Differential capability of human cutaneous dendritic cell subsets to initiate Th17 responses

Journal of Immunology

Volumn 182, Issue 2, 2009, Pages 921-933

  Mathers, Alicia R ^a   Janelsins, Brian M ^a   Rubin, Joseph P ^a   Tkacheva, Olga A ^a   Shufesky, William J ^a   Watkins, Simon C ^a   Morelli, Adrian E ^a   Larregina, Adriana T ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 15; INTERLEUKIN 6; AUTACOID; INTERLEUKIN 17;

ARTICLE; CD4+ T LYMPHOCYTE; CELL FUNCTION; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; LANGERHANS CELL; LYMPHOCYTE DIFFERENTIATION; NORMAL HUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKIN; SKIN MIGRATORY LANGERHANS CELL; TH1 CELL; TH17 CELL; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL MOTION; COCULTURE; COMPARATIVE STUDY; CULTURE TECHNIQUE; HELPER CELL; IMMUNOLOGY; METABOLISM; MIXED LYMPHOCYTE CULTURE; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PHYSIOLOGY; SECRETION;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL MOVEMENT; COCULTURE TECHNIQUES; DENDRITIC CELLS; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-15; INTERLEUKIN-17; INTERLEUKIN-6; LANGERHANS CELLS; LYMPHOCYTE CULTURE TEST, MIXED; ORGAN CULTURE TECHNIQUES; SIGNAL TRANSDUCTION; SKIN; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS;

EID: 60549093645     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.2.921     Document Type: Article

References (62)

1. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
2. Larregina, A. T., and L. D. Falo, Jr. 2005. Changing paradigms in cutaneous immunology: adapting with dendritic cells. J. Invest. Dermatol. 124: 1-12.
3. Stockinger, B., and M. Veldhoen. 2007. Differentiation and function of Th17 T cells. Curr. Opin. Immunol. 19: 281-286.
4. H-17 cells in relapsing EAE. Nat. Immunol. 8: 172-180.
5. Kikly, K., L. Liu, S. Na, and J. D. Sedgwick. 2006. The IL-23/Th(17) axis: therapeutic targets for autoimmune inflammation. Curr. Opin. Immunol. 18: 670-675.
6. Li, J., X. Chen, Z. Liu, Q. Yue, and H. Liu. 2007. Expression of Th17 cytokines in skin lesions of patients with psoriasis. J. Huazhong Univ. Sci. Technolog. Med. Sci. 27: 330-332.
7. Röhn, T. A., G. T. Jennings, M. Hernandez, P. Grest, M. Beck, Y. Zou, M. Kopf, and M. F. Bachmann. 2006. Vaccination against IL-17 suppresses autoimmune arthritis and encephalomyelitis. Eur. J. Immunol. 36: 2857-2867.
8. Bettelli, E., T. Korn, M. Oukka, and V. K. Kuchroo. 2008. Induction and effector functions of TH17 cells. Nature 453: 1051-1057.
9. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
10. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-β induces development of the TH17 lineage. Nature 441: 231-234.
11. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189.
12. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132.
13. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141.
14. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8: 942-949.
15. Wilson, N. J., K. Boniface, J. R. Chan, B. S. McKenzie, W. M. Blumenschein, J. D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, et al. 2007. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8: 950-957.
16. Evans, H. G., T. Suddason, I. Jackson, L. S. Taams, and G. M. Lord. 2007. Optimal induction of T helper 17 cells in humans requires T cell receptor ligation in the context of Toll-like receptor-activated monocytes. Proc. Natl. Acad. Sci. USA 104: 17034-17039.
17. H-17 cells requires transforming growth factor-β and induction of the nuclear receptor RORγt. Nat. Immunol. 9: 641-649.
18. Yang, L., D. E. Anderson, C. Baecher-Allan, W. D. Hastings, E. Bettelli, M. Oukka, V. K. Kuchroo, and D. A. Hafler. 2008. IL-21 and TGF-β are required for differentiation of human TH17 cells. Nature 454: 350-352.
19. H-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8: 967-974.
20. Hoeve, M. A., N. D. L. Savage, T. de Boer, D. M. L. Langenberg, R. de Waal Malefyt, T. H. M. Ottenhoff, and F. A. W. Verreck. 2006. Divergent effects of IL-12 and IL-23 on the production of IL-17 by human T cells. Eur. J. Immunol. 36: 661-670.
21. + T cell responses elicited by different subsets of human skin migratory dendritic cells. J. Immunol. 175: 7905-7915.
22. + cells differentiate into Langerhans cells. Nat. Immunol. 2: 1151-1158.
23. Teunissen, M. B., C. W. Koomen, R. de Waal Malefyt, E. A. Wierenga, and J. D. Bos. 1998. Interleukin-17 and interferon-γ synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J. Invest. Dermatol. 111: 645-649.
24. van Beelen, A. J., M. B. Teunissen, M. L. Kapsenberg, and E. C. de Jong. 2007. Interleukin-17 in inflammatory skin disorders. Curr. Opin. Allergy Clin. Immunol. 7: 374-381.
25. Nestle, F. O., X. G. Zheng, C. B. Thompson, L. A. Turka, and B. J. Nickoloff. 1993. Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets [published erratum appears in 1994 J. Immunol. 152: 376.] J. Immunol. 151: 6535-6545.
26. Brand, C. U., R. E. Hunger, N. Yawalkar, H. A. Gerber, T. Schaffner, and L. R. Braathen. 1999. Characterization of human skin-derived CD1a-positive lymph cells. Arch. Dermatol. Res. 291: 65-72.
27. Morelli, A., A. Larregina, I. Chuluyan, E. Kolkowski, and L. Fainboim. 1996. Expression and modulation of C5a receptor (CD88) on skin dendritic cells: chemotactic effect of C5a on skin migratory dendritic cells. Immunology 89: 126-134.
28. Vogelsang, G. B., A. D. Hess, A. W. Berkman, P. J. Tutschka, E. R. Farmer, P. J. Converse, and G. W. Santos. 1985. An in vitro predictive test for graft versus host disease in patients with genotypic HLA-identical bone marrow transplants. N. Engl. J. Med. 313: 645-650.
29. Pope, M., M. G. Betjes, N. Romani, H. Hirmand, P. U. Cameron, L. Hoffman, S. Gezelter, G. Schuler, and R. M. Steinman. 1994. Conjugates of dendritic cells and memory T lymphocytes from skin facilitate productive infection with HIV-1. Cell 78: 389-398.
30. Richters, C. D., M. J. Hoekstra, J. van Baare, J. S. DuPont, E. C. Hoefsmit, and E. W. Kamperdijk. 1994. Isolation and characterization of migratory human skin dendritic cells. Clin. Exp. Immunol. 98: 330-336.
31. Larregina, A. T., A. E. Morelli, E. Kolkowski, N. Sanjuan, M. E. Barboza, and L. Fainboim. 1997. Pattern of cytokine receptors expressed by human dendritic cells migrated from dermal explants. Immunology 91: 303-313.
32. Dickinson, A. M., L. Sviland, P. Carey, M. M. Reid, P. J. Hamilton, A. J. Pearson, and S. J. Proctor. 1988. Skin explant culture as a model for cutaneous graft-versus-host disease in humans. Bone Marrow Transplant. 3: 323-329.
33. Dickinson, A. M., X. N. Wang, L. Sviland, F. A. Vyth-Dreese, G. H. Jackson, T. N. Schumacher, J. B. Haanen, T. Mutis, and E. Goulmy. 2002. In situ dissection of the graft-versus-host activities of cytotoxic T cells specific for minor histocompatibility antigens. Nat. Med. 8: 410-414.
34. Ebner, S., G. Ratzinger, B. Krosbacher, M. Schmuth, A. Weiss, D. Reider, R. A. Kroczek, M. Herold, C. Heufler, P. Fritsch, and N. Romani. 2001. Production of IL-12 by human monocyte-derived dendritic cells is optimal when the stimulus is given at the onset of maturation, and is further enhanced by IL-4. J. Immunol. 166: 633-641.
35. Zheng, Y., D. M. Danilenko, P. Valdez, I. Kasman, J. Eastham-Anderson, J. Wu, and W. Ouyang. 2007. Interleukin-22, a TH17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445: 648-651.
36. Kishimoto, T. 2006. Interleukin-6: discovery of a pleiotropic cytokine. Arthritis Res. Ther. 8(Suppl. 2): S2.
37. Lu, Z. Y., J. Brochier, J. Wijdenes, H. Brailly, R. Bataille, and B. Klein. 1992. High amounts of circulating interleukin (IL)-6 in the form of monomeric immune complexes during anti-IL-6 therapy: towards a new methodology for measuring overall cytokine production in human in vivo. Eur. J. Immunol. 22: 2819-2824.
38. Rose-John, S., J. Scheller, G. Elson, and S. A. Jones. 2006. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J. Leukocyte Biol. 80: 227-236.
39. + Treg development and function during allergic airway inflammation in vivo. J. Clin. Invest. 115: 313-325.
40. Munz, C., T. Dao, G. Ferlazzo, M. A. de Cos, K. Goodman, and J. W. Young. 2005. Mature myeloid dendritic cell subsets have distinct roles for activation and viability of circulating human natural killer cells. Blood 105: 266-273.
41. + hematopoietic progenitors stimulate greater cytolytic T lymphocyte activity in the absence of bioactive IL-12p70, by either single peptide presentation or cross-priming, than do dermal-interstitial or monocyte-derived dendritic cells. J. Immunol. 173: 2780-2791.
42. Elder, J. T. 2007. IL-15 and psoriasis: another genetic link to Th17? J. Invest. Dermatol. 127: 2495-2497.
43. Ziolkowska, M., A. Koc, G. Luszczykiewicz, K. Ksiezopolska-Pietrzak, E. Klimczak, H. Chwalinska-Sadowska, and W. Maslinski. 2000. High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism. J. Immunol. 164: 2832-2838.
44. Acosta-Rodriguez, E. V., L. Rivino, J. Geginat, D. Jarrossay, M. Gattorno, A. Lanzavecchia, F. Sallusto, and G. Napolitani. 2007. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8: 639-646.
45. Ebert, L. M., P. Schaerli, and B. Moser. 2005. Chemokine-mediated control of T cell traffic in lymphoid and peripheral tissues. Mol. Immunol. 42: 799-809.
46. Pope, M., M. G. Betjes, H. Hirmand, L. Hoffman, and R. M. Steinman. 1995. Both dendritic cells and memory T lymphocytes emigrate from organ cultures of human skin and form distinctive dendritic-T-cell conjugates. J. Invest. Dermatol. 104: 11-17.
47. Lukas, M., H. Stossel, L. Hefel, S. Imamura, P. Fritsch, N. T. Sepp, G. Schuler, and N. Romani. 1996. Human cutaneous dendritic cells migrate through dermal lymphatic vessels in a skin organ culture model. J. Invest. Dermatol. 106: 1293-1299.
48. + T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8: 369-377.
49. Zaba, L. C., J. Fuentes-Duculan, N. J. Eungdamrong, M. V. Abello, I. Novitskaya, K. C. Pierson, J. Gonzalez, J. G. Krueger, and M. A. Lowes. 2008. Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. J. Invest. Dermatol. In press.
50. Zaba, L. C., I. Cardinale, P. Gilleaudeau, M. Sullivan-Whalen, M. S. Farinas, J. Fuentes-Duculan, I. Novitskaya, A. Khatcherian, M. J. Bluth, M. A. Lowes, and J. G. Krueger. 2007. Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J. Exp. Med. 204: 3183-3194.
51. Lowes, M. A., T. Kikuchi, J. Fuentes-Duculan, I. Cardinale, L. C. Zaba, A. S. Haider, E. P. Bowman, and J. G. Krueger. 2008. Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J. Invest. Dermatol. 128: 1207-1211.
52. Happel, K. I., P. J. Dubin, M. Zheng, N. Ghilardi, C. Lockhart, L. J. Quinton, A. R. Odden, J. E. Shellito, G. J. Bagby, S. Nelson, and J. K. Kolls. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202: 761-769.
53. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
54. Lee, E., W. L. Trepicchio, J. L. Oestreicher, D. Pittman, F. Wang, F. Chamian, M. Dhodapkar, and J. G. Krueger. 2004. Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J. Exp. Med. 199: 125-130.
55. Vaknin-Dembinsky, A., K. Balashov, and H. L. Weiner. 2006. 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: 7768 -7774.
56. Waibler, Z., U. Kalinke, J. Will, M. H. S. Juan, J. M. Pfeilschifter, and H. H. Radeke. 2007. TLR-ligand stimulated interleukin-23 subunit expression and assembly is regulated differentially in murine plasmacytoid and myeloid dendritic cells. Mol. Immunol. 44: 1483-1489.
57. Zhao, X., E. Deak, K. Soderberg, M. Linehan, D. Spezzano, J. Zhu, D. M. Knipe, and A. Iwasaki. 2003. Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J. Exp. Med. 197: 153-162.
58. + dendritic cells but not by Langerhans cells. Science 301: 1925-1928.
59. Kissenpfennig, A., S. Henri, B. Dubois, C. Laplace-Builhe, P. Perrin, N. Romani, C. H. Tripp, P. Douillard, L. Leserman, D. Kaiserlian, et al. 2005. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22: 643-654.
60. Kaplan, D. H., M. C. Jenison, S. Saeland, W. D. Shlomchik, and M. J. Shlomchik. 2005. Epidermal Langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23: 611-620.
61. H17 cell differentiation. Nature 455: 808-812.
62. van der Aar, A. M. G., R. M. R. Sylva-Steenland, J. D. Bos, M. L. Kapsenberg, E. C. de Jong, and M. B. M. Teunissen. 2007. Cutting edge: Loss of TLR2, TLR4, and TLR5 on Langerhans cells abolishes bacterial recognition. J. Immunol. 178: 1986-1990.