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J. Biol. Chem., Vol. 279, Issue 32, 33343-33351, August 6, 2004

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The T-cell Lymphokine Interleukin-26 Targets Epithelial Cells through the Interleukin-20 Receptor 1 and Interleukin-10 Receptor 2 Chains^*

Simon Hör¶, Heide Pirzer¶, Laure Dumoutier||, Finn Bauer**, Sabine Wittmann, Heinrich Sticht**, Jean-Christophe Renauld||, René de Waal Malefyt, and Helmut Fickenscher¶¶

From the Virology Department, Ruprecht-Karls University, D-69120 Heidelberg, Germany, Cambridge Institute for Medical Research, Cambridge CB2 2XY, United Kingdom, the ^||Ludwig Institute for Cancer Research, Université Catholique de Louvain, B-1200 Brussels, Belgium, the ^**Bioinformatics Unit, Biochemistry Department, University Erlangen-Nuremberg, D-91054 Erlangen, Germany, the Institute for Clinical and Molecular Virology, University Erlangen-Nuremberg, D-91054 Erlangen, Germany, and the Department of Pharmacology, DNAX Research Institute of Molecular and Cellular Biology Inc., Palo Alto, California 94304

The cellular members of the interleukin-10 (IL-10) cytokine family share sequence homology with IL-10, whereas their sites of expression and their functions are divergent. One of these factors, AK155 or IL-26, was discovered because of its overexpression in human T lymphocytes after growth transformation by the simian rhadinovirus herpesvirus saimiri. In addition, the gene is transcribed in various types of primary and immortalized T-cells. Here we describe epithelial cells, namely colon carcinoma cells and keratinocytes, as targets of this T-cellular lymphokine. Purified recombinant IL-26 induced the rapid phosphorylation of the signal transducer and activator of transcription factors 1 and 3. As a result, secretion of IL-10 and IL-8, as well as cell surface expression of CD54 were enhanced. Moreover, we show that the IL-26 protein binds to heparin, is released from the cell surface, and can be functionally inhibited by heparin. The sensitivity to recombinant IL-26 of various cell lines strictly correlated with the expression of the long chain of the IL-20 receptor. Because blocking antibodies against either the short chain of the IL-10 receptor or the long chain of the IL-20 receptor inhibited IL-26-dependent signal transduction, and transient expression of these receptor chains induced IL-26 responsivity in non-sensitive cells, we propose that the IL-20 receptor 1 and IL-10 receptor 2 chains participate in forming the IL-26 receptor. Targeting epithelial cells, the T-cell lymphokine IL-26 is likely to play a role in local mechanisms of mucosal and cutaneous immunity.

Received for publication, May 5, 2004 , and in revised form, June 1, 2004.

^* This work was supported by the Deutsche Forschungsgemeinschaft. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ Both authors contributed equally to this work.

^¶¶ To whom correspondence should be addressed: Virology Dept., Ruprecht-Karls University Heidelberg, Im Neuenheimer Feld 324, D-69120 Heidelberg, Germany. Tel.: 49-6221-56-5006; Fax: 49-6221-56-4551; E-mail: helmut.fickenscher{at}med.uni-heidelberg.de.

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