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J. Biol. Chem., Vol. 279, Issue 36, 38055-38061, September 3, 2004

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SOX7 and SOX17 Regulate the Parietal Endoderm-specific Enhancer Activity of Mouse Laminin 1 Gene^*

Tomoaki Niimi, Yoshitaka Hayashi, Sugiko Futaki, and Kiyotoshi Sekiguchi¶

From the Sekiguchi Biomatrix Signaling Project, ERATO, Japan Science and Technology Agency, Aichi Medical University, Karimata, Yazako, Nagakute, Aichi 480-1195 and ^¶Division of Protein Chemistry, Institute for Protein Research, Osaka University, Yamadaoka, Suita, Osaka 565-0871, Japan

Laminin-1 is the major component of embryonic basement membrane and consists of 1, 1, and 1 chains. The expression of laminin-1 is induced in mouse F9 embryonal carcinoma cells upon differentiation into parietal endoderm cells. We recently identified a parietal endoderm-specific enhancer in the mouse laminin 1 (Lama1) gene and showed that Sp1/Sp3 and YY1 transcription factors were involved in the enhancer activity. Although here we identified that NF-Y binds to the enhancer sequence between Sp1/Sp3- and YY1-binding sites, all these transcription factors are ubiquitously expressed and thus are not sufficient to explain parietal endoderm-specific enhancer activity. In the present study, we further showed that SOX7 and SOX17 are involved in the regulation of parietal endoderm-specific enhancer activity of the mouse Lama1 gene. Northern blot analysis revealed that the steady-state levels of mouse Sox7 and Sox17 mRNAs increased in parallel with that of Lama1 mRNA during the differentiation of F9 cells. Both SOX7 and SOX17 markedly trans-activated the transcription of the Lama1 enhancer-reporter construct in undifferentiated F9 cells in a manner dependent on high mobility group box-mediated DNA binding. Electrophoretic mobility shift assays and mutational analyses revealed that SOX7 and SOX17 bound specifically to two SOX-binding sites within the Lama1 enhancer, and that these SOX-binding sites functioned synergistically to confer the trans-activation by SOX7 and SOX17. Furthermore, this trans-activation was dependent on the integrity of the binding sites for Sp1/Sp3 and NF-Y located at upstream of the two SOX-binding sites. These results indicate that the transcription of the mouse Lama1 gene during the differentiation of F9 cells is controlled by a combination of the actions of the ubiquitous factors, Sp1/Sp3 and NF-Y, and the parietal endoderm-specific factors, SOX7 and SOX17.

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

^* 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: Sekiguchi Biomatrix Signaling Project, ERATO, Japan Science and Technology Agency, Aichi Medical University, 21, Karimata, Yazako, Nagakute, Aichi 480-1195, Japan. Tel.: 81-561-64-5020; Fax: 81-561-64-2773; E-mail: hayashiy{at}aichi-med-u.ac.jp.

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