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J. Biol. Chem., Vol. 281, Issue 23, 15605-15614, June 9, 2006

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Orphan Nuclear Receptor Nur77 Induces Zinc Finger Protein GIOT-1 Gene Expression, and GIOT-1 Acts as a Novel Corepressor of Orphan Nuclear Receptor SF-1 via Recruitment of HDAC2^*

Kwang-Hoon Song¹, Yun-Yong Park¹, Hae Jin Kee, Cheol Yi Hong, Yong-Soo Lee, Seung-Won Ahn, Hye-Jin Kim^¶, Keesook Lee, Hyun Kook, In-Kyu Lee^¶, and Hueng-Sik Choi²

From the Hormone Research Center, School of Biological Sciences and Technology, Chonnam National University, Gwangju 500-757, the Research Institute of Medical Sciences and Medical Research Center for Gene Regulation, Chonnam National University Medical School, Gwangju 501-757, and the ^¶Section of Endocrinology, Department of Internal Medicine, Kyungpook National University Hospital, School of Medicine, Kyungpook National University, Taegu 700-721, Republic of Korea

Kruppel-associated box (KRAB) domain-containing proteins consist of potential transcriptional repression modules. Previously, gonadotropin-inducible ovarian transcription factor-1 (GIOT-1) was identified as a novel KRAB-containing zinc finger protein and shown to have transcriptional repression activity. Here, we demonstrate that orphan nuclear receptor Nur77 regulates GIOT-1 gene expression in testicular Leydig cell lines and that GIOT-1 acts as a novel corepressor of the orphan nuclear receptor steroidogenic factor 1 (SF-1). Mutation analysis of the GIOT-1 promoter and overexpression analysis of dominant-negative Nur77 revealed that luteinizing hormone activates GIOT-1 gene expression through Nur77. Electrophoretic mobility shift and chromatin immunoprecipitation assays showed that Nur77 directly binds to the GIOT-1 promoter. GIOT-1 represses the SF-1 transactivation, and specific interaction between GIOT-1 and SF-1 was observed. We also demonstrate an interaction between GIOT-1 and histone deacetylase 2 (HDAC2). GIOT-1-mediated transrepression was recovered by down-regulation of HDAC2 expression with small interfering RNA of HDAC2. Knock down of the endogenous GIOT-1 results in significant enhancement of CYP17 expression in Leydig cells. In conclusion, this study of cross-talk between GIOT-1 and orphan nuclear receptors will provide new insights into the role of KRAB-containing zinc finger proteins in nuclear receptor action.

Received for publication, June 1, 2005 , and in revised form, April 1, 2006.

^* This work was supported by the National Research Laboratory program (GrantM1-0500-4705J-4710), the Korea Science and Engineering Foundation (Grant C00126 [GenBank] ), MarineBio21, the BK21 program, and the Ministry of Environment. 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.

¹ Both authors contributed equally to this work.

² To whom correspondence should be addressed: Tel.: 82-62-530-0503; Fax: 82-62-530-0500; E-mail: hsc{at}chonnam.ac.kr.

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