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J. Biol. Chem., Vol. 278, Issue 44, 43470-43479, October 31, 2003
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Interferes with Transforming Growth Factor-
Signaling through Direct Interaction of YB-1 with Smad3*
From the
Environmental Health Science Laboratory, Sumitomo Chemical Co., Ltd., Konohana-ku, Osaka 554-8558, Japan, the ¶Department of Community Health, Tokai University School of Medicine, Isehara, Kanagawa 259-1193, Japan, and the ||Allergy Research Center, Juntendo University School of Medicine, Bunkyo-ku, Tokyo 113-8421, Japan
Transforming growth factor-
(TGF-) and interferon-
(IFN-) exert antagonistic effects on collagen synthesis in human dermal fibroblasts. We have recently shown that Y box-binding protein YB-1 mediates the inhibitory effects of IFN- on 
2(I) procollagen gene (COL1A2) transcription through the IFN- response element located between –161 and –150. Here we report that YB-1 counter-represses TGF--stimulated COL1A2 transcription by interfering with Smad3 bound to the upstream sequence around –265 and subsequently by interrupting the Smad3-p300 interaction. Western blot and immunofluorescence analyses using inhibitors for Janus kinases or casein kinase II suggested that the casein kinase II-dependent signaling pathway mediates IFN--induced nuclear translocation of YB-1. Down-regulation of endogenous YB-1 expression by double-stranded YB-1-specific RNA abrogated the transcriptional repression of COL1A2 by IFN- in the absence and presence of TGF-. In transient transfection assays, overexpression of YB-1 in human dermal fibroblasts exhibited antagonistic actions against TGF- and Smad3. Physical interaction between Smad3 and YB-1 was demonstrated by immunoprecipitation-Western blot analyses, and electrophoretic mobility shift assays using the recombinant Smad3 and YB-1 proteins indicated that YB-1 forms a complex with Smad3 bound to the Smad-binding element. Glutathione S-transferase pull-down assays showed that YB-1 binds to the MH1 domain of Smad3, whereas the central and carboxyl-terminal regions of YB-1 were required for its interaction with Smad3. YB-1 also interferes with the Smad3-p300 interaction by its preferential binding to p300. Altogether, the results provide a novel insight into the mechanism by which IFN-/YB-1 counteracts TGF-/Smad3. They also indicate that IFN-/YB-1 inhibits COL1A2 transcription by dual actions: via the IFN- response element and through a cross-talk with the TGF-/Smad signaling pathway.
Received for publication, March 6, 2003 , and in revised form, July 25, 2003.
* 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.
To whom correspondence should be addressed. Tel.: 81-6-6466-5306; Fax: 81-6-6466-5319; E-mail: higashik2{at}sc.sumitomo-chem.co.jp.
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