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Department of Developmental Biology (T.K., H.M., T.M., H.O., K.-I.M.), National Institute for Basic Biology, Okazaki 444-8787, Japan; School of Life Science (T.K., K.-I.M.), The Graduate University for Advanced Studies, Okazaki 444-8585, Japan; Core Research for Evolutional Science and Technology (CREST) (H.M., S.H., K.I.N., K.-I.M.), Japan Science and Technology Corporation, Kawaguchi 332-0012, Japan; Graduate School of Integrated Science (D.B., M.S.), Yokohama City University, Yokohama 230-0045, Japan; Department of Molecular and Cellular Biology (S.H., K.I.N.), Medical Institute of Bioregulation, Kyushu University, Fukuoka 812-8582, Japan; and Department of Biochemistry (H.Y., A.K.), Graduate School of Biomedical Sciences, Hiroshima University, Hiroshima 734-8551, Japan
Address all correspondence and requests for reprints to: Ken-ichirou Morohashi, Prof., Ph.D., Department of Developmental Biology, National Institute for Basic Biology, Myodaiji-cho, Okazaki 444-8787, Japan. E-mail: moro{at}nibb.ac.jp.
An orphan nuclear receptor, Ad4 binding protein/steroidogenic factor 1 (Ad4BP/SF-1), is essential for the development and function of steroidogenic tissues. To examine the transcriptional regulation of Ad4BP/SF-1, two-hybrid screening was performed, and the sumoylation [conjugation of a small ubiqutin-like modifier (SUMO-1)] components Ubc9, protein inhibitor of activated STAT 1 (PIAS1), and protein inhibitor of activated STAT 3 (PIAS3) were isolated. Cultured cell and in vitro studies revealed that Ad4BP/SF-1 is sumoylated at K119 and K194. Because K194 lies within the synergy control (SC) motif defined to repress synergistic transcription from promoters containing multiple binding sites, correlation between the functions of the SC motif and sumoylation was investigated. The K194R mutant of Ad4BP/SF-1, which cannot be sumoylated, showed enhanced synergistic transcription from a promoter containing multiple Ad4/SF-1 sites, suggesting that sumoylation is necessary for repression of transcriptional synergy through the SC motif. It has been established that the Müllerian inhibiting substance gene is transcribed predominantly under the control of Ad4BP/SF-1 and, moreover, its transcription is regulated synergistically with Sox9, Gata4, and Wt1. Interestingly, it was found that all of these factors are sumoylated, and these sumoylation sites occur within SC motifs. Based on the observation that SC motif mutants of Ad4BP/SF-1 and Sox9 resulted in the enhancement of their synergistic transcription, it was concluded that the SC motif regulates synergistic transcription even between distinct types of transcription factors. Considering that both mutants cannot be sumoylated, it is likely that sumoylation is implicated in this regulation. Because it was revealed with an in vitro sumoylated Ad4BP/SF-1 that DNA binding activity and interaction with Sox9 were unaffected, sumoylation may regulate transcription through affecting selective and cooperative interaction among factors constituting transcriptional complexes.
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