IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis

Journal of Experimental Medicine

Volumn 203, Issue 12, 2006, Pages 2577-2587

  Chan, Jason R ^a   Blumenschein, Wendy ^b   Murphy, Erin ^b   Diveu, Caroline ^a   Wiekowski, Maria ^c   Abbondanzo, Susan ^c   Lucian, Linda ^a   Geissler, Richard ^c   Brodie, Scott ^c   Kimball, Alexa B ^d,e   Gorman, Daniel M ^b   Smith, Kathleen ^b   Malefyt, Rene De Waal ^a   Kastelein, Robert A ^a   McClanahan, Terrill K ^b   Bowman, Edward P ^a  

^a Discovery Research   (United States)

^b Experimental Pathology and Pharmacology   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 19; INTERLEUKIN 20; INTERLEUKIN 23; INTERLEUKIN 24; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EPIDERMIS HYPERPLASIA; ERYTHEMA; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MOUSE; NONHUMAN; PARAKERATOSIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSORIASIS;

ANIMALS; EPIDERMIS; HUMANS; HYPERPLASIA; INTERLEUKIN-23; MICE; MICE, KNOCKOUT; PSORIASIS; RECEPTORS, INTERLEUKIN; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33751546237     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20060244     Document Type: Article

References (52)

1. Schon, M.P., and W.H. Boehncke. 2005. Psoriasis. N. Engl. J. Med. 352:1899-1912.
2. Nickoloff, B.J., and F.O. Nestle. 2004. Recent insights into the immunopathogenesis of psoriasis provide new therapeutic opportunities. J. Clin. Invest. 113:1664-1675.
3. Bos, J.D., M.A. de Rie, M.B. Teunissen, and G. Piskin. 2005. Psoriasis: dysregulation of innate immunity. Br. J. Dermatol. 152:1098-1107.
4. 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.
5. Nickoloff, B.J., B. Bonish, B.B. Huang, and S.A. Porcelli. 2000. Characterization of a T cell line bearing natural killer receptors and capable of creating psoriasis in a SCID mouse model system. J. Dermatol. Sci. 24:212-225.
6. Boyman, O., C. Conrad, C. Dudli, E. Kielhorn, B.J. Nickoloff, and F.O. Nestle. 2005. Activation of dendritic antigen-presenting cells expressing common heat shock protein receptor CD91 during induction of psoriasis. Br. J. Dermatol. 152:1211-1218.
7. Nickoloff, B.J. 1991. The cytokine network in psoriasis. Arch. Dermatol. 127:871-884.
8. Ghoreschi, K., P. Thomas, S. Breit, M. Dugas, R. Mailhammer, W. van Eden, R. van der Zee, T. Biedermann, J. Prinz, M. Mack, et al. 2003. Interleukin-4 therapy of psoriasis induces Th2 responses and improves human autoimmune disease. Nat. Med. 9:40-46.
9. Romer, J., E. Hasselager, P.L. Norby, T. Steiniche, J. Thorn Clausen, and K. Kragballe. 2003. Epidermal overexpression of interleukin-19 and -20 mRNA in psoriatic skin disappears after short-term treatment with cyclosporine a or calcipotriol. J. Invest. Dermatol. 121:1306-1311.
10. Oppmann, B., R. Lesley, B. Blom, J.C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity. 13:715-725.
11. Parham, C., M. Chirica, J. Timans, E. Vaisberg, M. Travis, J. Cheung, S. Pflanz, R. Zhang, K.P. Singh, F. Vega, et al. 2002. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J. Immunol. 168:5699-5708.
12. Presky, D.H., H. Yang, L.J. Minetti, A.O. Chua, N. Nabavi, C.Y. Wu, M.K. Gately, and U. Gubler. 1996. A functional interleukin 12 receptor complex is composed of two beta-type cytokine receptor subunits. Proc. Natl. Acad. Sci. USA. 93:14002-14007.
13. Murphy, C.A., C.L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R.A. Kastelein, J.D. Sedgwick, and D.J. Cua. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198:1951-1957.
14. Cua, D.J., J. Sherlock, Y. Chen, C.A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 421:744-748.
15. Kopp, T., P. Lenz, C. Bello-Fernandez, R.A. Kastelein, T.S. Kupper, and G. Stingl. 2003. IL-23 production by cosecretion of endogenous p19 and transgenic p40 in keratin 14/p40 transgenic mice: evidence for enhanced cutaneous immunity. J. Immunol. 170:5438-5444.
16. Wiekowski, M.T., M.W. Leach, E.W. Evans, L. Sullivan, S.C. Chen, G. Vassileva, J.F. Bazan, D.M. Gorman, R.A. Kastelein, S. Narula, and S.A. Lira. 2001. Ubiquitous transgenic expression of the IL-23 subunit p19 induces multiorgan inflammation, runting, infertility, and premature death. J. Immunol. 166:7563-7570.
17. Fedele, G., P. Stefanelli, F. Spensieri, C. Fazio, P. Mastrantonio, and C.M. Ausiello. 2005. Bordetella pertussis-infected human monocyte-derived dendritic cells undergo maturation and induce Th1 polarization and interleukin-23 expression. Infect. Immun. 73:1590-1597.
18. Verreck, F.A., T. de Boer, D.M. Langenberg, M.A. Hoeve, M. Kramer, E. Vaisberg, R. Kastelein, A. Kolk, R. de Waal-Malefyt, and T.H. Ottenhoff. 2004. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc. Natl. Acad. Sci. USA. 101:4560-4565.
19. Veckman, V., M. Miettinen, J. Pirhonen, J. Siren, S. Matikainen, and I. Julkunen. 2004. Streptococcus pyogenes and Lactobacillus rhamnosus differentially induce maturation and production of Th1-type cytokines and chemokines in human monocyte-derived dendritic cells. J. Leukoc. Biol. 75:764-771.
20. Happel, K.I., M. Zheng, E. Young, L.J. Quinton, E. Lockhart, A.J. Ramsay, J.E. Shellito, J.R. Schurr, G.J. Bagby, S. Nelson, and J.K. Kolls. 2003. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J. Immunol. 170:4432-4436.
21. 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.
22. Jamieson, T., D.N. Cook, R.J. Nibbs, A. Rot, C. Nixon, P. McLean, A. Alcami, S.A. Lira, M. Wiekowski, and G.J. Graham. 2005. The chemokine receptor D6 limits the inflammatory response in vivo. Nat. Immunol. 6:403-411.
23. 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.
24. Koenders, M.I., J.K. Kolls, B. Oppers-Walgreen, L. van den Bersselaar, L.A. Joosten, J.R. Schurr, P. Schwarzenberger, W.B. van den Berg, and E. Lubberts. 2005. Interleukin-17 receptor deficiency results in impaired synovial expression of interleukin-1 and matrix metalloproteinases 3, 9, and 13 and prevents cartilage destruction during chronic reactivated streptococcal cell wall-induced arthritis. Arthritis Rheum. 52:3239-3247.
25. Fossiez, F., O. Djossou, P. Chomarat, L. Flores-Romo, S. Ait-Yahia, C. Maat, J.J. Pin, P. Garrone, E. Garcia, S. Saeland, et al. 1996. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J. Exp. Med. 183:2593-2603.
26. Chen, Y., C.L. Langrish, B. McKenzie, B. Joyce-Shaikh, J.S. Stumhofer, T. McClanahan, W. Blumenschein, T. Churakovsa, J. Low, L. Presta, et al. 2006. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Invest. 116:1317-1326.
27. Leonardi, C.L., J.L. Powers, R.T. Matheson, B.S. Goffe, R. Zitnik, A. Wang, and A.B. Gottlieb. 2003. Etanercept as monotherapy in patients with psoriasis. N. Engl. J. Med. 349:2014-2022.
28. Chaudhari, U., P. Romano, L.D. Mulcahy, L.T. Dooley, D.G. Baker, and A.B. Gottlieb. 2001. Efficacy and safety of infliximab monotherapy for plaque-type psoriasis: a randomised trial. Lancet. 357:1842-1847.
29. Leigh, I.M., H. Navsaria, P.E. Purkis, I.A. McKay, P.E. Bowden, and P.N. Riddle. 1995. Keratins (K16 and K17) as markers of keratinocyte hyperproliferation in psoriasis in vivo and in vitro. Br. J. Dermatol. 133:501-511.
30. Parrish-Novak, J., W. Xu, T. Brender, L. Yao, C. Jones, J. West, C. Brandt, L. Jelinek, K. Madden, P.A. McKernan, et al. 2002. Interleukins 19, 20, and 24 signal through two distinct receptor complexes. Differences in receptor-ligand interactions mediate unique biological functions. J. Biol. Chem. 277:47517-47523.
31. Wang, M., Z. Tan, R. Zhang, S.V. Kotenko, and P. Liang. 2002. Interleukin 24 (MDA-7/MOB-5) signals through two heterodimeric receptors, IL-22R1/IL-20R2 and IL-20R1/IL-20R2. J. Biol. Chem. 277:7341-7347.
32. Blumberg, H., D. Conklin, W.F. Xu, A. Grossmann, T. Brender, S. Carollo, M. Eagan, D. Foster, B.A. Haldeman, A. Hammond, et al. 2001. Interleukin 20: discovery, receptor identification, and role in epidermal function. Cell. 104:9-19.
33. Kauffman, C.L., N. Aria, E. Toichi, T.S. McCormick, K.D. Cooper, A.B. Gottlieb, D.E. Everitt, B. Frederick, Y. Zhu, M.A. Graham, et al. 2004. A phase I study evaluating the safety, pharmacokinetics, and clinical response of a human IL-12 p40 antibody in subjects with plaque psoriasis. J. Invest. Dermatol. 123:1037-1044.
34. Lew, W., A.M. Bowcock, and J.G. Krueger. 2004. Psoriasis vulgaris: cutaneous lymphoid tissue supports T-cell activation and "Type 1" inflammatory gene expression. Trends Immunol. 25:295-305.
35. Bowcock, A.M. 2004. Psoriasis genetics: the way forward. J. Invest. Dermatol. 122:xv-xvii.
36. Aggarwal, S., N. Ghilardi, M.H. Xie, F.J. de Sauvage, and A.L. Gurney. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278:1910-1914.
37. McAllister, F., A. Henry, J.L. Kreindler, P.J. Dubin, L. Ulrich, C. Steele, J.D. Finder, J.M. Pilewski, B.M. Carreno, S.J. Goldman, et al. 2005. Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J. Immunol. 175:404-412.
38. Henseler, T., and E. Christophers. 1995. Disease concomitance in psoriasis. J. Am. Acad. Dermatol. 32:982-986.
39. Kawaguchi, M., F. Kokubu, S. Matsukura, K. Ieki, M. Odaka, S. Watanabe, S. Suzuki, M. Adachi, and S.K. Huang. 2003. Induction of C-X-C chemokines, growth-related oncogene alpha expression, and epithelial cell-derived neutrophil-activating protein-78 by ML-1 (interleukin-17F) involves activation of Raf1-mitogen-activated protein kinase kinase-extracellular signal-regulated kinase 1/2 pathway. J. Pharmacol. Exp. Ther. 307:1213-1220.
40. Laan, M., Z.H. Cui, H. Hoshino, J. Lotvall, M. Sjostrand, D.C. Gruenert, B.E. Skoogh, and A. Linden. 1999. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J. Immunol. 162:2347-2352.
41. Kao, C.Y., Y. Chen, P. Thai, S. Wachi, F. Huang, C. Kim, R.W. Harper, and R. Wu. 2004. IL-17 markedly up-regulates beta-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways. J. Immunol. 173:3482-3491.
42. Gottlieb, A.B., F. Chamian, S. Masud, I. Cardinale, M.V. Abello, M.A. Lowes, F. Chen, M. Magliocco, and J.G. Krueger. 2005. TNF inhibition rapidly down-regulates multiple proinflammatory pathways in psoriasis plaques. J. Immunol. 175:2721-2729.
43. Gallagher, G., J. Eskdale, W. Jordan, J. Peat, J. Campbell, M. Boniotto, G.P. Lennon, H. Dickensheets, and R.P. Donnelly. 2004. Human interleukin-19 and its receptor: a potential role in the induction of Th2 responses. Int. Immunopharmacol. 4:615-626.
44. Su, Z.Z., M.T. Madireddi, J.J. Lin, C.S. Young, S. Kitada, J.C. Reed, N.I. Goldstein, and P.B. Fisher. 1998. The cancer growth suppressor gene mda-7 selectively induces apoptosis in human breast cancer cells and inhibits tumor growth in nude mice. Proc. Natl. Acad. Sci. USA. 95:14400-14405.
45. Soo, C., W.W. Shaw, E. Freymiller, M.T. Longaker, C.N. Bertolami, R. Chiu, A. Tieu, and K. Ting. 1999. Cutaneous rat wounds express c49a, a novel gene with homology to the human melanoma differentiation associated gene, mda-7. J. Cell. Biochem. 74:1-10.
46. Wolk, K., S. Kunz, E. Witte, M. Friedrich, K. Asadullah, and R. Sabat. 2004. IL-22 increases the innate immunity of tissues. Immunity. 21:241-254.
47. Boniface, K., F.X. Bernard, M. Garcia, A.L. Gurney, J.C. Lecron, and F. Morel. 2005. IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J. Immunol. 174:3695-3702.
48. Wolk, K., E. Witte, E. Wallace, W.D. Docke, S. Kunz, K. Asadullah, H.D. Volk, W. Sterry, and R. Sabat. 2006. IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis. Eur. J. Immunol. 36:1309-1323.
49. Schon, M., D. Denzer, R.C. Kubitza, T. Ruzicka, and M.P. Schon. 2000. Critical role of neutrophils for the generation of psoriasiform skin lesions in flaky skin mice. J. Invest. Dermatol. 114:976-983.
50. Nagalakshmi, M.L., E. Murphy, T. McClanahan, and R. de Waal Malefyt. 2004. Expression patterns of IL-10 ligand and receptor gene families provide leads for biological characterization. Int. Immunopharmacol. 4:577-592.
51. Abrams, J.S., M.G. Roncarolo, H. Yssel, U. Andersson, G.J. Gleich, and J.E. Silver. 1992. Strategies of anti-cytokine monoclonal antibody development: immunoassay of IL-10 and IL-5 in clinical samples. Immunol. Rev. 127:5-24.
52. Krane, J.F., D.P. Murphy, D.M. Carter, and J.G. Krueger. 1991. Synergistic effects of epidermal growth factor (EGF) and insulin-like growth factor I/somatomedin C (IGF-I) on keratinocyte proliferation may be mediated by IGF-I transmodulation of the EGF receptor. J. Invest. Dermatol. 96:419-424.