Tumor necrosis factor receptor signaling in keratinocytes triggers interleukin-24-dependent psoriasis-like skin inflammation in mice

Immunity

Volumn 39, Issue 5, 2013, Pages 899-911

  Kumari, Snehlata ^a,b   Bonnet, Marion C ^b,h   Ulvmar, Maria H ^c,i   Wolk, Kerstin ^d   Karagianni, Niki ^e,f   Witte, Ellen ^d   Uthoff Hachenberg, Claudia ^b   Renauld, Jean Christophe ^g   Kollias, George ^e   Toftgard, Rune ^c   Sabat, Robert ^d   Pasparakis, Manolis ^b   Haase, Ingo ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c KAROLINSKA INSTITUTE   (Sweden)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^f Biomedcode Hellas SA   (Greece)

^g UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^h SAINT LOUIS HOSPITAL   (France)

ⁱ UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 19; INTERLEUKIN 24; STAT3 PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR 1; CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; I KAPPA B KINASE; IKBKB PROTEIN, MOUSE; IL24 PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE; INTERLEUKIN RECEPTOR; INTERLEUKIN-22 RECEPTOR; INTERLEUKIN-24; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN, MOUSE; TNFRSF1A PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DERMATITIS; DISEASE COURSE; EPIDERMIS; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSORIASIS; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; CROSS BREEDING; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; CROSSES, GENETIC; CYTOKINES; DISEASE MODELS, ANIMAL; EPIDERMIS; GENE EXPRESSION REGULATION; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; I-KAPPA B KINASE; INTERLEUKINS; KERATINOCYTES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NF-KAPPA B; PSORIASIS; REACTIVE OXYGEN SPECIES; RECEPTORS, INTERLEUKIN; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; STAT3 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84887617139     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.10.009     Document Type: Article

References (47)

1. Apostolaki M., Armaka M., Victoratos P., Kollias G. Cellular mechanisms of TNF function in models of inflammation and autoimmunity. Curr. Dir. Autoimmun. 2010, 11:1-26.
2. Bonnet M.C., Preukschat D., Welz P.S., van Loo G., Ermolaeva M.A., Bloch W., Haase I., Pasparakis M. The adaptor protein FADD protects epidermal keratinocytes from necroptosis invivo and prevents skin inflammation. Immunity 2011, 35:572-582.
3. Clark K., Peggie M., Plater L., Sorcek R.J., Young E.R., Madwed J.B., Hough J., McIver E.G., Cohen P. Novel cross-talk within the IKK family controls innate immunity. Biochem. J. 2011, 434:93-104.
4. Conti P., Kempuraj D., Frydas S., Kandere K., Boucher W., Letourneau R., Madhappan B., Sagimoto K., Christodoulou S., Theoharides T.C. IL-10 subfamily members: IL-19, IL-20, IL-22, IL-24 and IL-26. Immunol. Lett. 2003, 88:171-174.
5. Dumoutier L., Leemans C., Lejeune D., Kotenko S.V., Renauld J.C. Cutting edge: STAT activation by IL-19, IL-20 and mda-7 throughIL-20 receptor complexes of two types. J.Immunol. 2001, 167:3545-3549.
6. Haase I., Hobbs R.M., Romero M.R., Broad S., Watt F.M. A role for mitogen-activated protein kinase activation by integrins in the pathogenesis of psoriasis. J.Clin. Invest. 2001, 108:527-536.
7. Hafner M., Wenk J., Nenci A., Pasparakis M., Scharffetter-Kochanek K., Smyth N., Peters T., Kess D., Holtkötter O., Shephard P., et al. Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis 2004, 38:176-181.
8. He M., Liang P. IL-24 transgenic mice: invivo evidence of overlapping functions for IL-20, IL-22, and IL-24 in the epidermis. J.Immunol. 2010, 184:1793-1798.
9. Hobbs R.M., Watt F.M. Regulation of interleukin-1alpha expression by integrins and epidermal growth factor receptor in keratinocytes from a mouse model of inflammatory skin disease. J.Biol. Chem. 2003, 278:19798-19807.
10. Hobbs R.M., Silva-Vargas V., Groves R., Watt F.M. Expression of activated MEK1 in differentiating epidermal cells is sufficient to generate hyperproliferative and inflammatory skin lesions. J.Invest. Dermatol. 2004, 123:503-515.
11. Jordan C.T., Cao L., Roberson E.D., Duan S., Helms C.A., Nair R.P., Duffin K.C., Stuart P.E., Goldgar D., Hayashi G., et al. Rare and common variants in CARD14, encoding an epidermal regulator of NF-kappaB, in psoriasis. Am. J. Hum. Genet. 2012, 90:796-808.
12. Kreymborg K., Etzensperger R., Dumoutier L., Haak S., Rebollo A., Buch T., Heppner F.L., Renauld J.C., Becher B. IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis. J.Immunol. 2007, 179:8098-8104.
13. Kunz S., Wolk K., Witte E., Witte K., Doecke W.D., Volk H.D., Sterry W., Asadullah K., Sabat R. Interleukin (IL)-19, IL-20 and IL-24 are produced by and act on keratinocytes and are distinct from classical ILs. Exp. Dermatol. 2006, 15:991-1004.
14. Leng R.X., Pan H.F., Tao J.H., Ye D.Q. IL-19, IL-20 and IL-24: potential therapeutic targets for autoimmune diseases. Expert Opin. Ther. Targets 2011, 15:119-126.
15. Lind M.H., Rozell B., Wallin R.P., van Hogerlinden M., Ljunggren H.G., Toftgård R., Sur I. Tumor necrosis factor receptor 1-mediated signaling is required for skin cancer development induced by NF-kappaB inhibition. Proc. Natl. Acad. Sci. USA 2004, 101:4972-4977.
16. Lowes M.A., Chamian F., Abello M.V., Fuentes-Duculan J., Lin S.L., Nussbaum R., Novitskaya I., Carbonaro H., Cardinale I., Kikuchi T., et al. Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc. Natl. Acad. Sci. USA 2005, 102:19057-19062.
17. Lowes M.A., Bowcock A.M., Krueger J.G. Pathogenesis and therapy of psoriasis. Nature 2007, 445:866-873.
18. Nair R.P., Duffin K.C., Helms C., Ding J., Stuart P.E., Goldgar D., Gudjonsson J.E., Li Y., Tejasvi T., Feng B.J., et al. Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat. Genet. 2009, 41:199-204. Collaborative Association Study of Psoriasis.
19. Nestle F.O., Kaplan D.H., Barker J. Psoriasis. N.Engl. J. Med. 2009, 361:496-509.
20. Nickoloff B.J., Wrone-Smith T. Injection of pre-psoriatic skin with CD4+ Tcells induces psoriasis. Am. J. Pathol. 1999, 155:145-158.
21. Nickoloff B.J., Schröder J.M., von den Driesch P., Raychaudhuri S.P., Farber E.M., Boehncke W.H., Morhenn V.B., Rosenberg E.W., Schön M.P., Holick M.F. Is psoriasis a T-cell disease?. Exp. Dermatol. 2000, 9:359-375.
22. Ouyang W., Rutz S., Crellin N.K., Valdez P.A., Hymowitz S.G. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu. Rev. Immunol. 2011, 29:71-109.
23. Parrish-Novak J., Xu W., Brender T., Yao L., Jones C., West J., Brandt C., Jelinek L., Madden K., McKernan P.A., et al. Interleukins 19, 20, and 24 signal through two distinct receptor complexes. Differences in receptor-ligand interactions mediate unique biological functions. J.Biol. Chem. 2002, 277:47517-47523.
24. Pasparakis M., Courtois G., Hafner M., Schmidt-Supprian M., Nenci A., Toksoy A., Krampert M., Goebeler M., Gillitzer R., Israel A., et al. TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature 2002, 417:861-866.
25. Pfeffer K., Matsuyama T., Kündig T.M., Wakeham A., Kishihara K., Shahinian A., Wiegmann K., Ohashi P.S., Krönke M., Mak T.W. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 1993, 73:457-467.
26. Rebholz B., Haase I., Eckelt B., Paxian S., Flaig M.J., Ghoreschi K., Nedospasov S.A., Mailhammer R., Debey-Pascher S., Schultze J.L., et al. Crosstalk between keratinocytes and adaptive immune cells in an IkappaBalpha protein-mediated inflammatory disease of the skin. Immunity 2007, 27:296-307.
27. Rømer J., Hasselager E., Nørby P.L., Steiniche T., Thorn Clausen J., Kragballe K. Epidermal overexpression of interleukin-19 and -20 mRNA in psoriatic skin disappears after short-term treatment with cyclosporine a or calcipotriol. J.Invest. Dermatol. 2003, 121:1306-1311.
28. Sabat R. IL-10 family of cytokines. Cytokine Growth Factor Rev. 2010, 21:315-324.
29. Sabat R., Philipp S., Höflich C., Kreutzer S., Wallace E., Asadullah K., Volk H.D., Sterry W., Wolk K. Immunopathogenesis of psoriasis. Exp. Dermatol. 2007, 16:779-798.
30. Sakon S., Xue X., Takekawa M., Sasazuki T., Okazaki T., Kojima Y., Piao J.H., Yagita H., Okumura K., Doi T., Nakano H. NF-kappaB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J. 2003, 22:3898-3909.
31. Sano S., Chan K.S., Carbajal S., Clifford J., Peavey M., Kiguchi K., Itami S., Nickoloff B.J., DiGiovanni J. Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat. Med. 2005, 11:43-49.
32. Stratis A., Pasparakis M., Rupec R.A., Markur D., Hartmann K., Scharffetter-Kochanek K., Peters T., van Rooijen N., Krieg T., Haase I. Pathogenic role for skin macrophages in a mouse model of keratinocyte-induced psoriasis-like skin inflammation. J.Clin. Invest. 2006, 116:2094-2104.
33. Takahashi H., Ibe M., Nakamura S., Ishida-Yamamoto A., Hashimoto Y., Iizuka H. Extracellular regulated kinase and c-Jun N-terminal kinase are activated in psoriatic involved epidermis. J.Dermatol. Sci. 2002, 30:94-99.
34. Tscharntke M., Pofahl R., Chrostek-Grashoff A., Smyth N., Niessen C., Niemann C., Hartwig B., Herzog V., Klein H.W., Krieg T., et al. Impaired epidermal wound healing invivo upon inhibition or deletion of Rac1. J.Cell Sci. 2007, 120:1480-1490.
35. Van Hauwermeiren F., Armaka M., Karagianni N., Kranidioti K., Vandenbroucke R.E., Loges S., Van Roy M., Staelens J., Puimège L., Palagani A., et al. Safe TNF-based antitumor therapy following p55TNFR reduction in intestinal epithelium. J.Clin. Invest. 2013, 123:2590-2603.
36. van Hogerlinden M., Rozell B.L., Ahrlund-Richter L., Toftgård R. Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-kappaB signaling. Cancer Res. 1999, 59:3299-3303.
37. Victoratos P., Lagnel J., Tzima S., Alimzhanov M.B., Rajewsky K., Pasparakis M., Kollias G. FDC-specific functions of p55TNFR and IKK2 in the development of FDC networks and of antibody responses. Immunity 2006, 24:65-77.
38. Walczak H. TNF and ubiquitin at the crossroads of gene activation, cell death, inflammation, and cancer. Immunol. Rev. 2011, 244:9-28.
39. Wang F., Smith N., Maier L., Xia W., Hammerberg C., Chubb H., Chen C., Riblett M., Johnston A., Gudjonsson J.E., et al. Etanercept suppresses regenerative hyperplasia in psoriasis by acutely downregulating epidermal expression of interleukin (IL)-19, IL-20 and IL-24. Br. J. Dermatol. 2012, 167:92-102.
40. Weiss B., Wolk K., Grünberg B.H., Volk H.D., Sterry W., Asadullah K., Sabat R. Cloning of murine IL-22 receptor alpha 2 and comparison with its human counterpart. Genes Immun. 2004, 5:330-336.
41. Wolk K., Kunz S., Witte E., Friedrich M., Asadullah K., Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004, 21:241-254.
42. Wolk K., Haugen H.S., Xu W., Witte E., Waggie K., Anderson M., Vom Baur E., Witte K., Warszawska K., Philipp S., et al. IL-22 and IL-20 are key mediators of the epidermal alterations in psoriasis while IL-17 and IFN-gamma are not. J.Mol. Med. 2009, 87:523-536.
43. Wolk K., Witte E., Warszawska K., Schulze-Tanzil G., Witte K., Philipp S., Kunz S., Döcke W.D., Asadullah K., Volk H.D., et al. The Th17 cytokine IL-22 induces IL-20 production in keratinocytes: a novel immunological cascade with potential relevance in psoriasis. Eur. J. Immunol. 2009, 39:3570-3581.
44. Wolk K., Warszawska K., Hoeflich C., Witte E., Schneider-Burrus S., Witte K., Kunz S., Buss A., Roewert H.J., Krause M., et al. Deficiency of IL-22 contributes to a chronic inflammatory disease: pathogenetic mechanisms in acne inversa. J.Immunol. 2011, 186:1228-1239.
45. Yang B.X., Duan Y.J., Dong C.Y., Zhang F., Gao W.F., Cui X.Y., Lin Y.M., Ma X.T. Novel functions for mda-7/IL-24 and IL-24 delE5: regulation of differentiation of acute myeloid leukemic cells. Mol. Cancer Ther. 2011, 10:615-625.
46. Zenz R., Eferl R., Kenner L., Florin L., Hummerich L., Mehic D., Scheuch H., Angel P., Tschachler E., Wagner E.F. Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 2005, 437:369-375.
47. Zheng Y., Danilenko D.M., Valdez P., Kasman I., Eastham-Anderson J., Wu J., Ouyang W. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007, 445:648-651.