade inhibits the induction of myelin antigen-specific Th17 cells and Th1 cells in experimental autoimmune encephalomyelitis. Proc. Natl Acad. Sci. USA 105, 9041-9046 (2008).
77. Akassoglou K, Bauer J, Kassiotis G et al. Oligodendrocyte apoptosis and primary demyelination induced by local TNF/p55TNF receptor signaling in the central nervous system of transgenic mice: Models for multiple sclerosis with primary oligodendrogliopathy. Am. J. Pathol. 153, 801-813 (1998).
78. Iliev AI, Stringaris AK, Nau R et al. Neuronal injury mediated via stimulation of microglial Toll-like receptor-9 (TLR9). FASEB J. 18, 412-414 (2004).
79. Pashenkov M, Huang YM, Kostulas V, Haglund M, Soderstrom M, Link H. Two subsets of dendritic cells are present in human cerebrospinal fluid. Brain 124(Pt 3), 480-492 (2001).
80. Lande R, Gafa V, Serafini B et al. Plasmacytoid dendritic cells in multiple sclerosis: Intracerebral recruitment and impaired maturation in response to interferon-beta. J. Neuropathol. Exp. Neurol. 67(5), 388-401 (2008).
81. Longhini AL, von Glehn F, Brandao CO et al. Plasmacytoid dendritic cells are increased in cerebrospinal fluid of untreated patients during multiple sclerosis relapse. J. Neuroinflammation 8(1), 2 (2011).
82. Pashenkov M, Teleshova N, Kouwenhoven M et al. Elevated expression of CCR5 by myeloid (CD11c+) blood dendritic cells in multiple sclerosis and acute optic neuritis. Clin. Exp. Immunol. 127(3), 519-526 (2002).
83. Lopez C, Comabella M, Al-Zayat H, Tintore M, Montalban X. Altered maturation of circulating dendritic cells in primary progressive MS patients. J. Neuroimmunol. 175(1-2), 183-191 (2006).
84. Stasiolek M, Bayas A, Kruse N et al. Impaired maturation and altered regulatory function of plasmacytoid dendritic cells in multiple sclerosis. Brain 129, 1293-1305 (2006).
85. Isaksson M, Ardesjo B, Ronnblom L et al. Plasmacytoid DC promote priming of autoimmune Th17 cells and EAE. Eur. J. Immunol. 39(10), 2925-2935 (2009).
86. Irla M, Kupfer N, Suter T et al. MHC class II-restricted antigen presentation by plasmacytoid dendritic cells inhibits T cell-mediated autoimmunity. J. Exp. Med. 207(9), 1891-1905 (2010).
87. Dhodapkar MV, Steinman RM, Krasovsky J et al. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193, 233-238 (2001).
88. Schwab N, Zozulya AL, Kieseier BC et al. An imbalance of two functionally and phenotypically different subsets of plasmacytoid dendritic cells characterizes the dysfunctional immune regulation in multiple sclerosis. J. Immunol. 184, 5368-5374 (2010).
89. Balashov KE, Aung LL, Vaknin-Dembinsky A et al. Interferon-beta inhibits Toll-like receptor 9 processing in multiple sclerosis. Ann. Neurol. 68(6), 899-906 (2010).
90. Aung LL, Fitzgerald-Bocarsly P, Dhib-Jalbut S, Balashov K. Plasmacytoid dendritic cells in multiple sclerosis: Chemokine and chemokine receptor modulation by interferon-beta. J. Neuroimmunol. 226, 158-164 (2010).
91. Aung LL, Brooks A, Greenberg SA, Rosenberg ML, Dhib-Jalbut S, Balashov KE. Multiple sclerosis-linked and interferon-beta-regulated gene expression in plasmacytoid dendritic cells. J. Neuroimmunol. 250(1-2), 99-105 (2012).
92. Segal BM, Chang JT, Shevach EM. CpG oligonucleotides are potent adjuvants for the activation of autoreactive encephalitogenic T cells in vivo. J. Immunol. 164(11), 5683-5688 (2000).
93. Ichikawa HT, Williams LP, Segal BM. Activation of APCs through CD40 or Toll-like receptor 9 overcomes tolerance and precipitates autoimmune disease. J. Immunol. 169(5), 2781-2787 (2002).
94. Waldner H, Collins M, Kuchroo VK. Activation of antigen-presenting cells by microbial products breaks self-tolerance and induces autoimmune disease. J. Clin. Invest. 113(7), 990-997 (2004).
95. Touil T, Fitzgerald D, Zhang GX et al. Cutting edge: TLR3 stimulation suppresses experimental autoimmune encephalomyelitis by inducing endogenous IFN-beta. J. Immunol. 177(11), 7505-7509 (2006).
96. Lenert P, Goeken AJ, Ashman RF. Extended sequence preferences for oligodeoxyribonucleotide activity. Immunology 117(4), 474-481 (2006).
97. Lenert PS. Targeting Toll-like receptor signaling in plasmacytoid dendritic cells and autoreactive B cells as a therapy for lupus. Arthritis Res. Ther. 8(1), 203 (2006).
98. Guiducci C, Gong M, Xu Z et al. TLR recognition of self-nucleic acids hampers glucocorticoid activity in lupus. Nature 465(7300), 937-941 (2010).
99. Levin LI, Munger KL, O'Reilly EJ et al. Primary infection with the Epstein-Barr virus and risk of multiple sclerosis. Ann. Neurol. 67, 824-830 (2010).
100. Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann. Neurol. 61, 288-299 (2007).
101. Hanabuchi S, Ito T, Park WR et al. Thymic stromal lymphopoietin-activated plasmacytoid dendritic cells induce the generation of FOXP3+ regulatory T cells in human thymus. J. Immunol. 184, 2999-3007 (2010).
102. Martin-Gayo E, Sierra-Filardi E, Corbi AL et al. Plasmacytoid dendritic cells resident in human thymus drive natural Treg cell development. Blood 115, 5366-5375 (2010).
103. Chen W, Liang X, Peterson AJ et al. The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J. Immunol. 181, 5396-5404 (2008).
104. Pallotta MT, Orabona C, Volpi C et al. Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat. Immunol. 12, 870-878 (2011). (Pubitemid 40685976)