Tolerogenic dendritic cells for reprogramming of lymphocyte responses in autoimmune diseases

Autoimmunity Reviews

Volumn 15, Issue 11, 2016, Pages 1071-1080

  García González, Paulina ^a,b   Ubilla Olguín, Gabriela ^a,b   Catalán, Diego ^a,b   Schinnerling, Katina ^a,b   Aguillón, Juan Carlos ^a,b  

^a UNIVERSITY OF CHILE   (Chile)

^b Pontificia Universidad Católica de Chile   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL KILLING; CLINICAL TRIAL (TOPIC); CLONAL ANERGY; DENDRITIC CELL; EFFECTOR CELL; HUMAN; IMMUNOMODULATION; INSULIN DEPENDENT DIABETES MELLITUS; MULTIPLE SCLEROSIS; NONHUMAN; NUCLEAR REPROGRAMMING; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; ANIMAL; AUTOIMMUNE DISEASES; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MOUSE;

ANIMALS; AUTOIMMUNE DISEASES; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; HUMANS; IMMUNE TOLERANCE; MICE;

EID: 84992478797     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2016.07.032     Document Type: Review

References (174)

1. [1] Hespel, C., Moser, M., Role of inflammatory dendritic cells in innate and adaptive immunity. Eur J Immunol 42 (2012), 2535–2543.
2. [2] Pulendran, B., Tang, H., Manicassamy, S., Programming dendritic cells to induce TH2 and tolerogenic responses. Nat Immunol 11 (2010), 647–655.
3. [3] Steinman, R.M., Hemmi, H., Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol 311 (2006), 17–58.
4. [4] Kapsenberg, M.L., Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol 3 (2003), 984–993.
5. [5] Wuest, S.C., Edwan, J.H., Martin, J.F., Han, S., Perry, J.S., Cartagena, C.M., et al. A role for interleukin-2 trans-presentation in dendritic cell-mediated T cell activation in humans, as revealed by daclizumab therapy. Nat Med 17 (2011), 604–609.
6. [6] Kalinski, P., Hilkens, C.M., Wierenga, E.A., Kapsenberg, M.L., T-cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol Today 20 (1999), 561–567.
7. [7] Wenink, M.H., Han, W., Toes, R.E., Radstake, T.R., Dendritic cells and their potential implication in pathology and treatment of rheumatoid arthritis. Handb Exp Pharmacol, 2009, 81–98.
8. [8] Bluestone, J.A., Herold, K., Eisenbarth, G., Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature 464 (2010), 1293–1300.
9. [9] Blanco, P., Palucka, A.K., Gill, M., Pascual, V., Banchereau, J., Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science (New York, N.Y.) 294 (2001), 1540–1543.
10. [10] Thewissen, K., Nuyts, A.H., Deckx, N., Van Wijmeersch, B., Nagels, G., D'Hooghe, M., et al. Circulating dendritic cells of multiple sclerosis patients are proinflammatory and their frequency is correlated with MS-associated genetic risk factors. Mult Scler 20 (2014), 548–557.
11. [11] Boks, M.A., Kager-Groenland, J.R., Haasjes, M.S., Zwaginga, J.J., van Ham, S.M., ten Brinke, A., IL-10-generated tolerogenic dendritic cells are optimal for functional regulatory T cell induction–a comparative study of human clinical-applicable DC. Clin Immunol 142 (2012), 332–342.
12. + T cells. J Immunol 184 (2010), 1765–1775.
13. [13] Bosma, B.M., Metselaar, H.J., Nagtzaam, N.M., de Haan, R., Mancham, S., van der Laan, L.J., et al. Dexamethasone transforms lipopolysaccharide-stimulated human blood myeloid dendritic cells into myeloid dendritic cells that prime interleukin-10 production in T cells. Immunology 125 (2008), 91–100.
14. [14] Lanzavecchia, A., Sallusto, F., Regulation of T cell immunity by dendritic cells. Cell 106 (2001), 263–266.
15. [15] Volchenkov, R., Karlsen, M., Jonsson, R., Appel, S., Type 1 regulatory T cells and regulatory B cells induced by tolerogenic dendritic cells. Scand J Immunol 77 (2013), 246–254.
16. [16] Boltjes, A., van Wijk, F., Human dendritic cell functional specialization in steady-state and inflammation. Front Immunol, 5, 2014, 131.
17. [17] Jaehn, P.S., Zaenker, K.S., Schmitz, J., Dzionek, A., Functional dichotomy of plasmacytoid dendritic cells: antigen-specific activation of T cells versus production of type I interferon. Eur J Immunol 38 (2008), 1822–1832.
18. [18] Cella, M., Jarrossay, D., Facchetti, F., Alebardi, O., Nakajima, H., Lanzavecchia, A., et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 5 (1999), 919–923.
19. + dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 207 (2010), 1247–1260.
20. [20] Hemont, C., Neel, A., Heslan, M., Braudeau, C., Josien, R., Human blood mDC subsets exhibit distinct TLR repertoire and responsiveness. J Leukoc Biol 93 (2013), 599–609.
21. [21] Campbell, I.K., van Nieuwenhuijze, A., Segura, E., O'Donnell, K., Coghill, E., Hommel, M., et al. Differentiation of inflammatory dendritic cells is mediated by NF-kappaB1-dependent GM-CSF production in CD4 T cells. J Immunol 186 (2011), 5468–5477.
22. [22] Segura, E., Touzot, M., Bohineust, A., Cappuccio, A., Chiocchia, G., Hosmalin, A., et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 38 (2013), 336–348.
23. [23] Chu, C.-C., Di Meglio, P., Nestle, F.O., Harnessing dendritic cells in inflammatory skin diseases. Semin Immunol 23 (2011), 28–41.
24. [24] Lowes, M.A., Chamian, F., Abello, M.V., Fuentes-Duculan, J., Lin, S.L., Nussbaum, R., et al. Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc Natl Acad Sci U S A 102 (2005), 19057–19062.
25. [25] van Kooten, C., Stax, A.S., Woltman, A.M., Gelderman, K.A., Handbook of experimental pharmacology “dendritic cells”: the use of dexamethasone in the induction of tolerogenic DCs. Handb Exp Pharmacol, 2009, 233–249.
26. [26] Merad, M., Ginhoux, F., Collin, M., Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 8 (2008), 935–947.
27. [27] Goval, J.-J., Greimers, R., Boniver, J., de Leval, L., Germinal center dendritic cells express more ICAM-1 than extrafollicular dendritic cells and ICAM-1/LFA-1 interactions are involved in the capacity of dendritic cells to induce PBMCs proliferation. J Histochem Cytochem 54 (2006), 75–84.
28. [28] Gregori, S., Dendritic cells in networks of immunological tolerance. Tissue Antigens 77 (2011), 89–99.
29. [29] Trombetta, E.S., Mellman, I., Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 23 (2005), 975–1028.
30. [30] Randolph, G.J., Ochando, J., Partida-Sanchez, S., Migration of dendritic cell subsets and their precursors. Annu Rev Immunol 26 (2008), 293–316.
31. [31] Platt, C.D., Ma, J.K., Chalouni, C., Ebersold, M., Bou-Reslan, H., Carano, R.A.D., et al. Mature dendritic cells use endocytic receptors to capture and present antigens. Proc Natl Acad Sci 107 (2010), 4287–4292.
32. [32] Piqueras, B., Connolly, J., Freitas, H., Palucka, A.K., Banchereau, J., Upon viral exposure, myeloid and plasmacytoid dendritic cells produce 3 waves of distinct chemokines to recruit immune effectors. Blood 107 (2006), 2613–2618.
33. [33] Chow, A., Toomre, D., Garrett, W., Mellman, I., Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 418 (2002), 988–994.
34. [34] Han, T.H., Jin, P., Ren, J., Slezak, S., Marincola, F.M., Stroncek, D.F., Evaluation of 3 clinical dendritic cell maturation protocols containing lipopolysaccharide and interferon-gamma. J Immunother 32 (2009), 399–407.
35. [35] Delgado-Martin, C., Escribano, C., Pablos, J.L., Riol-Blanco, L., Rodriguez-Fernandez, J.L., Chemokine CXCL12 uses CXCR4 and a signaling core formed by bifunctional Akt, extracellular signal-regulated kinase (ERK)1/2, and mammalian target of rapamycin complex 1 (mTORC1) proteins to control chemotaxis and survival simultaneously in mature dendritic cells. J Biol Chem 286 (2011), 37222–37236.
36. [36] Tanaka, H., Demeure, C.E., Rubio, M., Delespesse, G., Sarfati, M., 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 (2000), 405–412.
37. + T cell responses elicited by different subsets of human skin migratory dendritic cells. J Immunol 175 (2005), 7905–7915.
38. [38] Banchereau, J., Steinman, R.M., Dendritic cells and the control of immunity. Nature 392 (1998), 245–252.
39. [39] Morelli, A.E., Thomson, A.W., Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7 (2007), 610–621.
40. [40] McCaughtry, T.M., Baldwin, T.A., Wilken, M.S., Hogquist, K.A., Clonal deletion of thymocytes can occur in the cortex with no involvement of the medulla. J Exp Med 205 (2008), 2575–2584.
41. + regulatory T cells in human thymus. Nature 436 (2005), 1181–1185.
42. + regulatory T cells in human thymus. J Immunol 184 (2010), 2999–3007.
43. [43] Steinman, R.M., Hawiger, D., Nussenzweig, M.C., Tolerogenic dendritic cells. Annu Rev Immunol 21 (2003), 685–711.
44. [44] Vitali, C., Mingozzi, F., Broggi, A., Barresi, S., Zolezzi, F., Bayry, J., et al. Migratory, and not lymphoid-resident, dendritic cells maintain peripheral self-tolerance and prevent autoimmunity via induction of iTreg cells. 2012.
45. + regulatory T cells. Eur J Immunol 41 (2011), 1420–1434.
46. [46] Takakubo, Y., Takagi, M., Maeda, K., Tamaki, Y., Sasaki, A., Asano, T., et al. Distribution of myeloid dendritic cells and plasmacytoid dendritic cells in the synovial tissues of rheumatoid arthritis. J Rheumatol 35 (2008), 1919–1931.
47. [47] Ding, D., Mehta, H., McCune, W.J., Kaplan, M.J., Aberrant phenotype and function of myeloid dendritic cells in systemic lupus erythematosus. J Immunol 177 (2006), 5878–5889.
48. [48] Tsark, E.C., Wang, W., Teng, Y.C., Arkfeld, D., Dodge, G.R., Kovats, S., Differential MHC class II-mediated presentation of rheumatoid arthritis autoantigens by human dendritic cells and macrophages. J Immunol 169 (2002), 6625–6633.
49. [49] Mok, M.Y., Tolerogenic dendritic cells: role and therapeutic implications in systemic lupus erythematosus. Int J Rheum Dis 18 (2015), 250–259.
50. [50] Santiago-Schwarz, F., Anand, P., Liu, S., Carsons, S.E., Dendritic cells (DCs) in rheumatoid arthritis (RA): progenitor cells and soluble factors contained in RA synovial fluid yield a subset of myeloid DCs that preferentially activate Th1 inflammatory-type responses. J Immunol 167 (2001), 1758–1768.
51. [51] Benson, R.A., Patakas, A., Conigliaro, P., Rush, C.M., Garside, P., McInnes, I.B., et al. Identifying the cells breaching self-tolerance in autoimmunity. J Immunol 184 (2010), 6378–6385.
52. [52] Mackern-Oberti, J.P., Llanos, C., Vega, F., Salazar-Onfray, F., Riedel, C.A., Bueno, S.M., et al. Role of dendritic cells in the initiation, progress and modulation of systemic autoimmune diseases. Autoimmun Rev 14 (2015), 127–139.
53. [53] Amodio, G., Gregori, S., Dendritic cells a double-edge sword in autoimmune responses. Front Immunol, 3, 2012, 233.
54. + myeloid dendritic cells - the inflammatory picture emerges. Arthritis Res Ther, 15, 2013, 128.
55. [55] Schinnerling, K., Soto, L., Garcia-Gonzalez, P., Catalan, D., Aguillon, J.C., Skewing dendritic cell differentiation towards a tolerogenic state for recovery of tolerance in rheumatoid arthritis. Autoimmun Rev 14:6 (2015), 517–527.
56. [56] Sallusto, F., Lanzavecchia, A., Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179 (1994), 1109–1118.
57. [57] Hilkens, C.M., Isaacs, J.D., Tolerogenic dendritic cell therapy for rheumatoid arthritis: where are we now?. Clin Exp Immunol 172 (2013), 148–157.
58. [58] Steinbrink, K., Wolfl, M., Jonuleit, H., Knop, J., Enk, A.H., Induction of tolerance by IL-10-treated dendritic cells. J Immunol 159 (1997), 4772–4780.
59. [59] Fogel-Petrovic, M., Long, J.A., Misso, N.L., Foster, P.S., Bhoola, K.D., Thompson, P.J., Physiological concentrations of transforming growth factor beta1 selectively inhibit human dendritic cell function. Int Immunopharmacol 7 (2007), 1924–1933.
60. [60] Song, S.S., Yuan, P.F., Chen, J.Y., Fu, J.J., Wu, H.X., Lu, J.T., et al. TGF-beta favors bone marrow-derived dendritic cells to acquire tolerogenic properties. Immunol Invest 43 (2014), 360–369.
61. [61] Brandt, K., Bulfone-Paus, S., Foster, D.C., Ruckert, R., Interleukin-21 inhibits dendritic cell activation and maturation. Blood 102 (2003), 4090–4098.
62. [62] Hegde, S., Pahne, J., Smola-Hess, S., Novel immunosuppressive properties of interleukin-6 in dendritic cells: inhibition of NF-kappaB binding activity and CCR7 expression. FASEB J 18 (2004), 1439–1441.
63. [63] Menges, M., Rossner, S., Voigtlander, C., Schindler, H., Kukutsch, N.A., Bogdan, C., et al. Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity. J Exp Med 195 (2002), 15–21.
64. + effector/memory T cells from type 1 diabetic individuals. J Clin Immunol 30 (2010), 659–668.
65. [65] Garate, D., Rojas-Colonelli, N., Pena, C., Salazar, L., Abello, P., Pesce, B., et al. Blocking of p38 and transforming growth factor beta receptor pathways impairs the ability of tolerogenic dendritic cells to suppress murine arthritis. Arthritis Rheum 65 (2013), 120–129.
66. [66] Salazar, L., Aravena, O., Abello, P., Escobar, A., Contreras-Levicoy, J., Rojas-Colonelli, N., et al. Modulation of established murine collagen-induced arthritis by a single inoculation of short-term lipopolysaccharide-stimulated dendritic cells. Ann Rheum Dis 67 (2008), 1235–1241.
67. [67] Zimmer, A., Bouley, J., Le Mignon, M., Pliquet, E., Horiot, S., Turfkruyer, M., et al. A regulatory dendritic cell signature correlates with the clinical efficacy of allergen-specific sublingual immunotherapy. J Allergy Clin Immunol 129 (2012), 1020–1030.
68. [68] Xia, C.Q., Peng, R., Beato, F., Clare-Salzler, M.J., Dexamethasone induces IL-10-producing monocyte-derived dendritic cells with durable immaturity. Scand J Immunol 62 (2005), 45–54.
69. [69] Fedoric, B., Krishnan, R., Rapamycin downregulates the inhibitory receptors ILT2, ILT3, ILT4 on human dendritic cells and yet induces T cell hyporesponsiveness independent of FoxP3 induction. Immunol Lett 120 (2008), 49–56.
70. [70] Hackstein, H., Taner, T., Zahorchak, A.F., Morelli, A.E., Logar, A.J., Gessner, A., et al. Rapamycin inhibits IL-4–induced dendritic cell maturation in vitro and dendritic cell mobilization and function in vivo. Blood 101 (2003), 4457–4463.
71. [71] Buckland, M., Jago, C., Fazekesova, H., George, A., Lechler, R., Lombardi, G., Aspirin modified dendritic cells are potent inducers of allo-specific regulatory T-cells. Int Immunopharmacol 6 (2006), 1895–1901.
72. [72] Buckland, M., Lombardi, G., Aspirin and the induction of tolerance by dendritic cells. Handb Exp Pharmacol, 2009, 197–213.
73. [73] Lee, J.I., Ganster, R.W., Geller, D.A., Burckart, G.J., Thomson, A.W., Lu, L., Cyclosporine A inhibits the expression of costimulatory molecules on in vitro-generated dendritic cells: association with reduced nuclear translocation of nuclear factor kappa B. Transplantation 68 (1999), 1255–1263.
74. [74] Iruretagoyena, M.I., Sepulveda, S.E., Lezana, J.P., Hermoso, M., Bronfman, M., Gutierrez, M.A., et al. Inhibition of nuclear factor-kappa B enhances the capacity of immature dendritic cells to induce antigen-specific tolerance in experimental autoimmune encephalomyelitis. J Pharmacol Exp Ther 318 (2006), 59–67.
75. + T cells’ allocytotoxicity. Int Immunol 26 (2014), 173–181.
76. [76] Kubo, S., Yamaoka, K., Kondo, M., Yamagata, K., Zhao, J., Iwata, S., et al. The JAK inhibitor, tofacitinib, reduces the T cell stimulatory capacity of human monocyte-derived dendritic cells. Ann Rheum Dis, 2013.
77. [77] Svajger, U., Obermajer, N., Jeras, M., Dendritic cells treated with resveratrol during differentiation from monocytes gain substantial tolerogenic properties upon activation. Immunology 129 (2010), 525–535.
78. [78] Rogers, N.M., Kireta, S., Coates, P.T., Curcumin induces maturation-arrested dendritic cells that expand regulatory T cells in vitro and in vivo. Clin Exp Immunol 162 (2010), 460–473.
79. [79] Geisel, J., Bruck, J., Glocova, I., Dengler, K., Sinnberg, T., Rothfuss, O., et al. Sulforaphane protects from T cell-mediated autoimmune disease by inhibition of IL-23 and IL-12 in dendritic cells. J Immunol 192 (2014), 3530–3539.
80. [80] Penna, G., Adorini, L., 1 Alpha,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J Immunol 164 (2000), 2405–2411.
81. [81] Harry, R.A., Anderson, A.E., Isaacs, J.D., Hilkens, C.M., Generation and characterisation of therapeutic tolerogenic dendritic cells for rheumatoid arthritis. Ann Rheum Dis 69 (2010), 2042–2050.
82. [82] Chorny, A., Gonzalez-Rey, E., Fernandez-Martin, A., Pozo, D., Ganea, D., Delgado, M., Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders. Proc Natl Acad Sci U S A 102 (2005), 13562–13567.
83. [83] Matsumoto, T., Hasegawa, H., Onishi, S., Ishizaki, J., Suemori, K., Yasukawa, M., Protein kinase C inhibitor generates stable human tolerogenic dendritic cells. J Immunol 191 (2013), 2247–2257.
84. + regulatory T cell population. J Autoimmun 34 (2010), 111–120.
85. [85] Henry, E., Desmet, C.J., Garze, V., Fievez, L., Bedoret, D., Heirman, C., et al. Dendritic cells genetically engineered to express IL-10 induce long-lasting antigen-specific tolerance in experimental asthma. J Immunol 181 (2008), 7230–7242.
86. [86] Kim, S.H., Kim, S., Evans, C.H., Ghivizzani, S.C., Oligino, T., Robbins, P.D., Effective treatment of established murine collagen-induced arthritis by systemic administration of dendritic cells genetically modified to express IL-4. J Immunol 166 (2001), 3499–3505.
87. + T cells. Hum Immunol 65 (2004), 1344–1355.
88. [88] Zheng, X., Suzuki, M., Ichim, T.E., Zhang, X., Sun, H., Zhu, F., et al. Treatment of autoimmune arthritis using RNA interference-modulated dendritic cells. J Immunol 184 (2010), 6457–6464.
89. [89] Kalantari, T., Karimi, M.H., Ciric, B., Yan, Y., Rostami, A., Kamali-Sarvestani, E., Tolerogenic dendritic cells produced by lentiviral-mediated CD40- and interleukin-23p19-specific shRNA can ameliorate experimental autoimmune encephalomyelitis by suppressing T helper type 17 cells. Clin Exp Immunol 176 (2014), 180–189.
90. [90] Li, R., Zheng, X., Popov, I., Zhang, X., Wang, H., Suzuki, M., et al. Gene silencing of IL-12 in dendritic cells inhibits autoimmune arthritis. J Transl Med, 10, 2012, 19.
91. [91] Naranjo-Gomez, M., Raich-Regue, D., Onate, C., Grau-Lopez, L., Ramo-Tello, C., Pujol-Borrell, R., et al. Comparative study of clinical grade human tolerogenic dendritic cells. J Transl Med, 9, 2011, 89.
92. [92] Chamorro, S., Garcia-Vallejo, J.J., Unger, W.W., Fernandes, R.J., Bruijns, S.C., Laban, S., et al. TLR triggering on tolerogenic dendritic cells results in TLR2 up-regulation and a reduced proinflammatory immune program. J Immunol 183 (2009), 2984–2994.
93. [93] Anderson, A.E., Swan, D.J., Sayers, B.L., Harry, R.A., Patterson, A.M., von Delwig, A., et al. LPS activation is required for migratory activity and antigen presentation by tolerogenic dendritic cells. J Leukoc Biol 85 (2009), 243–250.
94. [94] Unger, W.W., Laban, S., Kleijwegt, F.S., van der Slik, A.R., Roep, B.O., Induction of Treg by monocyte-derived DC modulated by vitamin D3 or dexamethasone: differential role for PD-L1. Eur J Immunol 39 (2009), 3147–3159.
95. + T cells by alternatively activated dendritic cells. J Leukoc Biol 84 (2008), 124–133.
96. + T cells, and induce long-term organ allograft survival in combination with CTLA4-Ig. J Immunol 177 (2006), 5868–5877.
97. [97] Garcia-Gonzalez, P., Morales, R., Hoyos, L., Maggi, J., Campos, J., Pesce, B., et al. A short protocol using dexamethasone and monophosphoryl lipid A generates tolerogenic dendritic cells that display a potent migratory capacity to lymphoid chemokines. J Transl Med, 11, 2013, 128.
98. [98] Roelen, D.L., van den Boogaardt, D.E., van Miert, P.P., Koekkoek, K., Offringa, R., Claas, F.H., Differentially modulated dendritic cells induce regulatory T cells with different characteristics. Transpl Immunol 19 (2008), 220–228.
99. [99] Haribhai, D., Williams, J.B., Jia, S., Nickerson, D., Schmitt, E.G., Edwards, B., et al. A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity. Immunity 35 (2011), 109–122.
100. [100] Huang, H., Ma, Y., Dawicki, W., Zhang, X., Gordon, J.R., Comparison of induced versus natural regulatory T cells of the same TCR specificity for induction of tolerance to an environmental antigen. J Immunol 191 (2013), 1136–1143.
101. [101] Roelen, D.L., Schuurhuis, D.H., van den Boogaardt, D.E., Koekkoek, K., van Miert, P.P., van Schip, J.J., et al. Prolongation of skin graft survival by modulation of the alloimmune response with alternatively activated dendritic cells. Transplantation 76 (2003), 1608–1615.
102. + regulatory T cells by 1,25-dihydroxyvitamin D3. Blood 106 (2005), 3490–3497.
103. [103] van Halteren, A.G., Tysma, O.M., van Etten, E., Mathieu, C., Roep, B.O., 1alpha,25-dihydroxyvitamin D3 or analogue treated dendritic cells modulate human autoreactive T cells via the selective induction of apoptosis. J Autoimmun 23 (2004), 233–239.
104. [104] Bakdash, G., van Capel, T.M.M., Mason, L.M.K., Kapsenberg, M.L., de Jong, E.C., Vitamin D3 metabolite calcidiol primes human dendritic cells to promote the development of immunomodulatory IL-10-producing T cells. Vaccine 32 (2014), 6294–6302.
105. [105] Pedersen, A.E., Gad, M., Walter, M.R., Claesson, M.H., Induction of regulatory dendritic cells by dexamethasone and 1alpha,25-Dihydroxyvitamin D(3). Immunol Lett 91 (2004), 63–69.
106. + regulatory T cell promotion. J Immunol 183 (2009), 2932–2945.
107. [107] Rojas-Canales, D., Krishnan, R., Jessup, C.F., Coates, P.T., Early exposure of interferon-gamma inhibits signal transducer and activator of transcription-6 signalling and nuclear factor kappaB activation in a short-term monocyte-derived dendritic cell culture promoting ‘FAST’ regulatory dendritic cells. Clin Exp Immunol 167 (2012), 447–458.
108. [108] Maldonado, R.A., von Andrian, U.H., How tolerogenic dendritic cells induce regulatory T cells. Adv Immunol 108 (2010), 111–165.
109. + regulatory T cells: more of the same or a division of labor?. Immunity 30 (2009), 626–635.
110. + T regulatory cells. J Immunol 183 (2009), 145–154.
111. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389 (1997), 737–742.
112. [112] Murai, M., Turovskaya, O., Kim, G., Madan, R., Karp, C.L., Cheroutre, H., et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 10 (2009), 1178–1184.
113. [113] Wakkach, A., Fournier, N., Brun, V., Breittmayer, J.P., Cottrez, F., Groux, H., Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 18 (2003), 605–617.
114. [114] Gregori, S., Tomasoni, D., Pacciani, V., Scirpoli, M., Battaglia, M., Magnani, C.F., et al. Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood 116 (2010), 935–944.
115. [115] Awasthi, A., Carrier, Y., Peron, J.P., Bettelli, E., Kamanaka, M., Flavell, R.A., et al. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol 8 (2007), 1380–1389.
116. [116] Ilarregui, J.M., Croci, D.O., Bianco, G.A., Toscano, M.A., Salatino, M., Vermeulen, M.E., et al. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat Immunol 10 (2009), 981–991.
117. + regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198 (2003), 1875–1886.
118. + T cell subsets. J Leukoc Biol 82 (2007), 335–346.
119. [119] Dillon, S., Agrawal, A., Van Dyke, T., Landreth, G., McCauley, L., Koh, A., et al. A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells. J Immunol 172 (2004), 4733–4743.
120. [120] Manicassamy, S., Ravindran, R., Deng, J., Oluoch, H., Denning, T.L., Kasturi, S.P., et al. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat Med 15 (2009), 401–409.
121. [121] Mucida, D., Pino-Lagos, K., Kim, G., Nowak, E., Benson, M.J., Kronenberg, M., et al. Retinoic acid can directly promote TGF-beta-mediated Foxp3(+) Treg cell conversion of naive T cells. Immunity 30 (2009), 471–472 [author reply 472-3].
122. [122] Sun, C.M., Hall, J.A., Blank, R.B., Bouladoux, N., Oukka, M., Mora, J.R., et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 204 (2007), 1775–1785.
123. + regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 204 (2007), 1757–1764.
124. [124] Oderup, C., LaJevic, M., Butcher, E.C., Canonical and noncanonical Wnt proteins program dendritic cell responses for tolerance. J Immunol 190 (2013), 6126–6134.
125. [125] Manicassamy, S., Reizis, B., Ravindran, R., Nakaya, H., Salazar-Gonzalez, R.M., Wang, Y.C., et al. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science (New York, N. Y.) 329 (2010), 849–853.
126. [126] Munn, D.H., Mellor, A.L., Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest 117 (2007), 1147–1154.
127. [127] Kushwah, R., Hu, J., Role of dendritic cells in the induction of regulatory T cells. Cell Biophys, 1, 2011, 20.
128. [128] Maggi, J., Schafer, C., Ubilla-Olguín, G., Catalán, D., Schinnerling, K., Aguillón, J.C., Therapeutic potential of hyporesponsive CD4(+) T cells in autoimmunity. Front Immunol, 6, 2015, 488.
129. [129] Schwartz, R.H., T cell anergy. Annu Rev Immunol 21 (2003), 305–334.
130. [130] Rea, D., van Kooten, C., van Meijgaarden, K.E., Ottenhoff, T.H., Melief, C.J., Offringa, R., Glucocorticoids transform CD40-triggering of dendritic cells into an alternative activation pathway resulting in antigen-presenting cells that secrete IL-10. Blood 95 (2000), 3162–3167.
131. [131] Steinbrink, K., Graulich, E., Kubsch, S., Knop, J., Enk, A.H., CD4(+) and CD8(+) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 99 (2002), 2468–2476.
132. [132] Kubsch, S., Graulich, E., Knop, J., Steinbrink, K., Suppressor activity of anergic T cells induced by IL-10-treated human dendritic cells: association with IL-2- and CTLA-4-dependent G1 arrest of the cell cycle regulated by p27Kip1. Eur J Immunol 33 (2003), 1988–1997.
133. [133] Sato, K., Yamashita, N., Matsuyama, T., Human peripheral blood monocyte-derived interleukin-10-induced semi-mature dendritic cells induce anergic CD4(+) and CD8(+) T cells via presentation of the internalized soluble antigen and cross-presentation of the phagocytosed necrotic cellular fragments. Cell Immunol 215 (2002), 186–194.
134. [134] McBride, J.M., Jung, T., de Vries, J.E., Aversa, G., IL-10 alters DC function via modulation of cell surface molecules resulting in impaired T-cell responses. Cell Immunol 215 (2002), 162–172.
135. [135] Tuettenberg, A., Huter, E., Hubo, M., Horn, J., Knop, J., Grimbacher, B., et al. The role of ICOS in directing T cell responses: ICOS-dependent induction of T cell anergy by tolerogenic dendritic cells. J Immunol 182 (2009), 3349–3356.
136. [136] Kleijwegt, F.S., Jansen, D.T., Teeler, J., Joosten, A.M., Laban, S., Nikolic, T., et al. Tolerogenic dendritic cells impede priming of naive CD8(+) T cells and deplete memory CD8(+) T cells. Eur J Immunol 43 (2013), 85–92.
137. [137] Mobergslien, A., Sioud, M., Galectin-1 and − 3 gene silencing in immature and mature dendritic cells enhances T cell activation and interferon-gamma production. J Leukoc Biol 91 (2012), 461–467.
138. [138] Seki, M., Oomizu, S., Sakata, K.M., Sakata, A., Arikawa, T., Watanabe, K., et al. Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin Immunol 127 (2008), 78–88.
139. [139] Zhu, C., Anderson, A.C., Schubart, A., Xiong, H., Imitola, J., Khoury, S.J., et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 6 (2005), 1245–1252.
140. [140] Kessel, A., Haj, T., Peri, R., Snir, A., Melamed, D., Sabo, E., et al. Human CD19(+)CD25(high) B regulatory cells suppress proliferation of CD4(+) T cells and enhance Foxp3 and CTLA-4 expression in T-regulatory cells. Autoimmun Rev 11 (2012), 670–677.
141. [141] Carter, N.A., Rosser, E.C., Mauri, C., Interleukin-10 produced by B cells is crucial for the suppression of Th17/Th1 responses, induction of T regulatory type 1 cells and reduction of collagen-induced arthritis. Arthritis Res Ther, 14, 2012, R32.
142. [142] Rosser, E.C., Mauri, C., Regulatory B cells: origin, phenotype, and function. Immunity 42 (2015), 607–612.
143. [143] Li, H., Wang, C.C., Zhang, M., Li, X.L., Zhang, P., Yue, L.T., et al. Statin-modified dendritic cells regulate humoral immunity in experimental autoimmune myasthenia gravis. Mol Cell Neurosci 68 (2015), 284–292.
144. [144] Qian, L., Qian, C., Chen, Y., Bai, Y., Bao, Y., Lu, L., et al. Regulatory dendritic cells program B cells to differentiate into CD19hiFcgammaIIbhi regulatory B cells through IFN-beta and CD40L. Blood 120 (2012), 581–591.
145. [145] Menon, M., Blair, P.A., Isenberg, D.A., Mauri, C., A regulatory feedback between plasmacytoid dendritic cells and regulatory B cells is aberrant in systemic lupus erythematosus. Immunity 44 (2016), 683–697.
146. [146] Giannoukakis, N., Phillips, B., Finegold, D., Harnaha, J., Trucco, M., Phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetic patients. Diabetes Care 34 (2011), 2026–2032.
147. [147] Giannoukakis, N., Trucco, M., A role for tolerogenic dendritic cell-induced B-regulatory cells in type 1 diabetes mellitus. Curr Opin Endocrinol Diabetes Obes 19 (2012), 279–287.
148. [148] Di Caro, V., Phillips, B., Engman, C., Harnaha, J., Trucco, M., Giannoukakis, N., Retinoic acid-producing, ex-vivo-generated human tolerogenic dendritic cells induce the proliferation of immunosuppressive B lymphocytes. Clin Exp Immunol 174 (2013), 302–317.
149. [149] Di Caro, V., Phillips, B., Engman, C., Harnaha, J., Trucco, M., Giannoukakis, N., Involvement of suppressive B-lymphocytes in the mechanism of tolerogenic dendritic cell reversal of type 1 diabetes in NOD mice. PLoS One, 9, 2014, e83575.
150. + regulatory T cells in systemic lupus erythematosus. Rheumatology (Oxford) 47 (2008), 789–794.
151. + T cells that lack the IL-7 receptor are increased intra-articularly and have impaired suppressive function in RA patients. Rheumatology (Oxford) 49 (2010), 2084–2089.
152. [152] Radstake, T.R.D.J., van Bon, L., Broen, J., Wenink, M., Santegoets, K., Deng, Y., et al. Increased frequency and compromised function of T regulatory cells in systemic sclerosis (SSc) is related to a diminished CD69 and TGFβ expression. PLoS One, 4, 2009, e5981.
153. + regulatory T cells in systemic sclerosis and other rheumatic diseases. Expert Rev Clin Immunol 7 (2011), 499–514.
154. + regulatory T-cell subpopulation in type 1 diabetes mellitus. Autoimmunity, 2014, 1–9.
155. [155] Elong Ngono, A., Pettre, S., Salou, M., Bahbouhi, B., Soulillou, J.P., Brouard, S., et al. Frequency of circulating autoreactive T cells committed to myelin determinants in relapsing–remitting multiple sclerosis patients. Clin Immunol 144 (2012), 117–126.
156. [156] Raiotach-Regue, D., Grau-Lopez, L., Naranjo-Gomez, M., Ramo-Tello, C., Pujol-Borrell, R., Martinez-Caceres, E., et al. Stable antigen-specific T-cell hyporesponsiveness induced by tolerogenic dendritic cells from multiple sclerosis patients. Eur J Immunol 42 (2012), 771–782.
157. + tolerogenic DCs and enhances Treg, reducing the severity of EAE. CNS Neurosci Ther 19 (2013), 269–277.
158. [158] Mansilla, M.J., Selles-Moreno, C., Fabregas-Puig, S., Amoedo, J., Navarro-Barriuso, J., Teniente-Serra, A., et al. Beneficial effect of tolerogenic dendritic cells pulsed with MOG autoantigen in experimental autoimmune encephalomyelitis. CNS Neurosci Ther 21 (2015), 222–230.
159. [159] Tai, N., Yasuda, H., Xiang, Y., Zhang, L., Rodriguez-Pinto, D., Yokono, K., et al. IL-10-conditioned dendritic cells prevent autoimmune diabetes in NOD and humanized HLA-DQ8/RIP-B7.1 mice. Clin Immunol 139 (2011), 336–349.
160. [160] Marin-Gallen, S., Clemente-Casares, X., Planas, R., Pujol-Autonell, I., Carrascal, J., Carrillo, J., et al. Dendritic cells pulsed with antigen-specific apoptotic bodies prevent experimental type 1 diabetes. Clin Exp Immunol 160 (2010), 207–214.
161. [161] Ferreira, G.B., van Etten, E., Verstuyf, A., Waer, M., Overbergh, L., Gysemans, C., et al. 1,25-Dihydroxyvitamin D3 alters murine dendritic cell behaviour in vitro and in vivo. Diabetes Metab Res Rev 27 (2011), 933–941.
162. [162] van Halteren, A.G., van Etten, E., de Jong, E.C., Bouillon, R., Roep, B.O., Mathieu, C., Redirection of human autoreactive T-cells Upon interaction with dendritic cells modulated by TX527, an analog of 1,25 dihydroxyvitamin D(3). Diabetes 51 (2002), 2119–2125.
163. [163] van Duivenvoorde, L.M., Han, W.G., Bakker, A.M., Louis-Plence, P., Charbonnier, L.M., Apparailly, F., et al. Immunomodulatory dendritic cells inhibit Th1 responses and arthritis via different mechanisms. J Immunol 179 (2007), 1506–1515.
164. [164] Stoop, J.N., Harry, R.A., von Delwig, A., Isaacs, J.D., Robinson, J.H., Hilkens, C.M., Therapeutic effect of tolerogenic dendritic cells in established collagen-induced arthritis is associated with a reduction in Th17 responses. Arthritis Rheum 62 (2010), 3656–3665.
165. [165] Orange, D.E., Blachere, N.E., Fak, J., Parveen, S., Frank, M.O., Herre, M., et al. Dendritic cells loaded with FK506 kill T cells in an antigen-specific manner and prevent autoimmunity in vivo. eLife, 2, 2013, e00105.
166. [166] Yang, J., Yang, Y., Ren, Y., Xie, R., Zou, H., Fan, H., A mouse model of adoptive immunotherapeutic targeting of autoimmune arthritis using allo-tolerogenic dendritic cells. PLoS One, 8, 2013, e77729.
167. [167] Ten Brinke, A., Hilkens, C.M., Cools, N., Geissler, E.K., Hutchinson, J.A., Lombardi, G., et al. Clinical use of tolerogenic dendritic cells-harmonization approach in european collaborative effort. Mediators Inflamm, 2015, 2015, 471719.
168. [168] Dhodapkar, M.V., Steinman, R.M., Krasovsky, J., Munz, C., Bhardwaj, N., Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J Exp Med 193 (2001), 233–238.
169. [169] Dhodapkar, M.V., Steinman, R.M., Antigen-bearing immature dendritic cells induce peptide-specific CD8(+) regulatory T cells in vivo in humans. Blood 100 (2002), 174–177.
170. [170] Benham, H., Nel, H.J., Law, S.C., Mehdi, A.M., Street, S., Ramnoruth, N., et al. Citrullinated peptide dendritic cell immunotherapy in HLA risk genotype-positive rheumatoid arthritis patients. Sci Transl Med, 7, 2015 [290ra87].
171. [171] Bell, G.M., Anderson, A.E., Diboll, J., Reece, R., Eltherington, O., Harry, R.A., et al. Autologous tolerogenic dendritic cells for rheumatoid and inflammatory arthritis. Ann Rheum Dis, 2016.
172. [172] Li, G., Abediankenari, S., Kim, Y.-J.J., Campbell, T.B., Ito, S., Graham-Evans, B., et al. TGF-beta combined with M-CSF and IL-4 induces generation of immune inhibitory cord blood dendritic cells capable of enhancing cytokine-induced ex vivo expansion of myeloid progenitors. Blood 110 (2007), 2872–2879.
173. [173] Buckland, M., Jago, C.B., Fazekasova, H., Scott, K., Tan, P.H., George, A.J., et al. Aspirin-treated human DCs up-regulate ILT-3 and induce hyporesponsiveness and regulatory activity in responder T cells. Am J Transplant Off J Am Soc Transplant Am Soc Transplant Surg 6 (2006), 2046–2059.
174. [174] Olivar, R., Luque, A., Cárdenas-Brito, S., Naranjo-Gómez, M., Blom, A.M., Borràs, F.E., et al. The Complement inhibitor factor H generates an anti-inflammatory and tolerogenic state in monocyte-derived dendritic cells. J Immunol, 2016.