Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis

Journal of Immunology

Volumn 182, Issue 9, 2009, Pages 5836-5845

  Van Der Fits, Leslie ^a   Mourits, Sabine ^a   Voerman, Jane S A ^a   Kant, Marius ^a   Boon, Louis ^b   Laman, Jon D ^a   Cornelissen, Ferry ^a   Mus, Anne Marie ^a   Florencia, Edwin ^a   Prens, Errol P ^a   Lubberts, Erik ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b BIOCEROS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN P 15095; IMIQUIMOD; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 17F; INTERLEUKIN 23; AMINOQUINOLINE DERIVATIVE; AUTACOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; DENDRITIC CELL; DERMATITIS; DISEASE MODEL; LYMPHOCYTIC INFILTRATION; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSORIASIS; SKIN ABSCESS; SKIN INFLAMMATION; TH17 CELL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL PROLIFERATION; CHEMICALLY INDUCED DISORDER; CONTACT DERMATITIS; DRUG EFFECT; GENETICS; HUMAN; IMMUNOLOGY; KERATINOCYTE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY;

AMINOQUINOLINES; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; DERMATITIS, CONTACT; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTERLEUKIN-23; KERATINOCYTES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PSORIASIS; RECEPTORS, INTERLEUKIN-17;

EID: 66949162673     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0802999     Document Type: Article

References (52)

1. Beutner, K. R., and S. Tyring. 1997. Human papillomavirus and human disease. Am. J. Med. 102: 9-15.
2. Szeimies, R. M., M. J. Gerritsen, G. Gupta, J. P. Ortonne, S. Serresi, J. Bichel, J. H. Lee, T. L. Fox, and A. Alomar. 2004. Imiquimod 5% cream for the treatment of actinic keratosis: results from a phase III, randomized, double-blind, vehicle-controlled, clinical trial with histology. J. Am. Acad. Dermatol. 51: 547-555.
3. Geisse, J. K., P. Rich, A. Pandya, K. Gross, K. Andres, A. Ginkel, and M. Owens. 2002. Imiquimod 5% cream for the treatment of superficial basal cell carcinoma: a double-blind, randomized, vehicle-controlled study. J. Am. Acad. Dermatol. 47: 390-398.
4. Gilliet, M., C. Conrad, M. Geiges, A. Cozzio, W. Thurlimann, G. Burg, F. O. Nestle, and R. Dummer. 2004. Psoriasis triggered by Toll-like receptor 7 agonist imiquimod in the presence of dermal plasmacytoid dendritic cell precursors. Arch. Dermatol. 140: 1490-1495. (Pubitemid 39627441)
5. Wu, J. K., G. Siller, and G. Strutton. 2004. Psoriasis induced by topical imiquimod. Australas. J. Dermatol. 45: 47-50.
6. Rajan, N., and J. A. Langtry. 2006. Generalized exacerbation of psoriasis associated with imiquimod cream treatment of superficial basal cell carcinomas. Clin. Exp. Dermatol. 31: 140-141.
7. Fanti, P. A., E. Dika, S. Vaccari, C. Miscial, and C. Varotti. 2006. Generalized psoriasis induced by topical treatment of actinic keratosis with imiquimod. Int. J. Dermatol. 45: 1464-1465. (Pubitemid 44869771)
8. Palamara, F., S. Meindl, M. Holcmann, P. Luhrs, G. Stingl, and M. Sibilia. 2004. Identification and characterization of pDC-like cells in normal mouse skin and melanomas treated with imiquimod. J. Immunol. 173: 3051-3061. (Pubitemid 39142011)
9. Schon, M. P., and M. Schon. 2007. Imiquimod: mode of action. Br. J. Dermatol. 157(Suppl. 2): 8-13.
10. Suzuki, H., B. Wang, G. M. Shivji, P. Toto, P. Amerio, M. A. Tomai, R. L. Miller, and D. N. Sauder. 2000. Imiquimod, a topical immune response modifier, induces migration of Langerhans cells. J. Invest. Dermatol. 114: 135-141. (Pubitemid 30195986)
11. Gibson, S. J., J. M. Lindh, T. R. Riter, R. M. Gleason, L. M. Rogers, A. E. Fuller, J. L. Oesterich, K. B. Gorden, X. Qiu, S. W. McKane, et al. 2002. Plasmacytoid dendritic cells produce cytokines and mature in response to the TLR7 agonists, imiquimod and resiquimod. Cell. Immunol. 218: 74-86.
12. Wagner, T. L., C. L. Ahonen, A. M. Couture, S. J. Gibson, R. L. Miller, R. M. Smith, M. J. Reiter, J. P. Vasilakos, and M. A. Tomai. 1999. Modulation of TH1 and TH2 cytokine production with the immune response modifiers, R-848 and imiquimod. Cell Immunol. 191: 10-19.
13. Fujisawa, H., G. M. Shivji, S. Kondo, B. Wang, M. A. Tomai, R. L. Miller, and D. N. Sauder. 1996. Effect of a novel topical immunomodulator, S-28463, on keratinocyte cytokine gene expression and production. J. Interferon Cytokine Res. 16: 555-559. (Pubitemid 26306958)
14. Kono, T., S. Kondo, S. Pastore, G. M. Shivji, M. A. Tomai, R. C. McKenzie, and D. N. Sauder. 1994. Effects of a novel topical immunomodulator, imiquimod, on keratinocyte cytokine gene expression. Lymphokine Cytokine Res. 13: 71-76. (Pubitemid 24136345)
15. Kollisch, G., B. N. Kalali, V. Voelcker, R. Wallich, H. Behrendt, J. Ring, S. Bauer, T. Jakob, M. Mempel, and M. Ollert. 2005. Various members of the Toll-like receptor family contribute to the innate immune response of human epidermal keratinocytes. Immunology 114: 531-541. (Pubitemid 40478147)
16. Lebre, M. C., A. M. van der Aar, L. van Baarsen, T. M. van Capel, J. H. Schuitemaker, M. L. Kapsenberg, and E. C. de Jong. 2007. Human keratinocytes express functional Toll-like receptor 3, 4, 5, and 9. J. Invest. Dermatol. 127: 331-341. (Pubitemid 46106911)
17. Schon, M. P., M. Schon, and K. N. Klotz. 2006. The small antitumoral immune response modifier imiquimod interacts with adenosine receptor signaling in a TLR7- and TLR8-independent fashion. J. Invest. Dermatol. 126: 1338-1347.
18. Boyman, O., H. P. Hefti, C. Conrad, B. J. Nickoloff, M. Suter, and F. O. Nestle. 2004. Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factor-α. J. Exp. Med. 199: 731-736. (Pubitemid 38316440)
19. Wrone-Smith, T., and B. J. Nickoloff. 1996. Dermal injection of immunocytes induces psoriasis. J. Clin. Invest. 98: 1878-1887. (Pubitemid 26359206)
20. 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. (Pubitemid 38076484)
21. Piskin, G., R. M. Sylva-Steenland, J. D. Bos, and M. B. Teunissen. 2006. In vitro and in situ expression of IL-23 by keratinocytes in healthy skin and psoriasis lesions: enhanced expression in psoriatic skin. J. Immunol. 176: 1908-1915. (Pubitemid 43134336)
22. 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.
23. Chan, J. R., W. Blumenschein, E. Murphy, C. Diveu, M. Wiekowski, S. Abbondanzo, L. Lucian, R. Geissler, S. Brodie, A. B. Kimball, et al. 2006. IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J. Exp. Med. 203: 2577-2587.
24. H17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445: 648-651.
25. Krueger, G. G., R. G. Langley, C. Leonardi, N. Yeilding, C. Guzzo, Y. Wang, L. T. Dooley, and M. Lebwohl. 2007. A human interleukin-12/23 monoclonal antibody for the treatment of psoriasis. N. Engl. J. Med. 356: 580-592. (Pubitemid 46220818)
26. Haider, A. S., M. A. Lowes, M. Suarez-Farinas, L. C. Zaba, I. Cardinale, A. Khatcherian, I. Novitskaya, K. M. Wittkowski, and J. G. Krueger. 2008. Identification of cellular pathways of "type 1," Th17 T cells, and TNF- and inducible nitric oxide synthase-producing dendritic cells in autoimmune inflammation through pharmacogenomic study of cyclosporine A in psoriasis. J. Immunol. 180: 1913-1920.
27. Zaba, L. C., I. Cardinale, P. Gilleaudeau, M. Sullivan-Whalen, F. M. Suarez, 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.
28. Bos, J. D. 2007. Psoriasis, innate immunity, and gene pools. J. Am. Acad. Dermatol. 56: 468-471.
29. Hollox, E. J., U. Huffmeier, P. L. Zeeuwen, R. Palla, J. Lascorz, D. Rodijk-Olthuis, P. C. van de Kerkhof, H. Traupe, G. de Jongh, M. den Heijer, et al. 2008. Psoriasis is associated with increased β-defensin genomic copy number. Nat. Genet. 40: 23-25.
30. Ghilardi, N., N. Kljavin, Q. Chen, S. Lucas, A. L. Gurney, and F. J. de Sauvage. 2004. Compromised humoral and delayed-type hypersensitivity responses in IL-23-deficient mice. J. Immunol. 172: 2827-2833. (Pubitemid 38263667)
31. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194: 519-527. (Pubitemid 32835046)
32. Wils, E. J., E. Braakman, G. M. Verjans, E. J. Rombouts, A. E. Broers, H. G. Niesters, G. Wagemaker, F. J. Staal, B. Lowenberg, H. Spits, and J. J. Cornelissen. 2007. Flt3 ligand expands lymphoid progenitors prior to recovery of thymopoiesis and accelerates T cell reconstitution after bone marrow transplantation. J. Immunol. 178: 3551-3557.
33. Mysliwietz, J., and S. Thierfelder. 1992. Antilymphocytic antibodies and marrow transplantation: XII. Suppression of graft-versus-host disease by T-cell-modulating and depleting antimouse CD3 antibody is most effective when preinjected in the marrow recipient. Blood 80: 2661-2667.
34. van der Fits, L., L. I. van der Wel, J. D. Laman, E. P. Prens, and M. C. Verschuren. 2004. In psoriasis lesional skin the type I interferon signaling pathway is activated, whereas interferon-α sensitivity is unaltered. J. Invest. Dermatol. 122: 51-60.
35. Asselin-Paturel, C., G. Brizard, J. J. Pin, F. Briere, and G. Trinchieri. 2003. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J. Immunol. 171: 6466-6477. (Pubitemid 37532075)
36. Gudjonsson, J. E., A. Johnston, H. Sigmundsdottir, and H. Valdimarsson. 2004. Immunopathogenic mechanisms in psoriasis. Clin. Exp. Immunol. 135: 1-8.
37. 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. (Pubitemid 43214587)
38. Steinman, L. 2008. A rush to judgment on Th17. J. Exp. Med. 205: 1517-1522.
39. Nakae, S., S. Saijo, R. Horai, K. Sudo, S. Mori, and Y. Iwakura. 2003. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc. Natl. Acad. Sci. USA 100: 5986-5990. (Pubitemid 36576918)
40. + Th cells that cause autoimmune arthritis. J. Exp. Med. 204: 41-47.
41. Schon, M. P. 1999. Animal models of psoriasis: what can we learn from them? J. Invest. Dermatol. 112: 405-410. (Pubitemid 29171927)
42. Gudjonsson, J. E., A. Johnston, M. Dyson, H. Valdimarsson, and J. T. Elder. 2007. Mouse models of psoriasis. J. Invest. Dermatol. 127: 1292-1308.
43. Mizutani, H., K. Yamanaka, H. Konishi, and T. Murakami. 2003. Animal models of psoriasis and pustular psoriasis. Arch. Dermatol. Res. 295(Suppl. 1): 67-68.
44. Nestle, F. O., and B. J. Nickoloff. 2006. Animal models of psoriasis: a brief update. J. Eur. Acad. Dermatol. Venereol. 20(Suppl. 2): 24-27. (Pubitemid 44615007)
45. Roark, C. L., J. D. French, M. A. Taylor, A. M. Bendele, W. K. Born, and R. L. O'Brien. 2007. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing γδ T cells. J. Immunol. 179: 5576-5583.
46. Jameson, J., and W. L. Havran. 2007. Skin γδ T-cell functions in homeostasis and wound healing. Immunol. Rev. 215: 114-122. (Pubitemid 46212234)
47. Nickoloff, B. J., B. K. Bonish, D. J. Marble, K. A. Schriedel, L. A. DiPietro, K. B. Gordon, and M. W. Lingen. 2006. Lessons learned from psoriatic plaques concerning mechanisms of tissue repair, remodeling, and inflammation. J. Investig. Dermatol. Symp. Proc. 11: 16-29.
48. Holtmeier, W., M. Pfander, A. Hennemann, T. M. Zollner, R. Kaufmann, and W. F. Caspary. 2001. The TCR-δ repertoire in normal human skin is restricted and distinct from the TCR-δ repertoire in the peripheral blood. J. Invest. Dermatol. 116: 275-280. (Pubitemid 32173732)
49. Stratis, A., M. Pasparakis, R. A. Rupec, D. Markur, K. Hartmann, K. Scharffetter-Kochanek, T. Peters, N. van Rooijen, T. Krieg, and I. Haase. 2006. Pathogenic role for skin macrophages in a mouse model of keratinocyte-induced psoriasis-like skin inflammation. J. Clin. Invest. 116: 2094-2104. (Pubitemid 44162318)
50. Wang, H., T. Peters, D. Kess, A. Sindrilaru, T. Oreshkova, N. van Rooijen, A. Stratis, A. C. Renkl, C. Sunderkotter, M. Wlaschek, et al. 2006. Activated macrophages are essential in a murine model for T cell-mediated chronic psoriasiform skin inflammation. J. Clin. Invest. 116: 2105-2114. (Pubitemid 44162319)
51. Nestle, F. O., C. Conrad, A. Tun-Kyi, B. Homey, M. Gombert, O. Boyman, G. Burg, Y. J. Liu, and M. Gilliet. 2005. Plasmacytoid predendritic cells initiate psoriasis through interferon-α production. J. Exp. Med. 202: 135-143.
52. Bennett, C. L., and B. E. Clausen. 2007. DC ablation in mice: promises, pitfalls, and challenges. Trends Immunol. 28: 525-531.