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Journal of Allergy
Volume 2012 (2012), Article ID 718725, 10 pages
http://dx.doi.org/10.1155/2012/718725
Review Article

Keratinocytes under Fire of Proinflammatory Cytokines: Bona Fide Innate Immune Cells Involved in the Physiopathology of Chronic Atopic Dermatitis and Psoriasis

1Laboratoire Inflammation, Tissus Épithéliaux et Cytokines, UPRES-EA 4331, CHU de Poitiers, Pole Biologie Santé, Université de Poitiers, Bâtiment B36, 1 rue G Bonnet, 86022 Poitiers, France
2BIOalternatives, 1 bis rue des Plantes, 86160 Gençay, France

Received 15 June 2012; Revised 5 October 2012; Accepted 5 October 2012

Academic Editor: Maria Leite-de-Moraes

Copyright © 2012 François-Xavier Bernard et al. 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. P. Di Meglio, K. Gayathri Perera, and F. O. Nestle, “The multitasking organ: recent insights into skin immune function,” Immunity, vol. 35, no. 6, pp. 857–869, 2011. View at Publisher · View at Google Scholar
  2. E. Guttman-Yassky, K. E. Nograles, and J. G. Krueger, “Contrasting pathogenesis of atopic dermatitis and psoriasis-part II: immune cell subsets and therapeutic concepts,” Journal of Allergy and Clinical Immunology, vol. 127, no. 6, pp. 1420–1432, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. E. Guttman-Yassky, K. E. Nograles, and J. G. Krueger, “Contrasting pathogenesis of atopic dermatitis and psoriasis-part I: clinical and pathologic concepts,” Journal of Allergy and Clinical Immunology, vol. 127, no. 5, pp. 1110–1118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. C. N. A. Palmer, A. D. Irvine, A. Terron-Kwiatkowski et al., “Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis,” Nature Genetics, vol. 38, no. 4, pp. 441–446, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Lecron, F. Morel, and K. Boniface, “Keratinocytes as targets for cytokines in skin inflammation,” in Recent Advances in Skin Immunology, S. Saeland, Ed., p. 46, Kerala, Kerala, India, 2008.
  6. K. Boniface, F. X. Bernard, M. Garcia, A. L. Gurney, J. C. Lecron, and F. Morel, “IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes,” Journal of Immunology, vol. 174, no. 6, pp. 3695–3702, 2005. View at Scopus
  7. K. Boniface, C. Diveu, F. Morel et al., “Oncostatin M secreted by skin infiltrating T lymphocytes is a potent keratinocyte activator involved in skin inflammation,” Journal of Immunology, vol. 178, no. 7, pp. 4615–4622, 2007. View at Scopus
  8. N. J. Wilson, K. Boniface, J. R. Chan et al., “Development, cytokine profile and function of human interleukin 17-producing helper T cells,” Nature Immunology, vol. 8, no. 9, pp. 950–957, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Caruso, E. Botti, M. Sarra et al., “Involvement of interleukin-21 in the epidermal hyperplasia of psoriasis,” Nature Medicine, vol. 15, no. 9, pp. 1013–1015, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Wittmann, R. Purwar, C. Hartmann, R. Gutzmer, and T. Werfel, “Human keratinocytes respond to interleukin-18: implication for the course of chronic inflammatory skin diseases,” Journal of Investigative Dermatology, vol. 124, no. 6, pp. 1225–1233, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Boniface, J. C. Lecron, F. X. Bernard et al., “Keratinocytes as targets for interleukin-10-related cytokines: a putative role in the pathogenesis of psoriasis,” European Cytokine Network, vol. 16, no. 4, pp. 309–319, 2005. View at Scopus
  12. S. M. Sa, P. A. Valdez, J. Wu et al., “The effects of IL-20 subfamily cytokines on reconstituted human epidermis suggest potential roles in cutaneous innate defense and pathogenic adaptive immunity in psoriasis,” Journal of Immunology, vol. 178, no. 11, pp. 2229–2240, 2007. View at Scopus
  13. R. Caruso, E. Botti, M. Sarra et al., “Involvement of interleukin-21 in the epidermal hyperplasia of psoriasis,” Nature Medicine, vol. 15, no. 9, pp. 1013–1015, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Guilloteau, I. Paris, N. Pedretti et al., “Skin inflammation induced by the synergistic action of IL-17A, IL-22, oncostatin M, IL-1α, and TNF-α recapitulates some features of psoriasis,” Journal of Immunology, vol. 184, no. 9, pp. 5263–5270, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Carrier, H. L. Ma, H. E. Ramon et al., “Inter-regulation of Th17 cytokines and the IL-36 cytokines in vitro and in vivo: implications in psoriasis pathogenesis,” Journal of Investigative Dermatology, vol. 131, pp. 2428–2437, 2011. View at Publisher · View at Google Scholar
  16. M. C. Lebre, A. M. G. Van Der Aar, L. Van Baarsen et al., “Human keratinocytes express functional toll-like receptor 3, 4, 5, and 9,” Journal of Investigative Dermatology, vol. 127, no. 2, pp. 331–341, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. L. S. Miller, “Toll-like receptors in skin,” Advances in Dermatology C, vol. 24, pp. 71–87, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Kinoshita, T. Takai, T. Anh Le et al., “Cytokine milieu modulates release of thymic stromal lymphopoietin from human keratinocytes stimulated with double-stranded RNA,” Journal of Allergy and Clinical Immunology, vol. 123, no. 1, pp. 179–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. K. E. Nograles, L. C. Zaba, E. Guttman-Yassky et al., “Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways,” British Journal of Dermatology, vol. 159, no. 5, pp. 1092–1102, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. B. M. Teunissen, C. W. Koomen, R. De Waal Malefyt, E. A. Wierenga, and J. D. Bos, “Interleukin-17 and interferon-γ synergize in the enhancement of proinflammatory cytokine production by human keratinocytes,” Journal of Investigative Dermatology, vol. 111, no. 4, pp. 645–649, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Albanesi, A. Cavani, and G. Girolomoni, “IL-17 is produced by nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocytes: synergistic or antagonist effects with IFN-γ and TNF-α,” Journal of Immunology, vol. 162, no. 1, pp. 494–502, 1999. View at Scopus
  22. S. C. Liang, X. Y. Tan, D. P. Luxenberg et al., “Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides,” Journal of Experimental Medicine, vol. 203, no. 10, pp. 2271–2279, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Ghannam, C. Dejou, N. Pedretti et al., “CCL20 and β-defensin-2 induce arrest of human Th17 cells on inflamed endothelium in vitro under flow conditions,” Journal of Immunology, vol. 186, no. 3, pp. 1411–1420, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Purwar, T. Werfel, and M. Wittmann, “IL-13-stimulated human keratinocytes preferentially attract CD4+ CCR4+ T cells: possible role in atopic dermatitis,” Journal of Investigative Dermatology, vol. 126, no. 5, pp. 1043–1051, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Albanesi, H. R. Fairchild, S. Madonna et al., “IL-4 and IL-13 negatively regulate TNF-β- and IFN-γ-induced β-defensin expression through STAT-6, suppressor of cytokine signaling (SOCS)-1, and SOCS-3,” Journal of Immunology, vol. 179, no. 2, pp. 984–992, 2007. View at Scopus
  26. I. Nomura, E. Goleva, M. D. Howell et al., “Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes,” Journal of Immunology, vol. 171, no. 6, pp. 3262–3269, 2003. View at Scopus
  27. P. Y. Ong, T. Ohtake, C. Brandt et al., “Endogenous antimicrobial peptides and skin infections in atopic dermatitis,” New England Journal of Medicine, vol. 347, no. 15, pp. 1151–1160, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. S. I. Bogiatzi, I. Fernandez, J. C. Bichet et al., “Cutting edge: proinflammatory and Th2 cytokines synergize to induce thymic stromal lymphopoietin production by human skin keratinocytes,” Journal of Immunology, vol. 178, no. 6, pp. 3373–3377, 2007. View at Scopus
  29. M. David, D. Ford, J. Bertoglio, A. L. Maizel, and J. Pierre, “Induction of the IL-13 receptor α2-chain by IL-4 and IL-13 in human keratinocytes: involvement of STAT6, ERK and p38 MAPK pathways,” Oncogene, vol. 20, no. 46, pp. 6660–6668, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Wongpiyabovorn, H. Suto, H. Ushio et al., “Up-regulation of interleukin-13 receptor α1 on human keratinocytes in the skin of psoriasis and atopic dermatitis,” Journal of Dermatological Science, vol. 33, no. 1, pp. 31–40, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. M. A. Farrar and R. D. Schreiber, “The molecular cell biology of interferon-γ and its receptor,” Annual Review of Immunology, vol. 11, pp. 571–611, 1993. View at Scopus
  32. I. Nomura, B. Gao, M. Boguniewicz, M. A. Darst, J. B. Travers, and D. Y. M. Leung, “Distinct patterns of gene expression in the skin lesions of atopic dermatitis and psoriasis: a gene microarray analysis,” Journal of Allergy and Clinical Immunology, vol. 112, no. 6, pp. 1195–1202, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Uyemura, M. Yamamura, D. F. Fivenson, R. L. Modlin, and B. J. Nickoloff, “The cytokine network in lesional and lesion-free psoriatic skin is characterized by a T-helper Type 1 cell-mediated response,” Journal of Investigative Dermatology, vol. 101, no. 5, pp. 701–705, 1993. View at Scopus
  34. A. Szegedi, M. Aleksza, A. Gonda et al., “Elevated rate of Thelper1 (TH1) lymphocytes and serum IFN-γ levels in psoriatic patients,” Immunology Letters, vol. 86, no. 3, pp. 277–280, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. L. M. Austin, M. Ozawa, T. Kikuchi, I. B. Walters, and J. G. Krueger, “The majority of epidermal T cells in psoriasis vulgaris lesions can produce type 1 cytokines, interferon-γ, interleukin-2, and tumor necrosis factor-α, defining TC1 (cytotoxic T lymphocyte) and TH1 effector populations: a type 1 differentiation bias is also measured in circulating blood T cells in psoriatic patients,” Journal of Investigative Dermatology, vol. 113, no. 5, pp. 752–759, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. W. L. Trepicchio, M. Ozawa, I. B. Walters et al., “Interleukin-11 therapy selectively downregulates type I cytokine proinflammatory pathways in psoriasis lesions,” Journal of Clinical Investigation, vol. 104, no. 11, pp. 1527–1537, 1999. View at Scopus
  37. K. Wolk, E. Witte, E. Wallace et al., “IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis,” European Journal of Immunology, vol. 36, no. 5, pp. 1309–1323, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Grewe, C. A. F. M. Bruijnzeel-Koomen, E. Schöpf et al., “A role for Th1 and Th2 cells in the immunopathogenesis of atopic dermatitis,” Immunology Today, vol. 19, no. 8, pp. 359–361, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. R. W. Groves, H. Mizutani, J. D. Kieffer, and T. S. Kupper, “Inflammatory skin disease in transgenic mice that express high levels of interleukin 1α in basal epidermis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 25, pp. 11874–11878, 1995. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Shepherd, M. C. Little, and M. J. H. Nicklin, “Psoriasis-like cutaneous inflammation in mice lacking interleukin-1 receptor antagonist,” Journal of Investigative Dermatology, vol. 122, no. 3, pp. 665–669, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Kondo and D. N. Sauder, “Tumor necrosis factor (TNF) receptor type 1 (p55) is a main mediator for TNF-α-induced skin inflammation,” European Journal of Immunology, vol. 27, no. 7, pp. 1713–1718, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Harder, J. Bartels, E. Christophers, and J. M. Schröder, “Isolation and characterization of human β-defensin-3, a novel human inducible peptide antibiotic,” Journal of Biological Chemistry, vol. 276, no. 8, pp. 5707–5713, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Ettehadi, M. W. Greaves, D. Wallach, D. Aderka, and R. D. R. Camp, “Elevated tumour necrosis factor-alpha (TNF-α) biological activity in psoriatic skin lesions,” Clinical and Experimental Immunology, vol. 96, no. 1, pp. 146–151, 1994. View at Scopus
  44. C. J. Oh, K. M. Das, and A. B. Gottlieb, “Treatment with anti-tumor necrosis factor α (TNF-α) monoclonal antibody dramatically decreases the clinical activity of psoriasis lesions,” Journal of the American Academy of Dermatology, vol. 42, no. 5, pp. 829–830, 2000. View at Scopus
  45. U. Chaudhari, P. Romano, L. D. Mulcahy, L. T. Dooley, D. G. Baker, and A. B. Gottlieb, “Efficacy and safety of infliximab monotherapy for plaque-type psoriasis: a randomised trial,” The Lancet, vol. 357, no. 9271, pp. 1842–1847, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. C. L. Leonardi, J. L. Powers, R. T. Matheson et al., “Etanercept as monotherapy in patients with psoriasis,” New England Journal of Medicine, vol. 349, no. 21, pp. 2014–2022, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Jacobi, C. Antoni, B. Manger, G. Schuler, and M. Hertl, “Infliximab in the treatment of moderate to severe atopic dermatitis.,” Journal of the American Academy of Dermatology, vol. 52, no. 3, pp. 522–526, 2005. View at Scopus
  48. C. Koga, K. Kabashima, N. Shiraishi, M. Kobayashi, and Y. Tokura, “Possible pathogenic role of Th17 cells for atopic dermatitis,” Journal of Investigative Dermatology, vol. 128, no. 11, pp. 2625–2630, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Toda, D. Y. M. Leung, S. Molet et al., “Polarized in vivo expression of IL-11 and IL-17 between acute and chronic skin lesions,” Journal of Allergy and Clinical Immunology, vol. 111, no. 4, pp. 875–881, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. K. E. Nograles, M. Suárez-Fariñas, A. Shemer et al., “Atopic dermatitis keratinocytes exhibit normal TH17 cytokine responses,” Journal of Allergy and Clinical Immunology, vol. 125, no. 3, pp. 744–e2, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. J. R. Chan, W. Blumenschein, E. Murphy et al., “IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis,” Journal of Experimental Medicine, vol. 203, no. 12, pp. 2577–2587, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Piskin, R. M. R. Sylva-Steenland, J. D. Bos, and M. B. M. Teunissen, “In vitro and in situ expression of IL-23 by keratinocytes in healthy skin and psoriasis lesions: enhanced expression in psoriatic skin,” Journal of Immunology, vol. 176, no. 3, pp. 1908–1915, 2006. View at Scopus
  53. E. Lee, W. L. Trepicchio, J. L. Oestreicher et al., “Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris,” Journal of Experimental Medicine, vol. 199, no. 1, pp. 125–130, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. A. M. Bowcock and J. G. Krueger, “Getting under the skin: the immunogenetics of psoriasis,” Nature Reviews Immunology, vol. 5, no. 9, pp. 699–711, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Boniface, E. Guignouard, N. Pedretti et al., “A role for T cell-derived interleukin 22 in psoriatic skin inflammation,” Clinical and Experimental Immunology, vol. 150, no. 3, pp. 407–415, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. M. A. Lowes, T. Kikuchi, J. Fuentes-Duculan et al., “Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells,” Journal of Investigative Dermatology, vol. 128, no. 5, pp. 1207–1211, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Pène, S. Chevalier, L. Preisser et al., “Chronically inflamed human tissues are infiltrated by highly differentiated Th17 lymphocytes,” Journal of Immunology, vol. 180, no. 11, pp. 7423–7430, 2008. View at Scopus
  58. E. E. Gray, K. Suzuki, and J. G. Cyster, “Cutting edge: identification of a motile IL-17-producing γδ T cell population in the dermis,” Journal of Immunology, vol. 186, no. 11, pp. 6091–6095, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Cai, X. Shen, C. Ding et al., “Pivotal role of dermal IL-17-producing gammadelta T cells in skin inflammation,” Immunity, vol. 35, no. 4, pp. 596–610, 2011. View at Publisher · View at Google Scholar
  60. M. L. Michel, A. C. Keller, C. Paget et al., “Identification of an IL-17-producing NK1.1neg iNKT cell population involved in airway neutrophilia,” Journal of Experimental Medicine, vol. 204, no. 5, pp. 995–1001, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. J. M. Doisne, C. Becourt, L. Amniai et al., “Skin and peripheral lymph node invariant NKT cells are mainly retinoic acid receptor-related orphan receptor γt+and respond preferentially under inflammatory conditions,” Journal of Immunology, vol. 183, no. 3, pp. 2142–2149, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. K. E. Nograles, L. C. Zaba, E. Guttman-Yassky et al., “Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways,” British Journal of Dermatology, vol. 159, no. 5, pp. 1092–1102, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Trifari, C. D. Kaplan, E. H. Tran, N. K. Crellin, and H. Spits, “Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from TH-17, TH1 and TH2 cells,” Nature Immunology, vol. 10, no. 8, pp. 864–871, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Duhen, R. Geiger, D. Jarrossay, A. Lanzavecchia, and F. Sallusto, “Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells,” Nature Immunology, vol. 10, no. 8, pp. 857–863, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Eyerich, K. Eyerich, D. Pennino et al., “Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling,” Journal of Clinical Investigation, vol. 119, no. 12, pp. 3573–3585, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. K. E. Nograles, L. C. Zaba, A. Shemer et al., “IL-22-producing "T22" T cells account for upregulated IL-22 in atopic dermatitis despite reduced IL-17-producing TH17 T cells,” Journal of Allergy and Clinical Immunology, vol. 123, no. 6, pp. 1244–e2, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Fujita, K. E. Nograles, T. Kikuchi, J. Gonzalez, J. A. Carucci, and J. G. Krueger, “Human Langerhans cells induce distinct IL-22-producing CD4+ T cells lacking IL-17 production,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 51, pp. 21795–21800, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. P. C. M. Res, G. Piskin, O. J. de Boer et al., “Overrepresentation of IL-17A and IL-22 Producing CD8 T Cells in Lesional Skin Suggests Their Involvement in the pathogenesis of psoriasis,” PLoS ONE, vol. 5, no. 11, Article ID e14108, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. A. B. Van Belle, M. de Heusch, M. M. Lemaire et al., “IL-22 is required for imiquimod-induced psoriasiform skin inflammation in mice,” Journal of Immunology, vol. 188, no. 1, pp. 462–469, 2012. View at Publisher · View at Google Scholar
  70. S. Eyerich, A. T. Onken, S. Weidinger et al., “Mutual antagonism of T cells causing psoriasis and atopic eczema,” New England Journal of Medicine, vol. 365, no. 3, pp. 231–238, 2011. View at Scopus
  71. M. Rosdy, B. Bertino, V. Butet, S. Gibbs, M. Ponec, and M. Darmon, “Retinoic Acid inhibits epidermal differentiation when applied topically on the stratum corneum of epidermis formed in vitro by human keratinocytes grown on defined medium,” In Vitro and Molecular Toxicology, vol. 10, no. 1, pp. 39–47, 1997. View at Scopus