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Clinical and Developmental Immunology
Volume 2013, Article ID 789814, 6 pages
http://dx.doi.org/10.1155/2013/789814
Review Article

Therapeutic Potential of Tolerogenic Dendritic Cells in IBD: From Animal Models to Clinical Application

1Fundació Clinic, Hospital Clínic i Provincial and Centre Esther Koplowitz, 08036 Barcelona, Spain
2Department of Experimental Gastroenterology, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Hospital Clínic i Provincial and Centre Esther Koplowitz, Carrer Roselló 149-153, 08036 Barcelona, Spain

Received 26 July 2013; Accepted 27 September 2013

Academic Editor: Lenin Pavón

Copyright © 2013 Raquel Cabezón and Daniel Benítez-Ribas. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. L. Hart, H. O. Al-Hassi, R. J. Rigby et al., “Characteristics of intestinal dendritic cells in inflammatory bowel diseases,” Gastroenterology, vol. 129, no. 1, pp. 50–65, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. J. L. Coombes and F. Powrie, “Dendritic cells in intestinal immune regulation,” Nature Reviews Immunology, vol. 8, no. 6, pp. 435–446, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. C. G. Figdor, I. J. de Vries, W. J. Lesterhuis, and C. J. Melief, “Dendritic cell immunotherapy: mapping the way,” Nature Medicine, vol. 10, no. 5, pp. 475–480, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. R. M. Steinman and J. Banchereau, “Taking dendritic cells into medicine,” Nature, vol. 449, no. 7161, pp. 419–426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. N. Giannoukakis, B. Phillips, D. Finegold, J. Harnaha, and M. Trucco, “Phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetic patients,” Diabetes Care, vol. 34, no. 9, pp. 2026–2032, 2011. View at Google Scholar
  6. C. M. Hilkens and J. D. Isaacs, “Tolerogenic dendritic cell therapy for rheumatoid arthritis: where are we now?” Clinical & Experimental Immunology, vol. 172, pp. 148–157, 2013. View at Google Scholar
  7. L. Piemonti, P. Monti, P. Allavena et al., “Glucocorticoids affect human dendritic cell differentiation and maturation,” Journal of Immunology, vol. 162, no. 11, pp. 6473–6481, 1999. View at Google Scholar · View at Scopus
  8. D. Rozkova, R. Horvath, J. Bartunkova, and R. Spisek, “Glucocorticoids severely impair differentiation and antigen presenting function of dendritic cells despite upregulation of Toll-like receptors,” Clinical Immunology, vol. 120, no. 3, pp. 260–271, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Lagaraine, R. Lemoine, C. Baron, H. Nivet, F. Velge-Roussel, and Y. Lebranchu, “Induction of human CD4+ regulatory T cells by mycophenolic acid-treated dendritic cells,” Journal of Leukocyte Biology, vol. 84, no. 4, pp. 1057–1064, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Penna and L. Adorini, “1α,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation,” Journal of Immunology, vol. 164, no. 5, pp. 2405–2411, 2000. View at Google Scholar · View at Scopus
  11. M. Naranjo-Gómez, D. Raïch-Regué, C. Oñate et al., “Comparative study of clinical grade human tolerogenic dendritic cells,” Journal of Translational Medicine, vol. 9, p. 89, 2011. View at Google Scholar · View at Scopus
  12. A. E. Pedersen, E. G. Schmidt, M. Gad, S. S. Poulsen, and M. H. Claesson, “Dexamethasone/1α-25-dihydroxyvitamin D3-treated dendritic cells suppress colitis in the SCID T-cell transfer model,” Immunology, vol. 127, no. 3, pp. 354–364, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. M. A. Boks, J. R. Kager-Groenland, M. S. Haasjes, J. J. Zwaginga, S. M. van Ham, and A. ten Brinke, “IL-10-generated tolerogenic dendritic cells are optimal for functional regulatory T cell induction—a comparative study of human clinical-applicable DC,” Clinical Immunology, vol. 142, no. 3, pp. 332–342, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Collin, N. McGovern, and M. Haniffa, “Human dendritic cell subsets,” Immunology, vol. 140, no. 1, pp. 22–30, 2013. View at Publisher · View at Google Scholar
  15. E. R. Mann, J. D. Landy, D. Bernardo et al., “Intestinal dendritic cells: their role in intestinal inflammation, manipulation by the gut microbiota and differences between mice and men,” Immunology Letters, vol. 150, pp. 30–40, 2013. View at Google Scholar
  16. J. L. Coombes, K. R. Siddiqui, C. V. Arancibia-Cárcamo et al., “A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β -and retinoic acid-dependent mechanism,” Journal of Experimental Medicine, vol. 204, no. 8, pp. 1757–1764, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. C. M. Sun, J. A. Hall, R. B. Blank et al., “Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid,” Journal of Experimental Medicine, vol. 204, no. 8, pp. 1775–1785, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Matteoli, E. Mazzini, I. D. Iliev et al., “Gut CD103+ dendritic cells express indoleamine 2,3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction,” Gut, vol. 59, no. 5, pp. 595–604, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Mahnke, E. Schmitt, L. Bonifaz, A. H. Enk, and H. Jonuleit, “Immature, but not inactive: the tolerogenic function of immature dendritic cells,” Immunology and Cell Biology, vol. 80, no. 5, pp. 477–483, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Cools, P. Ponsaerts, V. F. van Tendeloo, and Z. N. Berneman, “Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells,” Journal of Leukocyte Biology, vol. 82, no. 6, pp. 1365–1374, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Rutella and F. Locatelli, “Intestinal dendritic cells in the pathogenesis of inflammatory bowel disease,” World Journal of Gastroenterology, vol. 17, no. 33, pp. 3761–3775, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Perona-Wright, S. M. Anderton, S. E. Howie, and D. Gray, “IL-10 permits transient activation of dendritic cells to tolerize T cells and protect from central nervous system autoimmune disease,” International Immunology, vol. 19, no. 9, pp. 1123–1134, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Kuwana, J. Kaburaki, T. M. Wright, Y. Kawakami, and Y. Ikeda, “Induction of antigen-specific human CD4+ T cell anergy by peripheral blood DC2 precursors,” European Journal of Immunology, vol. 31, pp. 2547–2557, 2001. View at Google Scholar
  24. P. Allavena, L. Piemonti, D. Longoni et al., “IL-10 prevents the differentiation of monocytes to dendritic cells but promotes their maturation to macrophages,” European Journal of Immunology, vol. 28, pp. 359–369, 1998. View at Google Scholar
  25. E. O. Glocker, D. Kotlarz, K. Boztug et al., “Inflammatory bowel disease and mutations affecting the interleukin-10 receptor,” The New England Journal of Medicine, vol. 361, no. 21, pp. 2033–2045, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Huber, N. Gagliani, E. Esplugues et al., “Th17 cells express interleukin-10 receptor and are controlled by Foxp3- and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner,” Immunity, vol. 34, no. 4, pp. 554–565, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. B. M. Matta, A. Castellaneta, and A. W. Thomson, “Tolerogenic plasmacytoid DC,” European Journal of Immunology, vol. 40, no. 10, pp. 2667–2676, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Martín-Gayo, E. Sierra-Filardi, A. L. Corbí, and M. L. Toribio, “Plasmacytoid dendritic cells resident in human thymus drive natural Treg cell development,” Blood, vol. 115, no. 26, pp. 5366–5375, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Hanabuchi, N. Watanabe, Y.-H. Wang et al., “Human plasmacytoid predendritic cells activate NK cells through glucocorticoid-induced tumor necrosis factor receptor-ligand (GITRL),” Blood, vol. 107, no. 9, pp. 3617–3623, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Castellaneta, T. L. Sumpter, L. Chen, D. Tokita, and A. W. Thomson, “NOD2 ligation subverts IFN-α production by liver plasmacytoid dendritic cells and inhibits their T cell allostimulatory activity via B7-H1 Up-regulation,” Journal of Immunology, vol. 183, no. 11, pp. 6922–6932, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. D. C. Baumgart, D. Metzke, O. Guckelberger et al., “Aberrant plasmacytoid dendritic cell distribution and function in patients with Crohn's disease and ulcerative colitis,” Clinical and Experimental Immunology, vol. 166, no. 1, pp. 46–54, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. D. C. Baumgart, D. Metzke, J. Schmitz et al., “Patients with active inflammatory bowel disease lack immature peripheral blood plasmacytoid and myeloid dendritic cells,” Gut, vol. 54, no. 2, pp. 228–236, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Wendland, N. Czeloth, N. Mach et al., “CCR9 is a homing receptor for plasmacytoid dendritic cells to the small intestine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 15, pp. 6347–6352, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Hadeiba, T. Sato, A. Habtezion, C. Oderup, J. Pan, and E. C. Butcher, “CCR9 expression defines tolerogenic plasmacytoid dendritic cells able to suppress acute graft-versus-host disease,” Nature Immunology, vol. 9, no. 11, pp. 1253–1260, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. P. J. Mannon, F. Leon, I. J. Fuss et al., “Successful granulocyte-colony stimulating factor treatment of Crohn's disease is associated with the appearance of circulating interleukin-10- producing T cells and increased lamina propria plasmacytoid dendritic cells,” Clinical and Experimental Immunology, vol. 155, no. 3, pp. 447–456, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. A. E. Pedersen, M. Gad, N. N. Kristensen, C. Haase, C. H. Nielsen, and M. H. Claesson, “Tolerogenic dendritic cells pulsed with enterobacterial extract suppress development of colitis in the severe combined immunodeficiency transfer model,” Immunology, vol. 121, no. 4, pp. 526–532, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Yamanishi, H. Murakami, Y. Ikeda et al., “Regulatory dendritic cells pulsed with carbonic anhydrase I protect mice from colitis induced by CD4+CD25- T cells,” Journal of Immunology, vol. 188, no. 5, pp. 2164–2172, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Gonzalez-Rey and M. Delgado, “Therapeutic treatment of experimental colitis with regulatory dendritic cells generated with vasoactive intestinal peptide,” Gastroenterology, vol. 131, no. 6, pp. 1799–1811, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Sakuraba, T. Sato, N. Kamada, M. Kitazume, A. Sugita, and T. Hibi, “Th1/Th17 immune response is induced by mesenteric lymph node dendritic cells in crohn's disease,” Gastroenterology, vol. 137, no. 5, pp. 1736–1745, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. M. F. Neurath, “Animal models of inflammatory bowel diseases: illuminating the pathogenesis of colitis, ileitis and cancer,” Digestive Diseases, vol. 30, supplement 1, pp. 91–94, 2012. View at Google Scholar
  41. R. Cabezon, E. Ricart, C. Espana, J. Panes, and D. Benitez-Ribas, “Gram-negative enterobacteria induce tolerogenic maturation in dexamethasone conditioned dendritic cells,” PLoS One, vol. 7, Article ID e52456, 2012. View at Google Scholar
  42. A. E. Anderson, D. J. Swan, B. L. Sayers et al., “LPS activation is required for migratory activity and antigen presentation by tolerogenic dendritic cells,” Journal of Leukocyte Biology, vol. 85, no. 2, pp. 243–250, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Raïch-Regué, L. Grau-López, M. Naranjo-Gómez et al., “Stable antigen-specific T-cell hyporesponsiveness induced by tolerogenic dendritic cells from multiple sclerosis patients,” European Journal of Immunology, vol. 42, no. 3, pp. 771–782, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. R. A. Harry, A. E. Anderson, J. D. Isaacs, and C. M. Hilkens, “Generation and characterisation of therapeutic tolerogenic dendritic cells for rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 69, no. 11, pp. 2042–2050, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Vermeire and P. Rutgeerts, “Antibody responses in crohn's disease,” Gastroenterology, vol. 126, no. 2, pp. 601–604, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. T. W. Hand, L. M. Dos Santos, N. Bouladoux et al., “Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses,” Science, vol. 337, pp. 1553–1556, 2012. View at Publisher · View at Google Scholar
  47. Y. Belkaid, N. Bouladoux, and T. W. Hand, “Effector and memory T cell responses to commensal bacteria,” Trends in Immunology, vol. 34, pp. 299–306, 2013. View at Google Scholar